38_Marine_00cover.indd 1 
SERIES PUBLICATIONS OF THE SMITHSONIAN INSTITUTION

Emphasis upon publication as a means of “diffusing knowledge” was 

expressed by the fi rst Secretary of the Smithsonian. In his formal plan 

for the Institution, Joseph Henry outlined a program that included 

the following statement: “It is proposed to publish a series of reports, 

giving an account of the new discoveries in science, and of the changes 

made from year to year in all branches of knowledge.” This theme of 

basic research has been adhered to through the years by thousands of 

titles issued in series publications under the Smithsonian imprint, commencing with Smithsonian Contributions to Knowledge in 1848 and 

continuing with the following active series: 

Smithsonian Contributions to Anthropology

Smithsonian Contributions to Botany

Smithsonian Contributions in History and Technology

Smithsonian Contributions to the Marine Sciences

Smithsonian Contributions to Museum Conservation

Smithsonian Contributions to Paleobiology

Smithsonian Contributions to Zoology

In these series, the Institution publishes small papers and full-scale 

monographs that report on the research and collections of its various 

museums and bureaus. The Smithsonian Contributions Series are 

distributed via mailing lists to libraries, universities, and similar institutions throughout the world. 

Manuscripts submitted for series publication are received by the 

Smithsonian Institution Scholarly Press from authors with direct affi liation with the various Smithsonian museums or bureaus and are subject 

to peer review and review for compliance with manuscript preparation 

guidelines. General requirements for manuscript preparation are on the 

inside back cover of printed volumes. For detailed submissions requirements and to review the “Manuscript Preparation and Style Guide for 

Authors,” visit the Submissions page at www.scholarlypress.si.edu.

38_Marine_00cover.indd 2 8_Marine_00cover.indd 2 
smithsonian contributions to the marine sciences • number 38

WASHINGTON D.C.

2009

Proceedings of the

Smithsonian 

Marine Science 

Symposium

Edited by 

Michael A. Lang, 

Ian G. Macintyre, and Klaus Rützler

00_FM_i-xii_Lang.indd i 0_FM_i-xii_Lang.indd i 9/24/09 9:19/24/09 9:19
ABSTRACT

Lang, Michael A., Ian G. Macintyre, and Klaus Rützler, editors. Proceedings of the Smithsonian 

Marine Science Symposium. Smithsonian Contributions to the Marine Sciences, number 38, 529 

pages, 217 fi gures, 47 tables, 2009.— The Smithsonian Marine Science Symposium was held on 

15– 16 November 2007 in Washington, D.C. It represented the fi rst major dissemination of marine research results since the establishment of the Smithsonian Marine Science Network (MSN). 

The 39 papers in this volume represent a wide range of marine research studies that demonstrate 

the breadth and diversity of science initiatives supported by the MSN. The fi rst section contains 

an overview of the MSN along with papers describing the multidisciplinary investigations spanning more than 37 years for the four Smithsonian marine facilities that constitute the Network: 

the Smithsonian Environmental Research Center at the Chesapeake Bay, Maryland; the National 

Museum of Natural History’s Smithsonian Marine Station at Fort Pierce, Florida; the Caribbean Coral Reef Ecosystems Program, with its Carrie Bow Marine Field Station in Belize; and 

the Smithsonian Tropical Research Institute in Panama. Subsequent papers represent fi ndings 

by Smithsonian scholars and their collaborators on overarching topics of marine biodiversity, 

evolution, and speciation; biogeography, invasive species, and marine conservation; and forces of 

ecological change in marine systems.

Cover images: (left) Aurelia aurita sea jelly with juvenile carangid jacks in its bell, Carrie Bow 

Cay, Belize; (middle) Dendronephthya soft corals and Anthias school, The Brothers Islands, Red 

Sea, Egypt; (right) grey reef shark Carcharhinus amblyrhynchos, Kingman Reef, Northern Line 

Islands (all photos by Michael A. Lang).

Published by Smithsonian Institution Scholarly Press

P.O. Box 37012

MRC 957

Washington, D.C._20013-7012

www.scholarlypress.si.edu

Library of Congress Cataloging-in-Publication Data

Smithsonian Marine Science Symposium (2007 : Washington D.C.)

 Proceedings of the Smithsonian Marine Science Symposium / edited by Michael A. Lang, Ian 

G. Macintyre, and Klaus Rützler.

 p. cm. — (Smithsonian contributions to the marine sciences, ISSN 0196-0768 ; no. 38)

 Includes bibliographical references and index.

 1. Marine sciences—Congresses. I. Lang, Michael A. II. Macintyre, Ian G. III. Rützler, Klaus. 

IV. Title

 GC2.S57 2007

 578.77—dc22

2009028023

ISSN (print): 0196-0768

ISSN (online): 1943-667X

The paper used in this publication meets the minimum requirements of the American National 

Standard for Permanence of Paper for Printed Library Materials Z39.48– 1992.

00_FM_i-xii_Lang.indd ii 0_FM_i-xii_Lang.indd ii 9/24/09 9:20/24/09 9:20
Contents

FOREWORD by Ira Rubinoff ix

EXECUTIVE SUMMARY by Michael A. Lang xi

OVERVIEW OF SMITHSONIAN MARINE SCIENCE

Introduction to the Smithsonian Marine Science Network 1

Michael A. Lang, Smithsonian Offi ce of the Under Secretary 

for Science

Land– Sea Interactions and Human Impacts in the Coastal Zone 11

Anson H. Hines, Smithsonian Environmental Research Center

Smithsonian Marine Station at Fort Pierce: Thirty-Eight Years 

of Research on the Marine Biodiversity of Florida 25

Valerie J. Paul, Smithsonian Marine Station at Fort Pierce

Julianne Piraino, Smithsonian Marine Station at Fort Pierce

Laura Diederick, Smithsonian Marine Station at Fort Pierce

Caribbean Coral Reef Ecosystems: Thirty-Five Years of Smithsonian 

Marine Science in Belize 43

Klaus Rützler, National Museum of Natural History, 

Smithsonian Institution

The Smithsonian Tropical Research Institute: Marine Research, 

Education, and Conservation in Panama 73

D. Ross Robertson, Smithsonian Tropical Research Institute

John H. Christy, Smithsonian Tropical Research Institute

Rachel Collin, Smithsonian Tropical Research Institute

Richard G. Cooke, Smithsonian Tropical Research Institute

Luis D’Croz, Smithsonian Tropical Research Institute

Karl W. Kaufmann, Smithsonian Tropical Research Institute

Stanley Heckadon Moreno, Smithsonian Tropical Research Institute

Juan L. Maté, Smithsonian Tropical Research Institute

Aaron O’Dea, Smithsonian Tropical Research Institute

Mark E. Torchin, Smithsonian Tropical Research Institute

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i v • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

MARINE BIODIVERSITY, EVOLUTION, AND SPECIATION

Protandric Simultaneous Hermaphroditism Is a Conserved Trait 

in Lysmata (Caridea: Lysmatidae): Implications for the Evolution 

of Hermaphroditism in the Genus 95

J. Antonio Baeza, Smithsonian Marine Station at Fort Pierce

Reconciling Genetic Lineages with Species in Western Atlantic 

Coryphopterus (Teleostei: Gobiidae) 111

Carole C. Baldwin, National Museum of Natural History, 

Smithsonian Institution

Lee A. Weigt, National Museum of Natural History, 

Smithsonian Institution

David G. Smith, National Museum of Natural History, 

Smithsonian Institution

Julie H. Mounts, National Museum of Natural History, 

Smithsonian Institution

Recent Insights into Cnidarian Phylogeny 139

Allen G. Collins, National Marine Fisheries Service Systematics 

Laboratory, National Museum of Natural History, 

Smithsonian Institution

Biodiversity and Abundance of Sponges in Caribbean Mangrove: 

Indicators of Environmental Quality 151

Maria Cristina Diaz, Museo Marino de Margarita, Venezuela

Klaus Rützler, National Museum of Natural History, 

Smithsonian Institution

Internal Transcribed Spacer 2 (ITS2) Variation in the Gorgonian Coral 

Pseudopterogorgia bipinnata in Belize and Panama 173

Daniel Dorado, Universidad de los Andes, Colombia

Juan A. Sánchez, Universidad de los Andes, Colombia

Obvious Invaders and Overlooked Infauna: Unexpected Constituents 

of the Decapod Crustacean Fauna at Twin Cays, Belize 181

Darryl L. Felder, University of Louisiana at Lafayette

Peter C. Dworschak, Naturhistorisches Museum in Wien

Rafael Robles, University of Louisiana at Lafayette

Heather D. Bracken, University of Louisiana at Lafayette

Amanda M. Windsor, University of Louisiana at Lafayette

Jennifer M. Felder, University of Louisiana at Lafayette

Rafael Lemaitre, National Museum of Natural History, 

Smithsonian Institution

Imposex in One of the World’s Busiest Shipping Zones 189

Carter Li, McGill University

Rachel Collin, Smithsonian Tropical Research Institute

Shorefi shes of the Tropical Eastern Pacifi c Online Information System 197

D. Ross Robertson, Smithsonian Tropical Research Institute

Nephasoma pellucidum: A Model Species for Sipunculan Development? 209

Anja Schulze, Texas A&M University at Galveston

Mary E. Rice, Smithsonian Marine Station at Fort Pierce

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NUMBER 38 • v

Mitochondrial Phylogeography of the Intertidal Isopod Excirolana 

braziliensis on the Two Sides of the Isthmus of Panama 219

Renate Sponer, Smithsonian Tropical Research Institute

Harilaos A. Lessios, Smithsonian Tropical Research Institute

Stability and Change in the Indian River Area Bryozoan Fauna 

over a Twenty-Four Year Period 229

Judith E. Winston, Virginia Museum of Natural History

BIOGEOGRAPHY, INVASIVE SPECIES, AND MARINE CONSERVATION

The Turtles’ Tale: Flagships and Instruments for Marine Research, 

Education, and Conservation 241

John G. Frazier, National Zoological Park, Smithsonian Institution

Latitudinal Gradients in Recruitment and Community Dynamics 

in Marine Epifaunal Communities: Implications 

for Invasion Success 247

Amy L. Freestone, Smithsonian Environmental Research Center

Richard W. Osman, Smithsonian Environmental Research Center

Robert B. Whitlatch, University of Connecticut

Ex Situ Culture of Caribbean and Pacifi c Coral Larvae Comparing 

Various Flow-Through Chambers 259

Mary Hagedorn, National Zoological Park, 

Smithsonian Institution

Virginia L. Carter, National Zoological Park, 

Smithsonian Institution

Lea Hollingsworth, University of Hawaii

JoAnne C. Leong, University of Hawaii

Roland Kanno, University of Hawaii

Eric H. Borneman, University of Houston

Dirk Petersen, Rotterdam Zoo

Michael Laterveer, Rotterdam Zoo

Michael Brittsan, Columbus Zoo and Aquarium

Mark Schick, John G. Shedd Aquarium

Worldwide Diving Discoveries of Living Fossil Animals 

from the Depths of Anchialine and Marine Caves 269

Thomas M. Iliffe, Texas A&M University at Galveston

Louis S. Kornicker, National Museum of Natural History, 

Smithsonian Institution

Decimating Mangrove Forests for Commercial Development 

in the Pelican Cays, Belize: Long-Term Ecological Loss 

for Short-Term Gain? 281

Ian G. Macintyre, National Museum of Natural History, 

Smithsonian Institution

Marguerite A. Toscano, National Museum of Natural History, 

Smithsonian Institution

Ilka C. Feller, Smithsonian Environmental Research Center

Maria A. Faust, National Museum of Natural History, 

Smithsonian Institution

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v i • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Using the Panama Canal to Test Predictions about Tropical 

Marine Invasions 291

Gregory M. Ruiz, Smithsonian Environmental Research Center

Mark E. Torchin, Smithsonian Tropical Research Institute

Katharine Grant, Smithsonian Environmental Research Center

Ciguatera Fish Poisoning in the Caribbean 301

Patricia A. Tester, National Ocean Service, NOAA

Rebecca L. Feldman, RLF Environmental

Amy W. Nau, National Ocean Service, NOAA

Maria A. Faust, National Museum of Natural History, 

Smithsonian Institution

R. Wayne Litaker, National Ocean Service, NOAA

FORCES OF ECOLOGICAL CHANGE IN MARINE SYSTEMS

History of Reef Coral Assemblages on the Rhomboid Shoals of Belize 313

Richard B. Aronson, Florida Institute of Technology

Ian G. Macintyre, National Museum of Natural History, 

Smithsonian Institution

Anke M. Moesinger, Dauphin Island Sea Lab

William F. Precht, Florida Keys National Marine 

Sanctuary, NOAA

Michael R. Dardeau, Dauphin Island Sea Lab

Climate and Hydrological Factors Affecting Variation in Chlorophyll 

Concentration and Water Clarity in the Bahia Almirante, Panama 323

Rachel Collin, Smithsonian Tropical Research Institute

Luis D’Croz, Smithsonian Tropical Research Institute

Plinio Gondola, Smithsonian Tropical Research Institute

Juan B. Del Rosario, Smithsonian Tropical Research Institute

Nutrient and Chlorophyll Dynamics in Pacifi c Central 

America (Panama) 335

Luis D’Croz, Smithsonian Tropical Research Institute

Aaron O’Dea, Smithsonian Tropical Research Institute

Growth and Nutrient Conservation in Rhizophora mangle in Response 

to Fertilization along Latitudinal and Tidal Gradients 345

Ilka C. Feller, Smithsonian Environmental Research Center

Catherine E. Lovelock, University of Queensland

Cyril Piou, Institut Nacional de la Recherche Agronomique, France

Underwater Spectral Energy Distribution and Seagrass Depth Limits 

along an Optical Water Quality Gradient 359

Charles L. Gallegos, Smithsonian Environmental 

Research Center

W. Judson Kenworthy, NOAA Center for Coastal Fisheries 

and Habitat Research

Patrick D. Biber, University of Southern Mississippi

Bret S. Wolfe, University of Virginia

00_FM_i-xii_Lang.indd vi 0_FM_i-xii_Lang.indd vi 9/24/09 9:20/24/09 9:20
NUMBER 38 • vii

Interannual Variation in Gelatinous Zooplankton and Their Prey 

in the Rhode River, Maryland 369

Eileen S. Graham, Smithsonian Environmental Research Center

Danielle M. Tuzzolino, Smithsonian Environmental 

Research Center

Rebecca B. Burrell, Smithsonian Environmental Research Center

Denise L. Breitburg, Smithsonian Environmental Research Center

Patterns of Water Quality and Movement in the Vicinity 

of Carrie Bow Cay, Belize 379

Karen H. Koltes, U.S. Department of the Interior

Thomas B. Opishinski, Interactive Oceanographics

Global Change and Marsh Elevation Dynamics: Experimenting 

Where Land Meets Sea and Biology Meets Geology 391

J. Adam Langley, Smithsonian Environmental Research Center

Marc V. Sigrist, Smithsonian Environmental Research Center

James Duls, Smithsonian Environmental Research Center

Donald R. Cahoon, U.S. Geological Survey

James C. Lynch, U.S. Geological Survey

J. Patrick Megonigal, Smithsonian Environmental Research Center

Herbivory, Nutrients, Stochastic Events, and Relative Dominances 

of Benthic Indicator Groups on Coral Reefs: A Review 

and Recommendations 401

Mark M. Littler, National Museum of Natural History, 

Smithsonian Institution

Diane S. Littler, National Museum of Natural History, 

Smithsonian Institution

Barrett L. Brooks, National Museum of Natural History, 

Smithsonian Institution

Impacts of Human Disturbance on Soil Erosion Potential and 

Habitat Stability of Mangrove-Dominated Islands in the 

Pelican Cays and Twin Cays Ranges, Belize 415

Karen L. McKee, U.S. Geological Survey

William C. Vervaeke, U.S. Geological Survey

An Overview of Symbiont-Bleaching in the Epiphytic Foraminiferan 

Sorites dominicensis 429

Susan L. Richardson, Smithsonian Marine Station at Fort Pierce

New Perspectives on Ecological Mechanisms Affecting Coral 

Recruitment on Reefs 437

Raphael Ritson-Williams, Smithsonian Marine Station 

at Fort Pierce

Suzanne N. Arnold, University of Maine

Nicole D. Fogarty, Florida State University

Robert S. Steneck, University of Maine

Mark J. A. Vermeij, CARMABI

Valerie J. Paul, Smithsonian Marine Station at Fort Pierce

00_FM_i-xii_Lang.indd vii 0_FM_i-xii_Lang.indd vii 9/24/09 9:20/24/09 9:20
viii • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Do Indian River Lagoon Wetland Impoundments (Eastern Florida) 

Negatively Impact Fiddler Crab (Genus Uca) Populations? 459

Bjorn G. Tunberg, Smithsonian Marine Station at Fort Pierce

Dynamic Hydrology of a Mangrove Island: Twin Cays, Belize 473

Daniel W. Urish, University of Rhode Island

Raymond M. Wright, University of Rhode Island

Ilka C. Feller, Smithsonian Environmental Research Center

Wilfrid Rodriguez, University of Rhode Island

Ecological Characteristics of Batis maritima in Florida and Belize 491

Dennis F. Whigham, Smithsonian Environmental Research Center

Michael C. Whigham, University of New Hampshire

Ilka C. Feller, Smithsonian Environmental Research Center

Wilfrid Rodriguez, University of Rhode Island

Ryan S. King, Baylor University

Sponge Community Dynamics on Caribbean Mangrove Roots: 

Signifi cance of Species Idiosyncrasies 501

Janie L. Wulff, Florida State University

INDEX 515

00_FM_i-xii_Lang.indd viii 0_FM_i-xii_Lang.indd viii 9/24/09 9:20/24/09 9:20
Foreword

Nearly two-thirds of Earth’s surface is covered by the ocean, a global 

system essential to all life. Impacts on one part of the ocean can have 

worldwide effects. The ocean moderates our climate, provides valuable resources, and produces at least half the oxygen we breathe: it 

makes our planet livable. We know little, however, about the physical, chemical, 

geological, and biological aspects of this crucial life support system.

The Smithsonian Institution, in efforts to increase knowledge about the 

ocean, has established a network of marine laboratories that monitors coastal 

habitats along a latitudinal gradient from the Chesapeake Bay through the 

Indian River Lagoon to the Mesoamerican barrier reef and on both sides of 

the Isthmus of Panama. The maintenance of long-term research projects and 

environmental monitoring is crucial to understanding changes that exceed in 

time the professional career of any given scientist. The information gained from 

such studies at stable sites enables scientists to differentiate between long-term 

changes and local or short-term environmental variations. Results contribute 

to our knowledge of systematics and ecology, physiology, behavioral sciences, 

geology, and paleoecology.

Our marine science universe comprises Smithsonian staff scientists and external collaborators and encourages the next generation of scientists, graduate 

students, and fellows. This symposium presents a Smithsonian-wide sample of 

marine science results.

Ira Rubinoff

Smithsonian Institution

Acting Under Secretary for Science, 2007– 2008

00_FM_i-xii_Lang.indd ix 0_FM_i-xii_Lang.indd ix 9/24/09 9:20/24/09 9:20
00_FM_i-xii_Lang.indd x 0_FM_i-xii_Lang.indd x 9/24/09 9:20

/24/09 9:20
Executive Summary

The results of the Smithsonian Marine Science Symposium, convened by 

the Marine Science Network on 15– 16 November 2007 in Washington, 

D.C., are reported in 39 papers in this volume. These proceedings cover 

a wide range of marine research studies that demonstrate the breadth 

and diversity of science initiatives supported by the Smithsonian Marine Science 

Network. The fi rst section treats an overview of the Smithsonian Marine Science 

Network established in 1998, and a brief background and history of multidisciplinary investigations spanning more than 37 years for each of the four marine 

facilities that constitute the Network: the Smithsonian Environmental Research 

Center at the Chesapeake Bay, Maryland; the National Museum of Natural History’s Smithsonian Marine Station at Fort Pierce, Florida; the Caribbean Coral 

Reef Ecosystems Program, with its Carrie Bow Marine Field Station in Belize; and 

the Smithsonian Tropical Research Institute in Panama. Subsequent papers in this 

volume represent fi ndings by Smithsonian scholars and their collaborators on overarching topics of marine biodiversity, evolution, and speciation; biogeography, invasive species, and marine conservation; and forces of ecological change in marine 

systems. The volume includes contributions on historical and geological aspects of 

coral reef and mangrove development; on biodiversity, developmental biology, and 

evolution (including molecular genetics) of sponges, cnidarians, sipunculan worms, 

crustaceans, and fi shes; on ecology and population dynamics of algae, sponges, 

bryozoans, zooplankton, and miscellaneous invasive species; on environmental parameters, including pollutants, oceanographic factors, and hydrological regimes, 

and their effects on primary and secondary productivity, bleaching of symbiotic foraminiferans, benthic community structure, herbivory, development of toxic algal 

blooms, and land– sea connectivity in coastal habitats, that is, temperate bays and 

lagoons and tropical reefs and mangroves; and on conservation and education initiatives encompassing a range of organisms from sponges and corals to sea turtles, 

as well as communities such as tidal marshes, mangrove swamps, and coral reefs. 

As we prepare to face the challenges of rapidly accelerating biodiversity loss and 

global environmental stresses, particularly in highly vulnerable tropical shallowwater ecosystems such as reefs and mangroves, the focus of our scientifi c expertise 

on the member laboratories of the Marine Science Network has, during decades 

of documentation, established ecological standards that will help us monitor and 

evaluate future changes or trends and contribute to forthcoming education and 

conservation initiatives.

Michael A. Lang

Smithsonian Institution

Offi ce of the Under Secretary for Science

April 2009

00_FM_i-xii_Lang.indd xi 0_FM_i-xii_Lang.indd xi 9/24/09 9:20/24/09 9:20
00_FM_i-xii_Lang.indd xii 0_FM_i-xii_Lang.indd xii 9/24/09 9:20

/24/09 9:20
Introduction to the Smithsonian 

Marine Science Network

Michael A. Lang

ABSTRACT. The “Smithsonian Marine Science Symposium” contained more than 70 

oral and poster presentations by Smithsonian scholars and collaborators and represented 

the fi rst major dissemination of marine research results since the establishment of the 

Marine Science Network (MSN) in 1998. The MSN operates a unique array of laboratories and research vessels that spans the latitudinal gradient of the western Atlantic 

(Chesapeake Bay, Indian River Lagoon, Mesoamerican Barrier Reef, and Panamanian 

Coast) and crosses the isthmus of Panama. The Network is dedicated to understanding 

the rich biodiversity and complex ecosystem dynamics that sustain coastal processes and 

productivity. We study evolutionary, ecological, and environmental change in the ocean’s 

coastal zones, increasing scientifi c knowledge of these environments and improving society’s appreciation of the ocean’s effect on our lives. Coastal environments are of immense 

economic and environmental importance and comprise 95% of the ocean’s fi sheries. Our 

coasts are the most densely populated and fastest growing communities in the USA. The 

MSN ensures integrated support of “Discovering and Understanding Life’s Diversity,” a 

core Smithsonian scientifi c mission. The MSN’s goals are to ensure that the whole of the 

integrated Network is larger than the sum of its parts, leading to enhanced productivity 

through collaborative and comparative research, marine infrastructure development and 

support, professional training and outreach, and effective allocation of resources.

INTRODUCTION

The “Smithsonian Marine Science Symposium” was held 15– 16 November 2007 to celebrate individual and long-term pan-institutional marine research, with a particular focus on highlights of the fi rst ten years since the 

establishment of the Marine Science Network (MSN) in 1998. The symposium 

was convened by the Offi ce of the Under Secretary for Science and represented 

the fi rst gathering, of this magnitude, of Smithsonian marine scientists. The 

symposium presented marine research fi ndings by Smithsonian scholars and 

their collaborators with emphasis on marine biodiversity, evolution, and speciation; biogeography, invasive species, and marine conservation, including 

life histories and microbial and behavioral ecology; and forces of ecological 

change in marine systems. The symposium carried on a tradition of Smithsonian marine science that began nearly 150 years ago and resulted in some of the 

world’s foremost collections of marine specimens. More than 70 presentations 

Michael A. Lang, Smithsonian Institution, Offi ce of the Under Secretary for Science, P.O. Box 

37012, MRC-009, Washington, D.C. 20013-

7012, USA (langm@si.edu). Manuscript received 

10 April 2009; accepted 20 April 2009.

01_Intro_001-010_Lang.indd 1 1_Intro_001-010_Lang.indd 1 9/24/09 9:30/24/09 9:30
and posters discussed results of marine research from the 

Chesapeake Bay, Indian River Lagoon and Florida Keys, 

the Mesoamerican Barrier Reef in Belize, the Atlantic 

and Pacifi c Coasts of the Isthmus of Panama, and other 

international research sites. Thirty-nine papers from this 

symposium are presented in this 38th volume of Smithsonian Contributions to the Marine Sciences, and additional marine education posters reside on http://www

.si.edu/marinescience. Smithsonian speakers included marine research leaders, collaborators, and fellows from the 

Smithsonian Environmental Research Center, National 

Zoological Park, National Museum of Natural History, 

Smithsonian Marine Station at Fort Pierce, Caribbean 

Coral Reef Ecosystems Program, Smithsonian Tropical 

Research Institute, and the Offi ce of the Under Secretary 

for Science.

The Smithsonian Institution operates a unique network of coastal laboratories and long-term research sites 

on the east coast of North and Central America that extends along the western Atlantic Ocean and bridges the 

Panamanian isthmus from the Caribbean Sea to the Pacifi c 

Ocean (Figure 1). Scientifi c diving supports a signifi cant 

amount of Smithsonian marine research throughout the 

Network and internationally (Lang and Baldwin, 1996; 

Lang, 2007).

The Marine Science Network concept was developed 

in 1998 from the bottom up and has achieved the following important milestones:

1998: Formalization of a pan-institutional Smithsonian 

Marine Science Network initiated at two-day inaugural workshop at Smithsonian Environmental 

Research Center, with more than 50 Smithsonian 

Institution participants.

1999: Dedication of new Carrie Bow Cay Marine Field 

Station.

1999: Dedication of new Smithsonian Marine Station at 

Fort Pierce.

2000: MSN concept and infrastructure allocations approved by the Under Secretary for Science.

2001: Launch of the MSN website

www.si.edu/marinescience.

2001: Annual MSN Calls for Proposals for infrastructure, 

marine research awards, and postdoctoral fellowships.

2003: Dedication of Bocas del Toro Marine Laboratory.

2006: Science Executive Committee review of Smithsonian marine science, including MSN.

2007: Formulation of Big Questions in Marine Science:

 1. What are the major spatial and temporal 

patterns in distribution of biodiversity?

 2. How does biodiversity, and the loss of biodiversity, affect the functioning of ecosystems?

 3. How are humans changing the magnitude 

and distribution of biodiversity and what 

are the patterns and consequences?

2007: Smithsonian Marine Science Symposium.

The MSN is administered as a pan-institutional program through the Offi ce of the Under Secretary for Science. It is governed by a seven-member Steering Committee 

composed of Michael Lang (Offi ce of the Under Secretaray for Science), Anson Hines (Smithsonian Environmental Research Center), Eldredge Bermingham (Smithsonian 

Tropical Research Institute), Klaus Ruetzler (National 

Museum of Natural History), Robert Fleischer (National 

Zoological Park), Valerie Paul (Smithsonian Marine Station at Fort Pierce), and Phillip Taylor (National Science 

Foundation). Additional Smithsonian scientists participate by invitation in MSN research proposals and postdoctoral fellowship review panels, MSN symposia and 

workshop committees, and special projects. Support for 

MSN infrastructure, research, and postdoctoral fellowships is provided by the Offi ce of the Under Secretary 

for Science’s Johnson and Hunterdon Oceanographic Research Endowments.

There are four main unifying disciplinary themes to 

Smithsonian marine research: systematics, evolutionary 

biology, ecology, and geology. Biogeography is a key research element, linking systematics, ecology, and evolutionary biology. Mechanisms of biogeographic isolation 

are central elements in evolutionary theory, population 

dynamics, conservation biology, and patterns of biodiversity. Biogeographic patterns are crucial data in the determination of introduced and native species. Site-specifi c, 

long-term measurements of environmental variables allow 

for analysis of change over multiple time scales, which 

is necessary to detect patterns in typically complex ecological data. The Smithsonian Marine Science Network 

is uniquely positioned to monitor long-term change at its 

component sites. It has an extensive array of programs 

that address many of the most pressing environmental issues in marine ecosystems, including biological invasions, 

eutrophication, harmful species and parasites, plankton 

blooms and red tides, linkages among coastal ecosystems, 

global warming including sea-level rise, El Niño/La Niña 

effects, UV radiation impacts, habitat destruction, fi sheries impacts, ecology of key habitats (estuaries, coral 

reefs, mangroves, seagrasses, wetlands), and biodiversity 

inventories.

The Smithsonian’s marine education programs consist of public outreach and professional training. A series 

2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

01_Intro_001-010_Lang.indd 2 1_Intro_001-010_Lang.indd 2 9/24/09 9:30/24/09 9:30
FIGURE 1. Map showing locations of the Smithsonian Marine Science Network members.

NUMBER 38 • 3

01_Intro_001-010_Lang.indd 3 1_Intro_001-010_Lang.indd 3 9/24/09 9:30/24/09 9:30
4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of these activities are aimed at promoting awareness and 

conservation of marine environments and at communicating the Smithsonian’s research fi ndings to the general 

public. By integrating research with education, the Smithsonian produces tomorrow’s discoverers while pursuing 

today’s discoveries. The public is engaged with interactive exhibits and scientists (e.g., the National Museum of 

Natural History’s Sant Ocean Hall), symposia, popular 

books, lectures, and fi lms about the marine environment. 

The Smithsonian Marine Science Network contributes 

to the public interest by disseminating novel environmental information around the globe. Its research helps 

build a solid foundation for informed decisions about 

environmental policy, natural resource management, and 

conservation.

Other recent coordinated Smithsonian marine science efforts of note are marine-terrestrial fl ora and fauna 

of Cayos Cochinos Archipelago, Honduras (Guzman, 

1998), natural history of the Pelican Cays (Macintyre and 

Rütz ler, 2000), the Twin Cays mangrove ecosystem, Belize (Macintyre et al., 2004), and investigations of the marine fauna and environments of Bocas del Toro, Panama 

(Collin, 2005). Smithsonian taxonomic fi eld guides and 

keys of algae, invertebrates, and fi shes (Littler and Littler, 

2000; Collin et al., 2005; Robertson, 2009) are valuable 

tools for biologists, divers, and fi shermen alike.

MARINE SCIENCE NETWORK MISSION AND VISION

The MSN mission is dedicated to understanding the 

rich biodiversity and complex ecosystem dynamics that 

sustain coastal processes and productivity, and its vision 

is “to increase scientifi c knowledge of marine coastal environments and to improve society’s appreciation of the 

ocean’s effect on our lives.”

MARINE SCIENCE NETWORK GOALS

The MSN provides integrated support of “Discovering and Understanding Life’s Diversity,” a core scientifi c 

mission of the 2005– 2010 Smithsonian Science Strategic Plan. The MSN ensures that the whole of the integrated Network is greater than the sum of its parts, leading to enhanced productivity through collaborative and 

comparative research facilitated by increased inter-unit 

coordination, marine infrastructure development and 

support, professional training and outreach, effective allocation of research funding, and transparent management, participation, and support for Smithsonian marine 

scientists through availability of shared resources and 

facility access.

SMITHSONIAN ENVIRONMENTAL 

RESEARCH CENTER (CHESAPEAKE BAY)

The Smithsonian Environmental Research Center 

(SERC) advances stewardship of the biosphere through 

interdisciplinary research and education. With a resident 

staff of more than 100 scientists, technicians, fellows, and 

students, SERC has experienced signifi cant growth in the 

last few years. The SERC laboratories, educational facilities, and primary fi eld sites are located 25 miles east of 

Washington, D.C., on the western shore of Chesapeake 

Bay. Its campus includes a growing complex of offi ces, 

laboratories, maintenance shops, a library, housing, and 

facilities for public programs. A dock, fl eet of research 

vessels, dive locker, wet laboratory, aquarium room, and 

large fi sh-weir are used in support of estuarine research.

The greatest resource at SERC is its main research site 

on the Rhode River subestuary, which includes more than 

1,072 ha of land and 26 km of undeveloped shoreline of 

the Chesapeake Bay. Since 1965, SERC’s long-term studies have focused on the interactions among ecosystems in 

complex landscapes, tidal marshes, and estuaries. With 

the Rhode River site as its hub, SERC research radiates to 

sites around the world to address effects of global change, 

landscape ecology, coastal ecosystems, and population 

and community ecology. Much of SERC’s comparative 

research across latitudes extends to the other sites of the 

MSN and includes studies of mangrove biocomplexity, invasive and native species biodiversity, estuarine food webs, 

land use impacts linked to water quality, carbon processing and global change, nutrient loading and low dissolved 

oxygen, ecosystem management of fi sheries and crucial 

habitats, and life history patterns and evolution. Research 

at SERC focuses on fi ve grand environmental challenges 

(Hines, 2009): (1) impacts of atmospheric change on climate, sea level, ultraviolet radiation, pollutant deposition, 

and carbon balance; (2) impacts of watershed nutrient discharges causing harmful algal blooms, depletion of oxygen, and destruction of submerged vegetation; (3) food 

web disruption by pollution and overfi shing; (4) invasive 

species; and (5) landscape disturbance by agriculture and 

development.

Goals of SERC in marine education include professional training (interns, graduate students, postdoctoral 

fellows, and visiting scientists), teacher training, site visits 

and public programs, and distance learning.

01_Intro_001-010_Lang.indd 4 1_Intro_001-010_Lang.indd 4 9/24/09 9:30/24/09 9:30
NUMBER 38 • 5

NATIONAL ZOOLOGICAL PARK 

(WASHINGTON, D.C.)

The Smithsonian’s National Zoological Park (NZP) 

was founded in 1889. Its mission is to provide leadership 

in animal care, science, education, and sustainability. Approximately 2,000 individuals of 400 different species 

constitute its animal collection. The NZP consists of a 163 

acre urban park located in Rock Creek Park in northwest 

Washington, D.C., and the 3,200 acre Conservation and 

Research Center in Front Royal, Virginia, emphasizing reproductive physiology, analysis of habitat and species relationships, and the training of conservation scientists.

The National Zoological Park conducts international 

marine research on sea turtles and sea birds, ecology of 

bottlenose dolphins, Weddell seal lactation, life history 

and reproductive strategies of gray and harbor seals, nutritional ecology of sea otters, and cryopreservation of endangered coral species. Marine exhibits include the Seal 

and Sea Lion Pool and the Invertebrate Exhibit, which 

opened in 1987, where marine invertebrates comprise 

75% of its live collections on display. The NZP’s tools 

to inspire, train, and empower successive generations to 

care for the world’s biological diversity are its exhibits, 

science, outreach, and education programs. Ultimately, 

efforts must be oriented toward protecting wildlife and 

other forms of biological diversity so that we, and future 

societies, continue to enjoy the incalculable benefi ts of our 

natural world.

NATIONAL MUSEUM OF NATURAL HISTORY 

(WASHINGTON, D.C.)

The National Museum of Natural History (NMNH) 

has a distinguished history of more than 150 years of sampling and collections-based research. Major collections 

represent algae and dinofl agellates, foraminifera, sponges, 

cnidarians, ctenophores, worms, crustaceans, mollusks, 

bryozoans, echinoderms, tunicates, fi shes, marine reptiles, birds, and mammals), now numbering more than 

33,000,000 specimens of plants and animals. Of approximately 2,415 families of marine invertebrates, nearly 67% 

are represented in the NMNH invertebrate collection, 

which is not limited solely to the diversity-rich tropics. 

The NMNH provides professional collection management 

services to the National Science Foundation United States 

Antarctic Program (USAP) and the international scientifi c 

community. A primary focus of this project is improving 

access to the collections through its cataloging (inventory) 

program (more than 900,000 USAP specimens) and loan 

program. More than 170,000 USAP specimens in 138 

separate transactions were either lent or returned from 

loan between 1995 and the end of 2004, supporting the 

research efforts of scientists in 22 countries. Several hundred lots of archive samples from the Palmer Long-Term 

Ecological Research Program were also accessioned (Lemaitre et al., 2009).

The focus of marine science at NMNH addresses the 

diversity of marine life, where species occur, how they are 

related to each other, how marine diversity developed and 

how it is maintained, what are the human impacts on marine life, and how marine life-forms are used by people.

The Museum administers the Laboratories of Analytical Biology for state-of-the art molecular work and two 

marine fi eld stations (Carrie Bow Cay, Belize, and Smithsonian Marine Station at Fort Pierce, Florida), member 

facilities of the MSN. Since 1966 the Museum has funded 

the Atoll Research Bulletin, which publishes research reports on the geology and ecology of islands and their adjacent coral reef and mangrove communities in tropical sites 

around the world.

The NMNH Ocean Initiative comprises the Sant 

Ocean Hall, the Ocean Web Portal, the Sant Chair in 

Marine Science, and interdisciplinary marine research at 

NMNH. Virtual access to the Museum’s key marine collections is being created. The Initiative aims to train future 

generations of marine scientists and educate the public 

about, and raise awareness of, the importance of the ocean 

as a global system.

SMITHSONIAN MARINE STATION 

AT FORT PIERCE (FLORIDA)

The Smithsonian Institution has had a presence in Fort 

Pierce, Florida, since 1969 and was known then as the 

Fort Pierce Bureau. From 1969 to 1981, the Fort Pierce 

Bureau carried out studies including underwater oceanography with research submersibles, a survey of the Indian 

River Lagoon, coral reef research, and research on life 

histories of marine invertebrates, partly in collaboration 

with the newly formed Harbor Branch Foundation (now 

the Harbor Branch Oceanographic Institution at Florida 

Atlantic University). In 1981, the Fort Pierce Bureau was 

dissolved, and in its place the Smithsonian Marine Station 

at Link Port was formally recognized as an organizational 

unit under the auspices of the National Museum of Natural History. The Station took over the barge, acquired originally by the Smithsonian in 1973 from federal surplus, that 

01_Intro_001-010_Lang.indd 5 1_Intro_001-010_Lang.indd 5 9/24/09 9:30/24/09 9:30
6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

was docked at the Harbor Branch campus. In 1996, the 

Smithsonian purchased, from the MacArthur Foundation, 

8 acres of property 7 miles south near the Fort Pierce Inlet 

with easement access to the Indian River Lagoon. St. Lucie 

County enacted a 25 year lease of a county dock and adjacent land at a site on the inlet across from the Station, whose 

main building was completed and dedicated in 1999.

The Smithsonian Marine Station at Fort Pierce 

(SMSFP) is a marine science research center located on the 

Indian River Lagoon along 156 miles of Florida’s central 

Atlantic coast. The Indian River Lagoon is a long, narrow, and shallow estuary adjacent to the Atlantic Ocean, 

separated by a strip of barrier islands. Biologists at SMSFP 

have the advantage of working just 20 miles from the Florida current, a stream of warm water from the Caribbean 

that moves northward past Florida’s coastline as part of 

the larger, complex system of currents known as the Gulf 

Stream. The current carries with it many tropical marine 

organisms, allowing researchers to work at the interface of 

the Northern Hemisphere’s tropical and temperate regions. 

Situated in a biogeographic transitional zone between the 

temperate and subtropical provinces, the SMSFP facility 

provides access to an extraordinary diversity of marine 

and estuarine species and to a variety of habitats, which 

include mangroves, salt marshes and sandy beaches, rocky 

intertidal substrates, seagrass beds, mud and sand fl ats, 

coral reefs, worm reefs, Coquina hard bottoms, deep coral 

rubble zones, shallow- to deep-water sandy plains, and the 

blue waters of the Gulf Stream.

The Marine Station supports and conducts scholarly 

research in the marine sciences, emphasizing studies of 

biodiversity, life histories, and ecology of marine organisms (Paul et al., 2009). The results of this research enable 

policy makers to make informed environmental decisions 

in guiding conservation and sustainable management of 

marine resources, as well as providing the basis for innovative applications in medicine, aquaculture, and the effective balance between development and conservation. 

For Smithsonian scientists, the SMSFP provides an important link with other MSN facilities in the tropics at the 

Smithsonian Tropical Research Institute (STRI) in Panama 

and Carrie Bow Cay in Belize and in the temperate region, 

the Smithsonian Environmental Research Center on the 

Chesapeake Bay.

The facilities at the Smithsonian Marine Station 

at Fort Pierce include an 8,000 square foot facility that 

houses a histology laboratory, an electron microscopy 

lab, a confocal microscope, a combination electrophoresis/DNA/chemistry laboratory, a photographic darkroom, 

fl ow-through seawater tables and aquaria, an industrial 

shop, and offi ces and laboratories for visiting scientists 

and fellowship recipients. The 39-foot R/V Sunburst and 

two smaller vessels are used for scientifi c diving, dredging, and trawling in the Indian River Lagoon, Continental 

Shelf, and Gulf Stream.

The Marine Station’s educational efforts include postdoctoral fellows and interns, public events and lectures, 

school programs and public tours, a web site, the Indian 

River Lagoon Species Inventory, and the Marine Ecosystems 

Exhibit, which was established in 2001 with the following 

ecosystems on display: coral reef, seagrass, mangrove, hardbottom and nearshore habitats, and Oculina reef).

CARIBBEAN CORAL REEF ECOSYSTEMS 

PROGRAM (CARRIE BOW CAY, BELIZE)

Coral reefs are unique biogeological structures that 

thrive in clear, nutrient-poor (oligotrophic) tropical oceans 

and support a rich and diverse biological community. Reef 

systems are driven by the symbiosis between scleractinian 

corals and microscopic dinofl agellate algae (zooxanthellae) 

as their chief energy source. The largest, best developed, least 

polluted, and least commercially exploited coral reef in the 

Atlantic region is the Mesoamerican Barrier Reef in Belize. It 

is a complex of reefs, atolls, islands, oceanic mangroves, and 

seagrass meadows that extends over 160 km. For its unique 

characteristics and unperturbed condition, the Belize barrier 

reef has been declared a World Heritage Site.

In the early 1970s, Rützler et al. (2009) discovered 

the formidable qualities of the Belize (then British Honduras) barrier reef. After careful comparison with other 

locations in the western Caribbean, it was chosen as the 

site of an interdisciplinary long-term study of systematics, 

ecology, behavior, and evolution of reef organisms and the 

dynamics and historical development of reef communities (Rütz ler and Macintyre, 1982). Carrie Bow Cay, only 

three hours by plane and boat from Miami, was found to 

be the ideal logistical base because of its location on top of 

the barrier reef, only meters away from a variety of habitat types (reef fl at, spur and groove, deep fore-reef slope, 

patch reefs, seagrass meadows, and mangroves), and its 

undisputed ownership by a Belizean family able to cater to 

all Smithsonian needs for lodging, food, local transportation, and contacts with government.

In 1985, as part of the U.S. Congress Caribbean Basin Initiative, the National Museum of Natural History 

received an increase to its budget base to continue and 

intensify study of Caribbean coral reef ecosystems. These 

funds allowed for the expansion of research facilities on 

01_Intro_001-010_Lang.indd 6 1_Intro_001-010_Lang.indd 6 9/24/09 9:30/24/09 9:30
NUMBER 38 • 7

Carrie Bow Cay and the update of CCRE equipment. In 

the years since, CCRE has accomplished the following: 

amassed thousands of specimens of marine plants, invertebrates, and fi shes, which are organized in an enormous 

database; assisted the government of Belize in shaping and 

justifying its coastal conservation policy; participated continuously in the Caribbean-wide reef monitoring network 

(CARICOMP); established the fi rst meteorological oceanographic monitoring station in coastal Belize; and, above 

all, published well over 850 scientifi c papers in reviewed 

journals, as well as several books, doctoral dissertations, 

popular articles, and photo and video documentaries. Between 60 and 80 scientists use Carrie Bow Cay each year 

as a part of ongoing CCRE research.

The Carrie Bow Cay Laboratory serves primarily in 

support of SI marine scientists’ research projects and their 

external collaborators. Seasonal hurricanes during the 

past 35 years could not destroy Carrie Bow Cay facilities 

to the extent that a devastating fi re did in December 1997. 

Improved facilities now include dry and wet labs, housing, 

generator, compressor, small boats and scuba cylinders, 

and essential facilities such as solar power, a runningseawater system, and weather station.

CCRE’s educational and outreach programs include 

its Belize teachers’ mangrove workshops, publications, 

symposia, advisory consults with Belizean Ministries, and 

fellows and interns.

SMITHSONIAN TROPICAL RESEARCH 

INSTITUTE (REPUBLIC OF PANAMA)

The Smithsonian Tropical Research Institute’s (STRI) 

marine research program in the Republic of Panama dates 

to 1964 when small laboratories were established on the 

Pacifi c and Caribbean coasts within the former Canal 

Zone. Today, STRI operates marine stations at Bocas del 

Toro and Galeta Point in the Caribbean and the Naos marine laboratory complex in the Pacifi c. Until 2008, the R/V 

Urraca, a 96 foot nearshore coastal oceanographic vessel, was outfi tted with remotely operated vehicle, scientifi c 

diving, and dredging capabilities, and was operated under 

University National Oceanographic Laboratory System 

(UNOLS) research fl eet standards.

At the Panama Canal, the Isthmus of Panama narrows 

to less than 100 km, separating oceans that are very different tropical marine ecosystems. The Caribbean is a relatively stable ocean, with small fl uctuations in temperature 

and relatively low tidal variation. Its transparent, nutrientpoor waters are ideal for the growth of reefs, and it ranks 

just behind the Indian Ocean and the Indo-West Pacifi c in 

terms of numbers of marine species. The tropical eastern 

Pacifi c, in contrast, exhibits much greater fl uctuations in 

tides and temperature, with seasonal upwelling locally and 

longer-term variation resulting from the El Niño southern oscillation cycle. Its more nutrient-rich waters support 

commercial fi sheries of major importance. The creation of 

these two distinct marine realms by the rise of the Isthmus 

of Panama during the past 10 million years also contributed to the formation of the modern biological and geological world. During this interval, the Gulf Stream was 

established, the mammals of North America conquered a 

newly connected South America, the Ice Ages began, and 

modern man arose. The Isthmus played a major role in 

this history, and set in motion a fascinating natural experiment, as the animals and plants of the two oceans went 

their separate evolutionary ways.

There are also major differences within each ocean. 

In the Pacifi c, seasonal upwelling of nutrient-rich waters is strong in the Gulf of Panama, where trade winds 

blow freely across the Isthmus, but absent in the Gulf of 

Chiriqui, where the high terrain blocks these winds. The 

more stable conditions in the Gulf of Chiriqui support the 

best developed coral reefs in the tropical eastern Pacifi c. 

On the Caribbean side, the San Blas Archipelago is bathed 

in clear oceanic waters, whereas the reefs and mangroves 

of the enormous Chiriqui Lagoon of Bocas del Toro are 

enriched by runoff from the land. Thus, Panama can be 

considered a nation of four ocean types, providing unique 

opportunities for understanding how and why marine ecosystems function as they do.

Understanding the history and ecology of Panama’s 

diverse marine environments has been a major theme of 

STRI’s research over the past four decades (Robertson et 

al., 2009). Major programs include between-ocean comparisons of physical and biological oceanography, geological reconstruction of events leading up to and following 

the rise of the Isthmus, studies of marine biodiversity, and 

analyses of the vulnerability of marine habitats to natural 

and anthropogenic change. In celebration of STRI’s role in 

coral reef research, the Smithsonian’s 150th anniversary, 

and the International Year of the Reef, the Smithsonian 

hosted the Eighth International Coral Reef Symposium 

in Panama in 1996. This meeting brought 1,500 reef scientists and managers to Panama from around the world 

and resulted in the publication of a two-volume proceedings (Lessios and Macintyre, 1997) and an international 

traveling exhibit that has already brought STRI’s marine 

discoveries to Miami, the District of Columbia, Honduras, 

and Jamaica.

01_Intro_001-010_Lang.indd 7 1_Intro_001-010_Lang.indd 7 9/24/09 9:30/24/09 9:30
8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

The Marine Environmental Sciences Program (MESP) 

at STRI collects and analyzes fundamental oceanographic 

information that provides critical information for studies 

such as El Niño and coral bleaching. The Panama Paleontology Project in Bocas del Toro seeks to record the history 

of the divergence between the two oceans over the past 

10 million years and the evolutionary response of marine 

organisms to these changes. Results from this project are 

the geological reconstruction of the closure of the Isthmus of Panama 3 million years ago and the discovery of a 

major extinction event in the Caribbean about 2 million 

years ago. Through a combination of molecular and paleontological information, STRI’s molecular evolution program has developed a model system for determining the 

rate at which organisms diverge genetically through time 

(Panama molecular clock). This achievement allows for 

the phylogenetic reconstruction of marine life elsewhere 

in the world.

Educational programs within STRI include a marine 

fellowship program, school group visits (Culebra Nature 

Center, Galeta Point Marine Lab, Bocas del Toro Lab), 

public seminars, advisory consults with the Panamanian 

government, and graduate courses.

CONCLUSION

The Smithsonian Institution is unique among federal 

agencies, research organizations, and universities with its 

investment in comprehensive, long-term marine studies 

of crucial ecosystems at a latitudinal gradient of stable 

sites. Thousands of marine science publications provide 

results and data for synthesis and a new baseline for modeling and forecasting. Continued opportunities remain for 

many important marine organisms to be identifi ed by conventional and molecular techniques and described. Deep 

reefs are becoming increasingly important as a focal area 

to understand how the reef system in toto functions and to 

quantify their physical, chemical, and biological contributions to the shallow reefs that we have studied for more 

than three decades (Lang and Smith, 2006). Life histories 

require further analysis to aid ecological understanding 

and fi sheries management. Thirty-fi ve-year multidisciplinary databases allow for early detection and evaluation 

of community changes, invertebrate diseases, invasive species, and recruitment caused by environmental degradation and catastrophic events.

The MSN continues to provide support for individual 

and pan-institutional collaborative research, postdoctoral 

marine science fellows, marine science staff and infrastructure support, marine outreach and education, and 

workshops and symposia: for example, Bocas del Toro 

taxonomy; coral reef management; mangrove ecology of 

Twin Cays, Belize; marine genetics; sea turtle conservation and population management; seagrass and mangrove 

ecosystems; neogastropod evolution; marine invasives of 

the Gulf of Mexico; and marine invasive species across 

latitudinal gradients. Outcomes of the integration of the 

Smithsonian marine facilities and programs since 1998 are 

the facilitated freedom of movement of scientists between 

units and the increased collaborations and co-authored 

publications. The MSN was highlighted as a model for 

pan-institutional Smithsonian programs by the Smithsonian Science Commission in 2003. The most likely keys to 

its success were the bottom-up development of the Network concept, starting with the Institution’s staff scientists, and the availability of research funding through the 

Offi ce of the Under Secretary for Science to enable marine 

research and postdoctoral fellowships.

The Smithsonian Marine Science Network and the 

Smithsonian Scientifi c Diving Program provide the facilities and support for the effi cient conduct of marine research. The primary objective of the marine research effort 

is the advancement of science. The deliverable is mainly in 

the form of peer-reviewed publications for dissemination 

throughout the scientifi c community and to the public.

The importance of the MSN is its contribution to the 

knowledge of complex ecosystems including seagrasses, 

mangrove islands, bays, estuaries, and coral reefs, and the 

preservation of these precious resources by learning about 

their rich biodiversity, function, and interconnectedness. 

Only a long-term commitment will allow us to understand 

the dynamics of coastal processes and organisms, obtain the 

cooperation of the public, and educate a new generation.

ACKNOWLEDGMENTS

Support for the Smithsonian Marine Science Network 

is provided by the Hunterdon and Johnson Oceanographic 

Research Endowments in the Offi ce of the Under Secretary 

for Science. I wish to extend appreciation to the Marine 

Science Symposium Committee: Biff Bermingham, Tuck 

Hines, Ian Macintyre, Olav Oftedal, Valerie Paul, Klaus 

Rützler, and Phil Taylor; and to Session Co-Chairs: Carole 

Baldwin, Allen Collins, Candy Feller, Ian Macintyre, Jon 

Norenburg, Valerie Paul, and Mark Torchin. I thank Ira 

Rubinoff for his long-term support of the Scientifi c Diving Program and MSN. Editorial collaboration with Ian 

Macintyre and Klaus Rützler on this volume was much 

appreciated, as was the assistance of Ginger Strader and 

01_Intro_001-010_Lang.indd 8 1_Intro_001-010_Lang.indd 8 9/24/09 9:30/24/09 9:30
NUMBER 38 • 9

her staff at the Smithsonian Institution Scholarly Press. I 

also thank the many anonymous peer reviewers. The authors’ contributions to this symposium proceedings volume highlighting the breadth and scope of Smithsonian 

marine research were invaluable.

LITERATURE CITED

Collin, R., ed. 2005. Marine Fauna and Environments of Bocas del Toro, 

Panama. Caribbean Journal of Science, 41(3):367– 707.

Collin, R., M. C. Diaz, J. L. Norenburg, R. M. Rocha, J. A. Sanchez, 

A. Schulze, M. L. Schwartz, and A. Valdes. 2005. Photographic 

Identifi cation Guide to Some Common Marine Invertebrates of 

Bocas Del Toro, Panama. Caribbean Journal of Science, 41(3):

638– 707.

Guzmán, H. M., ed. 1998. Marine– Terrestrial Flora and Fauna of Cayos 

Cochinos Archipelago, Honduras. Revista Biologia Tropical, 46(4) 

(Suppl.):1– 200.

Hines, A. H. 2009. “Land–Sea Interactions and Human Impacts in 

the Coastal Zone.” In Proceedings of the Smithsonian Marine 

Science Symposium, ed. M. A. Lang, I. G. Macintyre, and K. 

Rützler, pp. 11–23. Smithsonian Contributions to the Marine 

Sciences, No. 38. Washington, D.C.: Smithsonian Institution 

Scholarly Press.

Lang, M. A. 2007. Scientifi c Diving in the United States: The Value of 

Scuba as Research Methodology. Journal of the Society for Underwater Technology, 27(3):95– 107.

Lang, M. A., and C. C. Baldwin, eds. 1996. Methods and Techniques 

of Underwater Research. Proceedings of the American Academy 

of Underwater Sciences Scientifi c Diving Symposium. Washington, 

D.C.: Smithsonian Institution.

Lang, M. A., and N. E. Smith, eds. 2006. Proceedings of the “Advanced 

Scientifi c Diving Workshop,” February 23– 24, 2006. Washington, 

D.C.: Smithsonian Institution.

Lemaitre, R., M. G. Harasewych, and J. Hammock, eds. 2009. ANTIZ v 

1.0: A Database of Antarctic and Subantarctic Marine Invertebrates. 

National Museum of Natural History, Smithsonian Institution. 

World Wide Web electronic publication. URL http://invertebrates

.si.edu/ANTIZ.

Lessios, H. A., and I. G. Macintyre, eds. 1997. Proceedings of the 8th 

International Coral Reef Symposium, Volumes 1 and 2. Smithsonian Tropical Research Institute, Republic of Panama.

Littler, D. S., and M. M. Littler. 2000. Caribbean Reef Plants: An Identifi -

cation Guide to the Reef Plants of the Caribbean, Bahamas, Florida 

and Gulf of Mexico. Offshore Graphics, Inc., Washington, D.C.

Macintyre, I. G., and K. Rützler, eds. 2000. Natural History of the Pelican Cays, Belize. Atoll Research Bulletin, Nos. 466-480:1– 333. 

Washington, D.C.: Smithsonian Institution.

Macintyre, I. G., K. Rützler, and I. C. Feller, eds. 2004. The Twin Cays 

Mangrove Ecosystem, Belize: Biodiversity, Geological History, and 

Two Decades of Change. Atoll Research Bulletin, Nos. 509-530. 

Washington, D.C.: Smithsonian Institution.

Paul, V. J., J. Piraino, and L. Diederick. 2009. “Smithsonian Marine Station at Fort Pierce: Thirty-Seven Years of Research on the Marine 

Biodiversity of Florida.” In Proceedings of the Smithsonian Marine Science Symposium, ed. M. A. Lang, I. G. Macintyre, and 

K. Rützler, pp. 25–41. Smithsonian Contributions to the Marine 

Sciences, No. 38. Washington, D.C.: Smithsonian Institution Scholarly Press.

Robertson, D. R. 2009. “Shorefi shes of the Tropical Eastern Pacifi c 

Online Information System.” In Proceedings of the Smithsonian 

Marine Science Symposium, ed. M. A. Lang, I. G. Macintyre, and 

K. Rützler, pp. 197–208. Smithsonian Contributions to the Marine 

Sciences, No. 38. Washington, D.C.: Smithsonian Institution Scholarly Press.

Robertson, D. R., J. H. Christy, R. Collin, R. G. Cooke, L. D’Croz, 

K. W. Kaufmann, S. Heckadon Moreno, J. L. Mate, A. O’Dea, and 

M. E. Torchin. 2009. “The Smithsonian Tropical Research Institute: Marine Research, Education, and Conservation in Panama.” 

In Proceedings of the Smithsonian Marine Science Symposium, ed. 

M. A. Lang, I. G. Macintyre, and K. Rützler, pp. 73–93. Smithsonian Contributions to the Marine Sciences, No. 38. Washington, 

D.C.: Smithsonian Institution Scholarly Press.

Rützler, K. 2009. “Caribbean Coral Reef Ecosystems: Thirty-fi ve Years 

of Smithsonian Marine Science in Belize.” In Proceedings of the 

Smithsonian Marine Science Symposium, ed. M. A. Lang, I. G. 

Mac intyre, and K. Rützler, pp. 43–71. Smithsonian Contributions 

to the Marine Sciences, No. 38. Washington, D.C.: Smithsonian 

Institution Scholarly Press.

Rützler, K., and I. G. Macintyre, eds. 1982. The Atlantic Barrier Reef 

Ecosystem at Carrie Bow Cay, Belize. 1: Structure and Communities. Smithsonian Contributions to the Marine Sciences, 12:1– 539. 

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/24/09 9:30
Land– Sea Interactions and Human Impacts 

in the Coastal Zone

Anson H. Hines

ABSTRACT. The Smithsonian Environmental Research Center (SERC) conducts research on land– sea interactions to understand natural processes and human impacts in 

linked ecosystems of the coastal zone. Coastal ecosystems support great biological productivity and are of immense ecological and economic importance. In addition, more 

than two-thirds of the human population resides in the coastal zone, where human 

activities cause chronic and acute disturbance of every habitat and marked degradation of ecological balance and productivity. The Chesapeake Bay and its Rhode River 

subestuary are used by SERC as model study systems to conduct long-term, intensive 

monitoring and experiments. Research at SERC focuses on fi ve grand environmental 

challenges: (I) impacts of atmospheric change on climate, sea level, ultraviolet radiation, 

pollutant deposition, and carbon balance; (II) impacts of watershed nutrient discharges 

causing harmful algal blooms, depletion of oxygen, and destruction of submerged vegetation; (III) food web disruption by pollution and overfi shing; (IV) invasive species; and 

(V) landscape disturbance by agriculture and development. Research by SERC on these 

grand challenges serves to advise policy and management from improved stewardship of 

coastal resources.

INTRODUCTION

The coastal zone is of immense economic and environmental importance. 

More than 50% of the Earth’s human population (3 billion people) resides in 

the coastal zone and relies on the goods and services of coastal ecosystems, and 

this number is expected to double by 2045 (Creel, 2003). Coastal communities 

are the most densely populated and fastest growing areas in the United States: 

14 of the nation’s largest 20 cities are in coastal locations; more than 50% of the 

U.S. population lives in 17% of the country’s land, comprising coastal counties; 

this population concentration is expected increase to 70% within 25 years; and 

23 of the 25 most densely populated counties encompass coastal cities and their 

surrounding sprawl (Crossett et al., 2004). The coastal environment includes the 

Earth’s most biologically productive ecosystems, and this diverse environment 

includes unmeasured reserves of strategic minerals, oil and gas, and other nonliving resources. The coastal zone encompasses major hubs of global transportation and commerce and unparalleled opportunities for recreation and tourism, 

as well as the majority of fi sheries and aquaculture industries. At the same time, 

Anson H. Hines, Smithsonian Environmental Research Center, P.O. Box 28, 647 Contees Wharf 

Road, Edgewater, Maryland 21037-0028, USA 

(hinesa@si.edu). Manuscript received 29 August 

2008; accepted 20 April 2009.

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1 2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

these activities cause chronic and acute disturbance of every coastal habitat: overfi shing has removed most large 

species at the top of the food web, and coastal waters receive most of the waste of urban centers and agricultural 

runoff of the coastal plain.

Research at the Smithsonian Environmental Research 

Center (SERC) focuses on land– sea interactions. Scientists 

at SERC study linked coastal ecosystems to understand 

natural processes and human impacts in the coastal zone. 

Ocean productivity is concentrated in the coastal fringe 

where nutrients run off the land and well up from the 

deep. The coastal environment includes the Earth’s most 

biologically diverse ecosystems: estuaries, wetlands, mangroves, seagrasses, coral and oyster reefs, kelp forests, and 

pelagic upwelling areas. Bottom communities and water 

column processes of the photic zone are most tightly coupled in the nearshore shallows. Coastal waters comprise 

95% of the oceans’ fi sheries. Thus, SERC research focuses 

on improved stewardship of these marine resources.

CHESAPEAKE BAY AND THE RHODE RIVER 

SUBESTUARY AS A MODEL SYSTEM

The Smithsonian Environmental Research Center 

utilizes the nation’s largest estuary, Chesapeake Bay and 

its 177,000 km2 watershed including six states and the 

District of Columbia (Figure 1), as its primary research 

landscape and main study site. In addition to SERC, this 

study area includes the Smithsonian’s museum complex, 

zoological exhibits, and administrative offi ces. An area 

with a long American history of exploitation of coastal resources, the Chesapeake watershed is home to 17 million 

people, who are mostly concentrated in the urban centers 

and suburban sprawl of Baltimore, Washington, D.C., and 

Norfolk. Agriculture, particularly row crops, is the major 

land use of the Chesapeake watershed, and farming has 

been the major source of disturbance to the eastern deciduous forest for 400 years.

Established in 1965, SERC owns a unique 1,072 ha 

land holding for long-term descriptive and experimental 

studies of linked ecosystems in a model subestuary and 

subwatershed of Chesapeake Bay— the Rhode River, 

which is located 40 km east of Washington, D.C., and 

10 km south of Annapolis, Maryland (Figure 2). The 

property at SERC includes cropland, forests in various 

successional stages, wetlands, and 26 km of undeveloped 

shoreline; this is the largest contiguous block of land 

dedicated to environmental research, science education, 

public access, and stewardship on the western shoreline 

of Chesapeake Bay. The 585 ha Rhode River subestuary 

is a shallow (maximum depth 4 m), soft-bottom embayment in the lower mesohaline zone of the Bay. The 

facilities at SERC provide strategic support for research 

at the site and ready access to the rest of the Chesapeake 

watershed and estuary.

GRAND CHALLENGES OF COASTAL 

ENVIRONMENTAL RESEARCH

The purpose of this paper is to present examples that 

highlight SERC’s coastal research on fi ve grand environmental challenges. With data sets extending back to the 

1970s and 1980s, SERC research monitors decadal-length 

changes to distinguish seasonal and annual fl uctuations 

from long-term trends in the environment. Importantly, 

SERC research seeks to determine mechanistic understanding of the causes of change at multiple spatial scales 

ranging from global change to landscape, watershed, ecosystem, and community levels of organization. The land 

and long-term studies at SERC’s Rhode River site afford 

multidisciplinary experimental analyses of mechanisms 

controlling ecological interactions. The research there 

addresses the grand challenges and advises environmental policy and management for improved stewardship of 

coastal resources.

GRAND CHALLENGE I: IMPACTS OF ATMOSPHERIC CHANGE

Human alterations of the atmosphere are causing 

rapid changes in climate, sea level, ultraviolet radiation, 

pollutant deposition, and ecosystem carbon balance. Research by SERC on the salt marshes of the Rhode River 

subestuary provides a good example of the ecological complexities of this challenge. B. G. Drake and colleagues have 

been conducting the world’s longest running experimental 

manipulation of CO2 on natural plant communities (1985 

to present), which has been testing the effects of rising atmospheric CO2 concentration in these salt marshes. The 

experiment measures response of the two dominant plant 

species at the site: Spartina patens and Scirpus olneyi. The 

experiment applied nine treatment combinations of three 

CO2 levels in open-top chambers (ambient air at 340 ppm; 

elevated CO2 at a twofold increase in concentration of 680 

ppm; and a control treatment without chambers) crossed 

with types of patches (nearly monospecifi c S. patens; nearly 

monospecifi c S. olneyi; and patches with mixes of the two 

species) (Drake et al., 1989). Chambers were replaced 

exactly on replicate marked plots of the nine treatment 

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FIGURE 1. Map of Chesapeake Bay and its watershed with six physiographic provinces. Arrow 

indicates the location of the Smithsonian Environmental Research Center on the Rhode River 

subestuary and watershed. Darkened areas indicate 17 clusters of 500 subwatersheds that differed in land use and were monitored for stream discharges of nutrients.

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1 4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

combinations for the duration of the growing season for 

the past 23 years (1995– 2008). Photosynthesis and respiration were measured in each chamber during the growing 

season, and plant production was measured at the end of 

each season. As predicted, Spartina patens is a C4 plant 

that responds weakly to rising CO2, whereas growth and 

production were greatly stimulated in Scirpus olneyi as a 

C3 plant (Drake and Rasse, 2003). However, the amount 

of stimulation of S. olneyi is signifi cantly inversely dependent on salinity (i.e., water stress), with lower production 

in years of high salinities (i.e., low rainfall) (Rasse et al., 

2005; and Figure 3).

Salt marsh research at SERC’s Rhode River site also 

explores other ecosystem complexities. New research is 

tracking the fate of the carbon added by growth stimulation of the plants, which appears to be sequestered in the 

peat-forming roots of the salt marsh (Carney et al., 2007). 

Research conducted by J. P. Megonigal and colleagues at 

the same marsh study site compares effects of increased 

CO2 interacting with nutrient additions to the marsh to 

determine whether peat accumulation is suffi cient to keep 

up with rising sea level. Their initial results indicate that 

the peat accumulation is equivalent to the current rate 

of sea-level rise of approximately 3 mm year2, allowing the marsh to persist instead of becoming submerged. 

Additionally, a nonnative species, Phragmites australis, is 

rapidly invading the marsh site, similar to most others 

in the region (King et al., 2007); and its responses to the 

interaction of rising CO2 and nutrients are unknown. The 

Chesapeake region has high levels of mercury deposition 

FIGURE 2. Map of land holdings (shaded green) of the Smithsonian Environmental Research Center (SERC) surrounding the Rhode River 

subestuary. Red outline shows the boundary of the watershed.

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NUMBER 38 • 1 5

FIGURE 3. Effect of (A) precipitation and (B) salinity (ppt parts per thousand) on the stimulation of 

photosynthesis by twofold increase in CO2 concentration on the sedge Scirpus olneyi in open-top chambers 

placed on a salt marsh of the Rhode River subestuary during a 17-year period (1989– 2003). (After Rasse 

et al., 2005.)

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1 6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

that is derived from coal-burning power plants. New work 

at the SERC salt marsh site shows that microbes rapidly 

activate the mercury (mercury-methylation) (Mitchell et 

al., 2008) deposited into marshes, thus feeding it into biological processes on the coastal food web (C. Mitchell and 

C. Gilmour, Smithsonian Environmental Research Center, 

2008, personal communication).

GRAND CHALLENGE II: 

IMPACTS OF NUTRIENT LOADING

Over-enrichment of coastal waters with nutrients 

causes harmful algal blooms, depletion of oxygen, and 

destruction of submerged vegetation. Eutrophication in 

Chesapeake Bay and many other coastal systems is causing “dead zones” of anoxic and hypoxic waters along 

deeper bottom areas. A major focus of the restoration 

efforts of the Environmental Protection Agency’s Chesapeake Bay Program has been to reduce nutrient loading 

by phosphorus and nitrogen runoff into the Bay. Longterm watershed and estuarine water quality monitoring 

by SERC at the Rhode River site and throughout Chesapeake Bay shows the dynamic interactions of stream discharge, nutrient inputs, and plankton responses affecting 

oxygen levels.

Watershed nutrient discharge occurs primarily in 

storm events and is related to both geologic position 

(e.g., Piedmont or Coastal Plain provinces of the Chesapeake watershed) and land use, especially development 

and agriculture (Figure 4). Plankton productivity is much 

higher in years with high runoff, which leads to plankton blooms (Figure 5). Long-term monitoring from 1986 

to 2004 shows that water clarity (Secchi disc depth) and 

near-bottom oxygen levels have declined signifi cantly in 

the Rhode River subestuary (Figure 6). Although oxygen 

levels at SERC’s long-term monitoring station in the shallow edge of the Bay generally do not fall below alarming levels of approximately 6 ppm, oxygen levels in the 

deeper mainstem of the Bay drop to very low levels (Hagy 

et al., 2004) and occasionally spill into the mouth of the 

Rhode River, killing benthic organisms (A. Hines, personal 

observations).

With the decline in water clarity, light levels are not 

suffi cient to support growth of seagrasses and other submerged aquatic vegetation, which had largely disappeared 

from the Rhode River subestuary and much of Chesapeake 

Bay by the early 1970s. These structured ecosystems are 

important nursery habitats for fi sh and crabs in coastal 

systems such as Chesapeake Bay. Recent SERC research 

emphasizes the linkage of submerged aquatic vegetation to 

watershed characteristics (Li et al., 2007).

GRAND CHALLENGE III: FOOD WEB DISRUPTION 

BY POLLUTION AND OVERFISHING

Pollution and overfi shing result in severe disruptions 

of coastal food webs (Jackson et al., 2001). The combined 

effects of low dissolved oxygen and loss of submerged 

aquatic vegetation comprise much of the major impact 

of pollution in coastal systems such as Chesapeake Bay. 

However, inputs of mercury and other toxic chemicals also 

markedly affect the food web as they become concentrated 

at its upper levels, often causing serious effects on seafood 

that affect human health (Krabbenhoft et al., 2007). Impacts of overfi shing and habitat loss have resulted in the 

loss of sustainable stocks for nearly every fi shery species in 

Chesapeake Bay and in nearly every coastal system worldwide. After a century of intense exploitation, disease, and 

ecosystem impacts, oysters, as the Bay’s most productive 

FIGURE 4. Effects of cropland on stream discharge of nitrogen 

for watersheds in the Piedmont and Coastal Plain physiographic 

provinces of Chesapeake Bay (see Figure 1). Nitrogen is shown as 

nitrate concentration on the y-axis; cropland is shown as a percentage of land use of the subwatershed area on the x-axis. (After 

Jordan et al., 1997.)

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NUMBER 38 • 1 7

fi shery historically, are now at only 1% of their biomass 

in 1900 (Rothschild et al., 1994). Eutrophication and 

overfi shing act as multiple stressors on coastal food webs, 

and management’s too narrow focus on single factors may 

have adverse consequences for restoring ecosystem health 

and fi shery production (Breitburg et al., 2009).

Blue crabs are the remaining major lucrative fi shery in 

the upper Bay, but the blue crab stock has also declined by 

60% since 1991 (CBSAC, 2008). Research by SERC at the 

Rhode River subestuary provides the most detailed analysis of blue crab ecology available (Hines, 2007). Nearly 30 

years of SERC experiments show that blue crabs are the 

dominant predator on benthic communities in the estuary, 

and their foraging limits abundance and species composition of infaunal invertebrates as well as causing major 

bioturbation of the upper 10 cm of sediments (Hines et 

al., 1990). Long-term monitoring of fi sh and blue crabs 

throughout the Rhode River subestuary shows the marked 

seasonal and annual variations in population abundance 

(Figure 7), as blue crabs migrate from the nursery habitat 

and become inactive below 9°C in winter. Annual variation in recruitment into the Rhode River causes more than 

a 10-fold fl uctuation in abundance, with obvious variation 

in effects of predation on infaunal invertebrates. Many upper Chesapeake Bay nursery habitats now appear to be below carrying capacity for juvenile blue crabs (Hines et al., 

2008). Recent SERC blue crab research has focused on deFIGURE 5. Comparison of carbon production in the Rhode River 

subestuary during two years, one with and one without a spring 

plankton bloom, which is mainly regulated by variation in spring 

precipitation and watershed discharge. (After Gallegos and Jordan, 1997.)

FIGURE 6. Long-term trends in water clarity as determined by Secchi (disk) depth (left) and in oxygen concentration (D.O. dissolved oxygen; 

right) in the Rhode River subestuary. (Figure courtesy of C. Gallegos.)

02_Hines_011-024_Lang.indd 17 2_Hines_011-024_Lang.indd 17 9/24/09 9:39/24/09 9:39
1 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 7. Seasonal and annual variation in abundance of blue crabs caught in 3 m otter trawls in the Rhode 

River subestuary. Abundance is the monthly mean of three trawls at each of three permanent stations within 

the estuary.

veloping innovative approaches to restoring the blue crab 

population in the Bay, especially by testing the feasibility 

of releasing hatchery-reared juvenile blue crabs into nursery areas such as the Rhode River (Hines et al., 2008).

GRAND CHALLENGE IV: INVASIVE SPECIES

Invasions of nonindigenous species are drastically altering biodiversity, structure, and function of coastal ecosystems (Ruiz et al., 2000). The largest, most comprehensive 

research program on marine invasive species in the USA 

is conducted by SERC. Rates of invasion into coastal 

ecosystems are increasing markedly as a result of a wide 

range of human-mediated vectors, but most importantly 

as a result of shipping, both ballast water discharge and 

hull fouling (Ruiz et al., 2000). The SERC database for 

invasive species (NEMESIS) documents more than 500 

invasive species of invertebrates, algae, and fi sh in North 

American coastal waters. For Chesapeake Bay approximately 176 species are documented as established invasions (Figure 8). Invasions are dynamic and ongoing in 

Chesapeake Bay, as indicated by recent records of Chinese mitten crabs (Ruiz et al., 2006). Many species are 

having large but poorly understood impacts in Chesapeake ecosystems, such as the salt marsh reed Phragmites 

australis (King et al., 2007).

GRAND CHALLENGE V: 

LANDSCAPE DISTURBANCE BY AGRICULTURE

AND DEVELOPMENT

Agriculture and urbanization are causing widespread 

modifi cations of landscape structure. Researchers at SERC 

recently analyzed various indicators of estuarine habitat 

quality for 31 Chesapeake subwatersheds that differed in 

fi ve categories of land use composition: forest, agriculture, 

developed, mixed agriculture, and mixed developed (Figure 9). These land uses have profound effects on estuarine 

habitat quality because they increase stormwater runoff and 

loading of nutrients. Nitrogen discharge into subestuaries of 

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NUMBER 38 • 1 9

agricultural and developed watersheds was high in both wet 

and dry years, but in dry years it was high only in developed 

watersheds, which continue to have high human water use 

regardless of rainfall (Figure 10) (Brooks et al., 2006). Land 

use also has marked effects on levels of toxic chemicals in 

the food webs of the subestuaries. Level of polychlorinated 

biphenyls (PCBs) was highly correlated with percentage of 

developed lands on the subwatershed (Figure 11).

In addition to effects on the watershed, development 

of the shoreline has large impacts on coastal ecosystems. 

Research by SERC in the Rhode River shows that the 

shallowest fringe of the subestuary serves as a critical refuge habitat for juvenile fi shes and crabs to avoid larger 

predators, which are restricted to deeper water (Ruiz et 

al., 1993; Hines and Ruiz, 1995). Coarse woody debris 

from forested shores also plays a valuable role as structural habitat and refuge from predators (Everett and 

Ruiz, 1993). As development results in cutting down the 

riparian forest and hardening the shoreline with bulkheads and riprap to prevent erosion, water depth at the 

shoreline increases and the source of woody debris is 

lost. With the loss of functional refuge in the nearshore 

shallows, juvenile fi sh and crabs become increasingly accessible to predators.

CONCLUSION

The decadal data sets generated by SERC for the 

linked ecosystems of the Rhode River and Chesapeake Bay 

clearly show the importance of sustaining long-term, intensive studies to distinguish natural variation and trends 

of human impacts. The rate of change associated with human impacts is increasing markedly as the effects of global 

change become manifest and as the human population of 

the watershed continues to grow rapidly, with another 

50% increase predicted in the next 25 to 50 years. The 

interactive effects of these multiple stressors require much 

more research to defi ne improved management solutions 

to restore and sustain these resources. Scientists at SERC 

also extend studies of the large-scale systems of the Rhode 

River and Chesapeake Bay through comparative studies 

with other coastal areas, especially latitudinal comparisons of systems in the Smithsonian Marine Science Network along the western Atlantic. Although each site has 

its idiosyncratic traits, the common impacts of the grand 

challenges of atmospheric change, nutrient loading, food 

web disruption by pollution and overfi shing, invasive species, and land development are all manifested pervasively 

in the linked ecosystems throughout the coastal zone.

FIGURE 8. Numbers of invasive species documented for algae, vascular plants, invertebrates, fi shes, and other 

vertebrates (total number 176 species) in Chesapeake Bay. Regular residents are species living in habitats 

below tidal infl uence; boundary residents are species primarily living either above the intertidal zone or in nontidal freshwater and that occasionally move into tidal portions of the Bay. (NIS noninvasive species.)

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2 0 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 9. Map of 31 subwatersheds of Chesapeake Bay that were sampled for effects of land 

use on estuarine habitats. Watersheds were categorized in the fi ve predominant categories shown: 

forest, agriculture, developed, mixed-agriculture, and mixed-developed.

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NUMBER 38 • 2 1

FIGURE 10. Effect of land use on nitrogen discharge from watersheds in the fi ve land use categories shown in 

Figure 9. Stream surface discharges are compared among land use categories between a dry year with record 

low rainfall (2002, left) and a wet year (2003, right) with high rainfall. (After Brooks et al., 2006.)

FIGURE 11. Concentration of toxic polychlorinated biphenyls (PCBs) in white 

perch (Morone americana) sampled from Chesapeake subestuaries with watersheds 

of varying percentages of commercially developed land use (IDW inverse distance 

weighted). Watersheds sampled are shown in Figure 9. (After King et al., 2004.)

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2 2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

ACKNOWLEDGMENTS

I thank my colleagues at SERC for use of their data 

and publications to illustrate this paper, especially Denise Breitburg, Bert Drake, Chuck Gallegos, Cindy 

Gilmour, Tom Jordan, Pat Megonigal, Rick Osman, 

and Greg Ruiz. I thank the Smithsonian Marine Science 

Network and the Smithsonian Environmental Sciences 

Program for long-term funding to SERC’s Rhode River 

research program. Thanks go to Michael Lang for his 

steady assistance in managing the Marine Science Network and for organizing the symposium and editing 

these proceedings.

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Smithsonian Marine Station at Fort Pierce: 

Thirty-Eight Years of Research on the Marine 

Biodiversity of Florida

Valerie J. Paul, Julianne Piraino, and Laura 

Diederick

ABSTRACT. The Smithsonian Marine Station at Fort Pierce, located on South Hutchinson Island in Fort Pierce, Florida, has had an ongoing program in the marine sciences 

since the early 1970s. Funded by a private trust from J. Seward Johnson, Sr., to the 

Smithsonian, the marine program has supported the research of Smithsonian scientists 

and their associates, postdoctoral fellows, resident scientists, and the operations of the 

station, including a small support staff. The station is administered by the National Museum of Natural History as a facility for research dedicated to the marine sciences. The 

Smithsonian Marine Station at Fort Pierce has developed a strong, broadly based research program focusing on ecology, evolution, systematics, and life histories of marine 

organisms. Ongoing studies address important issues in biodiversity, including global 

climate change, invasive species, harmful algal blooms, larval ecology, and evolutionary 

developmental biology.

INTRODUCTION

The Smithsonian Marine Station at Fort Pierce (SMS) is dedicated to studying the rich diversity of marine life of the Indian River Lagoon and Florida coast. 

In sharing its fi ndings with the scientifi c community, resource managers, and the 

general public, the Marine Station promotes the conservation and stewardship 

of Florida’s vast marine resources. Research activities focus on the Smithsonian 

Institution’s core scientifi c emphasis of discovering and understanding life’s diversity. Although most research projects focus on biodiversity, life histories, and 

ecology of marine and estuarine organisms, complementary studies of physical and chemical processes related to the marine environment are also part of 

the Station’s investigations. The insights gained by the research conducted at 

SMS are widely disseminated through scientifi c publications (more than 780 to 

date; see complete listing on the Station’s website www.sms.si.edu), scientifi c 

and public presentations, popular articles, and the media, thus contributing to 

the broader mission of the Smithsonian Institution for the “increase and diffusion of knowledge.”

The Smithsonian’s presence in Fort Pierce, Florida, began in 1969 through 

an association with Edwin Link, an inventor and engineer who was involved 

at that time in the design of research submersibles, and J. Seward Johnson, Sr., 

Valerie J. Paul, Julianne Piraino, and Laura Diederick, Smithsonian Marine Station at Fort Pierce, 

701 Seaway Drive, Fort Pierce, Florida 34949, 

USA. Corresponding author: V. Paul (paul@si.edu). 

Manuscript received 29 August 2008; accepted 20 

April 2009.

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2 6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

founder of the Harbor Branch Foundation, now known 

as the Harbor Branch Oceanographic Institute (HBOI) at 

Florida Atlantic University (Figure 1). In late 1969, the 

Smithsonian was given two trust funds through the generosity of J. Seward Johnson, Sr., for the development and 

maintenance of a submersible (then under construction) 

and for research in underwater oceanography. At its completion in 1971, the submersible, the Johnson Sea-Link I, 

was donated to the Smithsonian. In 1973, after a tragic 

accident in the Johnson Sea-Link in which two men died, 

the Smithsonian transferred ownership of the submersible 

to Harbor Branch. Following the transfer of the submersible, the Smithsonian’s marine research program in Fort 

Pierce continued to be supported by income from both 

trust funds, then later, after certain legal resolutions, by 

one of the two funds, designated as the Hunterdon Fund. 

The Smithsonian carried out its activities in Fort Pierce on 

the grounds of the Harbor Branch Foundation (Link Port) 

under the auspices of the Fort Pierce Bureau, a unit administered directly by the Offi ce of the Secretary and then later 

by the Assistant Secretary for Science. In March 1981 this 

Bureau was dissolved as an organizational entity, and the 

administrative responsibility for the Smithsonian research 

programs at Link Port was transferred to the Director 

of the National Museum of Natural History (NMNH). 

The organization was then retitled by the Secretary of the 

Smithsonian as the Smithsonian Marine Station at Link 

Port. At the time of the transfer of administrative responsibility, the directive from the Offi ce of the Assistant Secretary for Science was that a strong research program in 

marine science should be established and that the program 

should be open to all marine scientists in the Smithsonian Institution. In response, Richard Fiske, then Director 

of NMNH, established an inter-unit advisory committee, 

appointing Catherine Kerby, his administrative assistant, 

as chair of the committee, and Mary Rice, Department 

of Invertebrate Zoology (on assignment to the Fort Pierce 

Bureau), as director of the facility and research programs 

at Link Port. Rice held this position until her retirement 

in 2002, at which time Valerie Paul was selected as her 

successor.

The Smithsonian Marine Station at Link Port was initially set up with a small on-site staff and well-equipped 

laboratories and fi eld facilities to provide opportunities for 

Smithsonian scientists and their colleagues to conduct fi eld 

research in a highly diverse subtropical marine environFIGURE 1. J. Seward Johnson, Sr. (left), and inventor Edwin Link were instrumental in providing funding and submersibles for the Smithsonian’s marine research program in Fort Pierce, 

Florida.

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NUMBER 38 • 2 7

ment. This plan gave Museum scientists the opportunity 

to extend and broaden their research from museum collections to fi eld studies in such areas as behavior, ecology, 

physiology, and life histories. Moreover, it provided the 

opportunity for all Smithsonian marine scientists to carry 

out comparative studies of the diverse ecosystems and biota within the Fort Pierce vicinity and peninsular Florida 

and, most importantly, to establish long-term databases 

and to conduct long-term studies. An important component of the plan was to include postdoctoral fellows, both 

to complement the research of Smithsonian scientists and 

to contribute to training of future generations of marine 

scientists. In addition, by serving many Smithsonian scientists (as opposed to a few resident scientists), the program 

was conceived to yield maximum productivity of highquality modern science and to be the most equitable and 

effective use of available funds.

For the fi rst 18 years the Smithsonian Marine Station 

at Link Port used a vintage WW II barge as a fl oating laboratory docked at Harbor Branch (Figure 2) as the base 

of operations for its highly successful research program, 

which was carried out primarily by visiting scientists from 

the Smithsonian, their colleagues, and postdoctoral fellows. Restrictions imposed by the space and structural 

limitations of the barge for many research activities as well 

as its high maintenance requirements led the Smithsonian 

to pursue plans for a land-based laboratory.

In May 1999 these plans were realized when, with the 

approval of J. Seward Johnson, Jr., and a signed Memo of 

Understanding, the Smithsonian Marine Station relocated 

to an 8 acre site acquired from the MacArthur Foundation 

near the Fort Pierce Inlet, 7 miles south of Harbor Branch. 

At this time the offi cial name of the station was changed to 

the Smithsonian Marine Station at Fort Pierce. The move 

was made into a newly constructed 8,000 square foot 

building with offi ces and laboratories for visiting scientists, resident staff and postdoctoral researchers, generaluse laboratories for chemistry, microscopy, and molecular research (Figures 3, 4), and a wet laboratory supplied 

by a small seawater system. In March 2003, a 2,400 

square foot storage building was completed. The building includes a workshop and storage for scientifi c supplies, 

scuba equipment, and other marine research equipment. 

In April 2004 a research dock was completed on the Indian River Lagoon, which is accessible by an easement on 

adjacent property. A fl ow-through seawater building was 

FIGURE 2. A retired World War II Army barge was remodeled to include two levels of offi ces and laboratories for use by the Smithsonian 

Marine Station scientists from the early 1970s to 1999.

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2 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

added to the campus in August 2005. The relocation to 

the new research building and campus provided the opportunity for the Smithsonian Marine Station to increase 

and strengthen the breadth and diversity of its research 

as well as to establish new collaborative interactions. The 

move also made it possible to expand the Station’s educational mission, initiating new cooperative ventures in education and public outreach.

In the struggle to understand life, how its diversity has 

come about, and the current rapid loss of biodiversity on a 

global scale, the Smithsonian Marine Station is positioned 

as are few laboratories in the world to study this exceptional diversity from an array of environments. The Smithsonian Marine Station is located on the Fort Pierce Inlet of 

the Indian River Lagoon (IRL) (see Figure 3), an estuary 

extending along one-third the length of the east coast of 

Florida. The IRL is widely recognized as one of the most 

diverse estuaries in North America, and it has been designated an estuary of national signifi cance by the Environmental Protection Agency. The Marine Station’s unique 

location on the Fort Pierce Inlet puts it in a prime position 

to access oceanic waters and to sample organisms from the 

Florida Current and other offshore habitats. This region of 

Florida’s coast, characterized as a transitional zone where 

temperate and tropical waters overlap, offers access to a 

great variety of habitats and an extraordinary diversity of 

species. To the south of Fort Pierce, within a few hours of 

travel, are Florida Bay and the Florida Keys, the only living 

tropical coral reefs in the continental United States.

Specialized equipment and instrumentation at the 

Smithsonian Marine Station include temperature-controlled aquaria and incubators, equipment for preparing 

tissues for light and electron microscopy, an ultracold 

freezer, equipment for electrophoresis, a thermocycler 

for DNA amplifi cation, high performance liquid chromatographs, a gas chromatograph/mass spectrometer, 

and a UV-visual spectrophotometer. For microscopic 

studies, equipment is available for light, epi-fl uorescent, 

and Nomarski microscopy, time-lapse and normal-speed 

cinematography, photomicrography, video recording and 

editing, inverted microscopy, scanning and transmission 

electron microscopy (Figure 5), and confocal laser scanning microscopy.

Confocal laser scanning microscopy (CLSM) has become an increasingly important tool in modern environmental microbiology, larval ecology, developmental biology, and biochemistry. CLSM involves the use of a light 

microscope, laser light sources, a computer, and special 

software to image a series of in-focus optical sections 

through thick specimens. The specimens, which can be 

live or fi xed, are stained with fl uorescent dyes that highlight specifi c structures when excited by the lasers. Once 

the stacks of two-dimensional (2-D) images are collected, 

the computer software constructs spectacular, informationrich, three-dimensional (3-D) images that yield a wealth of 

information. In June 2008, the Smithsonian Marine Station 

acquired a Zeiss LSM510 confocal system that is already 

providing data in the cutting-edge studies of Postdoctoral 

FIGURE 3. This aerial view shows the location of the Smithsonian Marine Station on the Fort Pierce Inlet of the Indian 

River Lagoon in Florida.

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NUMBER 38 • 2 9

FIGURE 4. Smithsonian Marine Science Network Postdoctoral Fellow Koty Sharp uses molecular methods to determine the diversity of bacteria associated with corals.

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3 0 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Fellow Koty Sharp on the presence and transmission of 

bacteria in corals, and in research conducted by Postdoctoral Fellow Kate Rawlinson on the fate of individual cells 

in the development of embryos of polyclad fl atworms. 

This new microscope will greatly increase the capabilities 

of Smithsonian marine scientists to conduct probe-based 

subcellular studies in biochemistry, microbiology, and developmental biology (Figure 6).

The Marine Station owns four boats for use in fi eld 

studies: a 17 foot Boston Whaler and a 21 foot Carolina 

Skiff for work in the shallow waters of the IRL, a 21 foot 

center-console boat to access nearshore waters, and a 39 

foot vessel, the R/V Sunburst, for offshore research activities. These vessels provide access to the diverse marine 

and estuarine environments in the vicinity of SMS. The 

excellent location, facilities, instrumentation, and skilled 

staff of the Smithsonian Marine Station facilitate research 

on many diverse topics in marine biology and marine 

biodiversity.

RESEARCH ACTIVITIES

The Smithsonian Marine Station at Fort Pierce is an 

important contributor to the marine research and collections at the National Museum of Natural History. It 

provides a vital link between tropical and temperate ecosystems in a coastal network of marine research stations 

known as the Smithsonian Marine Science Network. The 

Marine Science Network (MSN) is an array of laboratories spanning the western Atlantic coastal zone and across 

the Isthmus of Panama, facilitating long-term interdisciplinary, comparative research among MSN sites, including 

the Smithsonian Environmental Research Center (SERC) 

FIGURE 5. Julie Piraino, Laboratory Manager, examines the larva of a sipunculan worm on the scanning electron microscope.

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NUMBER 38 • 3 1

FIGURE 6. Left: Confocal microscopy captures 

an oxidative burst reaction by the green alga Dictyosphaeria cavernosa following exposure to the 

fungus Lindra thalassiae. An oxidative burst is 

an explosive production of reactive oxygen species (hydrogen peroxide is an example) intended 

to act as fi rst defense against invading pathogens. 

Middle: Confocal image shows development of 

musculature and nervous system in a larva of a 

sipunculan worm. Right: Confocal laser scanning micrograph of the musculature of a Müller’s 

larva of the fl atworm Cycloporus variegatus. 

Phalloidin staining shows circular and longitudinal muscles (cm, lm, respectively) and the ciliary 

band (cb). Scale 30 m.

in Maryland, the Carrie Bow Cay Marine Field Station 

in Belize, and the Smithsonian Tropical Research Institute 

(STRI) in Panama.

Research at SMS continues to be carried out by Smithsonian scientists from various units within the Institution 

along with their colleagues from other national and international institutions, as well as by resident SMS scientists, 

postdoctoral fellows, and graduate students (Figure 7). 

Ongoing research programs by resident scientists at the 

Smithsonian Marine Station involve coral reef research, 

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3 2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

monitoring that is supporting restoration of the Florida Everglades, harmful algal blooms, marine natural products, 

and invertebrate larval life histories, evolution, and development. The Smithsonian Marine Station promotes the 

education of emerging scientists by offering pre- and postdoctoral research fellowships and supporting the work of 

student interns. Examples of ongoing research activities 

are discussed below.

MARINE BIODIVERSITY

The Smithsonian Marine Station has long had a central focus on documenting biodiversity of marine life in the 

most diverse coastal waters of the continental United States. 

NMNH invertebrate zoologist David Pawson has discovered 

and documented echinoderms (sea urchins, sand dollars, sea 

cucumbers) in shallow and deep waters of Florida for more 

than 25 years (Hendler et al., 1995). He has found sand dollars that are probably hybrids between two species in the 

offshore waters of Fort Pierce. Other groups of organisms 

that have been well studied by NMNH researchers for many 

decades include the marine algae (Mark and Diane Littler), 

foraminifera (Marty Buzas), crustaceans (Rafael Lemaitre 

and colleagues), deep- and shallow-water mollusks (Jerry 

Harasewych and Ellen Strong), and meiofaunal organisms 

(animals less than 1 mm in size that live in sand and sediments) (Jon Norenburg and coworkers). Additionally, many 

SMS scientists, including former director Mary Rice, have 

focused on understanding the diversity and distribution of 

larval forms of different groups of marine invertebrates. 

These larval stages are morphologically and ecologically 

very different from adult life stages and are extremely important for the transport and propagation of marine species, 

sometimes over long distances (Figure 8). Tuck Hines and 

Richard Osman (SERC) have also studied recruitment patterns and larval ecology for a variety of invertebrate larval 

forms in the IRL. A few examples of the many biodiversity 

studies conducted at SMS are highlighted below.

FIGURE 7. Visiting Scientist Anastasia Mayorova (kneeling) collects sipunculan worms with the assistance of Mary 

Rice, Director Emeritus of SMS (left), and Research Technician Woody Lee.

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NUMBER 38 • 3 3

With much of their research focused on ecology, physiology, and pollution-oriented work, Mark and Diane Littler observed a growing need for an easier means for fi eld 

scientists and resource managers to identify the diverse 

and abundant marine algal species in the fi eld. They have 

published user-friendly fi eld guides, including the awardwinning book Caribbean Reef Plants (Littler and Littler, 

2000), with much of their laboratory and fi eld research 

based at SMS. More recently, with co-author M. Dennis 

Hanisak (Harbor Branch Oceanographic Institute), they 

published Submersed Plants of the Indian River Lagoon: 

A Floristic Inventory and Field Guide (Littler et al., 2008), 

a book rich with photography and illustrations depicting 

the taxonomy and distributional patterns of more than 

250 species of submersed plants in the Indian River Lagoon. The book was based on six years of fi eld and laboratory work along the central east coast of Florida.

D. Wayne Coats, a protistan ecologist at the Smithsonian Environmental Research Center, has worked on the 

biology and ecology of free-living and symbiotic protists 

for 20 years. His work has enabled comparisons between 

the Chesapeake Bay and Indian River Lagoon estuaries 

and provided enhanced understanding of how eukaryotic 

microbes infl uence the structure of marine food webs (Snoeyenbos-West et al., 2004). Much of Coats’ work at SMS 

has considered the biodiversity and trophic biology of protists living in coastal waters of Florida or associated with 

local marine fauna. He has shown parasitism of planktonic ciliates in the Indian River Lagoon to be a major 

pathway for recycling material within the microbial loop. 

Coats and his graduate students have also shown that many 

free-living photosynthetic dinofl agellates have the ability 

to feed on ciliate protozoa. Although ingestion rates are 

typically low, the high densities attained by red-tide dinofl agellates in the Indian River Lagoon and Chesapeake Bay 

make their ability to ingest ciliates an important microbial 

food web interaction. Feeding on ciliates and other protists may help sustain blooms when nutrient resources for 

photosynthesis are limited. Coats and his colleagues have 

also revealed a rich and poorly known ciliate fauna associated with the respiratory tract of bottle-nosed dolphins 

and other cetaceans (Ma et al., 2006). Previously reported 

to be parasitic, these ciliates appear not to directly impact 

the health of animals held in captivity. Through his work 

at SMS, Coats has helped defi ne the signifi cance of protists within the marine ecosystem. In some instances, these 

protists compete directly with zooplankton for food resources, thus limiting the upward movement of energy and 

matter in the food web. In other instances, they can recycle 

biomass not readily grazed by zooplankton, thus repackaging it in a form that can move more readily through the 

food web.

Mary Rice, former director of SMS, established a program of life history studies more than 30 years ago involving numerous postdoctoral fellows and visiting scientists 

who have worked on a variety of marine invertebrates. 

Her research has focused on an enigmatic group of marine worms known as sipunculans. Presumably a primitive 

group related to annelids and mollusks, sipunculans are 

unique in their complete lack of segmentation and single 

unpaired ventral nerve cord. One of several objectives of 

her studies has been the use of developmental studies to 

understand phylogenetic affi nities both within the group 

and with other spiralian phyla (Schulze and Rice, 2009). 

Other objectives have been comparative studies of reproductive biology and ecology of shallow-water and deep-sea 

species, an investigation of the biology of oceanic larvae, 

including their metamorphosis and their role in species 

distribution, and a systematic survey of the Sipuncula of 

Florida and the Caribbean.

In studies of reproductive biology, comparative information was gathered for numerous species on gametogenesis, spawning, egg sizes, egg maturation, fertilization, 

and reproductive seasonality (Rice, 1989). Year-long observations of reproductive activity in Phascolion cryptum, 

FIGURE 8. Examples of marine invertebrates, the larval development of which has been studied by Mary Rice and colleagues at SMS 

for more than 30 years. Organisms shown here, clockwise from upper left, are a starfi sh brachiolarian larva, a sipunculan pelagosphera 

larva, a brachiopod larva, and a fl atworm Muller’s larva.

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3 4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

a small species inhabiting discarded gastropod shells in 

the subtidal waters of the Indian River Lagoon, revealed 

that— in contrast to temperate species— animals were 

reproductive throughout the year. A collaborative ultrastructural study of spermiogenesis was also conducted. 

The most abundant sipunculan of the Indian River Lagoon, this species was recorded in densities up to 2,000 

to 3,000 per square meter. No longer found in these densities, the population has declined for reasons unknown 

(Rice et al., 1983).

Studies of larval biology by Rice and collaborators 

have concentrated on the oceanic pelagosphera larvae of 

sipunculans that occur in abundance in the Florida Current, a component of the Gulf Stream System that fl ows 

along the edge of the Continental Shelf offshore from Fort 

Pierce. Reported in warm water currents throughout the 

world’s oceans, these larvae are known to be long lived, 

existing in the larval stage for 6 to 7 months, and hence to 

have the potential for widespread species dispersal (Rice, 

1981). Continuing for more than three decades, the studies have included descriptions of the various larval morphotypes through light and scanning microscopy, as well as an 

investigation of factors inducing metamorphosis and the 

identifi cation of species by rearing larvae to adulthood. 

Several of the larvae were identifi ed by rearing, surviving 

in the laboratory for periods of 3 to 26 years as adults. In 

more recent collaborative studies (with Postdoctoral Fellow Anja Schulze and staff of the NMNH Laboratory of 

Analytical Biology), genomic analysis, comparing larval 

and known adult sequences, was utilized to identify additional larval types. These analyses suggested the presence 

of two cryptic species, characterized by morphologically 

similar adults but different larval types.

Jon Norenburg (NMNH), together with students, 

postdoctoral fellows, and collaborators, has been and is 

focused on discovering nemertean diversity in Florida and 

using that diversity to address broader questions. In short 

visits over the course of 20 years they have collected as 

many as 70 putative species, primarily from the shoreline 

and shallow coastal waters, from a region with 24 previously known species. Many of the additional species are 

potential range extensions that await confi rmation with 

specimens from type locales, especially those in southern 

Brazil, which is the nearest subtropical nemertean fauna 

that also is well documented. There also are tantalizing 

preliminary data for close genetic links with European 

species (Maslakova and Norenburg, 2008). New species have been named, and another 10 to 15 potential 

new species await additional specimens or genetic work. 

Most nemerteans have few to no external diagnostics to 

characterize and discriminate species unambiguously. Almost all the species collected in Florida by Norenburg 

and coworkers in the past 15 years were processed with 

genetic work in mind, which will resolve some questions 

of identity and yield realistic estimates of true diversity 

and contribute important samples for studying diversifi -

cation of the phylum (Thollesson and Norenburg, 2003). 

That effort in Florida is an important component of two 

global-scale nemertean projects headed by Norenburg: 

(1) diversity and coevolution of the specialized, ectosymbiotic carcinonemertid worms with their decapod crustacean hosts (mostly crabs), and (2) phylogeny and biogeography of Ototyphlonemertes, which are specialized 

and miniaturized worms occupying the aqueous pore 

space in coarse sediments, such as coarse sand beaches 

and in high-current subtidal habitats. Norenburg’s study 

of nemerteans in Florida has contributed important original observations about developmental biology of nemerteans, and one species in particular has revolutionized 

our understanding of nemertean evolution (Maslakova 

et al., 2004).

Carole Baldwin and Lee Weigt from the National 

Museum of Natural History are studying fi sh diversity, 

including larval fi shes, through DNA barcoding methods. 

Fish taxonomists have traditionally classifi ed fi shes based 

on morphological features that can be seen and described. 

However, many families of fi shes, such as parrotfi shes and 

gobies, have members that look so similar they are virtually indistinguishable without examining the genetic material. Baldwin and her research team have now cataloged 

more than 200 species (from more than 1,000 specimens) 

from the Indian River Lagoon. Processing involved identifying and measuring each fi sh, photographing its live coloration, taking a tissue sample for DNA analysis, and preserving the rest of the specimen as a voucher for NMNH 

archival collections. Tissue samples from each specimen 

were used to create a DNA barcode, which is unique to 

the individual fi sh species and can be used for identifi cation purposes. Not only will this work be important for 

establishing a database of genetic information for fi shes 

of the Indian River Lagoon, it will greatly increase our 

understanding of shorefi sh diversity. The overall goal of 

the work is to provide a new, more realistic estimate of 

species diversity in the Caribbean, Florida, and adjacent 

areas. Having amassed DNA extractions from fi shes from 

a variety of taxa and from multiple localities in the tropical Atlantic, the investigators can now examine interspecifi c phylogenetic relationships to investigate patterns of 

speciation and potential patterns of morphological divergence accompanying speciation.

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NUMBER 38 • 3 5

Important reasons often cited for understanding 

biological diversity are the possible benefi ts these species might yield as foods, medicines, or for other human 

uses. Valerie Paul, Director of SMS, and members of her 

research group investigate the chemical diversity of marine organisms by studying marine natural products, small 

molecules produced as chemical signals or as toxins or 

chemical defenses. Members of Paul’s research team isolate and characterize natural products from Florida’s marine life (seaweeds and invertebrates) and have discovered 

compounds that have never previously been found in nature. A current area of interest for her research group is 

the biodiversity and chemical diversity of benthic marine 

Cyanobacteria. Through collaborations with medicinal 

chemists, they are actively investigating the benefi cial uses 

of these compounds for treatment of human diseases such 

as cancer and bacterial infections.

MARINE ECOLOGY

Valerie Paul studies marine plant– animal interactions 

in coral reef habitats. Coral reefs in Florida and throughout the world are declining, in part the consequence of 

shifts from coral- to algal-dominated communities. Paul 

and members of her research team study grazing by reef 

fi shes and sea urchins and the effects of herbivory on 

coral reef community structure (Paul et al., 2007). They 

have found that chemical defenses of marine algae allow some well-defended marine plants to dominate on 

coral reefs despite grazing pressure. Key to the recovery 

of coral reefs is the successful recruitment of coral larvae 

to become juvenile and eventually adult corals (RitsonWilliams et al., 2009). Paul’s research group and their 

collaborators examine positive and negative interactions 

between coral larvae and the marine algae that dominate 

coral reef habitats. Some of the same species of algae 

that are chemically protected from grazers can inhibit the 

settlement of coral larvae, thus preventing the successful 

recovery of coral reefs.

Algae are an essential part of marine ecosystems 

and when maintained in balance can provide food, shelter, oxygen, and more to millions of organisms, including people. But some algae can produce harmful toxins 

and, under certain conditions, can grow out of control. 

These so-called harmful algal blooms have been increasing in frequency and severity along the world’s coastlines. 

NMNH scientist Maria Faust has been investigating the 

types of planktonic harmful algae, often called red tides, 

which occur along Florida’s east coast (Faust and Tester, 

2004). Valerie Paul, NMNH Statistician Lee-Ann Hayek, 

and Postdoctoral Fellows Karen Arthur and Kate Semon 

have been studying formation of blooms of marine cyanobacteria in Florida’s estuaries and coral reefs and trying to elucidate environmental factors that contribute to 

bloom formation (Paul et al., 2005). Increased nutrients 

from land-based sources, such as runoff from fertilizers 

and sewage treatment plants, may help to fuel some of 

these algal blooms. The biological and biochemical diversity of harmful algae is the subject of ongoing research, 

which has led to the discovery of novel toxins produced 

by these cyanobacteria.

Estuaries and coasts around the world are approaching 

critical levels of degradation, and the southern Indian River 

Lagoon is no exception. Large-scale, collaborative efforts 

are underway to restore biodiversity and the vital ecological functions these ecosystems provide. Bjorn Tunberg and 

members of his benthic ecology research team at SMS are 

involved in one of the most ambitious of these projects, the 

Comprehensive Everglades Restoration Plan (CERP). Extensive modifi cations to the southern IRL watershed over 

the past 100 years have decreased the system’s ability to 

store water and have increased nutrient-rich stormwater 

runoff. The CERP plan, under the direction of the South 

Florida Water Management District and the U.S. Army 

Corps of Engineers, aims to restore wetlands and build 

water storage basins to improve estuarine health. Tunberg 

and his team established a benthic monitoring program 

fi ve years ago to provide a baseline data set of species distribution and abundance in the sediments of the Indian 

River Lagoon. This team is acquiring quarterly data that 

will allow them to detect and predict long-term changes 

in the benthic communities throughout the central and 

southern Indian River Lagoon.

The location of the Smithsonian Marine Station on 

the Indian River Lagoon for 37 years has allowed Smithsonian researchers to establish long-term and intensive 

research projects that are valuable in understanding and 

assessing marine biodiversity. Long-term biological monitoring is most effectively carried out on organisms with 

high densities, many species, short generation times, quick 

responses to changes in environmental variables, and a 

long history of extensive study on a worldwide basis. 

The benthic foraminifera fi t these requirements, and their 

populations have been monitored in the Indian River Lagoon for more than 30 years by Marty Buzas (NMNH).

At one station near the Harbor Branch Oceanographic 

Institute, monthly replicate sampling of foraminifera living in the sediment has been carried out since 1977. These 

data indicate signifi cant differences between seasons, as 

well as among years, but no overall increase or decrease 

03_Paul_025-042_Lang.indd 35 3_Paul_025-042_Lang.indd 35 9/24/09 9:19/24/09 9:19
over a longer time span. The spatial distribution of the 

foraminifera forms an environmental mosaic of patches 

whose densities change with time. This newly discovered 

phenomenon was termed pulsating patches (Buzas et al., 

2002; Buzas and Hayek, 2005). At the St. Lucie Inlet, observations were made in 1975– 1976 and again 30 years 

later in 2005. Species richness had greatly declined over 

30 years, and the community structure of the foraminifera 

in this area was completely destroyed (Hayek and Buzas, 

2006). Monitoring at this Inlet during 2007– 2008 has 

shown that species richness has increased; however, except for the abundant species, the fauna does not contain 

the same species as it did 30 years ago. Monitoring efforts 

are continuing, and Buzas and Hayek have also begun a 

coring program to determine the effects of both natural 

and anthropogenic effects on community changes during 

the past 150 years.

Candy Feller, Dennis Whigham, coworkers from the 

Smithsonian Environmental Research Center (SERC), and 

national and international collaborators have conducted 

long-term studies of the mangrove ecosystems of the Indian River Lagoon. The overall goal of this project is to 

collect hydrological, nutrient, microbial, and vegetation 

data in support of their long-term ecological studies of 

factors that control the structure and function of mangrove ecosystems (Figure 9, top). Feller has continued a 

study of how nutrient enrichment affects the mangrove 

communities along the Atlantic coast of Florida for the 

past 10 years. Fertilization experiments designed to enrich nitrogen (N) and phosphorus (P) in sediments have 

shown that black mangrove forests in Florida are nitrogen 

limited. When nitrogen was added in the IRL, the black 

mangroves grew out of their dwarf form (Feller et al., 

2003). Addition of N also affected internal dynamics of 

N and P, caused increases in rates of photosynthesis, and 

altered patterns of herbivory (Lovelock and Feller, 2003). 

These fi ndings contrast with results for mangrove forests 

in Belize and Panama where the seaward fringe was Nlimited but the dwarf zone was P-limited. Their studies 

have demonstrated that patterns of nutrient limitation in 

mangrove ecosystems are complex, that not all processes 

respond similarly to the same nutrient, and that similar 

habitats are not limited by the same nutrient when different mangrove forests are compared (Lovelock et al., 2006; 

Feller et al., 2007).

Feller and her colleagues have also studied the effects of the 2004 hurricanes Frances and Jeanne on the 

mangrove communities (Figure 9, bottom). Over the past 

4 years they have continued to monitor and quantify the 

recovery of the mangroves, documenting tree height, leaf 

area index, mangrove type, mangrove defoliation and 

recovery, hydrology, and salinity. Damage to the mangroves was higher in the fringe and transition zones than 

in the dwarf zone. The N-fertilized trees sustained signifi cantly higher damage than controls in all zones and 

have been slower to recover. After 2.5 years, the leaf area 

index (LAI) of P-fertilized and control trees was equal to 

pre-storm levels, whereas N trees were less than 90% 

recovered. LAI again decreased dramatically in January 2007, presumably as the result of an intense 2 year 

drought in Florida.

Dennis Whigham and colleagues from the University 

of Utrecht, The Netherlands Institute for Ecology– Centre 

for Limnology, and the University of South Florida are 

determining the relationships between the structure and 

productivity of different mangrove habitat types and 

hydrological processes and nitrogen cycling, including 

characteristics of the microbial community associated 

with nitrogen cycling. Their hydrological studies have 

shown that there is no evidence of freshwater input from 

groundwater into their study site and that the groundwater chemistry is primarily infl uenced by evapotranspiration. Subsequently, salt pans and dwarf mangrove 

communities develop in areas that are characterized by 

hypersaline conditions associated with evapotranspiraton. Growth rates are lower in the salt pan and dwarf 

mangrove habitats, and preliminary results indicate that 

the microbial community in those habitats differs from 

other habitats.

The studies described above document the morphological, genetic, and biochemical diversity of Florida’s 

marine life. Collectively, these biodiversity and ecological 

studies and investigations of long-term changes in Florida’s coastal waters, including the Indian River Lagoon, 

mangrove ecosystems in Florida, and coral reef habitats 

of southeast Florida and the Florida Keys, give us the 

background essential to document changes in biodiversity 

resulting from human and climatic impacts on Florida’s 

coastal environments.

EDUCATION AND OUTREACH

As a resource for educators, students, researchers, and 

the public, the Marine Station maintains a species inventory of plants and animals in the Indian River Lagoon. 

The Indian River Lagoon Species Inventory website (www

.sms.si.edu/IRLspec) is continually expanding and now includes more than 3,000 species with many photographs 

and scientifi c references. In addition to individual species 

3 6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

03_Paul_025-042_Lang.indd 36 3_Paul_025-042_Lang.indd 36 9/24/09 9:19/24/09 9:19
FIGURE 9. Top: From front to back, Smithsonian Marine Station graduate fellow Juliane Vogt (University 

of Dresden), postdoctoral fellow Cyril Piou, and volunteer Rainer Feller explore the mangrove at Hutchinson 

Island, Florida, looking for light gaps. Bottom: Sharon Ewe (on left) and Anne Chamberlain examine damage 

to the mangroves at Hutchinson Island, Florida, immediately after Hurricane Jeanne.

NUMBER 38 • 3 7

03_Paul_025-042_Lang.indd 37 3_Paul_025-042_Lang.indd 37 9/24/09 9:19/24/09 9:19
3 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

reports that give habitat, distribution, life history, population biology, physical tolerance, and community ecology 

information, the database includes information on nonnative and endangered, threatened, and special-status species. An electronic companion publication to the Species 

Inventory is the Field Guide to the Indian River Lagoon 

(www.sms.si.edu/IRLfi eldguide). Both projects have been 

supported by the Indian River Lagoon National Estuary 

Program administered by the St. Johns River Water Management District. Features such as an interactive glossary, 

enhanced indexing, and links to other relevant websites 

add to the educational value of these websites.

The Smithsonian Marine Ecosystems Exhibit in the 

St. Lucie County Marine Center celebrated its seventh anniversary in August 2008. Administered by the Smithsonian Marine Station, the exhibit showcases the Caribbean 

coral reef ecosystem that was a popular exhibit at the National Museum of Natural History for more than 20 years 

and the fi rst living model of an Atlantic coral reef ecosystem available for public viewing. Through an outpouring 

of local interest and support, the exhibit was transferred 

to Fort Pierce to a building constructed and maintained by 

St. Lucie County for the sole purpose of housing this educational attraction. At the Ecosystems Exhibit, visitors are 

invited to explore six Florida marine habitats and learn 

about the complexity and importance of these ecosystems 

(Figure 10). The largest aquarium houses a Caribbean 

coral reef display. Additional aquaria depict a seagrass bed, 

red mangrove coastline, estuarine and nearshore habitats, 

and a deep-water Oculina coral reef. Smaller aquarium 

displays highlight single species of interest, and a touch 

tank offers visitors personal interaction with various local invertebrates, such as horseshoe crabs, sea urchins, sea 

cucumbers, and peppermint shrimp.

This public aquarium is unlike any other, providing an 

accurate representation of the underwater worlds of the Indian River Lagoon and Atlantic Ocean. Although these waters are a common sight to many coastal Florida residents, 

few have experienced the unsurpassed diversity of life just 

below their surface. By highlighting this diversity and displaying local ecosystems as complex communities of organisms interacting in their environments, the Exhibit aims to 

provide the public with a better understanding of the fragile 

coastal ecosystems of the Indian River Lagoon and the surrounding area, including the impacts people have on them.

The Smithsonian Marine Ecosystems Exhibit is a 

fi eld trip destination for thousands of school-aged children each year (Figure 11). Although some choose a 

self-guided visit, most participate in one of several structured programs facilitated by Education staff members. 

Program options are age- and grade-appropriate and are 

structured in compliance with Florida’s Sunshine State 

Standards. Activities include scavenger hunts, water quality experiments, food web and energy transfer studies, 

simulated benthic sampling, and fi eld experiences in the 

Indian River Lagoon.

In 2005, education staff at the Exhibit began offering community and visitor programs. Ranging from informative breakfast programs to sleepovers and summer 

camps, the new programs target traditional visitor groups 

in new ways, providing more focused and in-depth learning experiences for those interested in taking advantage 

of the many resources the Smithsonian has to offer. The 

enthusiastic response from the community has resulted in 

continual additions to the events calendar.

In addition to being a physical destination for the 

local community, the Ecosystems Exhibit has also established itself as a valuable resource for local schools and 

community organizations that do not have the means to 

travel. Education staff provides classroom outreach programs, bringing the wonders of the underwater world to 

hundreds of students each school year. Education staff 

members have also developed Resource Loan Kits for area 

teachers to borrow for in-classroom use for a two-week 

time period. The Exhibit website also hosts three webcams 

that provide live feeds to three of the Exhibit’s displays. 

Online visitors have alternate, unparalleled views into 

the seagrass and coral reef model ecosystems, as well as 

through the lens of a laboratory microscope. Future plans 

include the development of online curricula and activities 

based on observations made via the webcams.

LOOKING TO THE FUTURE

During the past 37 years the Smithsonian Marine Station at Fort Pierce has developed a strong, broadly based 

program in marine biodiversity research focusing on systematics, ecology, and life histories of marine organisms. 

With nearly four decades of research along the IRL, the 

Smithsonian Marine Station has been able to establish 

long-term and intensive research projects that are valuable 

in understanding and assessing marine biodiversity as well 

as the changes in biodiversity occurring on a global scale. 

As a result of its excellent location, modern facilities, and 

experienced staff, the Marine Station is well positioned 

to continue to address important research topics including global climate change, invasive species, harmful algal 

blooms, systematics, larval ecology, and evolutionary developmental biology.

03_Paul_025-042_Lang.indd 38 3_Paul_025-042_Lang.indd 38 9/24/09 9:19/24/09 9:19
NUMBER 38 • 3 9

The Smithsonian Marine Ecosystems Exhibit makes 

the work of Smithsonian marine researchers accessible to a 

broad, non-scientifi c audience. The living displays capture 

the dynamic quality of natural ecosystems, and the educational offerings are a refl ection of the same. Programs, displays, and live exhibits are constantly changing, evolving, 

and taking on new life, providing a foundation to ensure 

the Exhibit’s future in an ever-changing community.

ACKNOWLEDGMENTS

The authors thank the Hunterdon Oceanographic Research Fund and the Florida Fish and Wildlife Conservation Commission (agreement numbers 05011 and 08017) 

for fi nancial support. We are grateful to the many Smithsonian scientists who provided input about their past and 

ongoing research activities at SMS. Mary Rice provided 

many helpful comments that greatly improved this manuscript. This is Smithsonian Marine Station at Fort Pierce 

Contribution No. 764.

LITERATURE CITED

Buzas, M. A., and L. C. Hayek. 2005. On Richness and Evenness within 

and between Communities. Paleobiology, 31:199– 220.

Buzas, M. A., L. C. Hayek, S. A. Reed, and J. A. Jett. 2002. Foraminiferal Densities over Five Years in the Indian River Lagoon, Florida: 

A Model of Pulsating Patches. Journal of Foraminiferal Research, 

32:68– 93.

Faust, M. A., and P. A. Tester. 2004. “Harmful Dinofl agellates in the 

Gulf Stream and Atlantic Barrier Coral Reef, Belize.” In Harmful 

FIGURE 10. The coral reef at the Smithsonian Marine Ecosystems Exhibit.

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FIGURE 11. Top: A young girl takes a closer look at the inhabitants of the seagrass ecosystem. 

Bottom: Excited children view the nearshore reef ecosystem. 

4 0 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

03_Paul_025-042_Lang.indd 40 3_Paul_025-042_Lang.indd 40 9/24/09 9:19/24/09 9:19
NUMBER 38 • 4 1

Algae 2002, ed. K. A. Steidinger, J. H. Landsberg, C. R. Tomas, 

and G. A. Vargo, pp. 326– 328. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and 

Intergovernmental Oceanographic Commission of UNESCO, St. 

Petersburg, Fla.

Feller, I. C., C. E. Lovelock, and K. L. McKee. 2007. Nutrient Addition 

Differentially Affects Ecological Processes of Avicennia germinans

in Nitrogen Versus Phosphorus Limited Mangrove Ecosystems. 

Ecosystems, 10:347– 359.

Feller, I. C., D. F. Whigham, K. L. McKee, and C. E. Lovelock. 2003. 

Nitrogen Limitation of Growth and Nutrient Dynamics in a Disturbed Mangrove Forest, Indian River Lagoon, Florida. Oecologia 

(Berlin), 134:405– 414.

Hayek, L. C., and M. A. Buzas. 2006. The Martyrdom of St. Lucie: Decimation of a Meiofauna. Bulletin of Marine Science, 79:341– 352.

Hendler, G., J. E. Miller, D. L. Pawson, and P. M. Kier. 1995. Starfi sh, 

Sea Urchins and Allies: Echinoderms of Florida and the Caribbean.

Washington, D.C.: Smithsonian Institution Press.

Littler, D. S., and M. M. Littler. 2000. Caribbean Reef Plants. Washington, D.C.: Offshore Graphics, Inc.

Littler, D. S., M. M. Littler, and M. D. Hanisak. 2008. Submersed Plants 

of the Indian River Lagoon: A Floristic Inventory and Field Guide.

Washington, D.C.: Offshore Graphics, Inc.

Lovelock, C. E., and I. C. Feller. 2003. Photosynthetic Performance and 

Resource Utilization of Two Mangrove Species Coexisting in a Hypersaline Scrub Forest. Oecologia (Berlin), 134:455– 462.

Lovelock, C. E., I. C. Feller, M. C. Ball, B. M. J. Engelbrecht, and 

M. L. Ewe. 2006. Differences in Plant Function in Phosphorusand Nitrogen-Limited Mangrove Ecosystems. New Phytologist, 

172:514– 522.

Ma, H., R. M. Overstreet, J. H. Sniezek, M. Solangi, and D. W. Coats. 

2006. Two New Species of Symbiotic Ciliates from the Respiratory Tract of Cetaceans with Establishment of a New Genus 

Planilamina n. gen. (Dysteriida, Kyaroikeidae). Journal of Eukaryotic Microbiology, 53:407– 419.

Maslakova, S. A., M. Q. Martindale, and J. L. Norenburg. 2004. The 

Vestigial Prototroch in a Basal Nemertean Carinoma tremaphoros (Nemertea; Palaeonemertea). Evolution and Development, 6:

219– 226.

Maslakova, S. A., and J. L. Norenburg. 2008. Revision of the Smiling 

Worm, Genus Prosorhochmus Keferstein, 1862 and Descriptions of 

a New Species, Prosorhochmus belizeanus sp. nov. (Prosorhochmidae, Hoplonemertea, Nemertea) from Florida and Belize. Journal of 

Natural History, 42:1219– 1260.

Paul, V. J., K. E. Arthur, R. Ritson-Williams, C. Ross, and K. Sharp. 

2007. Chemical Defenses: From Compounds to Communities. Biological Bulletin, 213:226– 251.

Paul, V. J., R. W. Thacker, K. Banks, and S. Golubic. 2005. Benthic Cyanobacterial Bloom Impacts the Reefs of South Florida (Broward 

County, USA). Coral Reefs, 24:693– 697.

Rice, M. E. 1981. Larvae Adrift: Patterns and Problems in Life Histories of Sipunculans. Past-Presidential Address. American Zoologist, 

21:605– 619.

— — — . 1989. “Comparative Observations of Gametes, Fertilization, 

and Maturation in Sipunculans.” In Reproduction, Genetics and 

Distributions of Marine Organisms, 23rd European Marine Biology Symposium, ed. J. S. Ryland and P. A. Tyler, pp. 167– 182. 

Fredensborg, Denmark: Olsen & Olsen.

Rice, M.E., J. Piraino, and H. F. Reichardt. 1983. Observations on the 

Ecology and Reproduction of the Sipunculan Phascolion cryptus in 

the Indian River Lagoon. Florida Scientist, 46:382– 396.

Ritson-Williams, R., S. N. Arnold, N. D. Fogarty, R. S. Steneck, M. Vermeij, and V. J. Paul. 2009. “New Perspectives on Ecological Mechanisms Affecting Coral Recruitment on Reefs.” In Proceedings of 

the Smithsonian Marine Science Symposium, ed. M. A. Lang, I. G. 

Macintyre, and K. Rützler, pp. 437–457. Smithsonian Contributions to the Marine Sciences, No. 38. Washington, D.C.: Smithsonian Institution Scholarly Press.

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Katz. 2004. Molecular Phylogeny of Phyllopharyngean Ciliates 

and Their Group I Introns. Journal of Eukaryotic Microbiology, 

51:441– 450.

Schulze, A., and M. E. Rice. 2009. Musculature in Sipunculan Worms: 

Ontogeny and Ancestral States. Evolution and Development, 

11(1):97– 108.

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Caribbean Coral Reef Ecosystems: 

Thirty-Five Years of Smithsonian 

Marine Science in Belize

Klaus Rützler

ABSTRACT. With foresight and tenacity, Smithsonian Institution marine scientists have 

devoted more than three decades to understanding and preserving one of the planet’s vital 

natural resources: the coral-reef ecosystem. In the late 1960s marine scientists from the 

Smithsonian National Museum of Natural History, Washington, founded a long-term 

Caribbean coral-reef fi eld program, now known as Caribbean Coral Reef Ecosystems 

(CCRE), to investigate the biodiversity, community structure and dynamics, and environmental processes that control this ecosystem. Its core group of botanists, zoologists, 

paleobiologists, and geologists found an ideal study site— with high biological diversity, 

signifi cant geological features, and minimal anthropogenic disturbance— on the barrier 

reef off Southern Belize, and in 1972 established a fi eld station on one of its tiny islands, 

Carrie Bow Cay. Within a radius of less than 2 km lie a great variety of richly populated 

habitats, from mangrove to fore-reef. The Belize mainland and three offshore atolls are 

within easy reach by small boat. Each year, up to 120 Smithsonian staff and associated scientists, with assisting students and technicians, study the area’s reefs, nearby mangroves, 

and seagrass meadows. Their “whole-organism” expertise encompasses many fi elds of 

biology— systematics, evolution, paleobiology, ecology, and ecophysiology— supported 

by molecular techniques to expand upon traditional morphological taxonomic analyses. 

An oceanographic-meteorological monitoring station on Carrie Bow Cay records environmental data, now available on the World Wide Web, and monitors the productivity 

of selected reef, mangrove, and seagrass communities. Field research is complemented by 

the large resources of the Smithsonian home base. Today, the CCRE program is a member of the Smithsonian’s Marine Science Network, which includes coastal laboratories in 

Panama, Florida, and Maryland. In these and other respects— CCRE now has more than 

800 papers in print— the program’s accomplishments are indeed impressive.

INTRODUCTION

How does one summarize in a few pages 35 years of research on a complex ecosystem by more than 200 investigators? Clearly, it cannot be done in a 

complete fashion. With apologies for any omissions, I present this review as a 

tribute to every single participant in the Caribbean Coral Reef Ecosystems program (CCRE) dating back to the late 1960s, when it was titled Investigations 

of Marine Shallow-Water Ecosystems (IMSWE). The founders’ unifying objective was to apply a multidisciplinary, long-term team approach to studies of 

marine shallow-water animals and plants, and to examine their interactions in 

Klaus Ruetzler, Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560-

0163, USA (ruetzler@si.edu). Manuscript received 

9 June 2008; accepted 20 April 2009.

04_Rutzler_043-072_Lang.indd 43 4_Rutzler_043-072_Lang.indd 43 9/24/09 9:28/24/09 9:28
4 4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

their environment— today as well as in the past— for information on the determinants of community structure and 

evolutionary change. A coral-reef ecosystem, we agreed, 

is the most extensive and biologically productive shallowwater community on Earth and thus would fully meet our 

purposes. After conducting literature reviews and several 

joint surveys throughout the Caribbean, we chose Belize 

(then British Honduras) as the program’s locale because 

of its pristine environment and high diversity of organisms 

and reef types.

PROGRAM FOUNDERS AND OBJECTIVES

Coral reefs are among the true wonders of the world: 

they cover 190 million km2 of the world’s ocean fl oors, 

are tremendously productive, protect tropical continental 

coasts and islands from the eroding forces of the oceans, 

supply humans with large quantities of high-quality protein, and are a unique recreational resource. For all their 

aesthetic and economic value, coral reefs remain invisible 

to most people unless they live close to tropical coasts 

or engage in skin or scuba diving. Without such contact, 

many are insensitive to the catastrophic effects of pollution and uncontrolled land development, which can rapidly decimate entire communities and thus their benefi ts, 

or are unaware of the effects of natural phenomena such 

as global warming and acid rain.

Fortunately, the unique composition of the Smithsonian Institution, with specialists in many disciplines of the 

life and earth sciences, provided a substantial number of 

researchers interested in reefs and willing to team up for 

the common good of an integrated study. Some experts 

from other institutions were expected to join for specifi c 

tasks. Our original team, all staff of the Natural Museum 

of Natural History (NMNH), consisted of Walter H. Adey, 

Department of Paleobiology, a specialist in fossil and modern coralline algae; Ian G. Macintyre, Paleobiology, a carbonate sedimentologist studying calcifi cation, reef-building 

organisms, and reef evolution; Arthur L. Dahl, Botany, an 

algal ecologist; Mary E. Rice, Invertebrate Zoology, an expert in sipunculan worm systematics and developmental 

biology; Tom Waller, Paleobiology, a malacologist focusing on the systematics and distribution of scallops in time 

and space; Arnfried Antonius, a postdoctoral fellow in Invertebrate Zoology working on stony corals; and myself, 

Invertebrate Zoology, a sponge biologist with an interest 

in reef ecology and bioerosion. We were joined in our early 

search for the optimal research site by David R. Stoddart, 

a geographer at the University of Cambridge, England; 

Porter M. Kier, an actuopaleontologist (later a director of 

the Natural History Museum) looking for modern clues 

to interpreting fossil echinoderm assemblages; Richard S. 

(Father Joe) Houbrick, a former priest turned malacologist and working at the Smithsonian Marine Sorting Center; Ernst Kirsteuer, an invertebrate zoologist specializing 

in nemertine worms at the American Museum of Natural 

History, New York; and Fred Hotchkiss, a postdoctoral 

fellow in Invertebrate Zoology specializing in ophiuroid 

echinoderms. David Stoddart was a particular asset because he had a wealth of research experience with the distribution, geomorphology, terrestrial botany, and dynamics of Belizean islands (cays), having been a member of the 

1959 Cambridge Expedition to British Honduras (Carr 

and Thorpe, 1961) and participant in numerous postHurricane Hattie (1961) surveys (Stoddart et al., 1982).

Our main objective was to study the historical and present conditions in a well-developed coral reef far removed 

from the stressful impacts of an industrial society with a 

view to compiling baseline data on how an established reef 

community adjusts to natural environmental parameters. 

These data would include information on diagenetic alteration of the reef structure, as revealed in drill cores. With 

the resulting information, we hoped to develop a predictive model of the impact of anthropogenic stress. As we 

quickly discovered, most previous reef studies consisted of 

short-term surveys during large-scale expeditions, with superfi cial sampling during a single season; moreover, many 

of the reports on reef fauna and fl ora had been prepared 

by specialists who had never observed the organisms and 

processes in the fi eld. A complex ecosystem such as a coral 

reef obviously required a more rigorous, long-term, and 

multidisciplinary approach if we had any hope of determining the relative importance of diversity, biomass, energy fl ow, and environment to community function.

CARRIE BOW CAY, BASE OF A NEW MARINE FIELD STATION

The team chose a Caribbean reef site for several reasons: most of us had already worked in that area, and it 

would be “close to home,” would permit comparison with 

the already-stressed reefs of Florida, and would minimize 

travel time and cost. Equally important, to be sure, was 

the fact that all the characteristic reef types and zones were 

within workable distance, reef growth was vigorous with 

a good geological record of past development, and the locale was remote from terrestrial and human infl uences.

Moving ahead with small grant awards from Smithsonian Institution endowments, we purchased an infl atable 

boat with an outboard motor, dive tanks, a small compressor, and tents for reconnaissance trips across the Carib04_Rutzler_043-072_Lang.indd 44 4_Rutzler_043-072_Lang.indd 44 9/24/09 9:28

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NUMBER 38 • 4 5

bean. In another step forward, the U.S. National Science 

Foundation provided support for a planning meeting on 

Glovers Reef atoll, Belize, attended by representatives of 

some 40 academic institutions. We envisioned starting up 

the program there and eventually conducting comparative 

studies on an Indo-Pacifi c atoll. As fate would have it, the 

proposal emanating from this meeting was not funded.

Returning to Glovers Reef in February 1972 to retrieve 

our IMSWE equipment from storage, Arnfried Antonius and 

I discovered a small unoccupied islet with three shuttered 

buildings on the southern Belize barrier reef. Its name, we 

learned, was Carrie Bow Cay (16°48N, 88°05W; originally spelled Caye), and it was owned by the family operating the Pelican Beach Motel in Dangriga (Stann Creek 

District), a small town on the mainland (Figures 1, 2). To 

our happy surprise, this reef tract met all our scientifi c requirements, studies there would garner generous cooperation from Belize’s Fisheries Department, and excellent local logistical support would be available. The motel, now 

called Pelican Beach Resort, was owned and operated by 

Henry Bowman, Jr., and his wife Alice. After negotiating 

storage for our equipment, we initiated a contract to lease 

part of Carrie Bow Cay, including the two smaller cottages, for a three-month research period that spring and 

summer.

Carrie Bow Cay was owned by Henry Junior’s father, 

Henry T. A. Bowman, a third-generation descendant of 

Scottish settlers. The enterprising Henry senior was a citrus grower, businessman, and one-time legislator who had 

bought the island from his father as a vacation retreat, 

changed its name (from Ellen or Bird Caye) to Carrie for 

his wife, and put up an old farmhouse that he had bought 

on the mainland and carried out to the cay in sections. 

With his love of fi shing, “Sir Henry” (as I referred to him 

when we became friends) and some of his relatives (daughter Norma and daughter-in-law Alice, in particular) developed a keen interest in the sea and the reef’s myriad 

animals and plants. This interest persuaded him to allow 

us unrestricted access to most of his island and provided 

many opportunities to share our observations over drinks 

during the sunset hour.

A great concern for both of us then, and for all of 

CCRE today, was the rate of coastal erosion, mainly the 

consequence of frequent hurricanes, which had reduced 

the size of the island from 2 acres (0.8 ha) in the 1940s to a 

little more than half that in the 1970s. In his delightful autobiography (Bowman, 1979), Henry took the blame himself, admitting that he had carelessly removed mangrove 

trees “that build and bind these cayes.” At the same time, 

he did make a signifi cant contribution to the island’s morphology: in 1942 he built a 27 m long concrete boat dock 

on the leeward (lagoon) side. It has remained unchanged 

to this day and has served as a reference in our mapping of 

the geomorphology and communities nearby.

Since then, both Henrys have passed away, but their 

naturalist spirit lives on. Therese Rath, who is Junior and 

Alice’s daughter (Sir Henry’s granddaughter), runs Pelican 

Beach with her mother and continues to offer us logistical 

support on Carrie Bow. Therese’s husband, Tony Rath— 

one of our early volunteer station managers who moved to 

Dangriga from Minnesota two decades ago— is a successful nature photographer and runs the premier web design 

business in Belize; he still helps us out as a naturalist adviser and provides documentary photography.

FACILITIES AT START-UP

Between 1972 and 1975, our team operated on a 

shoestring. The relatively small grants available to us 

(the Smithsonian has no direct access to National Science 

Foundation funding) kept the fi eld station open for no 

more than four months a year and supported up to 25 

scientists and assistants per season. Our facilities consisted 

of a small three-room building with a tin roof to the south 

of the main house (it contained our lab, living quarters for 

two, and a kitchen); a 4 m2 shed that could house two; and 

a tent, when needed, that could accommodate up to six. 

The dive compressor and a small generator were installed 

in improvised shelters.

Our shower consisted of a spray-head on a pipe 

screwed into the bottom of a huge wooden vat that collected rainwater running off the roof of the main building. To preserve decency, there was an enclosure (its sign 

read: “Save Water, Shower with a Friend”). The toilets for 

all island occupants were two outhouses accessed from a 

wooden pier extending over the reef fl at to the island’s 

east. The cabin’s seats were rough-cut planks with holes. 

However, its window opening allowed a spectacular view 

of the reef fl at, barrier reef, and unobstructed horizon, 

with pelicans and 1 m long parrotfi sh jumping and feeding in the foreground.

After getting used to us, Sir Henry turned his children’s “museum” in the main house into a station manager’s quarters by adding some wood siding for walls and 

a door. It was a roofed-over corner of the house’s wide, 

upper-level porch, where Norma and Alice had kept and 

displayed an assortment of shells, corals, quirky driftwood, and stranded and mummifi ed algae, invertebrates, 

and fi shes. Working for a museum ourselves, we found 

that a quaint step forward.

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FIGURE 1. Map of research area in coastal Belize, Central America. The barrier reef and other reef tracts appear in pink.

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NUMBER 38 • 4 7

FIGURE 2. The original Investigations of Marine Shallow-Water Ecosystems (IMSWE) survey team, the Belize barrier reef, and Carrie Bow 

facilities in the early 1970s. Upper left: The team included (left to right) Walter Adey, Arthur Dahl, Tom Waller, Klaus Ruetzler, and Arnfried 

Antonius (missing from the picture are Porter Kier, Ian Macintyre, and Mary Rice). Upper right: Belize barrier reef looking south, with South 

Water Cay in foreground and Carrie Bow Cay near center. Center left: Carrie Bow Cay looking southwest, with ocean-side reef fl at in foreground. Center right: Carrie Bow facilities looking south, the Bowmans’ “Big House” to the right and our lab building in the center. Lower left: 

Photographer Kjell Sandved working in the aquarium area. Lower right: Scientists in the lab are Anne Cohen (left) and Jim Thomas.

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4 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

For the “lab,” we removed some of the cottage partitions that originally defi ned the bedroom space for the 

parents and three children, built a long bench along the 

oceanfront wall with a supply cabinet and photo table 

opposite it, and weatherproofed windows by inserting acrylic panes in the lower half to allow the wooden 

shutters to remain open under most weather conditions 

and thus let in more light. The sun gave us light for microscopy and photography, with a couple of small gasoline-driven generators doing the job whenever needed. 

We brought microscopes, cameras, some portable instruments, labware, and boating and dive gear from 

home but improvised on most additional laboratory or 

fi eld needs. Our original IMSWE infl atable boat and 25 

horsepower outboard engine were still in working order, 

supplemented by a similar infl atable recently added. A 

shortwave radio provided contact with Pelican Beach in 

Dangriga for ordering supplies, brought out once a week. 

A local cook prepared our meals and lived in a room 

under the big house; next to her was the simple residence 

of a native fi sherman who served as caretaker and watchman, particularly when the island was deserted during 

the off-season. Our station manager was usually one of 

us, or one of our enthusiastic young museum technicians, 

or some other volunteer with technical know-how. When 

the lab was closed, all valuables were stored in high 

places (in case of storm fl oods), the windows shuttered, 

and the door padlocked and nailed to its frame. (“This,” 

the locals said, “does not keep the crooks out but keeps 

the honest people honest.”) During hurricane season, all 

major equipment was taken to Dangriga and stored in 

the Maya Hut behind Pelican Beach.

ANALYZING A COMPLEX ECOSYSTEM

THE EARLY YEARS

The program’s fi rst targets were to map the reefs and 

other habitats near the fi eld station, including Carrie Bow 

Cay itself, and to identify the key organisms in the communities (Figures 3, 4). Because the north– south-oriented barrier reef is the dominant feature separating the lagoon from 

open ocean, we established a transect perpendicular to its 

trend, originating well inside the lagoon in a seagrass bed 

2 m deep; it then crossed the barrier-reef crest some 150 m 

north of Carrie Bow and extended due east across the reef 

and down the fore-reef slope to a depth of 30 m. This transect would become the baseline reference for all our topographic studies and future observations and experiments.

We also tried to develop some standard methods of 

sampling, extracting interstitial organisms, and determining biomass (Dahl, 1973; Macintyre, 1975; Rützler, 

1978a). Because of the complexity of the reef framework 

(with its three-dimensional structure) and the diversity 

and size range of its inhabitants (which varied by at least 

three orders of magnitude), we had to modify many of the 

commonly used ecological methods to ensure compatible 

results.

Unable to employ self-contained recording instruments to monitor important environmental parameters, 

we established a manual routine for taking tide and temperature readings, and for observing solar radiation, wind 

speed and direction, precipitation, humidity, cloud cover, 

wave action, and turbidity with simple handheld devices. 

For specifi c projects, we measured salinity, oxygen concentration, pH values, water current speed, and submarine 

daylight with off-the-shelf instruments for which we built 

waterproof housings when necessary. These data, along 

with the fi rst reef maps and results from transect surveys, 

were summarized in our 1975 progress report and distributed to program participants and supporters.

Many colleagues helped identify key organisms and 

determine biomass and spatial and temporal distribution 

(Adey and Macintyre, 1973; Kier, 1975; Pawson, 1976). 

Early on, we discovered unexpectedly high numbers of 

new species in almost all taxa, which was surprising because the Caribbean Sea is generally considered among the 

best-studied oceanic regions of the world. Using in situ 

methods, we identifi ed and quantifi ed environmental parameters such as light, water fl ow, and sediments making 

up the “microclimate” of particular organisms (Graus and 

Macintyre, 1976). We also investigated important associations and interactions between organisms, such as symbioses and space competition, predation, diets, and behavioral 

patterns. In addition, we measured primary production of 

benthic macroalgae and symbiotic microalgae, and growth 

and reproduction rates of reef-forming organisms, the fi rst 

steps toward determining key metabolic processes (Macintyre et al., 1974).

Some geologists and biologists collaborated in the 

study of geological processes such as the construction and 

destruction of the coral-reef framework and the calcifi cation rates of corals, coralline algae, and other bioherms. 

Others studied physical and biological erosion and sediment production rates (Rützler, 1975), sediment sorting 

and colonization by meiofauna, and processes of recementation. Ian Macintyre initiated a drilling project with colleagues from the U.S. Geological Survey’s Energy Resource 

Division to learn about the historical development of the 

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NUMBER 38 • 4 9

FIGURE 3. Some early program participants. Clockwise, from top left: Ian Macintyre about to enter the submarine Colombus Cay Cave; 

Arnfried Antonius setting up time-lapse camera for study of black band coral disease; Klaus Ruetzler catching the evening sun for a microscope 

examination; view of entrance of station; Mike Carpenter fi xing an underwater viewer; Joan Ferraris measuring oxygen consumption of benthic 

community on the Carrie Bow reef fl at; and Ilka Feller surveying red-mangrove insects at Twin Cays.

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FIGURE 4. Principal marine habitats near Carrie Bow Cay. Top row: left, patch reef near the south tip of the island; right, barrier reef

crest composed of elkhorn and fi re coral (Acropora, Millepora). Middle row: left, outer fore-reef with corals, sponges, and gorgonians; 

center, small cave in the fore-reef framework; right, seagrass stand in the barrier-reef lagoon. Bottom row: left, red mangrove at Twin 

Cays, with Carrie Bow Cay in the background; center, gorgonian and barrel-sponge community on the outer fore-reef; right, diver on 

the fore-reef slope.

5 0 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

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barrier reef. Cores from a series of holes yielded information on past community patterns and successions as well as 

the distribution of contemporaneous submarine cements 

within the reef structure (Macintyre et al., 1981).

Detailed maps and inventories of terrestrial plants on 

several Belizean cays, including Carrie Bow, from 1960, 

1962, and 1972 (see Stoddart et al., 1982) aided in our 

observation of morphological and fl oral changes, particularly in relationship to the frequent hurricanes in the region. In 1974, only two years into our presence on Carrie 

Bow, Hurricane Fifi , which destroyed large coastal areas of 

Honduras, hit the barrier reef just south of our island. Although our reef habitats experienced only minor changes, 

primarily local breakdown of the framework and accumulation of rubble, most terrestrial life on Carrie Bow, particularly vascular plants, was killed by fl ooding— except 

for coconut trees, which suffered about a 20% loss (16 

trees)— and there was severe coastal erosion. Upon remapping the island in the wake of this event, we noted some 

redepositing of beach sand and recolonization by plants 

through drift and windblown seeds.

GAINING MOMENTUM

Our venture took a signifi cant step forward with the 

award, in 1975, of an annual grant by the Exxon Corporation from the company’s public relations budget for 

Central America. Although relatively small, the funds 

nearly doubled our support and had no strings attached, 

except they were to be dedicated to Caribbean coral reef 

research. Added to this welcome development was a new 

and benefi cial relationship with Captain Graham Thomas 

of the Royal Signals Detachment in Belize, a helicopter 

pilot detailed to support the training of British forces in 

jungle environments. Graham was able to equip his helicopter with an aerial camera and take vertical pictures of 

the Carrie Bow reefs that provided excellent photo coverage for a detailed mapping of the area’s reef structures at 

a scale of 1:800 and to a depth of 10 m. This information constituted enormous progress over available nautical charts (with a scale of 1:125,000) that dated back to 

British surveys in the 1830s and were only partly updated 

in the 1940s. Even greater resolution in aerial mapping 

(but at the expense of areal coverage) was achieved by introducing a helium weather balloon equipped with a remotely operated camera. This technique (Rützler, 1978b), 

like several others devised by our team, was documented 

in a volume on coral reef research methodology sponsored 

by the United Nations Educational, Scientifi c and Cultural 

Organization (UNESCO) (Stoddart and Johannes, 1978).

In 1977, in association with the Third International 

Symposium on Coral Reefs in Miami, several of our team 

organized a well-received fi eld trip to Belize, highlighted 

by a detailed fi eld guide based on maps, transect data, and 

aerial and underwater habitat photographs emanating 

from the program (Miller and Macintyre, 1977). In short 

order, the program launched several new projects (Figure 5) to investigate the fate of siliceous skeletons in the 

calcium carbonate environment of the reef (Rützler and 

Macintyre, 1978), the feeding behavior of scyphomedusae (Larson, 1979), and the systematics of the unexpectedly diverse ostracod crustaceans (Kornicker and Cohen, 

1978). Other innovative and pioneering work focused on 

the fi ne structure of bivalve anatomy as revealed through 

scanning electron microscopy (Waller, 1980) and, with 

collaborators from the Scripps Institution of Oceanography, on the chemistry of marine plant and invertebrate 

secondary metabolites that showed promise as antibiotics 

or other therapeutical substances (Kokke et al., 1979). By 

the end of 1978, more than 50 papers had been published 

or were in press to document the biology, ecology, and 

geology of the Belize barrier reef in the vicinity of Carrie 

Bow Cay.

The program’s success appeared to be short lived, 

however: in late September 1978, Hurricane Greta passed 

across the Belize barrier reef just 6 km north of Carrie 

Bow. Four lives were lost in Dangriga, the citrus harvest in 

the valley to the west was destroyed, and there was heavy 

beach erosion at Pelican Beach Motel. Although no members of our group were on location because we had closed 

down for the season, part of our equipment was damaged 

when ocean storm surge and rain fl ooded the storage area. 

Storm waves from the east and strong backlashing winds 

from the northwest caused severe erosion of beach sand 

on Carrie Bow and wiped out some 30 coconut trees, the 

small house, and the outhouses. The ocean-side wall of the 

laboratory building also caved in, exposing equipment and 

supplies to saltwater spray. Following the storm, visibility 

in the usually very clear ocean water remained at less than 

3 m for two weeks, most elkhorn (Acropora palmata) and 

fi re coral (Millepora complanata) near the reef crest was 

reduced to rubble, and the salinity in the lagoon dropped 

from the usual 35‰ to 25‰.

Despite this setback, we decided to press our team 

and collaborators to complete work in progress and prepare a state-of-the-art summary of our accomplishments. 

The resulting volume (Rützler and Macintyre, 1982), later 

known as the Blue Book (for the color of the hard cover), 

became a platform for the next phase of investigations, as 

well as for raising funds. The fi rst section presented a 

NUMBER 38 • 5 1

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5 2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 5. A few examples of research activities of the 1970s to 1980s. Clockwise, from top left: boat operator Frank (Pelican Beach Resort) 

helps Ron Larson to lower plankton net from the stern of the boat; Ian Macintyre’s group drill-coring down a sand groove on the fore-reef; 

Joan Ferraris (left) tending incubation chambers to measure temperature-salinity tolerance of invertebrates and Sara Lewis preparing aquaria 

for fi sh herbivory experiments; Sara measuring algal abundance in a quadrat frame on the reef fl at; Klaus Ruetzler retrieving trace paper from 

tide recorder on Carrie Bow dock; Mark and Diane Littler’s team assessing effects of nutrients on algal growth.

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NUMBER 38 • 5 3

detailed overview of the physical and biological environment of our study site— its habitats and community structure, geological history, tides, water currents, climate, and 

terrestrial conditions— compiled by Ian Macintyre and 

myself and various outside collaborators, including Björn 

Kjerve (University of South Carolina, Colombia), Joan Ferraris (Mount Desert Island Biological Laboratory, Maine), 

and Eugene Shinn (U.S. Geological Survey, Miami). The 

next section focused on the benthic and planktonic communities— the carbonate microborers, micro- and macrobenthos, zooplankton, and the populations of a large 

submarine cave at nearby Columbus Cay— and their productivity. The principal collaborators were Joan Ferraris, 

Paul Hargraves (University of Rhode Island, Kingston), 

Jeffrey May (Rice University, Houston), and David Young 

(Department of the Navy, Mississippi). A section on biodiversity included many important groups of reef organisms, 

notably the algae and seagrasses (James Norris, NMNH), 

hydroids (Barry Spracklin, University of New Hampshire, 

Durham), medusae (Ronald Larson, a former NMNH 

technician who moved on to the University of Victoria, 

Colombia), stony corals (Stephen Cairns, NMNH), octocorals (Katie Muzik, postdoctoral fellow, NMNH), sipunculan worms (Mary Rice, NMNH), crustaceans and 

pycnogonids (Brian Kensley, Allan Child, NMNH), and 

echinoderms ( Frederick Hotchkiss, postdoctoral fellow, 

NMNH; Bradford Macurda, Jr., University of Michigan, 

Ann Arbor). The most unusual discovery was that chironomid insect larvae, caught in emergence traps, are part of 

the offshore benthic community and live in fore-reef sand 

bottoms to depths of 30 m (Gernot Bretschko, Biological 

Station Lunz, Austria). A section on species interactions 

and responses to the environment addressed chemical defense in algae (James Norris), the life history and ecology 

of cnidarians (Ronald Larsen), growth patterns of reef 

corals (Richard Graus, NMNH), sponge– zoanthid associations (Sara Lewis, Duke University, Durham), bivalve 

larval settlement (Thomas Waller, NMNH), and resource 

partitioning in chaenopsid, coral-associated fi shes (David 

Greenfi eld, Field Museum of Natural History, Chicago). 

The concluding chapter puts Carrie Bow Cay and its reefs 

in the larger context of the Belize barrier reef complex 

(contributed by Randolf Burke, North Dakota Geological 

Survey, Grand Forks, and David Stoddart).

Having overcome many of the start-up problems, 

including setbacks caused by the hurricanes, we forged 

ahead in the new decade with increasing productivity and 

innovation. CCRE members authored a number of important monographs and other reports on reef biodiversity. 

We started a series of papers on the fungi (Kohlmeyer, 

1984) and algae (Littler and Littler, 1985); prepared analyses of several large crustacean groups, including parasitic 

copepods on fi shes (Cressey, 1981), decapods (Kensley 

and Gore, 1981), isopods (Kensley, 1984), and amphipods 

(Thomas and Barnard, 1983); and published the fi rst survey of local moss animals, bryozoans, by a colleague then 

at the American Museum of Natural History in New York 

(Winston, 1984).

We also conducted a series of day and night plankton 

tows over the fore-reef and over lagoon seagrass bottoms, 

which were surprisingly devoid of larval stages of some of 

the area’s common animals, such as an assortment of cnidarians and sponges. We speculated that the larvae might 

be swimming close to or within the reef framework, where 

our boat-towed nets could not be operated, and decided to 

tow or push the plankton nets by hand, while swimming 

close to the bottom. Although more successful, this technique took time and effort to obtain suffi cient samples. 

Eventually, we hit on the idea of building a stationary 

net supported by a frame that could be placed close to or 

among the coral heads or branches. For locations without 

strong directional currents, we added a waterproof electric motor with propeller and a fl ow meter to measure the 

volume of water that passed through the net. This setup 

ultimately produced excellent samples of great diversity 

considerably beyond the composition of plankton tows by 

boat (Rützler et al., 1980).

Having a small budget and intent on disturbing our 

study environment as little as possible, we sought creative 

fi eld and laboratory techniques that would not require 

sophisticated instrumentation or climate control. In keeping with these goals, our colleague Sara Lewis, for one, 

completed the experimental fi eldwork for her entire dissertation on fi sh herbivory on the Carrie Bow reef fl at, 

just a few meters east of the lab building (Lewis, 1986). 

Some of our Museum’s phycologists experimented with 

the infl uence of algal growth forms on herbivores at the 

same location (Littler et al., 1983). Ecophysiological work 

on temperature and salinity tolerance of polychaetes and 

other reef invertebrates was accomplished in situ and with 

simple, specially designed acrylic incubation chambers 

(Ferraris, 1981; Ferraris et al., 1989). Submarine cementation processes were determined experimentally in the karst 

cave habitat of Columbus Cay (Macintyre, 1984). Benefi ts 

of algal symbionts to sponge hosts were explored by in situ 

trials on a nearby patch reef (Rützler, 1981). And, with an 

innovative underwater time-lapse camera with strobe light 

borrowed from its inventor, Harald Edgerton at the Massachusetts Institute of Technology, we recorded several 

unattended day– night activities on the reef, including the 

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5 4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

nocturnal feeding behavior of basket stars (Astrophyton) 

(Hendler, 1982).

During reef surveys in the early phase of our program, 

we were already seeing a number of dead or damaged corals with no clear sign of the common physical impacts 

related to storms or boat anchors. Our postdoctoral fellow Arnfried Antonius pioneered these observations at 

Carrie Bow and elsewhere in the Caribbean, as well as 

in the Indo-Pacifi c (Antonius, 1982). One notable feature 

of many of these fl agging corals was a black line between 

live coral tissue and recently dead (white) skeleton. During 

collaborative studies, we determined that the black band 

consisted of a mat of entangled fi lamentous cyanobacteria, 

with a number of associated microbes, and that the photosynthetic bacteria had an appetite for coral tissue, thereby 

causing what has been called “black band disease” (Rützler et al., 1983).

OCEANIC MANGROVE SWAMPS

Anyone looking through our 1982 “Blue Book” will 

notice that mangroves are barely mentioned, except for a 

few remarks about Twin Cays, a mangrove island in the 

lagoon just over 3 km northwest of Carrie Bow (Figure 6). 

This lack should not be taken as a sign of little interest. 

CCRE workers have in fact been highly impressed by the 

relatively clear (for a swamp) water in the tidal channels 

and the rich fl ora and fauna, particularly the sponges, covering the stilt roots of red mangrove (Rhizophora mangle).

On an earlier visit to a very similar mangrove island, East Bimini in the Bahamas, I had been so struck 

by its subtidal diversity that it seemed an ideal community for multidisciplinary study. The “discovery” of Twin 

Cays during the early 1980s rekindled this interest, and 

coincidentally our Exxon supporters indicated that they 

wanted to diversify their generosity in Central America 

beyond coral reef research. We therefore submitted a new 

proposal to their open competition for the comprehensive study of a Caribbean mangrove ecosystem at Twin 

Cays. A factor in our favor was that oil pollution caused 

by tanker ballast-water discharge or wrecks was affecting Caribbean beaches and reefs at that time. Indeed, a 

colleague and I had studied the effect of such an oil spill 

at Galeta Island, Caribbean Panama, a decade earlier and 

found that the subtidal reef corals were barely affected by 

the spill but that the oil slick had caused severe damage 

to the nearby intertidal mangrove community (Rützler 

and Sterrer, 1971). Our proposal won another fi ve years 

of research grants, and we named our initiative SWAMP 

(Smithsonian Western Atlantic Mangrove Program). This 

support was supplemented by internal grants for specifi c 

purposes, notably Fluid Research Funds travel awards, a 

Scholarly Studies grant for mangrove research, a Smithsonian Associates Women’s Committee award for scientifi c 

illustration, W. R. Bacon Scholarships (for external collaborators), Seidell Funds for library enhancements, and 

National Science Foundation grants to outside collaborators (who were to some extent also supported by their 

home institutions).

Because mangroves are tidal communities with terrestrial, intertidal, and subtidal components, we could expand 

our fi elds of interest, adapt our methods to the new environment, and add a number of disciplines to our study that 

are not usually applicable in the subtidal reef environment 

(Rützler and Feller, 1988; Figure 7). With a wider biodiversity horizon, we could now conduct surveys of microbes, 

fungi, algae, sponges and their endofauna, polychaetes, 

crustaceans, echinoderms, and bryozoans. We were fortunate to have a rare expert on the quantitatively important 

ascidian tunicates join us at this time, Ivan Goodbody of 

the University of the West Indies, Jamaica. Our team also 

explored the geological history of the mangrove by coring 

through massive peat accumulations and dating the different horizons and also initiated terrestrial studies of the 

mangrove’s lichens, insects, spiders, reptiles, and birds.

An important fi rst step was to explore and map Twin 

Cays and name the many bays, ponds, creeks, mud fl ats, 

and lakes and give them coordinates (before Global Positioning System [GPS] devices were available) that would 

allow us to relocate research sites. We also wanted to garner more interest in the mangrove ecosystem, but because 

swamps tend to be viewed as undesirable environments, 

it took considerable effort to win over our sponsors, local 

hosts, and even many colleagues. Good photography was 

a decided help, but even the best pictures convey but a tiny 

segment of a process in nature, although they are absolutely 

necessary for documenting shapes, expressions, or colors, 

of course. To depict the entirety of, say, an animal– plant 

association, we needed to capture the obvious and the hidden, the large and the small (in proper detail and perspective), and the dynamics of day versus night— in a word, we 

needed to combine art with science. We did just that in a 

new project called Art in a SWAMP (Figure 8). The lead 

artist was Ilka (“Candy”) Feller, a contract illustrator at 

the time with vast experience in the fi elds of botany and 

entomology, having worked with numerous colleagues in 

those departments in our Museum over many years. Candy 

not only employed her artistic talent in the illustration of 

mangrove communities, but she was so captivated by the 

entire ecosystem that she resumed academic studies (after 

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NUMBER 38 • 5 5

FIGURE 6. Twin Cays mangrove habitats. Clockwise, from top left: the island viewed southwest toward Carrie Bow Cay and the barrier reef;

mangrove fringe lining the Main Channel; sponge clusters in one of the tidal channels supported by red-mangrove stilt roots; diverse community 

of sponges and ascidians on a root substrate; a newly discovered and described sponge (genus Haliclona) anchored on and in the mangrove-peat 

bank that lines many channels; juvenile barracuda hiding among mangrove roots; a snorkeler exploring Hidden Creek, which connects a shallow mangrove lake with the open Main Channel.

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NUMBER 38 • 5 7

FIGURE 7. (facing page) Examples of projects initiated at Twin Cays. Clockwise, from top left: mapping and exploring team landing on the western shore; our weather station erected in a large tidal mud fl at; scientifi c illustrator Mary Parrish sketching mangrove communities; Molly Ryan 

photographing community samples returned to the lab at Carrie Bow for one of her scientifi c illustrations; student volunteer helping to collect 

specimens; ichthyologists Will Davis and C. Lavett Smith comparing catches; Ilka Feller measuring salinity in Hidden Lake, the location of one 

of her mangrove fertilization and growth experiments; Ian Macintyre, with Ilka, dissecting termite nest during an exploration of the mangrove’s 

interior.

having raised two daughters), completed a dissertation on 

the Twin Cays mangrove, and became one of the foremost 

mangrove ecologists working on communities between 

Florida and Brazil and as far away as Australia and New 

Zealand. Other artists on the project were Mary Parrish, 

fi rst a staff member in my department and now illustrator 

in the Department of Paleobiology; Molly Kelly Ryan, Invertebrate Zoology staff illustrator; and Jennifer Biggers, 

then my contract research assistant and illustrator. This 

team, along with Paleobiology’s Ian Macintyre, Natural 

History Museum photographer Chip Clark, Invertebrate 

Zoology technician Mike Carpenter, and several more associates and volunteers engaged in detailed surveys and 

mapping of Twin Cays geomorphology and in analysis and 

graphic reconstruction of habitats and communities, ranging from epiphytic sponges to intertidal algae– invertebrate 

associations to red mangrove– insect interactions, and an 

entire mudfl at population (Rützler and Feller, 1996).

Our growing familiarity with mangrove organisms 

raised a number of signifi cant ecological and behavioral 

questions concerning the composition and ecology of 

fl oating cyanobacterial mats (addressed by Maria Faust 

in the Department of Botany; Faust and Gulledge, 1996) 

and herbivory in macroalgal communities (investigated 

by Mark and Diane Littler and colleagues; e.g., Littler 

et al., 1983). A rare immune disease was discovered in 

a sponge (Rützler, 1988) in which the usually benefi cial 

microbial symbionts turn against their host. The dynamics 

and behavioral patterns of swarming copepod crustaceans 

among mangrove roots were investigated by Frank Ferrari, Invertebrate Zoology, and colleagues (Buskey, 1998; 

Ferrari et al., 2003). Also, new work was done on invertebrates living in complex burrows in the sediment substrata 

of mangrove channels (Dworschak and Ott, 1993), and on 

the importance of mangroves for the recruitment and protection of commercial species such as spiny lobster (Acosta 

and Butler, 1997). In research on another puzzling question— the role of sponge cyanobacterial symbionts in both 

mangrove and reef nutrient cycling— it was shown that 

nitrogen fi xing by bacteriosponges is indeed an important 

input to the community (Diaz and Ward, 1997). With the 

new emphasis on the biology of the Twin Cays mangrove, 

Ian Macintyre applied geological techniques over several 

years to reveal its biological history: using a portable vibracore, he mapped and carbon-dated the subsurface layering of peat, sand, and rubble, all the way to Pleistocene 

level (Macintyre et al., 2004b).

As our fi nancial situation improved, we were able to 

address the bothersome problem of coping without automated instrumentation for continuous monitoring of basic meteorological and oceanographic parameters. Up to 

then we had documented the tidal regime at Carrie Bow 

Cay with a pressure sensor (Kjerfve et al., 1982) and relied on various borrowed or leased instruments to meet 

the needs of specifi c projects for monitoring water currents, temperature, solar radiation precipitation, or wind 

(Greer and Kjerfve, 1982; Rützler and Ferraris, 1982). 

None of these improvised methods provided long-term, 

reliable records even if we were on site. With the help of 

contract engineer George Hagerman, we adapted a leased 

Anderaa (Bergen, Norway) automatic weather station for 

our purposes and installed it on a massive, elevated wood 

platform in an extended tidal mud fl at to the north of 

Twin Cays. This setup provided us with continuous data 

for several years until it became outdated and fell victim 

to vandalism.

CARIBBEAN CORAL REEF ECOSYSTEMS:

A BREAKTHROUGH

In the early 1980s, Richard Fiske, then Director of 

the National Museum of Natural History, asked for proposals that would interest our sponsors in the U.S. Congress, who at that point appeared to favor the expansion 

of promising research already in progress. To our surprise, 

the Museum received an increase to its budget base for 

the study of Caribbean Coral Reef Ecosystems beginning 

in 1985. Modeled on the IMSWE-SWAMP initiatives, the 

CCRE program encompassed reef, mangrove, seagrass, 

and plankton communities, with a primary focus on the 

Carrie Bow Cay region.

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5 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 8. Examples of illustrations of mangrove swamp communities. Clockwise, from top left: characteristic intertidal red algal cover (Bostrychietum) on red-mangrove prop root, with mangrove oyster, mangrove crab, and periwinkle; tidal mudfl at showing developed red-mangrove 

seedlings, black-mangrove pneumatophores, driftwood, and a marbled godwit; cut-away view of mangrove channel bottom showing characteristic benthic organisms including decapod burrowers; close-up of peat-bottom community with algae, fallen mangrove leaves, sea anemone, 

and sabellid tube worms.

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NUMBER 38 • 5 9

Under a new administrative structure approved by 

Director Fiske, CCRE would be governed by a steering 

committee chaired by me and composed of representatives of different departments and disciplines, including 

outside advisers. Marsha Sitnik, who worked with all the 

Museum’s interdepartmental biodiversity initiatives, became program administrator. Now we could afford the 

important position of operations manager, fi lled by Mike 

Carpenter, who serves as fi eld station logistics director and 

has trained and supervised our volunteer station managers, each of whom typically spends three to six weeks at 

Carrie Bow Cay.

The new funding allowed us to lease all of Carrie 

Bow Cay year round and remodel the big house for muchneeded dry-lab space for instruments, a library, computer, 

and additional living accommodations. We built a separate, sound-insulated compressor-generator shed, added 

propane gas refrigerators to kitchen and labs, and improved radio-communication and other safety features for 

boating and diving. New equipment included microscopes, 

balances, centrifuge, and other analytical equipment. We 

also upgraded our weather station with real-time data access and connected it with the Belize Meteorological Offi ce, which had no offshore monitoring facility. Even more 

important, we had a modest budget for travel stipends to 

attract outside collaborators to work on organisms or disciplines not covered by Smithsonian staff scientists.

At the end of the fi rst CCRE program year, our publication list exceeded 200 entries. Several of the projects 

mentioned earlier were continued or completed and new 

ones begun with like-minded colleagues whose expertise 

fi lled the gaps in our experience. To name a few of these 

projects, some focused on the control of reef zonation by 

light and wave energy (Graus and Macintyre, 1989), the 

taxonomy and ecology of hydroids (Calder, 1991), oligochaete worms (Erséus, 1988), mysid crustaceans (Modlin, 

1987), and ascidians (Goodbody, 1995); the predation 

and feeding ecology of sponges (Wilkinson, 1987), echinoderms (Aronson, 1987), and fi shes (Wainwright, 1988); 

the ecophysiology of invertebrate– bacterial symbiosis 

supporting life in hydrogen sulfi de environments (Ott and 

Novak, 1989; Ott et al., 1991) and mangrove-tree metabolism (McKee et al., 1988); and island groundwater 

hydrology (Urish, 1988).

In 1988 we held a workshop at the Calvert Marine 

Museum in Solomons, Maryland, to review the accomplishments and gaps in our research on the Twin Cays 

mangrove ecosystem. Close to 40 program participants 

summarized the progress of their work on internal structure, development over time, sedimentology, meteorology, 

hydrology, vegetation, productivity, nutrient cycling, 

temperature-salinity tolerance, and biodiversity of fauna 

and fl ora from microbes to amphibious fi shes. The most 

obvious defi ciencies were in oceanography, a number of 

important organism groups such as mollusks and fi shes, 

and marine benthic and terrestrial ecology. One of the 

highlights was a report on a complementary team study of 

the Holocene geological history, peat composition, and terrestrial and marine vegetation of Tobacco Range, another 

large mangrove island about 3.5 km north of Twin Cays 

(Littler et al., 1995). This atoll-like range drew CCRE’s attention when a large area of fractured and slumped fossil 

peat was discovered off its west shore.

At a subsequent planning workshop in Jamaica, CCRE 

established a protocol for studies at Twin Cays and Carrie 

Bow Cay. This initiative, called Caribbean Coastal Marine 

Productivity (CARICOMP), calls for simple but universally applicable methodologies in the monitoring of major 

oceanographic parameters and health of the Caribbean’s 

principal communities. To this end, we established representative plots and transects in mangrove, seagrass meadow, 

and fore-reef, which are being evaluated yearly for changes 

in structure and productivity, while climatic factors are determined on a weekly basis (Koltes et al., 1998).

As our scientifi c drawing and photography of swamp 

communities gained scientifi c importance and aesthetic 

value, we were invited display some of this work to the 

public at the Smithsonian’s S. Dillon Ripley Center in an 

exhibition titled “Science as Art.” It included a video documentary on mangrove swamp biology, produced in collaboration with colleagues from the University of Vienna 

(Joerg Ott and Alexander Bochdansky). The video also 

served as a teaching aid in an annual educational workshop for Belize high school teachers, conducted by Candy 

Feller and Marsha Sitnik in collaboration with the Belize 

Fisheries and Forestry departments and titled “Mangrove 

Conservation through Education.” This was a timely 

workshop, indeed: our research area at Twin Cays was 

showing the fi rst signs of anthropogenic stress in response 

to tourist visitation, garbage dumping, vandalism (of our 

weather station and boat dock), and the clear-cutting of 

mangrove trees to gain land for development. These developments had a particularly adverse impact on Candy 

and her colleagues, whose work on mangrove plant ecology required extended undisturbed natural conditions to 

single out parameters (nutrients, in particular) that enhance or impede growth (Feller, 1995; Feller et al., 1999). 

Fortunately, at our urging, Belize’s Forestry and Natural 

Resources Departments helped slow the disturbances and 

started work on a conservation plan for the South Water 

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6 0 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Cay Marine Protected Area (MPA) that would include 

Carrie Bow and Twin Cays.

Side-tracked by the discovery of the Pelican Cays 

biodiversity hotspot (see the next section), the impact 

of a hurricane, and coral bleaching events, we were unable to convene another Twin Cays symposium until 

2003. Meeting at the Smithsonian Marine Station in Fort 

Pierce, Florida, we found our mangrove program had accumulated enough scientifi c results not only to fi ll a volume of multidisciplinary papers but also to demonstrate 

changes in the structure of the ecosystem over a span of 

two decades (Macintyre et al., 2004a). Articles on geological history and sedimentary conditions were spearheaded by Ian Macintyre and those on aquatic ecology 

by Rütz ler and colleagues. Other contributions covered a 

wide range of topics: changes in the mangrove landscape, 

documented through aerial and satellite imagery by Wilfrid Rodriguez and Ilka Feller at the Smithsonian Environmental Research Center; marine botany, investigated by 

Maria Faust and the Littler team; Foraminifera, by Susan 

Richardson of the Smithsonian Marine Science Network 

(MSN); symbiotic ciliates, by Joerg Ott; sponge ecology, 

by Cristina Diaz (then an MSN Fellow with me) and Janie 

Wulff (now at the Florida State University, Tallahassee); 

and two very different worm groups, the interstitial gnathostomulids by Wolfgang Sterrer (Natural History Museum, Bermuda), and the burrowing sipunculans, by Anja 

Schulze, postdoctoral fellow, and Mary Rice, emeritus 

scientist, both at SMS, Ft. Pierce, Florida (Mary is also 

the founding director of that laboratory). William Browne 

(University of Hawaii, Honolulu) summarized years of 

genetic and developmental research on mangrove crustaceans, Judith Winston her work on bryozoans, and Ivan 

Goodbody his observations on ascidian diversity. Years of 

genetic research at Twin Cays on a highly unusual amphibious fi sh, the mangrove rivulus, was summarized by 

Scott Taylor and his collaborators, and terrestrial biology 

received a welcome boost from observations by Seabird 

McKeon (then at SERC) and Stephen Mitten (University 

of Missouri, St. Louis, now based in Belize). Energy fl ow 

was also examined in a paper on nutrients derived from 

microbial mats by Samantha Joye (University of Georgia, 

Athens), and another on the planktonic food web by Edward Buskey (University of Texas at Austin). To round 

out the reports, Mary Parrish explained the important role 

of scientifi c fi eld illustration— a collaboration between scientist and artist— in analyzing and explaining mangrove 

communities.

CCRE’s recent accomplishments also include two 

far-reaching initiatives. The fi rst, begun by collaborator Emmett Duffy from the Virginia Institute of Marine 

Science (Gloucester Point), is a study of the systematics 

and ecology of snapping shrimp (Alpheidae) that live in 

reef sponges with a large interior cavity system, such as 

the genus Agelas. As the work progressed with various 

specialists and graduate students coming on board, alpheids were found to have much more genetic diversity 

and ecological complexity than previously thought. Another discovery, a fi rst among marine life, was that these 

crustaceans have the same advanced social structure (eusociality) as some well-studied terrestrial animals, such 

as termites (Duffy, 1996). Second, a logistical breakthrough, made possible through our collaboration with 

colleagues at the University of Rhode Island, was the 

development of a new integrated environmental sensing system with a radio-telemetry link to the Internet 

(Opishinski et al., 2001).

PELICAN CAYS, BIODIVERSITY HOTSPOT

In the early 1990s, our neighbors on Wee Wee Cay, 

Paul and Mary Shave, alerted us to another amazing 

ecosystem: the Pelican Cays (16°59.8N, 88°11.5W), a 

biologically rich mangrove island group less than 20 m 

south-southwest of our Carrie Bow station (Figure 9). We 

now had an 8 m boat, more substantial than any before, 

that could take us there in about an hour. Ivan Goodbody, the fi rst to visit the Pelicans on the rumor of an 

FIGURE 9. (facing page) The Pelican Cays “mangreef.” Clockwise, from top left: aerial photograph of Cat Cay showing mangrove, reef ridges, 

and deep lagoons (Manatee Cay, left, and Fisherman’s Cay are in the background); diver swimming over coral (Agaricia) below the canopy of a 

red-mangrove tree; Rich Aronson and Ian Macintyre operating a hand corer to retrieve subbottom coral and other deposits; close-up of ascidian 

(Clavellina)– sponge (Monanchora, Spirastrella) community, enveloped by brittle star arms, on Manatee Cay mangrove root; Klaus Ruetzler 

sampling sponges (Aplysina) in a marine pond on Fisherman’s Cay; Coral Ridge (Agaricia, Palythoa) with sponges (Chondrilla) at Cat Cay 

lagoon entrance (sponge-covered mangrove roots in background).

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6 2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

ascidian paradise there, found the area teeming with ascidians— and much more. Many of us followed in short 

order, eager to investigate the Pelicans’ atoll-like reef, an 

elongate north– south-oriented structure measuring almost 

10  3 km and studded with about a dozen mangrove 

cays on its northern rim. Most of the islands enclose deep 

circular ponds that support and protect a diverse community of marine plants and sessile fi lter feeders— particularly sponges and ascidians— fl ourishing on red-mangrove 

stilt roots and peat banks. A wealth of other invertebrates 

and fi shes live just below the tide line, a mix of reef and 

mangrove organisms, some species previously seen only 

in much deeper water on the barrier fore-reef, although 

the Pelican Cays are situated deep inside the barrier-reef 

lagoon, halfway between the reef and the mainland.

We were so impressed by the unusual diversity and 

ecological complexity of the Pelican Cays ecosystem that 

we asked the Belize Coastal Zone Management and Fisheries units to include the region in the South Water Cay 

MPA. Tony Rath (NaturaLight, Dangriga) and Jimmie 

Smith (Islands from the Sky, Houston, Texas) helped with 

aerial photography, Molly Ryan with mapping, and our 

research team along with outside collaborators addressed 

the new scientifi c perspectives (Macintyre and Rützler, 

2000). Macintyre and his team, and Karen McKee (U.S. 

Geological Survey, Lafayette, Louisiana), spearheaded the 

study of geological underpinnings and vegetation history, 

Dan Urish (University of Rhode Island) and Tracy Villareal (University of Texas at Austin) the hydrography of the 

ponds, Thomas Shyka (National Oceanographic and Atmospheric Agency, Silver Spring, Maryland) the nutrient 

cycle and water fl ow patterns in the ponds, Steve Morton (Bigelow Laboratory, West Boothbay Harbor, Maine) 

and Maria Faust the phytoplankton, Mark and Diane 

Littler the marine algae and seagrasses, Susan Richardson (then at Yale University, New Haven, Connecticut) 

the epiphytic foraminiferans, Rützler and colleagues the 

sponges, Janie Wulff (then at Middlebury College, Vermont) sponge predation, Wolfgang Sterrer the gnathostomulids, Gordon Hendler (Natural History Museum, Los 

Angeles, California) the echinoderms, and Ivan Goodbody the tunicates. At the height of these investigations, 

we were able to introduce the spectacular coral communities of the cays to participants of the 8th International 

Coral Reef Symposium, along with other points of interests, such as community changes in the reef zones of the 

Carrie Bow reference transect over the past two decades 

(Macintyre and Aronson, 1997). The fi shes of the Pelicans were investigated (just after the edited volume was 

published) by a team of ichthyologists led by our Museum’s James Tyler and included former American Museum 

of Natural History curator (now retired) C. Lavett Smith 

(Smith et al., 2003). More recently, important suspension 

feeders that had not been covered by the earlier surveys, 

the bryozoans, were studied by our long-time collaborator Judith Winston of the Virginia Museum of Natural 

History (Winston, 2007).

Although still uncertain of the causes of this archipelago’s unusually high biodiversity, CCRE researchers saw 

ample evidence of its fragility and warned of the irreparable harm that could come to its delicate communities 

from careless visitors or water warming during long periods of calm (as observed in course of some hurricanes). 

Little did we know that our concerns would soon prove 

to be well founded. In the course of a number of routine 

survey fl ights over the reef, we noted disturbing signs of 

land “development” on several of the Pelican islands, subsequently confi rmed by ground-truthing: we found large 

areas of mangrove clear-cut and bottom sediments near 

the cays dredged to obtain fi ll material on which homes 

and resorts could be built. We reported our observations 

to the authorities because by that time the cays were already part of the South Water Cay MPA and mangrove 

cutting was illegal without a special permit. At the time of 

this writing, the activities have stopped and are under investigation by the government of Belize. Unfortunately, a 

great natural treasure has been severely damaged, without 

any clear sense of whether and how soon a recovery will 

be possible.

A MEMORABLE YEAR, 1997

In CCRE’s 35-year history, 1997 stands out for its 

remarkable highs— and lows. Scientifi cally, many signifi -

cant fi eld projects were launched or carried to completion: 

investigations of coral bleaching, a new and unsettling 

phenomenon on the barrier reef (Aronson et al., 2000); 

ecophysiological analysis of periodic crustacean swarming 

among red-mangrove stilt roots (Buskey, 1998); a pioneering initiative to match poorly known fi sh larvae to the 

adults of the species, fi rst by morphological means after 

rearing in the laboratory, later by DNA analyses (Baldwin 

and Smith, 2003); and a workshop on Caribbean sponge 

systematics with experts from fi ve nations that led to a 

better understanding of the barrier-reef and mangrove 

poriferan fauna (Rützler et al., 2000). This was also the 

International Year of the Reef, and to celebrate the occasion we made every effort to share our enthusiasm for this 

unique environment with students and the general public 

through numerous lectures, poster sessions, and demon04_Rutzler_043-072_Lang.indd 62 4_Rutzler_043-072_Lang.indd 62 9/24/09 9:29

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NUMBER 38 • 6 3

strations, on site in Belize and back home at the National 

Museum of Natural History. To add to the festivities, our 

Carrie Bow fi eld station, the logistical base and catalyst 

of our program, had reached the respectable age of 25 

(1972– 1997).

But the Gods of the Sea must have had other plans 

for this venerable facility. On 6 December 1997 an accidental fi re broke out, aided by old, termite-riddled lumber and fanned by a strong northerly wind. Most of the 

station was reduced to ashes— laboratory, kitchen, living 

quarters, even wooden vats fi lled with water, all except 

a small cottage and the generator hut, which were isolated on the south end of the island. The blaze destroyed 

much valuable equipment, including microscopes, balances, solar system, weather station, and the contents of 

the library. As a result, little fi eldwork could be done in 

the following year, although we did investigate the fi re’s 

damage to the island (20 or more coconut trees were 

lost) and the impact of recent complete fl ooding (which 

caused substantial coastal erosion). Two other points of 

interest were the impact on the reef after being subjected 

to stormy seas with waves up to 6 m and to an extensive 

calm period with shallow-water warming that appeared 

to precipitate the bleaching and death of large numbers 

of corals.

At this juncture, we gave serious consideration to terminating the CCRE program at this location— but not for 

long. Buoyed by the positive spirit of the Bowman family 

(and some insurance payback) and the talent of a young 

Cuban-trained architect, Hedel Gongora, we designed 

a new fi eld laboratory to take the place of the old main 

house. It was built by local carpenters with lumber from 

pine forest in the west of the country, complete with wet 

lab, dry lab, library, running seawater system, workshop, 

and kitchen (Figures 10, 11). The facility was rededicated 

as the Carrie Bow Marine Field Station in August 1999, 

with more than 100 visitors in attendance to celebrate the 

occasion, including local fi shermen, cooks, the Minister 

of Environment, the U.S. ambassador to Belize, scientists, 

and representatives of all major conservation societies. 

Over the next two years, we added one cottage for living quarters and rebuilt the one spared by the fi re. With 

generous donations from a number of U.S. companies and 

individuals, we replaced and improved most laboratory 

equipment and instrumentation, and Tom Opishinski installed a new meteorological-oceanographic monitoring 

station enhanced by COASTMAP software (donated by 

the University of Rhode Island). By the beginning of 2000, 

CCRE was back on its feet, functioning as a year-round 

scientifi c program.

RESURGENCE AND BIOCOMPLEXITY

With a renovated fi eld station, CCRE’s scientifi c momentum took off once again, with new scientifi c opportunities as well as challenges. Nearly 80 scientifi c staff 

resumed fi eld research disrupted by the fi re or initiated 

new projects. A number centered on the sad effects of environmental stress or degradation on delicate but essential reef-building corals. To aid in the understanding of 

possible coral revival, Ken Sebens (then at the University 

of Maryland) and colleagues evaluated the benefi t of water currents for the growth of the reef-building shallowwater coral Agaricia, which has been adversely affected 

by extended calm periods during hurricanes (Sebens et 

al., 2003). A parallel ecophysiological study found different tolerances to elevated temperature among species 

of Agaricia and speculated that their abundance may 

therefore vary with environmental disturbance (Robbart 

et al., 2004). However, corals that have survived such 

events may have their recovery impeded by the grazing 

of parrotfi sh, which are otherwise considered benefi cial 

to the health of reefs (Rotjan et al., 2006). According to 

a series of investigations on predators and competitors of 

reef and mangrove sponges, these aggressors help defense 

mechanisms in sponges evolve (Wulff, 2005). In another 

sponge study, we concluded that encrusting excavating 

sponges have a competitive edge over reef corals weakened by elevated temperatures: the sponges can undermine the weakened opponent as well as displace its living tissue (Rützler, 2002). Assessments by Rich Aronson 

(Dauphin Island Sea Lab, Alabama), with collaborators, 

showed alarming recent changes in the composition of 

reef-building coral species as a result of stress and disease (Aronson et al., 2002, 2005), while John Pandolfi 

(then, Paleobiology) identifi ed trends responsible for the 

decline of coral-reef ecosystems worldwide (Pandolfi et 

al., 2003). A discovery with harmful implications for 

human consumption of seafood (ciguatera poisoning) 

was the increase in toxic dinofl agellate algal blooms in 

our area (Faust and Tester, 2004), a phenomenon attributed to increased nutrient levels in lagoon waters, earlier 

considered a potential threat (Morton and Faust, 1997). 

On a more positive note, studies by Ana Signorovitch 

(then a graduate student at Yale University) applying 

innovative molecular methods to the enigmatic Trichoplax in the one-species phylum Placozoa found considerable genetic diversity there as well as signs of sexual 

reproduction (Signorovitch et al., 2005). Using a new 

approach to sponge systematics from the cytochrome 

oxidase subunit 1 gene tree, Sandra Duran (postdoctoral 

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6 4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 10. New Carrie Bow Marine Field Station (2000) and Biocomplexity Program. Top row: left, aerial view of Carrie Bow Cay looking north (see details on map, Figure 11); right upper, the island with laboratory and living facilities as seen from the barrier reef (open-ocean 

side) and, image immediately below, view from the dock (lagoon side). Center row: left, fl ow-through seawater system photographed from the 

storage tank above; center, dock-mounted oceanographic sensors; right, view of upper-level dry lab. Bottom row: Starting the Twin Cays Biocomplexity Program on mangrove nutrient cycle: left, Ilka Feller with experimental enclosure in a tidal mudfl at surrounded by black mangrove; 

right, subtidal bacterial mat with decaying mangrove leaves, an early stage in the cycle.

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NUMBER 38 • 6 5

FIGURE 11. Map of Carrie Bow Cay (in 2000) identifying principal structures (number of coconut palms reduced for clarity).

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6 6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

fellow with Valerie Paul at SMS, Ft. Pierce) uncovered 

important information on rDNA phylogenies and an interesting case of ecological speciation wherein populations from reefs and mangroves in close vicinity were 

genetically more distant than those from similar habitats 

separated by thousands of kilometers (Duran and Rützler, 2006; Erpenbeck et al., 2007).

One breakthrough during this period was the fi veyear multidisciplinary “Mangrove Biocomplexity Study 

at Twin Cays: Microbial and Nutrient Controls,” funded 

by the National Science Foundation and headed by Ilka 

Feller, with nine collaborators from outside institutions 

(see Figure 10). Several important contributions to an 

understanding of nutrient production, cycling, limitation, effects on organisms, and related ecophysiological phenomena have already been published (Feller et 

al., 2002, 2007; Lovelock et al., 2006; Cheeseman and 

Lovelock, 2004), but many more are expected in the near 

future now that the fi eldwork phase of the Biocomplexity Program has come to a conclusion. One surprising 

discovery, in a complementary project by CCRE postdoctoral fellow Amy Erickson, was that the intertidal 

tree crab Aratus, long thought to be a mangrove leaf 

eater, actually prefers an animal diet if given a choice 

(Erickson et al., 2008). Another important fi nding, by 

a group from the University of Vienna, related to the 

micro environment of sessile ciliates growing on mangrove peat banks and associated with chemoautotrophic 

bacteria coating their surface. By analyzing motion behavior of the ciliate and measuring microelectrodes in 

situ, scientists could show that the hydrogen sulfi de required by the symbionts seeped into the boundary layer 

between the peat surface and oxygenated water column 

(Vopel et al., 2002).

CONCLUSION AND OUTLOOK

In 1972 a group of enthusiastic, like-minded young 

scientists embarked on a comprehensive, long-term fi eld 

investigation of unprecedented dimensions for the Museum of Natural History. The team was unifi ed in its belief 

that organisms had to be studied in their natural settings 

for a clear understanding of their features and role in their 

community (Figures 12, 13). Only then could a preserved 

museum collection aid in documenting the building blocks 

of an ecosystem. This approach was particularly true for 

coral reefs, which were all but inaccessible to scientists 

until scuba diving allowed in situ observations and experimental study. Similarly, it was essential to probe and sample substrata to better understand the structure of communities, present and past. The team directed its attention 

to the Caribbean because it is the Americas’ tropical sea, 

to which our own nation is connected by weather, ocean 

currents, and marine resources, as well as by cultural and 

economic exchange.

In the beginning, we were convinced that together, 

and with the cooperation of selected specialized collaborators, we could pierce most of the secrets of a functioning 

coral reef in little more than a decade and generate models 

for predicting future trends. It did not take long for the restrictions of space, limits of available talents, and chronic 

shortage of funds to show us how naïve we were. Besides, 

as all scientists know, every resolved problem opens up 

new questions. Nevertheless, we can look back on over a 

third of a century of substantial progress, with more than 

800 research papers in print and many more under way, 

all focused on a particular reef ecosystem and covering a 

signifi cant time span. Our investigators addressed a vast 

array of subjects: biodiversity, from microbe to mammal; 

the geological and sedimentological setting and its developmental history; the physical and chemical factor regime; 

developmental biology, genetics, food chains, nutrient 

production, and cycling; behavior, competition, predation, 

and disease; and fi sheries and conservation. We produced 

an impressive database that a new generation of motivated 

researchers can build upon with the benefi t of technical advancements such as molecular analysis, which should shed 

further light on eutrophication, climate change, and other 

stress factors responsible for the increasing occurrence of 

algal blooms and devastating invertebrate diseases. These 

topics and more will need our full attention to help guide 

resource management and conservation efforts— and, 

above all, to preserve the aesthetic and economic value of 

the world’s reefs.

Over the past few years our program has once again 

come up against a number of hurdles. Financial shortages 

in the Natural History Museum’s budget have eroded our 

funding, while staff has been reduced and not replaced, 

leaving our scientifi c and management capabilities somewhat shaky. However, some of the slack was picked up by 

endowed funds, and our fi eld station became part of the 

Smithsonian-wide Marine Science Network, joining the 

ranks of our “big brothers,” the Environmental Research 

Center at Chesapeake Bay, the Marine Station in Florida, 

and the Tropical Research Institute in Panama.

It is gratifying to fi nd that half the papers in this volume of the Smithsonian Contributions to Marine Science

series emanated from our CCRE program and the Carrie Bow Marine Field Station. The scientifi c advances 

04_Rutzler_043-072_Lang.indd 66 4_Rutzler_043-072_Lang.indd 66 9/24/09 9:29/24/09 9:29
FIGURE 12. Examples of recent projects conducted at Carrie Bow. Top row: left, diver sampling fi sh larvae in situ, a project on larval rearing 

and molecular identifi cation headed by Carole Baldwin and Lee Weigt; right, Juan Sanchez setting up in situ experiment for study of gorgonian ecology and growth. Middle row: left, Randi Rotjan recording fi sh bites on coral (Porites) on the reef shallows (inset below: larval fi sh 

[Rypticus] reared by the Baldwin team in the Carrie Bow seawater system to develop characteristics used in identifi cation of adults); center, 

colonial ciliates (Zoothammnium), barely 15 mm tall, with bacterial ectobiont, dwell on mangrove peat and are studied by Joerg Ott’s group; 

right, collaborator Kay Vopel measuring the microclimate surrounding Zoothamnium, primarily the oxygen versus hydrogen sulfi de balance. 

Bottom row: left, Klaus Ruetzler recording progress of an excavating encrusting sponge (Cliona) that competes with temperature-stressed coral 

(Diploria) (center); right, new records of sponge disease are exemplifi ed by this specimen (Callyspongia).

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FIGURE 13. Research in progress and unanticipated new opportunities. Top row: left, Klaus Ruetzler initiated (with Carla Piantoni) a study 

of cryptic and cave-dwelling reef communities in shallow-water (center, upper photo) and deep-water (center, lower photo) habitats with little 

or no light exposure; right, Laurie Penland assists recording cave fauna using a digital HD video camera. Middle row: left, water warming 

during hurricanes killed many shallow-water corals in the Pelican Cays, which became overgrown by sponges (Chondrilla) that benefi t starfi sh 

(Oreaster) as a source of food, thus starting a new ecological cycle; right, clear-cutting of mangrove and fi lling in resulting tidal fl ats with coral 

sand for “land development” started here at Twin Cays in the 1990s and continued at the Pelican Cays. Bottom row: left, Manatee Cay shown 

in 2008; right, this environmental disaster, recently stopped by the government of Belize, offers opportunities to study parameters of recovery 

of stressed and depleted marine and terrestrial communities.

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NUMBER 38 • 6 9

achieved through CCRE research indicate that our decisions and actions over the years have blazed a fertile trail 

for the future of our science.

ACKNOWLEDGMENTS

A program of this length would not have been possible without the help of countless supporters— too many 

to name individually. But all associated with us will know 

that they are being thanked because the spirit and camaraderie generated by our joint endeavor is unprecedented. 

No more than a handful of naysayers have attempted to 

slow our progress or dampen our enthusiasm— obviously 

without success. Above all, we are grateful to the Bowman 

family of Dangriga for leasing their Carrie Bow Cay to our 

program and for taking a serious interest in our work from 

the fi rst day. The government of Belize, the Department 

of Fisheries in particular, hosted our scientifi c efforts and 

granted us necessary permits. Many of the people of Belize, from Dangriga Town in particular, helped us with logistics by sharing their knowledge of the country’s coastal 

resources, their skilled and dedicated cooks, boatmen, carpenters, hotel services, and provisions. Back home, we received invaluable cooperation and support from scientifi c 

colleagues, private and federal funding sources, and Smithsonian staff from all levels of administration and science 

units, including the Natural History Museum’s Director’s 

Offi ce, the Smithsonian Scientifi c Diving Program and its 

staff, and many of the Museum’s research assistants, scientifi c illustrators, photographers, and collection managers. 

For my part, I could not have directed and inspired our 

program without the assistance of many dedicated collaborators: Mike Carpenter, CCRE operations manager; Marsha Sitnik, program administrator; and Kathleen Smith, 

Michelle Nestlerode, Martha Robbart, Robyn Spittle, and 

Carla Piantoni, research assistants.

Photographs and art in this contribution were contributed by Mike Carpenter, Chip Clark, Ilka Feller, Ron 

Larson, Kathy Larson, Sara Lewis, Diane Littler, Ian Macintyre, Vicky Macintyre, Julie Mount, Aaron O’Dea, 

Tom Opishinski, Mary Parrish, Laurie Penland, Carla 

Piantoni, Tony Rath, Mary Rice, Randi Rotjan, Klaus 

Ruetzler, Molly Kelly Ryan, Juan Sanchez, Kjell Sandved, 

Jimmie Smith, Kathleen Smith, Kay Vopel, all of whom 

are (or were at the time) affi liated with the Smithsonian 

Institution, and two undetermined photographers.

This is contribution number 850 of the Caribbean 

Coral Reef Ecosystems Program (CCRE), Smithsonian 

Institution, supported in part by the Hunterdon Oceanographic Research Fund.

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The Smithsonian Tropical Research Institute: 

Marine Research, Education, 

and Conservation in Panama

D. Ross Robertson, John H. Christy, Rachel 

Collin, Richard G. Cooke, Luis D’Croz, Karl 

W. Kaufmann, Stanley Heckadon Moreno, Juan 

L. Maté, Aaron O’Dea, and Mark E. Torchin

ABSTRACT. A grand geological experiment with a global reach to its biological impact, 

the formation of the isthmus of Panama between 15 and 3 million years ago split the 

tropical Interamerican Seaway into two and substantially changed the physical oceanography of each part. That event subjected the now-divided halves of the neotropical marine biota to new environmental conditions that forced each along a different evolutionary trajectory. For the past 45 years the Smithsonian Tropical Research Institute (STRI) 

marine sciences program has taken full advantage of this event by sponsoring research on 

a great diversity of topics relating to the evolutionary effects of the formation of the isthmus. That research, which has been supported by multiple laboratories on each coast and 

a series of research vessels, has produced more than 1,800 publications. Here we provide 

an overview of the environmental setting for marine research in Panama and an historical 

perspective to research by STRI’s scientifi c staff at the different marine facilities.

INTRODUCTION

The unique geological history of Panama encourages a wider variety of research on tropical marine organisms than can be accomplished anywhere else in 

the world. The Central American Isthmus narrows in Panama to approximately 

70 km, separating oceans that have very different oceanographic regimes and 

marine ecosystems. The formation of the central American isthmus, starting 

approximately 15 million years ago (Ma) and fi nishing in Panama about 3 Ma, 

had wide ramifi cations not only for the nature of the modern biological and geological world of the Americas but also for the entire global oceanic circulation. 

With the completion of this process the Gulf Stream strengthened, changing the 

Atlantic circulation. That change was soon followed by Northern Hemisphere 

glaciation, which in turn brought about a period of climate change in Africa that 

may have stimulated the origins of modern man. From a more local perspective, 

the completion of the isthmus set in motion a vast natural experiment: single 

populations of marine animals and plants were split and isolated in different 

and changing environments that forced their evolutionary divergence and fundamental changes in their biology.

D. Ross Robertson, John H. Christy, Rachel Collin, Richard G. Cooke, Luis D’Croz, Karl W. 

Kaufmann, Stanley Heckadon Moreno, Juan L. 

Maté, Aaron O’Dea, and Mark E. Torchin, Smithsonian Tropical Research Institute, Box 0843-

03092, Balboa, Panama. Corresponding author: 

R. Robertson (drr@stri.org). Manuscript received 

15 August 2008; accepted 20 April 2009.

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7 4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

The Smithsonian Tropical Research Institute (STRI) 

marine research program in the Republic of Panama has 

taken full advantage of this globally signifi cant geological 

event. In 1964 STRI established its fi rst laboratories on the 

Pacifi c and Caribbean coasts within what then constituted 

the Panama Canal Zone. Since that time, marine research at 

STRI has expanded greatly and made major contributions 

to understanding of tropical marine biodiversity: the geological history of the isthmus and the development of environmental differences in the Caribbean and eastern Pacifi c, 

patterns of biodiversity in neotropical marine habitats, coral 

reef development, coral symbioses and diseases, the modes 

and tempo of species formation and diversifi cation, evolutionary change within many groups of organisms relating to 

environmental differences on the two sides of the isthmus of 

Panama, and invasions by marine organisms facilitated by 

the Panama Canal and its shipping activity. To date marine 

research at STRI has resulted in more than 1,800 scientifi c 

publications; half of these have been produced by staff scientists and more than 200 published in high-profi le journals 

such as Science, Nature, Proceedings of the National Academy of Sciences of the United States of America, Proceedings of the Royal Society, American Naturalist, Evolution, 

Ecology, and Annual Review of Systematics and Ecology.

In celebration of its role in coral reef research, the 

Smithsonian’s 150th anniversary, and the International Year 

of the Reef, STRI hosted the Eighth International Coral 

Reef Symposium in Panama in 1996. This meeting brought 

1,500 reef scientists and managers to Panama from around 

the world, resulting in the publication of a two-volume 

proceedings (Lessios and Macintyre, 1997), and an international traveling exhibit of coral reefs that is now resident at 

the Bocas del Toro Research Station.

Here we present an overview of the marine setting of 

Panama that clearly indicates its potential for research, 

and a historical summary of the diversity of marine studies conducted at the different STRI marine facilities. We 

then briefl y outline STRI’s marine education and outreach 

activities. Although this review focuses on the research activities of STRI’s marine staff scientists, a strong fellowship program and a larger suite of visiting students and 

scientifi c collaborators have acted as substantial multipliers of STRI scientists’ activities.

THE COASTAL OCEANOGRAPHIC SETTING 

OF THE ISTHMUS OF PANAMA

The emergence of the Isthmus of Panamá likely was 

the most crucial event for tropical marine ecosystems 

in the last 15 million years of earth’s history. In Central America the marine environment experienced drastic 

changes in the two seas formed by the isthmus. As the 

isthmus approached closure, the Caribbean gradually became cut off from the eastward fl ow of Pacifi c water and 

became warmer, saltier (westward winds carried away 

evaporated moisture), and more oligotrophic. The Caribbean now is a relatively stable sea, with small fl uctuations in temperature, relatively low tidal variation, and 

a relatively high salinity. Its relatively clear and nutrientpoor waters (D’Croz and Robertson, 1997; D’Croz et 

al., 2005; Collin et al., 2009) are ideal for the growth 

of coral reefs, and the wider Caribbean area ranks third 

behind the Indian Ocean and the Indo-West Pacifi c in 

terms of numbers of marine species. Annual rainfall is 

high on the Caribbean coast of Panama and follows 

the same basic seasonal pattern as on the lower-rainfall 

Pacifi c side of the isthmus (Kaufmann and Thompson, 

2005). Relative to the Caribbean, the Tropical Eastern 

Pacifi c (TEP) exhibits much greater fl uctuations in tides 

and temperature and has substantially lower salinity as 

a consquence of an area of very high rainfall along the 

Intertropical Convergence Zone. The TEP also has more 

and much larger areas of seasonal upwelling than the Caribbean. In addition, and in contrast to the Caribbean, 

the TEP also experiences strong longer-term variation 

in temperature and productivity from the infl uence of El 

Niño– Southern Oscillation Cycle (ENSO) events (D’Croz 

and O’Dea, 2009). Sea warming related to ENSO (which 

occurs at intervals of four to nine years) has drastic affects on coral reef development in the TEP. The direct 

marine effects of ENSO events in the tropical and warm 

temperate parts of the eastern Pacifi c are stronger than 

anywhere else in the world. Although coastal biological 

productivity is strongly related to benthic communities in 

the Caribbean, pelagic productivity and high availability 

of ocean-derived dissolved nutrients dominate the TEP, 

with high variability in those nutrient levels producing 

matching variability in the abundance of pelagic organisms (Miglietta et al., 2008). In Panama the nutrient-rich 

waters of its Pacifi c coast support commercial fi sheries of 

major importance, fi sheries that have no counterpart on 

the Caribbean coast.

The coastal marine communities of Panama are affected not only by inter-ocean differences in oceanography but also by marked local variation in shoreline 

environmental conditions along each coast. The Pacifi c 

shelf of Panama is wide and is divided, by the southwardprojecting Azuero Peninsula, into two large areas, the 

(eastern) Gulf of Panama and the (western) Gulf of 

Chiriquí. The Gulf of Panama is subject to strong seasonal wind-driven upwelling, but the Gulf of Chiriquí is 

05_Robertson_073-094_Lang.indd 74 5_Robertson_073-094_Lang.indd 74 9/24/09 9:23/24/09 9:23
NUMBER 38 • 7 5

not (Figure 1; and see D’Croz and Robertson, 1997). In 

the latter Gulf, high mountains block the wind and prevent wind-induced upwelling (D’Croz and O’Dea, 2007). 

In contrast, the Caribbean coast of Panama is relatively 

straight and has a narrow continental shelf, except in the 

(western) Bocas del Toro Archipelago. Hydrological conditions vary substantially along the Caribbean coast, ranging from the nutrient- and plankton-poor waters in the 

(eastern) San Blas Archipelago, where river discharge is 

low and the infl uence of open ocean water is high (D’Croz 

et al., 1999), to the more turbid environments of the Bocas 

del Toro Archipelago, where rainfall and river discharge 

are higher as a result of the blockage of westward moisture fl ow by the highest mountains in Panama (D’Croz et 

al., 2005; Collin et al., 2009). Thus, Panama lays claim to 

having “four oceans,” providing unique opportunities for 

FIGURE 1. Temperature regimes on the Atlantic and Pacifi c coasts during the seasonal upwelling in the Gulf of Panama.

05_Robertson_073-094_Lang.indd 75 5_Robertson_073-094_Lang.indd 75 9/24/09 9:23/24/09 9:23
7 6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

understanding how and why marine ecosystems vary and 

function as they do.

A HISTORICAL RESUME OF RESEARCH 

AT STRI MARINE FACILITIES

Marine research began at STRI in 1961with the doctoral work of STRI Director (Emeritus) Ira Rubinoff on 

trans-isthmian sister species of fi shes (Rubinoff and Rubinoff, 1971), which led to STRI’s fi rst marine publication, based on work done near Punta Galeta (Rubinoff 

and Rubinoff, 1962). Since then the marine program has 

undergone exponential growth in its productivity. STRI 

currently operates two land facilities on the Caribbean 

coast of Panama, Punta Galeta Laboratory and Bocas del 

Toro Research Station, and two on the Pacifi c coast, Naos 

Island Laboratory complex and Rancheria Island fi eld 

station. Between 1977 and 1997 STRI also operated a 

small, highly productive fi eld station in the San Blas islands 

(Figure 2). In addition, STRI has maintained a series of 

small coastal research vessels that greatly expanded the 

geographic reach of its activities well beyond STRI’s land 

facilities and, in fact, far beyond Panama.

MARINE ENVIRONMENTAL SCIENCES PROGRAM (MESP)

Monitoring the Physical Environment

In 1974, the Smithsonian Institution Tropical Environmental Sciences Program began monitoring physical environmental variables at Galeta, recording rainfall, wind speed and direction, solar radiation, reef fl at 

water level, and air and water temperature hourly with 

automated equipment. Today, such physical data are recorded more frequently, automatically sent to a central 

processing facility via radio and internet, and added to a 

database that is available online at http://striweb.si.edu/

esp/physical_monitoring/index_phy_mon.htm. Organization of physical data collection from Galeta has now been 

combined with that from Barro Colorado Island, Bocas 

del Toro, and several other sites, under the management 

of Karl Kaufmann. Recording of sea-surface temperature 

started at Galeta in 1988, and this monitoring now covers 

33 shallow-water stations throughout the coastal waters 

on both coasts of Panama. Published summaries of the 

marine physical data include Meyer et al. (1974), Cubit et 

al. (1988), and Kaufmann and Thompson (2005). Physical 

environmental monitoring was conducted at the San Blas 

station from 1991 until its closure in 1998 and has been in 

progress at Bocas del Toro since 1999.

Monitoring the Biological Environment

The fi rst phase of biological monitoring consisted of 

work done at Galeta that was stimulated by the two oil 

spills and formed part of their resultant studies. At San 

Blas, biological (plankton) monitoring co-occurred with 

the physical monitoring. At Bocas del Toro, biological 

monitoring that started in 1999 includes minor activity 

directed at seagrasses and mangroves in connection with 

CARICOMP. The major activity however, has been an expanding set of monitoring surveys of coral reefs by Hector Guzman, which now cover reefs scattered along both 

coasts of Panama (see http://striweb.si.edu/esp/mesp/reef

_monitoring_intro.htm). This program developed from a 

survey of coral reefs in the general vicinity of Galeta made 

in 1985 (Guzman et al., 1991; and see also Guzman et al., 

2008b).

 GALETA POINT MARINE LABORATORY

The Galeta Point installation became a STRI laboratory in 1964 when a military building constructed in 1942 

on a fringing reef fl at was turned over to STRI, thanks 

to the efforts of Ira Rubinoff. From his research on inshore fi shes in that area (Rubinoff and Rubinoff, 1962) 

Rubinoff recognized its value as an easily accessible Caribbean study site. By 1971 Galeta Point was STRI’s primary 

marine research site, providing access to a fringing reef 

fl at, seagrass beds, and mangroves within a few meters of 

a laboratory building, with housing in nearby Coco Solo. 

Early work emphasized the comparison of reefs on both 

sides of the isthmus (Glynn, 1972) and the geological 

structure and history of the reefs (Macintyre and Glynn, 

1976). Fundamental insights into differences between the 

Caribbean and eastern Pacifi c at Panama also were developed by Chuck Birkeland (Birkeland, 1977) when, during 

his long-term residence at Galeta, he analyzed patterns of 

biomass accumulation on settling plates deployed on both 

sides of the isthmus.

Permanent monitoring of the biota at Galeta Point 

was started in 1970 by Chuck Birkeland, David Meyer, 

and Gordon Hendler to provide baseline data on a tropical Caribbean reef fl at; this was done to determine the effect of the Witwater oil spill, which occurred in December 

1968 about 5 km east of Galeta. Because no baseline data 

were available to determine effects of that spill on reef 

communities, the US Environmental Protection Agency 

provided funds to set up the study and to perform experiments testing susceptibility of corals to oil. Transects were 

established at both Galeta Point and Punta Paitilla on the 

05_Robertson_073-094_Lang.indd 76 5_Robertson_073-094_Lang.indd 76 9/24/09 9:24/24/09 9:24
NUMBER 38 

• 7 7 FIGURE 2. Map of Panama showing the distribution of Smithsonian Tropical Research Institute (STRI) marine facilities.

05_Robertson_073-094_Lang.indd 77 5_Robertson_073-094_Lang.indd 779/24/09 9:24/24/09 9:24
7 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Pacifi c side to compare community structure, recruitment 

patterns, and the effect of oil on both communities (Birkeland et al., 1973).

In April 1986 a storage tank ruptured at an oil refi nery about 4 km east of the laboratory, spilling 60,000– 

100,000 barrels of oil into the sea. The reef fl at, grass 

beds, and mangroves around the Galeta laboratory were 

heavily oiled. This time a substantial amount of baseline 

data was available, thanks to the original transects set up 

by Birkeland, Meyer, and Hendler, whose monitoring had 

ended in 1982, and to the wider reef surveys in that area 

by Ernesto Weil. The Minerals Management Service of the 

U.S. Department of the Interior bestowed a 5 year grant 

to STRI to study the effects of the second oil spill in tropical areas (Keller and Jackson, 1993). That effort involved 

a considerable expansion of the types of data gathered, 

organisms studied, and habitats monitored over those in 

the fi rst oil spill study. Subsequent to the second oil spill 

study the center of STRI research on coral reefs shifted 

fi rst to San Blas then to Bocas del Toro. A long-term study 

(since 1988) of mangrove forest dynamics by Wayne 

Sousa (Sousa, 2007), occasional short-term projects, and 

physical environmental monitoring by MESP (see below) 

have continued at Galeta. The site also supports public 

education and outreach programs organized by Stanley 

Heckadon (see below). To date 315 publications include 

data obtained at Galeta laboratory, and the lab itself has 

produced 288 marine publications.

SAN BLAS FIELD STATION

The sparsely populated San Blas archipelago, in the autonomous Kuna Yala comarca, consists of several hundred 

sand cays scattered along the relatively sparsely populated 

eastern third of the Caribbean coast of Panama. The archipelago has the richest and most extensive development of 

coral reefs and associated fauna (including reef fi shes) and 

fl ora in Caribbean Panama. Marine research sponsored 

by STRI began in San Blas in 1970, and research activity 

increased greatly in the late 1970s following the gradual 

construction by STRI from 1977 onward of a small fi eld 

station that provided basic living accommodations and so 

allowed year-round research.

The San Blas fi eld station, with its year-round access 

to a 15 km2 area of rich reefs in calm, clear water, was the 

Caribbean base for many of STRI’s comparative studies of 

the biology of closely related organisms on the Atlantic and 

Pacifi c sides of the Isthmus of Panama. Early research by 

STRI staff in San Blas included studies by STRI’s founding 

director, Martin Moynihan, on the behavior of cephalopods (Moynihan, 1975; Moynihan and Rodaniche, 1982) 

and by Peter Glynn in the 1970s on coral reef development 

(Glynn, 1973). These investigations were followed by others on a broad range of organisms: Ross Robertson on 

the sexual patterns of labroid fi shes, with Robert Warner 

(Warner et al., 1975; Robertson and Warner, 1978; Warner and Robertson 1978), and the recruitment dynamics 

and demography of reef-fi shes (Robertson et al., 1999, 

2005); Haris Lessios on the evolution and biology of 

echinoderms on the two coasts of the isthmus of Panama 

(Lessios, 1979, 1981, 2005); deputy director Eric Fischer 

on the sexual biology of simultaneously hermaphroditic 

groupers (Fischer, 1980, 1981; Fischer and Petersen, 

1987); Nancy Knowlton on the biology and evolution of 

snapping shrimps and the reproductive biology, coral– 

algal symbioses, and evolution of corals (Rowan et al., 

1997; Knowlton et al., 1977, 1992; Knowlton and Weigt, 

1998); Jeremy Jackson on the comparative population and 

reproductive biology and evolutionary history of bryozoans on both sides of the Isthmus of Panama (O’Dea and 

Jackson, 2002; Dick et al., 2003; O’Dea et al., 2004); Luis 

D’Croz on comparative oceanographic conditions on the 

Caribbean and Pacifi c coasts of Panama (D’Croz and Robertson, 1997); and Hector Guzman on coral reef distribution and conservation (Andrefouet and Guzmán, 2005). 

During this period STRI also sponsored several anthropological projects on traditional Kuna society, acted as a 

conduit for international funding of Kuna marine management and conservation activities, and provide fellowships 

to Kuna University students.

The San Blas station provided essential support for 

projects on long-term ecological change on surrounding 

coral reefs. The combination of ease of access to shallow 

reefs, access as good as anywhere in the world, and the 

ability to do much work while on snorkel rather than 

scuba meant that it was possible to accumulate enormous 

data sets involving daily or shorter time period observations over months or years. These kinds of data are all too 

rarely available for tropical marine systems.

In early 1983 a Caribbean-wide mass die-off of an 

ecologically key organism on Caribbean reefs, the black 

sea urchin Diadema antillarum, began near San Blas and 

spread within the year throughout the entire Greater Caribbean. The year-round presence of biologists conducting 

long term studies of reef organisms at STRI’s fi eld station 

enabled the documentation of the start and spread of that 

event, which produced large, long-term effects on algal and 

coral growth on Caribbean coral reefs. Haris Lessios has 

followed the population and evolutionary consequences 

of that event for the urchin since it started (Lessios et al., 

05_Robertson_073-094_Lang.indd 78 5_Robertson_073-094_Lang.indd 78 9/24/09 9:24/24/09 9:24
NUMBER 38 • 7 9

1984; Lessios, 2005). Year-round monitoring of reef-fi sh 

populations on reefs around that station over a 20 year 

period contributed key information to a meta-population 

study that documents a gradual Caribbean-wide decline 

in the overall abundance of reef fi shes since the Diadema

dieoff (Paddack et al., 2009). Long-term monitoring of climatic and oceanographic conditions by MESP enabled detailed examination of linkages between environmental dynamics and the dynamics of recruitment of pelagic larvae 

of reef-fi shes (Robertson et al., 1999). In addition regular 

station visitors accumulated the world’s only long-term 

data sets on gorgonians and sponges. The former work includes data on a combination of population dynamics and 

genetics of clone structure obtained by Howie Lasker and 

Mary-Alice Coffroth (Coffroth et al., 1992; Lasker, 1991; 

Lasker et al., 1996). The latter work includes data on the 

dynamics of sponge communities collected by Janie Wulff 

(Wulff, 1991, 1997).

Over the 20 years of its existence, research supported 

by the San Blas fi eld station produced 363 publications 

on the biology of plants and animals living on the coral 

reefs around the station, at a peak annual operating cost 

of about US$100,000. The cheapness of this operation 

provides a startling example of how effective a small station can be for very little expense, so long as the necessary 

tools for fi eld research are supplied: grass huts for living, 

rainwater for drinking and washing, communal kitchens, 

small boats, a scuba compressor, and, above all, fi eld sites 

in calm clear water at the station’s doorstep.

Local political events in this autonomously governed 

indigenous reserve led to the closure of the San Blas station 

in 1998. Although this closure terminated the activities of 

STRI staff scientists in that area for some time, several external researchers were able to make private arrangements 

to continue their work there. After the closure of the San 

Blas station the center of STRI’s Caribbean research efforts moved to Bocas del Toro Province, at the opposite 

end of the Caribbean coast of Panama.

BOCAS DEL TORO RESEARCH STATION (BRS)

The Smithsonian Institution (SI) has a long history 

of terrestrial and geological research in Bocas del Toro 

Province. In the 1970s and 1980s Charles Handley of the 

Natural History Museum mounted a number of expeditions to the province to survey the mammal and bird fauna 

(Handley, 1993; Anderson and Handley, 2002). This phase 

was followed with ground-breaking geological work by 

STRI’s deputy director, Anthony Coates. He used the rock 

outcrops in the province, which contain the most complete 

record of marine environments of the last 10 million years 

in the southern Caribbean, to help clarify events associated with the rise of the Isthmus of Panama (Collins et al., 

1995; Collins and Coates, 1999; Coates et al., 2005).

In 1998 STRI purchased 6 hectares (ha) just outside 

the town of Bocas del Toro on Isla Colon. A dormitory 

was built on the site in 2001 and a modern, well-equipped 

laboratory in 2003. The BRS now houses 28 resident scientists and will soon add accommodation for 16 more. 

BRS can now host approximately 325 scientifi c visitors 

from more than 30 countries each year: 40% undergraduates, 25% graduate students, 10% postdoctoral fellows, 

and 25% researchers. About half the postdoctoral fellows 

and researchers are SI scientists. Research at the station 

has resulted in 201 scientifi c publications in the fi ve years 

since its inauguration in 2003, with Rachel Collin as its 

director.

The BRS is now among the preeminent research stations in the Caribbean. It is better equipped and provides 

access to a larger diversity of habitats than almost any 

other research facility in that region. The wealth of natural diversity available near BRS combined with technical 

support facilities is refl ected in the wide range of research 

projects that are conducted at the station. Signifi cant research has focused on the coral bleaching response to stress 

and disease. These studies have shown that sugars are one 

of the most damaging components in pollution from rain 

runoff (Kline et al., 2006) and that coral disease is related 

to temperature stress. An SI fellow identifi ed candidate 

genes that participate in coral’s bleaching response to elevated temperature (DeSalvo et al., 2008). Research at the 

laboratory also has shown that some coral disease and 

death in the Caribbean results from a protozoan infection. 

Another strong line of research at the BRS is the investigation of the factors that lead to speciation in the marine 

environment. Groundbreaking work on hamlet fi shes has 

shown that mate choice based on color pattern may drive 

divergence and that color patterns may evolve via aggressive mimicry, a previously undemonstrated mechanism of 

diversifi cation (Puebla et al., 2007, 2008).

The BRS is also a local focus of taxonomic work and 

studies aimed at documenting marine biodiversity that 

were published in a special issue of the Caribbean Journal 

of Science dedicated to the marine environment and fauna 

of Bocas del Toro (Collin, 2005a, 2005b). Extensive work 

has been done there on the taxonomy of marine shrimps 

(Anker et al., 2008a, 2008b, 2008c). Bocas del Toro is a 

global hotspot of shrimp diversity and ranks within the 

top 10 sites in the world. More than 20 new shrimp species 

from Bocas del Toro have been described in the past fi ve 

05_Robertson_073-094_Lang.indd 79 5_Robertson_073-094_Lang.indd 79 9/24/09 9:24/24/09 9:24
8 0 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

years. New species of other marine organisms, including 

snails, tunicates, sponges, fl atworms, and meiofauna, have 

also been described on the basis of work at the BRS. As 

a result of these taxonomic and faunal studies, Bocas del 

Toro has the highest recorded tunicate diversity anywhere 

in the Caribbean and the third highest sponge diversity.

Other long-term projects based at BRS include studies focused on breeding success at major Caribbean turtle 

nesting beaches, the effects of noise polluction and tour 

boat operations on dolphin vocalization and behavior, effects of anthropogenic substrates, such as docks, on invasive tunicate abundance, effect of nutrient limitation on 

mangrove forest structure and diversity, emerging sponge 

diseases, and Caribbean-wide speciation in Montastraea

corals caused by temporal shifts in spawning cycles.

NAOS ISLAND LABORATORIES

Naos is one of a cluster of four islands at the end of a 

2 km long causeway at the Pacifi c entrance to the Panama 

Canal. STRI’s fi rst marine laboratory was established there 

in 1964 in an old military bunker and has since expanded 

to four buildings, three of them ex-US Navy buildings refurbished by STRI. This laboratory provides ready access 

to the upper bay of Panama with its extensive mangroves 

and a scattering of inshore islands, plus the coral reefs of 

the Perlas Archipelago, 50 km away. The laboratory complex, with a fl ow-through aquarium system, diving locker, 

small boat support, research vessel, and molecular laboratories, supports a wide range of research by all the marine 

scientifi c staff. Organismal studies based primarily at Naos 

cover or have covered the following topics: the Panama 

Canal as a hub for marine invasions, rocky intertidal community ecology, physiological ecology, behavioral ecology 

of intertidal organisms, coral reef development in the TEP, 

molecular evolution of marine organisms, life history evolution and evolution of mode of development, and marine 

zooarchaeology.

Panama as a Hub for Marine Invasions

Biological invasions are a potent force for change 

across the globe. Once established, introduced species can 

become numerically or functionally dominant, threatening native biodiversity and altering ecosystem processes. 

The fl ip side to the damage they cause is that introduced 

species can provide opportunities for insight as large-scale 

experiments to understand ecological and evolutionary 

processes. In marine and coastal environments, shipping 

is a major pathway for biological invasions and appears 

largely responsible for the recent dramatic increase in 

invasions.

Beginning with the studies of Hildebrand (1939) in the 

1930s, followed by several investigations surrounding the 

potential problems associated with the construction of a 

sea-level Canal in Central America (Rubinoff, 1965, 1968; 

Rubinoff and Rubinoff, 1969), STRI has been central in 

evaluating the role of the Canal as a passageway for shorefi shes. Interestingly, despite the Canal’s 100 years of existence and the occurrence of approximately 1,500 species 

of marine and brackish-water fi shes on the two coasts of 

Panama, only a handful of such species have successfully 

passed through the Panama canal and established populations in the “other” ocean. For example, only 8 species 

of such successful immigrants are known in the tropical 

eastern Pacifi c and only 3 have spread beyond the immediate confi nes of the Pacifi c entrance to the canal. Why are 

there so few successful invasions through a short, suitable 

corridor? Why do some invasions fail and others succeed? 

Panama and its canal have much to offer studies aimed at 

determining success or failure of invasions.

STRI is ideally situated to study marine and coastal 

invasions. Panama is one of the world’s largest hubs for 

shipping. The Canal serves as an aquatic corridor connecting the Atlantic and Pacifi c Ocean basins, and ports 

on either side serve as hubs for international trade. Since 

its opening in 1914, approximately 800,000 ocean-going 

commercial vessels have passed through the Canal. Today, approximately 12,000 to 14,000 commercial ships 

transit the Canal annually (Ruiz et al., 2009). Moreover, 

Panama is initiating a major effort to expand shipping in 

the Canal by constructing additional locks on the Pacifi c 

and Atlantic coasts. Although the freshwaters of Lake Gatun, a large lake that constitutes the bulk of the canal, 

have strongly limited the inter-oceanic invasions of purely 

marine species, the new locks being added to the canal 

have the potential to increase the salinity of Gatun Lake 

and increase such interchange. With the Naos and Galeta 

marine laboratories strategically located at the Pacifi c and 

Atlantic entrances to the Canal, STRI is well positioned 

to continue to conduct a broad range of basic research on 

marine invasions.

In contrast to the limited exchange of fi shes across 

the Isthmus, various introduced invertebrate species have 

been documented recently in the Canal, underscoring the 

fact that invasions are occurring. Some examples include 

a North American mud crab that has established a population in the Panama Canal expansion area (Roche and 

Torchin, 2007) and an invasive Japanese clam that reaches 

densities greater than 100 m2 in the Canal, as well as an 

05_Robertson_073-094_Lang.indd 80 5_Robertson_073-094_Lang.indd 80 9/24/09 9:24/24/09 9:24
NUMBER 38 • 8 1

invasive snail that is known to host medically important 

trematode parasites. Although there are likely other such 

species, with few exceptions (Abele and Kim, 1989) invertebrate diversity of the Canal remains largely unexplored. 

Recently, STRI and SERC scientists teamed up to evaluate 

the role of the Canal in biological invasions and determine 

how patterns and processes driving invasions in tropical 

and temperate regions may differ.

Although the potential for invasions in Panama is likely 

to be high, with the exception of studies on fi shes that have 

passed through the Canal in the past 40 to 50 years, we 

know surprisingly little about other coastal invasions that 

have resulted, and many established invasions probably 

have been overlooked (Miglietta and Lessios, 2009). With 

the current expansion of the Panama Canal, evaluating the 

importance of the Canal in regional and global invasions 

is arguably an imperative goal for the conservation of our 

coastal resources and an ideal opportunity to illuminate 

our understanding of biological invasions.

Rocky Intertidal Community Ecology

The rocky intertidal zone of the TEP appears to be 

largely bare rock, with very little macroalgal cover and few 

sessile invertebrates, which are not distributed in clear zones 

according to tidal height or wave exposure. The striking 

contrast between this system and those of temperate North 

America and Europe, which are well vegetated and have 

an abundance of invertebrates in regularly arranged zones, 

drew researchers such as Jane Lubchenco (currently director 

of the NOAA) and Bruce Menge to STRI in the late 1970s to 

seek an explanation. Their fi eld exclusion experiments indicated that year-round predation and herbivory by a diverse 

community of highly mobile fi shes, crabs, and mollusks 

forces their prey into refugia in cracks and under boulders 

and regulates directly, or indirectly, species interactions such 

that species capable of dominating space are kept in check 

(Menge and Lubchenco, 1981; Menge et al., 1986).

Physiological Ecology

The marine environment of the eastern Pacifi c is much 

more variable than that of the Caribbean, especially so 

during upwelling and in shallow-water and intertidal habitats. Temperatures in tidal pools at Naos range between 

approximately 18°C and more than 50°C. Jeffery Graham 

made contributions to basic understanding of how fi shes 

and sea snakes contend with this and other physiological challenges in the TEP (Graham, 1970, 1971) and later 

investigated heat regulation in tunas (Graham, 1975). Ira 

Rubinoff, together with Graham and Panamanian cardiologist Jorge Motta, performed pioneering work on the 

temperature physiology and diving behavior and respiratory physiology of the neotropics’ only sea snake species 

(Graham et al., 1971; Rubinoff et al., 1986).

Behavioral Ecology of Intertidal Animals

Marine behavioral and estuarine (soft-bottom) ecology has been the focus of long-term research programs by 

John Christy and his students on the reproductive ecology 

(larval release cycles in relation to predation risks; Morgan and Christy, 1995) and behavior (burrow ornaments 

as sexual signals; Christy et al., 2002) of intertidal crabs, 

particularly fi ddler crabs. The latter reach their highest 

species diversity in the world on the Pacifi c coast of Central America (Sturmbauer et al., 1996). Christy recently 

completed fi ve years of daily observations of the reproductive timing of a fi ddler crab on Culebra beach, the results 

of which demonstrate that these crabs have a remarkable 

ability to track, on several time scales, complex variation 

in environmental conditions suitable for larval release. Research by Christy’s lab on mechanisms of mate choice in 

fi ddler crabs has shown that male courtship signals elicit 

responses in females that have been selected by predation, 

not because the signals lead to choice of the best male as 

a mate. This research has provided the best empirical support to date for the “sensory trap” mechanism of sexual 

signal evolution (Christy, 1995; Backwell et al., 2000, Kim 

et al., 2009). Together with work by terrestrial biologists 

at STRI, this research has made STRI a global center for 

the study of the evolution of sexual signals.

Coral Reef Development 

in the Tropical Eastern Pacifi c (TEP)

Following the closure of the isthmus, different components of the tropical biota of the TEP reacted in different ways to resultant dramatic changes in the local marine environment. Most of the coral fauna was wiped out 

(85% of the current, depauperate fauna is derived from 

Indo-Central Pacifi c immigrants), probably largely by extreme environmental fl uctuations during ENSO events. 

Documentation of effects of environmental changes on 

coral reef development in that area has been the focus of 

35 years of studies by Peter Glynn and his collaborators, 

not only in Panama but also further afi eld in the TEP in 

places such as the Galapagos (Glynn et al., 1979; Glynn 

and Wellington, 1983). STRI research on Panama’s Pacifi c 

coral reefs began in the earlier 1970s, when, contrary to 

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8 2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

previous ideas, fully developed coral reefs were found in 

the Gulfs of Panama and Chiriquí (Glynn, 1972; Glynn 

et al., 1972; Glynn and Stewart, 1973). It also became 

evident that differences in reef growth in those gulfs were 

related to their different temperature regimes (Glynn and 

Stewart, 1973). Coral reefs in the Gulf of Panama are 

mainly confi ned to the warmer sides of the Pearl islands 

and grow at lower rates than reefs in the year-round 

warmth of the Gulf of Chiriquí (Glynn and Macintyre, 

1977). The latter reefs grow at rates comparable to those 

on the Caribbean coast of Panama (Macintyre and Glynn, 

1976), and corals in each gulf differ in their responses to 

temperature (D’Croz et al., 2001; Schloeder and D’Croz, 

2004). A major thrust of work on TEP reefs has been to 

understand the effects of ENSO warming events on the 

survival and dynamics of reef ecosystems. Observations 

linked coral bleaching in Panama to high-temperature 

anomalies of the severe 1982– 1983 ENSO (Glynn et 

al., 1988; Glynn and D’Croz, 1990; Glynn et al., 2001). 

Such bleaching led to region-wide mass coral mortality 

during the intense 1982– 1983 and 1997– 1998 ENSO 

events (Glynn, 1984; Glynn et al., 2001). Microcosm experiments at STRI confi rmed that temperature stress produced bleaching and mass mortality of corals (Glynn and 

D’Croz, 1990) and that slow-growing massive species are 

more resistant than branching types to temperature-induced 

beaching (Huerkamp et al., 2001). There has been continuous monitoring of reef recovery since the mass coral mortality produced by the 1982– 1983 ENSO, providing one of 

the longest term databases of this type in the world (Glynn, 

1984, 1990; Glynn and Colgan, 1992; Glynn et al., 2001). 

Major efforts have also been made to investigate the reproductive ecology of corals, relating fecundity, spawning 

activity, and recruitment of surviving species to community 

recovery and reef resilience in Pacifi c Panama (Glynn et al., 

1991, 1994, 1996, 2008; Colley et al., 2006; Manzello et 

al., 2008). Bleaching patterns have been related not only to 

the diversity of zooxanthellae symbionts of corals (Glynn 

et al., 2001) but also to coral genotypes (D’Croz and Maté, 

2004), with both factors likely playing an important role 

in adaptive responses by corals to climate change. Research 

on corals in Pacifi c Panamá additionally involves the taxonomy and biogeography of gorgonian soft corals (Vargas 

et al., 2008; Guzman and Breedy, 2008).

Molecular Evolution of Marine Organisms

STRI has played a leading role in development of molecular techniques for studies of marine organisms, not 

only in relationship to trans-isthmian biology of neotropical taxa (reviewed by Lessios, 2008) but also in studying 

the global biogeography of pantropical groups. A 30 year 

history of such work, the longest in SI, began with studies 

of sea urchins by Haris Lessios (Lessios, 1979). That work, 

although centered at the molecular laboraties at Naos 

Laboratory, has relied on all other STRI marine facilities 

for collections and maintenance of live organisms. Since 

that start, molecular evolution studies at STRI have undergone explosive growth. Such studies include assessments 

of effects of the rise of the isthmus on the ecology and biology of neotropical organisms (Collin, 2003a) and patterns 

and processes involved in the evolutionary divergence of 

such taxa (Knowlton and Weigt, 1998; Hurt et al., 2009). 

Molecular studies also have led to the delineation of species boundaries in marine organisms (Knowlton, 2000) 

and understanding of global historical biogeography of 

pantropical groups (Lessios et al., 1999, 2001; Collin, 

2003a, 2003b, 2005a; Quenoiville et al., 2004), invasions 

of the tropical Atlantic by Indo-Pacifi c taxa around southern Africa (Bowen et al., 2001; Rocha et al., 2005a), patterns of dispersal among different tropical biogeographic 

regions within the Atlantic (Lessios et al., 1999; Rocha 

et al., 2002, 2005b), physiological mechanisms involved 

in species formation (McCartney and Lessios, 2002; Zigler and Lessios, 2004), non-allopatric speciation within 

biogeographic regions (Rocha et al., 2005a; Puebla et al., 

2007, 2008), patterns and processes involved in speciation 

of corals (Fukami et al., 2004), and the history of two-way 

transfers of species across the 4,000– 7,000 km wide Eastern Pacifi c Barrier, the world’s widest stretch of deep open 

ocean (Lessios and Robertson, 2006). Molecular evolution studies at STRI have produced 163 marine-themed 

publications to date.

Marine Archaeology: Historical Human 

Reliance on Marine Resources in Panama

Zooarchaeology has played an important role in 

STRI’s anthropology program for the past 40 years (Linares and Ranere, 1980) through studies originated by Richard Cooke of pre-Columbian usage of marine resources 

in Panama, primarily in Panama Bay (Cooke, 1981). The 

expanding reference collection of 1,540 skeletons of 340 

species of fi shes and other organisms used in this research 

has also enhanced knowledge of the zoogeography of these 

organisms (Cooke and Jiménez, 2008b). This work has 

charted the time course of geographic changes in patterns 

of marine resource usage in Panama Bay. By 7,000– 4,500 

bp, humans on the shores of that bay exploited a wide 

variety of inshore marine resources, including more than 

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NUMBER 38 • 8 3

80 species of marine fi shes (bony fi shes, sharks, sawfi sh, 

sting rays) taken in a variety of different habitats (beaches, 

mangroves, estuaries, reefs, open water) using various 

methods (hook-and-line, nets, stationary wood-and-stone 

traps) (Cooke, 1992; Cooke and Jiménez, 2004, 2008a; 

Cooke et al., 2008). Other marine resources used include 

sea turtles, dolphins, manatees, and seabirds. The ritual 

importance of marine animals in pre-Columbian Panama 

is underlined by frequent images of sea turtles, fi sh, and 

marine invertebrates on pottery and goldwork (Linares, 

1977; Cooke, 2004a, 2004b). Although currently there 

is no convincing zooarchaeological evidence for overfi shing in pre-Columbian times in Panama, ongoing research 

in the Pearl Islands seems likely to identify pressures that 

produced changes to populations of mollusks and reef fi sh 

around individual islands. Intensive collection of colorful marine shells and marine birds for making ornaments 

likely led to local impacts on populations of these taxa.

RANCHERIA ISLAND FIELD STATION

Rancheria Island is situated in the center of the largest 

and best managed marine reserve in Panama: the Coiba 

National Park (and World Heritage Site) in the Gulf of 

Chiriqui. The park area has a long history of environmental protection (Coiba acted as a “free-range” prison 

island for almost 85 years) and hosts the largest area of 

coral reefs and richest [number of species] accumulation 

of corals on the entire continental shore of the TEP. A tiny, 

relatively undeveloped fi eld station at Rancheria has supported research on coral reefs in the surrounding area by 

Peter Glynn and his collaborators (see above).

THE RESEARCH VESSELS

Four vessels were operated by STRI between 1970 and 

2008: the 65-foot Tethys (1970– 1972), the 45-foot RV 

Stenella (1972– 1978), the 63-foot RV Benjamin (1978– 

1994), and the 96-foot RV Urraca from 1994 to 2008. 

None of those vessels was purpose built. The equipping of 

the Urraca, after its purchase, with an A-frame and oceanographic winch allowed intensive trawling and dredging 

activities (to depths of 250 m) and thus greatly extended 

the range of studies that could be supported beyond the 

previous emphasis on scuba-based research. These research vessels, and particularly the Urraca, enabled fi eldwork in remote locations that lacked land bases for marine 

research and thus vastly extended the geographic reach of 

STRI biologists. The Urraca acted as such a base not only 

throughout Panama’s territorial waters but also in localities as far afi eld as Clipperton Island (1,000 km west of 

Acapulco) in the Pacifi c (Robertson and Allen, 2008) and 

Honduras in the Caribbean (Guzman, 1998).

To date, 14 years service by the Urraca has produced 

350 scientifi c publications. Research supported by the Urraca proved vital to the declaration of two large Marine 

Protected Areas (MPAs) on the Pacifi c coast of Panama, 

principally through the research activities of H. Guzman 

on coral diversity and conservation (see below). Urraca

support of collecting along the entire Pacifi c coast of Panama, as well as Costa Rica, Clipperton and Cocos Islands 

(remote oceanic islands in the eastern Pacifi c), and El Salvador was essential for the development of the world’s fi rst 

online information system on a regional shorefi sh fauna 

(www.stri.org/sftep). In addition the Urraca provided extensive and extended support to the Panama Paleontology 

Program (see below) and for collecting fi shes (Bermingham, Robertson), echinoderms (Lessios), soft corals (Guzman), and mollusks (Collin) for taxonomic and evolutionary studies, and hydrologic surveys (D’Croz).

HISTORICAL MARINE ECOLOGY: 

THE PANAMA PALEONTOLOGY PROJECT

STRI is unique in having an institutional marine program that includes both biology and geology, as well as 

a series of strong programs in various aspects of tropical 

terrestrial biology. Intellectual cross-fertilizations between 

scientists steeped in terrestrial and marine systems have 

maintained STRI as a place known for creative research.

The striking differences in environmental conditions 

and ecology from opposite sides of the Isthmus of Panama 

today, and their changes over time during Isthmus closure, 

provides marine paleontologists with a “natural experiment” with which to address, on an evolutionary and ecologically large scale, the impact of environmental change 

and genetic isolation on marine invertebrate faunas. In 

1986 the Panama Paleontology Project (PPP) was initiated 

by Jeremy Jackson and Anthony Coates. Their aim was to 

survey coastal sediments of the isthmian area to establish 

if the fossil record were suffi ciently complete to explore 

the evolutionary responses of marine communities to the 

gradual emergence of the Isthmus of Panama.

Stratigraphically complete Neogene deposits were 

soon discovered in the Panama Canal basin and Bocas 

del Toro, and excavations were subsequently extended 

to several other richly fossiliferous regions of Panama 

and Costa Rica, Venezuela, Ecuador, Jamaica, and the 

Dominican Republic. In addition, large-scale benthic 

05_Robertson_073-094_Lang.indd 83 5_Robertson_073-094_Lang.indd 83 9/24/09 9:24/24/09 9:24
8 4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

surveys of modern shallow-water communities across the 

Caribbean and Tropical Eastern Pacifi c serve as a baseline 

for understanding biotic changes through geological time.

The PPP has so far involved more than 50 scientists 

from 20 institutions in seven countries and undertaken 

almost 40 expeditions to eight countries. The resultant 

collections comprise thousands of replicated samples and 

many millions of individual, quantitatively collected fossil 

specimens. The rigorous paleontological framework of the 

PPP presents evolutionary biologists with a unique view 

of 15 million years of life and environments in a tropical 

region. Using these samples and framework, the PPP has 

documented the environmental, lithologic, and biological 

changes in Isthmian nearshore marine habitats from 15 

Ma to the present day, producing almost 200 publications 

to date (see http://www.fi u.edu/collinsl/pppcon.html).

Placing igneous and sedimentary rock formations in 

sequence established a high-resolution stratigraphic system that was critical to effectively reconstruct patterns 

of biological change (Coates et al., 1992, 2005; Collins 

et al., 1996b; Collins and Coates, 1999). Aligned with 

taxonomic and paleoenvironmental analyses, these geological studies also permit reconstructions of land and 

water masses as the isthmus shoaled, providing dates of 

fi nal closure that are essential for estimates of the timing 

of divergence of modern marine organisms (Collins et al., 

1995; Coates and Obando, 1996) (Figure 3).

Data from PPP studies have revealed the following. 

(i) Faunal composition of Caribbean and Pacifi c fossil assemblages and the timing of paleoenvironmental change 

demonstrate that major cross-isthmian marine connections ceased approximately 3 Ma (Collins et al., 1995, 

1996a; Coates et al., 2003, 2005; O’Dea et al., 2007a), 

consistent with dates from previous (non-PPP) oceanographic studies. (ii) Seasonal upwelling was strong in 

what is now the southwestern Caribbean (SWC) before 

isthmian closure, and constriction of the forming isthmus 

led to a rapid decline in upwelling intensity, resulting in 

a collapse in primary productivity from around 5 to 3 

Ma (Collins, 1996). The increasing oligotrophy allowed 

reefal habitats to expand in the SWC while reducing the 

amount of fi lter-feeding molluscan habitat, and the cessation of upwelling also stabilized environments to modernFIGURE 3. Formation of the Isthmus of Panama during the last 20 

million years (Ma  million years ago). Arrows indicate direction of 

principal water fl ow through the Central American Seaway. (From 

O’Dea et al., 2007b.)

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NUMBER 38 • 8 5

day conditions (O’Dea et al., 2007a; Jackson et al., 1999). 

Meanwhile, upwelling continued in what is now the TEP 

to the present day. (iii) A wide assortment of marine taxa 

experienced a major turnover in the now-SWC during the 

last 10 million years (Jackson et al., 1993; Jackson and 

Johnson, 2000; O’Dea et al., 2007a; Smith and Jackson, 

2009). Origination of new species in all major groups of 

macroinvertebrates peaked at about 5– 3 Ma, coincident 

with the formation of new habitat along the SWC coast 

of the Isthmus. (iv) From approximately 5– 3 Ma the SWC 

remained connected to the TEP but coastal conditions became instable. This transition period saw most SWC faunas reach their peaks in diversity (Jackson and Johnson, 

2000; Todd et al., 2002; Smith and Jackson, 2009). As old 

and new species coexisted in time, richness of most groups 

was around 30% to 60% higher than in the modern SWC. 

(v) Following isthmus closure and the birth of the modernday Caribbean, a widespread extinction reduced numbers 

of gastropod, bivalve, coral, and bryozoan taxa by 30% 

to 95%. (vi) This massive extinction was strongly selective against nutriphilic taxa, indicating that the collapse 

in primary productivity was the causal mechanism. However, fi ne-scale environmental and community composition data reveal that extinction in most groups lagged well 

behind the shift to more oligotrophic conditions as the 

Isthmus closed (O’Dea et al., 2007a) (Figure 4). Time lags 

of this scale challenge the conventional wisdom that cause 

and effect have to be contemporaneous in macroevolution. (vii) Other ecological characteristics of organisms 

also shifted dramatically. Average coral colony and snail 

egg-size increased, larval durations of scallops decreased, 

and rates of clonality in free-living bryozoans declined 

dramatically. Ongoing fi eld and laboratory work aims to 

analyze the fates and trajectories of clades that preserve 

modes of life, life histories, and feeding strategies in fossils within the rigorous framework provided by the PPP. 

This approach will help tease apart the drivers of macroevolutionary change in the neotropical seas (Jackson and 

Erwin, 2006).

MARINE EDUCATION AND OUTREACH

At the level of both the institution and the individual 

scientist, STRI, along with other SI bureaus, has become 

deeply involved in two global efforts connected with 

marine biodiversity: the Census of Marine Life (COML) 

and the Consortium for the Barcode of Life (CBOL). 

The COML aims to provide rapid and full documentation of marine biodiversity, while CBOL provides easy 

FIGURE 4. The sequence of environmental and ecological changes in the southwest Caribbean in response to the closure of the isthmus of 

Panama (Ma  million years ago). A. Upwelling intensity, as estimated by the mean annual range of temperature (MART), shifted rapidly from 

high values similar to the modern-day tropical eastern Pacifi c values to modern Caribbean values. B. Carbonate levels in sediments followed 

suit, with an increase in the Caribbean. C. Biotic assemblages shifted from mollusk-dominated to a mix of coral-, algae-, and mollusk-dominated 

communities (PCA  principal components analysis). D. Extinction rates of corals and mollusks peaked 1– 2 million years after the environmental and ecological changes. (From O’Dea et al., 2007a.)

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8 6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

molecular means to confi rm the identities of a broad array of species in both marine and terrestrial ecosystems. 

Substantial contributions of information on neotropical marine organisms have been made by STRI to both 

those efforts. Recently, the Encyclopedia of Life (EOL) 

began to make use of information generated by STRI scientists, and STRI also recently became part of the United 

States Geological Survey’s Caribbean tsunami monitoring network.

Educational and outreach programs at STRI include a 

marine fellowship program for graduate students (worldwide, plus targeted to Latin America), hosting of K– 12 

school groups and teacher training (at Galeta Point Marine Laboratory and Bocas del Toro Research Station), 

conducting public seminars, responding to requests for 

information from Panamanian government entities, and 

supporting graduate student courses. The public marine 

education program at STRI consists of a series of activities aimed at promoting awareness and conservation of 

marine environments and communicating its research to 

the general public. Since 1992 the program has consisted 

of docent-led educational visits, seminars for teachers, and 

the development of educational materials (posters, newspapers and supplements, exhibits), and curricular materials for the classroom.

CULEBRA ISLAND EDUCATION CENTER

The Punta Culebra Nature Center (PCNC) of STRI 

lies at the Pacifi c entrance to the Panama Canal immediately adjacent to the Naos Laboratory. For nearly a 

century, access to Culebra was restricted to U.S. military 

personnel, a practice that protected Culebra’s shoreline 

organisms, which now exist in abundances not seen elsewhere in Panama Bay. The general health of the intertidal 

and shallow-water marine communities at Culebra makes 

the area especially attractive for research. Culebra has 

been a major research site for John Christy (since 1983), 

Mark Torchin (since 2004), and their students.

The PCNC relies on the support of the Smithsonian 

Foundation of Panama and international entities. The academic and public programs at Culebra encourage direct 

experiences with organisms in the local habitats and in 

touch pools. Exhibits promote environmental awareness, 

understanding, and conservation, emphasizing marine systems. Since it opened in 1996, 750,000 people have visited 

PCNC, with about 25,000 schoolchildren annually taking 

part in its educational program. The PCNC also fosters research on site, which allows visitors to see STRI scientists 

and students “in action.”

GALETA POINT MARINE LABORATORY

The education and outreach program at Galeta Laboratory was initiated by Stanley Hecakdon in 2000 to build 

bridges between research at Galeta on coral reefs, seagrass 

beds, and mangrove forests and the schools of Colon and 

wider Panama. The program seeks to motivate public 

interest on the importance of the sciences and the value 

of coastal tropical habitats, currently under severe threat 

because of a destructive style of economic development. 

Private donors have been vital to the success of this program, funding the construction of enhancements to Galeta 

buildings, a 300 m long mangrove boardwalk, and science 

equipment used by the program.

Attendance in the student education program climbed 

from 200 from an orphanage in nearby Colon in 2000 to a 

current 10,000 per year from all over Panama. These programs are hosted by 12 nature guides and 19 volunteers. 

Recently, the fi rst live Internet broadcast was made from 

Galeta to elementary schools in New Jersey. The next step 

will be an online program to schools in Colon and, eventually, the rest of Panama. Galeta’s public outreach program began in 2003 with the support of students from 

McGill University’s “Panama Field Semester Studies.” The 

fi rst project was a socioeconomic study of a local fi shing 

community, with fi shermen then being trained in nature 

tourism to provide an alternative source of income. In 

2006 Galeta began the Smithsonian Talk of the Month, 

at which STRI researchers share their work with the people of Colon. Teacher training aimed at raising the quality of science education in Colon started in 2007. To date 

120 local elementary and high school teachers have been 

trained. Galeta laboratory also participates in a variety of 

community events: the yearly community beach cleanup; 

scientifi c and environmental fairs; and events such as Bio 

Diversity Day, World Mangrove Day, and Earth Day.

BOCAS DEL TORO RESEARCH STATION

The BRS has had active public programs, almost entirely funded by income from station fees, since the completion of the main laboratory building in 2003. Activities organized by the BRS for the general public include 

bimonthly public seminars given by researchers working 

at the station as well as weekly open houses and an annual 

Earth Day beach clean-up. In addition the Station opens 

its doors to the public during the annual Feria Ambiental weekend, at which environmental non-governmental 

organizations (NGOs) and governmental organizations 

from the region present information to the public, debate 

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NUMBER 38 • 8 7

local conservation issues in a round-table format, and give 

public lectures on their projects. This Feria has proven to 

be highly successful, with representatives form organizations such as IUCN (International Union for Conservation 

of Nature) and The Nature Conservancy attending from 

Costa Rica and Panama City.

The BRS also has an active program working with local schools. School groups visit the station three days a 

week during the school year, and a biodiversity summer 

program is available for interested children on Isla Colon 

and Bastimentos. More than 1,000 children per year participate in these programs or, in more remote areas, receive 

visits from presenters of the public programs. Finally, the 

Station presents an annual teacher training workshop, 

which offers teachers development credit for learning 

about environmental issues and conservation.

The BRS is also active in undergraduate and graduate 

teaching. The station hosts undergraduate courses from 12 

institutions from the USA, Colombia, Canada, and Germany and trains graduate students in the advanced Training in Tropical Taxonomy Program. This program aims to 

bring taxonomic experts and experts in training together 

in the fi eld to provide hands-on training in taxonomy. This 

program focuses on groups for which taxonomic expertise 

is in immediate danger of disappearing. This program, the 

only one of its kind in the Neotropics, has so far trained 

100 students from 30 countries and receives some funding from the National Science Foundation Pan-American 

Advanced Studies Institutes (NSF PASI) program as well 

as individual Assembling-the-Tree-of-Life grants.

The Online BRS Bilingual Biodiversity Database

The public face of the Bocas del Toro Research Station 

extends into cyberspace. The Online BRS Bilingual Biodiversity Database, available at http://biogeodb.stri.si.edu

/bocas_database/?&langeng, has resulted from work at 

the BRS and now includes 6,000 species and 8,000 photos 

of organisms from Bocas del Toro province. This website 

is supplemented by printed identifi cation guides to local 

organisms (Collin et al., 2005).

MARINE ZOOARCHAEOLOGY

The zooarchaeology reference collection at STRI is 

frequently used by students and researchers to identify 

archaeofaunal materials. Specimens are often loaned or 

donated to outside institutions. Panamanians have strong 

interests in their cultural heritage, and STRI zooarcheologists frequently give public lectures in Panama on the 

history of human– animal interactions in Panama and the 

relevance of zooarchaeology to tropical zoogeography 

and biodiversity. STRI’s Bioinformatics offi ce recently 

started work on an online database that will provide photographic, geographic, and biometric information on all 

identifi ed zooarchaeological materials and specimens from 

Panamanian sites.

ONLINE INFORMATION SYSTEM ON TROPICAL EASTERN

PACIFIC SHOREFISHES

This Shorefi shes of the Tropical Eastern Pacifi c Online 

Information System (www.stri.org/sftep) exemplifi es the 

Smithsonian’s commitment to carrying information that 

its research generates to the widest possible audience. It 

provides free, public access to comprehensive information 

on the biology of almost 1,300 shorefi sh species. Systems 

such as these are useful for managers, biologists, students, 

and fi shers wanting to identify fi shes and obtain information about their biology. The information that systems such 

as this bring together allows comprehensive assessments 

of our level of knowledge about biodiversity (Zapata and 

Robertson, 2006) and regional geographic distribution of 

that diversity (Mora and Robertson, 2005; Robertson and 

Cramer, 2009).

MARINE CONSERVATION ACTIVITIES

The work that STRI biologists, notably Hector 

Guzmán, have done on organisms as diverse as corals, 

sea cucumbers (Guzman et al., 2003), conchs (Tewfi k and 

Guzman, 2003), lobsters, and crabs (Guzman and Tewfi k, 2004) has been instrumental in the establishment not 

only of management regulations for specifi c organisms 

but also of a large marine reserve on the Pacifi c coast of 

Panama: the Pearl Islands Special Managment Area in the 

Gulf of Panama (Guzman et al., 2008a). In addition, efforts by Todd Capson and research on corals by Hector 

Guzman (see Guzman et al., 2004) were instrumental in 

the declaration of Coiba National Park (where Rancheria 

Island is situated) as a World Heritage Site in 2005. In 

2009 Panama’s government established the Matumbal Reserve, a STRI-managed marine reserve that protects 34 ha 

of reefs, seagrass beds, and mangroves immediately adjacent to BRS. This reserve will ensure maintenance of the 

research potential of the station in an area of explosive 

tourism and developmental growth. During 2008– 2009 

STRI (primarily through the efforts of Juan Maté) has 

been involved with the recently completed development 

05_Robertson_073-094_Lang.indd 87 5_Robertson_073-094_Lang.indd 87 9/24/09 9:24/24/09 9:24
8 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of a comprehensive zoning and management plan for 

Coiba Park and workshops aimed at informing government resource managers about the utility, methods, and 

needs of STRI’s marine research activities.

The online information system on TEP shorefi shes 

(see above) provided the primary database used in the 

fi rst comprehensive IUCN Redlist Assessment of an entire regional shorefi sh fauna through workshops held in 

Costa Rica (2008) and Panama (2007). An equivalent information system encompassing more than 1,500 species 

of Greater Caribbean shorefi shes, currently in production, 

will facilitate an equivalent Redlist assessment planned for 

the Greater Caribbean regional shorefi sh fauna.

Marine conservation activities by STRI staff also have 

a global and historical reach through the work of J. B. C. 

Jackson and colleagues on historical declines of coral reef 

growth and organisms induced by human activities, and 

the depletion of their marine resources, in the Caribbean 

area and throughout the rest of the tropics (Jackson, 1997, 

2001; Jackson et al., 2001; Pandolfi et al., 2003, 2005; 

Pandolfi and Jackson, 2006).

BRS has been a member of CARICOMP (the Caribbean Coastal Marine Productivity Program) since 1997, 

contributing data to Caribbean-wide monitoring of seagrasses, corals, and mangroves (Collin, 2005a; Collin et 

al., 2009; Guzman et al., 2005). BRS also recently became 

part of a global IUCN program to assess the resilience of 

coral reefs worldwide. As part of this program, rapid assessments of the state of coral reefs at each site are linked 

to long-term monitoring of physical environmental data to 

predict the local response to future bleaching stress from 

elevated temperatures. Since 2000 STRI has also been involved with Conservation International, the United Nations Environmental Program, the International Union 

for the Conservation of Nature, and the governments of 

Panama, Costa Rica, Colombia, and Ecuador in an effort 

to develop the Eastern Tropical Pacifi c Seascape. This 2.1 

million km2 marine conservation area, in the equatorial 

part of the TEP, is based on a cluster of Marine Protected 

Areas, among them the Coiba National Park (see also 

Guzman et al., 2008a).

2008— A TIME OF TRANSITION

After 48 years and 1,800 publications the marine program, which remains an integral part of research at STRI, 

is undergoing rapid change. The year 2008 marked the 

end of an era, with the retirement of Ira Rubinoff and the 

succession of Eldredge Bermingham as STRI director. It 

also marked the start of a hiatus in the research vessel program, with the retirement of the RV Urraca, as its absence 

leaves a signifi cant gap in research capability that STRI 

seeks to rapidly fi ll. The continuing development of the 

laboratory at Bocas del Toro will open up new opportunities for research. The development of a facility at Rancheria Island, and, perhaps, the Pearl Islands would greatly 

enhance accessibility of coral reefs and other marine habitats in the two largest nearshore archipelagos in the equatorial part of the eastern Pacifi c, archipelagos that to date 

have experienced relatively low impacts from economic 

development. STRI geologist Carlos Jaramillo is currently 

taking advantage of a unique event— major excavations 

to widen the Panama Canal— to clarify the history of the 

formation of the isthmus and thus help shed light on the 

history of changes in the neotropical marine ecosystems 

and the evolution of their organisms. In future STRI also 

will emphasize the development of tools that exploit the 

World Wide Web to enhance the diffustion of knowledge 

derived from its marine research, both through its own 

Bioinformatics offi ce and through participation in global 

enterprises such as the Census of Marine Life, the Consortium for the Barcode of Life, and the Encyclopedia of Life. 

STRI’s marine program will play an increasingly important role in efforts to understand the role of the oceans in 

global climate variability, interactions between terrestrial 

and marine ecosystems, and the response of marine ecosystems to climate change and more direct human-induced 

stresses.

ACKNOWLEDGMENTS

STRI’s marine program thanks Panama for its cooperation in hosting STRI, and for the long-term support of the Panamanian government entities that manage marine resources and marine reserves and cooperate 

with STRI’s research activities (the Autoridad Maritima 

de Panamá, the Autoridad Nacional del Ambiente, and 

the Autoridad de los Recursos Acuaticos de Panamá). 

Many local and international donors have contributed 

generously to the development of STRI facilities and to 

its education and research programs, notably D. Cofrin, 

F. Hoch, P. Peck, K. and E. Himmelfarb, the Upton Trust, 

and the Fundación Smithsonian de Panamá. Marine science at STRI also has benefi tted immensely over the years 

from grants made by the National Science Foundation, 

the Secretaría Nacional de Ciencia Tecnología de Panamá (SENACYT), Conservation International, the Darwin Initiative, the Nature Conservancy, the National 

Geographic Society, and various Smithsonian entities: the 

05_Robertson_073-094_Lang.indd 88 9/29/09 1:49
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Scholarly Studies Program, the Women’s Committee, the 

Hunterdon and Johnson Oceanographic Research Funds, 

and the Marine Science Network.

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Protandric Simultaneous Hermaphroditism 

Is a Conserved Trait in Lysmata (Caridea: 

Lysmatidae): Implications for the Evolution 

of Hermaphroditism in the Genus

J. Antonio Baeza

ABSTRACT. Shrimps from the genus Lysmata are unusual because of their peculiar 

sexual system. Individuals in a population fi rst reproduce as males, to change later in life 

to functional simultaneous hermaphrodites. The evolutionary origin of this sexual system, called protandric simultaneous hermaphroditism (PSH), is a longstanding question 

overdue for consideration. A previously proposed “historical contingency” hypothesis 

suggested that PSH evolved in the tropics from an ancestral protandric species of Lysmata that became socially monogamous and symbiotic with sea anemones. The restricted 

probability of encountering mating partners by shrimps because of their association with 

their hosts would have favored PSH. Here, I fi rst provide evidence that PSH is a fi xed 

trait within the genus. Second, I examine whether the historical contingency hypothesis 

appropriately explains the origin of PSH in the genus. Using anatomical observations 

and laboratory experiments combined, I demonstrate that two shrimps from the genus 

Lysmata, L. galapagensis and L. boggessi, feature PSH. Study of museum specimens suggests that nine other species of Lysmata are protandric simultaneous hermaphrodites. 

The foregoing information indicates that PSH represents a fi xed trait in the genus Lysmata. Ancestral character state reconstruction using Bayesian inference allowed testing 

whether the ancestral Lysmata featured a symbiotic lifestyle and a socially monogamous 

mating system, as proposed by the historical contingency hypothesis. In agreement with 

this hypothesis, analysis indicated that the most common recent ancestor of Lysmata was 

most likely socially monogamous. However, the ancestral lifestyle was equally likely to 

be free-living or symbiotic. Thus, the present study provides partial support for the historical contingency hypothesis. Studies on the sexual system and lifestyle of more species 

and development of a more robust phylogeny are needed to reveal the evolutionary origin 

of PSH in the genus Lysmata.

INTRODUCTION

In decapod crustaceans, the greatest diversity of sexual systems is found in 

the infraorder Caridea. Most caridean shrimps are gonochoric, with individuals 

in a population producing only male or female gametes during their entire life. 

Well-studied examples include Rhynchocinetes typus (Correa et al., 2000), Hippolyte obliquimanus (Terossi et al., 2008), Pontonia margarita (Baeza, 2008a), 

and Hippolyte williamsi (Espinoza-Fuenzalida et al., 2008). The second most 

common sexual system is protandry. In at least 31 species of shrimps, individuals in a population reproduce fi rst as males and change to females later in life 

J. Antonio Baeza, Smithsonian Tropical Research 

Institute, Panama, and Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort Pierce, 

Florida 34949, USA (baezaa@si.edu). Received 9 

June 2008; accepted 20 April 2009.

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9 6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

(Bauer, 2000). Although several variants of protandry 

have been reported (e.g., protandry with primary females 

in Crangon crangon; Schatte and Saborowski, 2006), no 

study has reported protogyny (changing sex from female to 

male) among shrimps. Most recently, a particular variant 

of simultaneous hermaphroditism, that is, adolescent protandry sensu Ghiselin (1974), protandric cosexuality sensu 

Policansky (1982), or protandric simultaneous hermaphroditism (PSH) sensu Bauer (2000), has been described for 

shrimps from the genera Lysmata (Baeza et al., 2008) and 

Exhippolysmata (Kagwade, 1982; Braga et al., 2009). It 

must be noticed that a recently developed molecular phylogeny for Lysmata and other related genera demonstrated 

that the genus Exhippolysmata represents a derived group 

of shrimps within the genus Lysmata (Baeza et al., 2009). 

Thus, species of Exhippolysmata are treated here as members of the genus Lysmata.

In protandric simultaneous hermaphroditic shrimps, 

juveniles consistently mature as functional male individuals (also called male-phase [MP] shrimps; Bauer and Holt, 

1998) bearing typical caridean male characters (i.e., coupling hoods and appendix masculina on the fi rst and second pleopods, respectively) (Bauer and Holt, 1998; Baeza, 

2008b; Baeza and Anker, 2008; Baeza et al., 2008). These 

functional males later attain female sexual function and 

develop into functional simultaneous hermaphrodites 

(hereafter, hermaphrodites; but also called female-phase 

[FP] shrimps; Bauer and Holt, 1998). Resembling females 

of caridean gonochoric species, hermaphrodites mate as 

females shortly after molting, spawn oocytes to an abdominal chamber where fertilization takes place, and brood 

their embryos for relatively long periods of time (e.g., 

10– 15 days in Lysmata wurdemanni; Baeza, 2006). These 

hermaphrodites retain testicular tissue, male ducts, and 

gonopores and thus have the ability to reproduce as both 

male and female (Bauer and Holt, 1998). After becoming 

hermaphrodites, individuals do not revert to males (Baeza, 

2007a), and no self-fertilization has been demonstrated 

(Bauer and Holt, 1998; Baeza, 2008b; Baeza and Anker, 

2008; Baeza et al., 2008).

So far, the various studies on the sexual biology of 

shrimps from the genus Lysmata suggest that all species 

exhibit PSH. Protandric simultaneous hermaphroditism 

is suspected to be a fi xed trait in the genus. Nonetheless, 

additional information from more species is needed to 

confi rm this notion. In turn, other life history traits differ 

within these two genera. Shrimps have been reported to 

inhabit the shallow subtidal and intertidal of subtropical 

and tropical rocky and coral reefs around the world. Some 

species of Lysmata live in groups, others are solitary, while 

some species are socially monogamous (pair-living; e.g., 

L. grabhami (Gordon, 1935)) (Wirtz, 1997). Several species with an inconspicuous coloration dwell freely among 

rocks in temperate zones, while other more colorful species inhabit tropical sponges (L. pederseni Rhyne and Lin, 

2006) (Rhyne and Lin, 2006). Other strikingly brilliant 

species clean fi shes (L. amboinensis (De Man, 1888)) 

(Limbaugh et al., 1961). Species from this genus represent 

ideal candidates to explore the role of ecological conditions in explaining evolutionary innovations in the marine 

environment (see Baeza and Thiel, 2007).

Recent studies have examined various aspects of the 

biology of various Lysmata and Exhippolysmata shrimps 

(Baeza, 2008b; Baeza and Anker, 2008; Baeza et al., 2008; 

Lopez-Greco et al., 2009). Furthermore, shrimps from the 

genera Lysmata and Exhippolysmata are currently being 

used as models in evolutionary biology and behavioral 

ecology because of their peculiar sexual system (Baeza and 

Bauer, 2004; Baeza, 2006, 2007a, 2007b, 2007c). In spite 

of the increasing knowledge regarding the behavior and 

ecology of several species of Lysmata, the evolutionary 

origins of PSH in the genus remain uncertain. Although 

recent studies have shown that the variety of lifestyles 

of Lysmata is greater than originally recognized (Baeza, 

2008b; Baeza and Anker, 2008; Baeza et al., 2008), an 

emerging dichotomy in social organization and ecology 

was noted in initial studies. One group of species (named 

“Crowd” species by Bauer, 2000) was described as inhabiting warm subtropical environments, occurring as dense 

aggregations in their refuges, and exhibiting no specialized 

fi sh-cleaning behavior (i.e., L. californica: Bauer and Newman, 2004; L. wurdemanni: Baeza, 2006). A second group 

(named “Pair” species by Bauer, 2000) was described as 

mostly tropical, occurring at low densities in the subtidal, 

and dwelling as socially monogamous pairs on sea anemones used as spots for fi sh-cleaning activities (i.e., L. grabhami: Wirtz, 1997; L. amboinensis: Fiedler, 1998). Based 

on this initial dichotomy, Bauer (2000) proposed that PSH 

evolved in the tropics from an ancestral symbiotic protandric species of Lysmata that became a specialized fi sh 

cleaner. Restricted mobility of individuals resulting from 

their association with the host and, hence, reduced probability of encountering mating partners would have favored PSH (also see Bauer, 2006). Under such a scenario, 

the “Crowd” warm temperate species that do not exhibit 

specialized cleaning behaviors would have evolved from 

tropical species with specialized cleaning behaviors and 

more complex mating systems (Bauer, 2006). A recent 

phylogeny developed for the genus found no support for 

Bauer’s hypothesis because socially monogamous species 

06_Baeza_095-110_Lang.indd 96 6_Baeza_095-110_Lang.indd 96 9/24/09 9:22/24/09 9:22
NUMBER 38 • 9 7

presented a more derived position than gregarious species 

(Baeza et al., 2009). However, no formal testing of Bauer’s 

ideas was conducted. Current advances in ancestral character state reconstruction using Bayesian inference (Pagel 

et al., 2004) make it possible to test whether the ancestral 

Lysmata featured a symbiotic lifestyle and a socially monogamous mating system, as proposed by Bauer (2000).

Here, I provide evidence that PSH is a fi xed trait 

within the genus Lysmata (including Exhippolysmata), 

as suspected by previous studies (see Bauer, 2000; Baeza, 

2008b; Baeza and Anker, 2008; Baeza et al., 2008). 

For this purpose, I examined the sexual system of two 

shrimps from the genus, L. galapagensis Schmitt, 1924 

and L. boggessi Rhyne and Lin, 2006, using anatomical observations and laboratory experiments. I also examined specimens from another nine species deposited 

at the National Museum of Natural History (NMNH), 

Washington, D.C. The information altogether strongly 

suggests that PSH is a conserved trait within the genus 

Lysmata. My second goal was to examine Bauer’s (2000) 

hypothesis regarding the evolution of PSH in Lysmata. 

I tested whether the ancestral Lysmata was socially monogamous (1) and strictly symbiotic with, for example, 

sea anemones (2), as proposed by this author. To accomplish this second goal, a review of the literature on the 

socioecology of Lysmata was conducted. Next, the lifestyle of shrimps was mapped onto the phylogeny of the 

genus, and the likelihood of specifi c traits to occur at 

particular ancestral nodes in the phylogeny was tested.

METHODS

COLLECTION AND MAINTENANCE OF SHRIMPS

Individuals from the two studied species were collected 

between February and August, 2006, at different localities 

in Panama and Florida, USA. Individuals from L. boggessi

were collected at night during low tides from seagrass beds 

at Madelaine Key (27°3851.87N, 82°4256.50W), Fort 

De Soto National Park, Florida. Specimens from L. galapagensis were collected from Islas Secas (7°5837.54N, 

82°0218.02W), Gulf of Chiriqui, Panama. Immediately after collection, specimens were transported to the 

R/V Urraca and then to the Naos Marine Laboratories, 

Panama (L. galapaguensis) or directly to the Smithsonian 

Marine Research Station at Fort Pierce, Florida (L. boggessi). Individuals were maintained in 15– 70 L aquaria at 

a water temperature of 22°– 33°C and 34– 36 ppt salinity 

and were fed every other day with shrimp pellets before 

being selected for dissections or experiments.

DISSECTIONS

Observations on reproductive anatomy were conducted as in Baeza (2008b) in a total of six specimens of 

each species, three presumptive males (3.6– 3.8 and 4.0– 4.6 

mm carapace length [CL] in Lysmata galapagensis and L. 

boggessi, respectively) and three presumptive hermaphrodites that were brooding embryos (4.4– 5.1 and 6.5– 5.6 mm 

CL in Lysmata galapagensis and L. boggessi, respectively). 

First, the presence or absence of male gonopores on the 

coxae of the fi fth pereiopods was recorded for each individual. Individuals with male gonopores (all) had sperm 

collected from the ejaculatory ducts using short electric 

shocks that results in the ejection of a spermatophore (as 

noted in Baeza, 2006, 2007c). Each individual was then 

dissected to extract the gonad for examination under the 

stereomicroscope. Finally, the fi rst and second pleopods 

were dissected and the presence or absence of appendices internae and masculinae, respectively, were recorded. 

Specimens were defi ned as males or hermaphrodites by the 

presence (males) or absence (hermaphrodites) of coupling 

hooks (cincinnuli) and appendices masculinae on the endopods of the fi rst and second pleopods, respectively (see 

Baeza, 2007c, 2008b).

EXPERIMENTS

Three experiments, as described in Baeza et al. 

(2008) and Baeza (2008b), were conducted to determine 

the sexual system of the three species under study. In 

summary, the different experiments determined whether 

(1) brooding shrimps (reproducing as females) were capable of mating as males, (2) brooding shrimps were capable of 

self-fertilization, and (3) males were capable of becoming 

hermaphrodites with time (see Results). In the fi rst experiment (n  5), pairs of brooding shrimps were maintained 

in 21 L aquaria. In the second experiment, fi ve brooding 

shrimp were each maintained alone. In the third experiment (n  5), pairs of males (small nonbrooding shrimp 

with no externally visible female gonads and visible cincinnuli and appendices masculinae) were maintained 

separately in 21 L aquaria for at least 50 days. Individuals were examined daily for hatching of the embryos, the 

presence of exuvia from molting, development of mature 

oocytes in the gonad (visible through the carapace), and 

spawning of a new batch of eggs. The development of any 

newly spawned embryos was examined in detail after four 

days of spawning.

Following the rationale developed by Baeza et al. 

(2008), if in the fi rst experiment ovigerous shrimps that 

06_Baeza_095-110_Lang.indd 97 6_Baeza_095-110_Lang.indd 97 9/24/09 9:22/24/09 9:22
9 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

paired together produced normally developing broods, 

then it was inferred that either the other ovigerous shrimp 

in the aquarium acted as a male to inseminate its partner, 

or that the shrimp was capable of self-fertilization. If in the 

second experiment shrimps in isolation failed to successfully produce and brood developing eggs, then the possibility of self-fertilization was eliminated. If in the third experiment individuals identifi ed as males at the beginning of the 

experiment developed the ovarian portion of the ovotestis 

and produced eggs, then I inferred that male shrimps mature as hermaphrodites (see Baeza et al., 2008).

POPULATION STRUCTURE, SEX RATIO, AND ABUNDANCE

Information on the abundance, population structure, 

and sex ratio (males to hermaphrodites) of each species 

was collected from the fi eld. The carapace length (CL) and 

number of shrimps of each sexual phase and each species 

captured during the different samplings were recorded. 

The sampling effort (total number of hours spent collecting shrimps) was calculated for each sampling event. Relative abundance of shrimps was estimated by dividing the 

sample abundance (number of shrimps captured) by the 

sampling effort.

MUSEUM SPECIMENS

Specimens from nine different species of Lysmata deposited at the Collection of Crustaceans, National Museum of Natural History (NMNH; Smithsonian Institution, Washington, D.C.) were examined. Dissection of 

specimens pertaining to the collection was not possible because only a few individuals were available from several of 

the examined species and many of the specimens were part 

of the type series used to describe the species. Therefore, 

the identifi cation of males and hermaphrodites was mostly 

based on external morphological characters (see foregoing). When identifying sexual phases, particular attention 

was given to the presence of male gonopores at the base 

of the coxae of the fi fth pair of pereiopods in brooding 

shrimps as a likely indicator of simultaneous hermaphroditism (see Results).

TESTING THE HISTORICAL CONTINGENCY HYPOTHESIS

To examine whether the historical contingency hypothesis proposed by Bauer (2000) appropriately explains 

the origins of PSH in shrimps from the genus Lysmata, the 

lifestyle (in terms of the propensity to develop symbiotic 

partnerships and natural group size) was reconstructed 

using BayesTraits (Pagel and Meade, 2006; available at 

www.evolution.rdg.ac.uk).

A pruned set of sequences (from the 16S mitochondrial 

gene) recently published by Baeza et al. (2009) was used to 

generate a phylogenetic hypothesis for the group on which 

to reconstruct the evolution of lifestyles in shrimps. The 

sequences pertained to 20 species of Lysmata and Exhippolysmata plus 3 other species (Merguia rhizophorae, Hippolyte williamsi, and H. inermis) used to root the trees 

during the initial phylogenetic analysis. The set of aligned 

sequences was fi rst imported to BayesPhylogenies (Pagel 

et al., 2004) to obtain a Bayesian posterior distribution 

of phylogenetic trees. Metropolis coupled– Markov chain– 

Monte Carlo analyses were conducted using a GTR  I 

(invariant)  G (gamma) model of nucleotide substitution. The analysis was run on two different simultaneous 

chains. A total of 6,000,000 iterations were conducted, 

and sampling was performed every 100th tree. The last 

1,000 posterior probability trees generated by BayesPhylogenies were then imported to BayesTraits. The submodule MultiState in BayesTraits uses Markov chain Monte 

Carlo (MCMC) methods to infer values of traits (that 

adopt a fi nite number of discrete states) at ancestral nodes 

of phylogenies. Additionally, this method permits testing 

for particular ancestral characters at specifi c nodes taking 

phylogenetic uncertainty into account (Pagel et al., 2004).

The two traits here analyzed have three states each. 

For group size, the states were (1) aggregations (including swarms), (2) small groups, and (3) pair-living (social 

monogamy). The three character states used for describing the symbiotic propensity of different shrimp species 

were (1) free-living, (2) facultative associate (with different moray eel species, such as L. californica and L. seticaudata; with sea anemones, such as L. ankeri), and (3) 

strictly symbiotic with either sponges (e.g., L. pederseni) 

or sea anemones (L. amboinensis, L. grabhami). Information on the lifestyle of each species was obtained by direct 

observation of shrimps in nature (personal observations), 

from the literature (see literature review), or from both 

sources.

During the analysis, a reversible-jump MCMC search 

was used with two independent chains that were run for 

6,000,000 iterations with a burn-in of 50,000. I choose 

the prior distribution of the parameters in the model with 

the option Hyperprior (see Pagel et al., 2004), seeding an 

exponential distribution from uniform on the interval 0.0 

to 30 and a rate deviation of 18. These values were selected considering preliminary runs and were used to keep 

the acceptance rate at approximately 0.3, as recommended 

by Pagel et al. (2004). Character states at internal nodes 

06_Baeza_095-110_Lang.indd 98 6_Baeza_095-110_Lang.indd 98 9/24/09 9:22/24/09 9:22
NUMBER 38 • 9 9

were reconstructed using the most recent common ancestor method. I tested hypotheses about particular character 

states at specifi c nodes when comparing the MCMC runin which the node was “fossilized” (constrained) to one 

state versus an alternative. The command Fossil allows 

testing whether a particular state is “signifi cantly” more 

likely at a specifi c node than an alternative state. For each 

tested character, the same set of conditions (prior distribution, burn-in) as used in the ancestral character state 

reconstructions already described were used. However, the 

MCMC was run 5 times for each trait state tested, and 

a total of 100,000,000 iterations were conducted. Bayes 

factors were calculated as the difference between the highest harmonic mean of the marginal likelihood from the 

fi ve MCMC runs for each state (Pagel et al., 2004). The 

strength of support for one model over another was measured using the scale from Kass and Raftery (1995).

RESULTS

DISSECTIONS

Dissections demonstrated that all shrimps (brooding 

or nonbrooding) from the two species had male gonopores 

at the coxae of the fi fth pair of pereiopods (Figure 1A). 

Female gonopores at the coxae of the third pair of pereiopods were more diffi cult to reliably observe. From all 

shrimps (brooding or nonbrooding), sperm cells shaped in 

the form of an inverted umbrella were retrieved from the 

male gonopores by electroshocks (Figure 1A,B). Dissections of the gonads from small shrimps not brooding embryos (presumptive males) demonstrated the presence of 

an ovotestes (Figure 1C) with an undeveloped anterior female portion full of immature oocytes (lacking coloration) 

(Figure 1D) and a posterior male gonad containing sperm 

cells with the same morphology as the sperm retrieved 

from the gonopores (see Figure 1B). Gonads dissected from 

brooding (presumptive hermaphrodites) shrimps also had 

ovotestes, but with a large ovarian portion full of mature 

oocytes and a relatively small posterior testicular portion 

with sperm (Figure 1E). In both brooding and nonbrooding shrimps, vas deferentia and oviducts extended laterally from the testicular and ovarian portions, respectively 

(Figure 1C,E).

Shrimps brooding embryos invariably lacked cincinnuli and appendices masculinae in the endopod of the fi rst 

and second pereiopods, respectively. In contrast, appendices masculinae bearing relatively long spines and numerous 

cincinnuli were observed in the second and fi rst pleopods, 

respectively, of nonbrooding shrimps (Figure 1F– H). Some 

minor differences between the two species were noticed 

regarding the relative length and number of spines borne 

by the appendix masculinae; in L. boggessi, the spines 

were more numerous and longer than those of L. galapagensis (Figure 1G,H). Overall, all the anatomical differences observed between brooding and nonbrooding 

shrimps indicate that the populations of all the Lysmata

species studied herein are indeed composed of males and 

hermaphrodites.

EXPERIMENTS

When two brooding individuals (presumed hermaphrodites) were paired, all individuals in the two 

species examined successfully hatched their embryos as 

larvae, molted, and spawned a new batch of oocytes 

below the abdomen. The oocytes remained attached to 

the pleopods and showed embryonic development as embryos (i.e., early blastulae formation) after three days. 

This embryological development suggests the ability of 

the other hermaphrodites in the same aquarium to reproduce as males or, alternatively, the possibility of selfing by the hermaphrodites acting as females. However, 

none of the 10 hermaphrodites (5 of each species) maintained in isolation from conspecifi cs successfully reared 

their embryos to larvae. These solitary shrimps molted 

and spawned oocytes to beneath the abdomen. However, 

the oocytes invariably disappeared from the pleopods 

within a few days after spawning. Overall, the observations from these fi rst two experiments strongly suggest 

that brooding hermaphrodites do not have the capability 

of self-fertilization. Therefore, brooding shrimps (hermaphrodites) maintained in pairs indeed acted as males 

and fertilized eggs when their partners molted and reproduced as females.

In the experiment conducted to determine whether 

males mature as hermaphrodites later in life, all six males 

of L. galapagensis turned into simultaneous hermaphrodites within four months. Males showed signs of ovarian 

maturation during intermolt periods. When the gonad was 

full of large green (vitellogenic) oocytes, the male shrimps 

molted into hermaphrodites. Most probably, these shrimps 

mated as females shortly after molting for the fi rst time in 

their lifetime because the spawned embryos beneath the 

abdomen were observed developing normally several days 

after spawning.

In contrast to L. galapagensis, all six male shrimps 

from L. boggessi died of unknown reasons within the 

fi rst month of the experiment. However, observations on 

three males of L. boggessi in the maintenance aquaria 

06_Baeza_095-110_Lang.indd 99 6_Baeza_095-110_Lang.indd 99 9/24/09 9:22/24/09 9:22
06_Baeza_095-110_Lang.indd 100 6_Baeza_095-110_Lang.indd 100 9/24/09 9:22

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NUMBER 38 • 101

indicated that they turn into hermaphrodites before four 

months. This change of sexual phase was accomplished 

after a single month, as observed in L galapagensis. Thus, 

it may be concluded that L. galapagensis and L. boggessi

are protandric simultaneous hermaphrodites, incapable of 

self-fertilization.

POPULATION STRUCTURE, SEX RATIO, AND ABUNDANCE

Abundances of L. galapagensis and L. boggessi at 

the different sampling locations were high and low, with 

a mean of 2.79 and 0.317 individuals collected per minute per sampling period, respectively. In the two species, 

population was biased toward males. The ratio of males 

to total shrimps collected during the sampling period was 

0.024 and 0.16 for L. galapagensis and L. boggessi, respectively. The range of body size registered for males 

varied from 1.9 to 3.8 and from 3.13 to 5.75 mm CL in 

L. galapagensis and L. boggessi, respectively. Hermaphrodites ranged in size between 4.1 and 5.1 and 5.63 and 

6.5 mm CL in L. galapagensis and L. boggessi, respectively (Figure 2).

MUSEUM SPECIMENS

A variable number of specimens from L. anchisteus, L. 

argentopunctata, L. chica, L. kuekenthali, L. moorei, L. 

philippinensis, L. rathbunae, L. trisetacea, and L. vittata

were available at the NMNH. Small shrimps in each species appear to be males as they have cincinnuli and appendices masculinae in the second and fi rst pleopod, respectively. In turn, shrimps brooding embryos (the great 

majority of them above average size) invariably lacked 

cincinnuli and appendices masculinae in the endopod of 

the fi rst and second pereiopods, respectively. This last observation suggests they were hermaphrodites. It was not 

possible to detect transitional individuals in these species 

because no dissections were possible and gonad condition was not easily observed. The carapace of formaldehyde- and alcohol-fi xed specimens is not translucent as it 

is in living or recently preserved specimens. Also, shrimps 

less than 3.0 mm CL were not sexed because of the risk 

of infl icting damage. For all species examined except L. 

anchisteus, L. argentopunctata, and L. philippinensis, 

a relatively large sample of specimens was available. 

The size– frequency distribution of the different species 

strongly resembled that of the two species studied above, 

with small shrimps resembling males and large shrimps 

resembling hermaphrodites (Figure 3). Observations of 

the coxae of the fi fth pair of pereiopods of the largest 

brooding shrimps in each species demonstrated the presence of male gonopores. Overall, the distribution of the 

sexes across size classes and the limited observations on 

the external male and female anatomy suggest that all 

these other Lysmata shrimps are protandric simultaneous 

hermaphrodites.

LITERATURE REVIEW

The literature review of the 41 species of Lysmata (including Exhippolysmata) described to date revealed that 

the geographic and bathymetric distribution, coloration, 

and habitat of these species are relatively well known. 

Shrimps from the genus Lysmata occur in tropical, subtropical, and temperate waters around the world and can 

be found among rocks or fossilized coral, live coral, seagrass blades, on muddy and shell bottoms, or associated 

with sponges or sea anemones in the intertidal or subtidal 

to 360 m depth. Most species have an inconspicuous coloration (red striped, translucent reddish with reddish fl agella 

on both pairs of antenna). Only 4 species are reported as 

featuring a striking color pattern (contrasting body colors, 

bright white fl agella on both antenna). This dichotomy in 

coloration was previously noticed by Bauer (2000). Lysmata splendida, one of the 4 species with a brilliant coloration, most probably is a cleaner shrimp. However, nothing is known about its reaction to fi sh and its propensity 

to clean them. Similarly, information regarding the degree 

of specialization of the cleaning behavior is unknown for 

most of the species (Table 1).

Information on the socioecology and sexual system 

is, in general, poorly known. Information on lifestyle 

FIGURE 1. (facing page) Lysmata galapagensis and Lysmata boggessi: anatomical and morphological differences between males and 

hermaphrodites. A, spermatophore (arrow) retrieved from gonopores of hermaphrodite (L. boggessi); B, sperm from male (L. galapagensis); C, ovotestes from male (anterior female and male portions 

on top and bottom, respectively; arrow points at left vas deferentia) 

(L. galapagensis); D, close-up of female gonad portion in male (arrow 

points at immature oocyte) (L. boggessi); E, ovotestes from dissected 

hermaphrodite (anterior female and male portions on the top and 

bottom, respectively; top and bottom arrows point at right oviduct 

and left vas deferentia, respectively) (L. galapagensis); F, endopod of 

fi rst pleopod in male (arrow points at cincinulli) (L. galapagensis); 

G, endopod of second pleopod in male (arrow points at appendix 

masculina) (L. galapagensis); H, endopod of second pleopod in male 

(arrow points at appendix masculina) (L. boggessi).

06_Baeza_095-110_Lang.indd 101 6_Baeza_095-110_Lang.indd 101 9/24/09 9:22/24/09 9:22
102 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

(socioecological attributes) is available only for 18 of the 

41 described species. Of these, 7 species live in crowds 

(aggregations), 7 species live in small groups, 3 species 

live in pairs (i.e., they are socially monogamous), and 1 

species is reported as living in extremely large aggregations (in swarms; Exhippolysmata oplophoroides). Demonstration of PSH using a combination of experimental, 

morphological, and anatomical fi ndings and population 

structure is available for 12 species. A strong indication 

of PSH exists for another 10 species. Although the information is incomplete (PSH has been reported for a 

total of 22 species, or 54% of the described species), this 

review clearly demonstrates that the lifestyle and socioecology of shrimps from this genus are more complex 

than originally thought and further confi rms the idea 

that PSH is a fi xed trait in the genus Lysmata (including 

Exhippolysmata).

TESTING THE HISTORICAL CONTINGENCY HYPOTHESIS

The 50% majority-rule consensus tree obtained during the initial phylogenetic analysis confi rms the existence 

of the three natural clades (tropical-American, cosmopolitan, and cleaner) noticed previously by Baeza et al. (2009). 

However, one important difference between the present 

consensus tree and that previously published is that L. 

olavoi is not supported as the most basal species within 

the genus. This difference between trees might (1) be an effect of the different set of species used for the phylogenetic 

analysis or (2) perhaps have occurred because the different software programs used for phylogenetic inference 

function with different algorithms. On the other hand, the 

monophyly of Lysmata is well supported in this new tree, 

with a 100% posterior probability (Figure 4; Baeza et al., 

2009: fi g. 1).

The lifestyle of shrimps mapped onto the consensus 

tree indicated that the most recent common ancestor of 

the species pertaining to the neotropical and cosmopolitan clades was gregarious. In contrast, the ancestor of 

the species comprising the cleaner clade most probably 

was socially monogamous (see Figure 4). On average, 

the node of the most common recent ancestor of all Lysmata species is reconstructed to be in state 2 (social monogamy) with 80% of certainty. The degree of certainty 

varied from tree to tree but was generally high, as indicated by the low standard deviation of this value (SD 

 0.03, calculated from 2,000,000 iterations using 1 of 

1,000 randomly sampled posterior probability distribution trees at each iteration). The largest harmonic loglikelihood obtained from fi ve independent runs when the 

node was fossilized to state 0 and 2 was – 22.309507 

and – 20.865237, respectively. The almost three log-unit 

improvement in likelihood (Bayes factor  2.89) of the 

model when the node was fossilized to state 2 represents 

evidence that the ancestral lifestyle of Lysmata was social monogamy.

With regard to the propensity for developing symbiotic interrelationships, the reconstructions suggest that 

the ancestor of the neotropical and cosmopolitan clades 

most probably had a free-living lifestyle and did not develop any symbiotic partnership with other macroinvertebrates. It should be noticed that the degree of certainty 

of these two inferences is relatively low, as indicated by 

the large standard deviations of the distribution of the 

character (see Figure 4). Also, the reconstructions indicate that, with a probability of 0.46  0.20 or 0.41 

0.18, either facultative partnerships or strict symbiosis, 

FIGURE 2. Lysmata galapagensis and L. boggessi population structure (n  178 and 22 shrimps, respectively, from L. galapagensis and 

L. boggessi; CL  carapace length).

06_Baeza_095-110_Lang.indd 102 6_Baeza_095-110_Lang.indd 102 9/24/09 9:22/24/09 9:22
NUMBER 38 • 103

FIGURE 3. Lysmata spp. Population structure of selected species from the National Museum of Natural History (n  71, 56, 22, 31, 70, and 57 shrimps from L. trisetacea, L. moorei, L. chica, L. rathbunae, L. vittata, 

and L. kuekenthali, respectively).

respectively, was the ancestral state of the genus Lysmata. The improvement in the likelihood of the model 

(Bayes factor  1.51) when the node was fossilized to 

state 2 (strict symbiosis) was low compared to when the 

node was fossilized to state 0 (free-living). Therefore, 

there is no evidence indicating that symbiosis is signifi -

cantly more likely than a free-living lifestyle in the ancestral Lysmata.

Overall, the present ancestral character state reconstruction provides partial support for Bauer’s (2000) hypothesis about the evolution of PSH in shrimps from the 

genus Lysmata.

06_Baeza_095-110_Lang.indd 103 6_Baeza_095-110_Lang.indd 103 9/24/09 9:23/24/09 9:23
104 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES TABLE 1. Diversity of lifestyles and sociobiology in shrimps from the genera Exhippolysmata and Lysmata. A question mark (?) indicates data not available. Bathymetric Geographic distribution Cleaning Sexual Evidence Species distribution (m) a Habitat b Latitude Lifestyle Coloration behavior c system (SS) d used forSS e Referencesf

E. ensirostris Indo-Pacifi c I & S ? Tropical ? ? ? PSH? E,M 1,10,13

E. hastatoides W. Africa 12– 48 ? Tropical ? ? ? ? ? 1

E. oplophoroides W. Atlantic 7– 27 R Subtropical Swarms ? ? PSH D,M,P 1,4,14

E. tugelae South Africa 22– 48 ? Subtropical ? ? ? ? ? 1L. amboinensis Red Sea, S S Tropical Pairs Brilliant S PSH E 1,15,26 Indo-Pacifi cL. anchisteus Caribbean 0– 3 R,M Tropical ? ? ? ? ? 1,3L. ankeri Caribbean 0– 2 S,C Tropical Groups Dull U PSH D,E,M,P 27L. argentopunctata E. Pacifi c 0– 35 R,C Tropical ? Dull ? ? ? 2

L. bahia W. Atlantic I F Subtropical Groups Dull U PSH D,E,M,P 16L. boggessi Caribbean 0– 2 S,R Tropical Crowd Dull U PSH D,E,M,P 29L. californica E. Pacifi c I & S R,S Tropical Crowd Dull U PSH D,E,M,P 1,2,17

L. chica Galapagos I & S R,C Tropical ? Dull ? ? ? 2

L. debelius Indo-Pacifi c 10– 28 R,S Tropical Pairs Brilliant S PSH ? 1,11,26

L. galapagensis E. Tropical 0– 2 R Tropical Crowd Dull U PSH D,E,M,P 1,2,29 Pacifi cL. grabhami Caribbean, Subtidal 

55 S Tropical Pairs Brilliant S PSH D,M 1,3,18,26

 AtlanticL. gracilirostris E. Tropical 0– 138 R Tropical ? Dull U PSH? M 2,27 Pacifi cL. hochi Caribbean I F Tropical Groups Dull U PSH D,E,M,P 19L. intermedia Caribbean, 0– 22 A,R,C Tropical Groups Dull U PSH D,E,M,P 1,3,16

 AtlanticL. kempi Burma 37 ? Tropical ? ? ? ? ? 1L. kuekenthali Red Sea, 0– 11 ? Tropical ? Dull ? PSH ? 1,10,27, 29

 Indo-Pacifi c,  South AfricaL. moorei Caribbean, I R,F Tropical Groups Dull U PSH? M 1,9,27 W. AtlanticL. morelandi New Zealand I & S R Temperate ? ? ? ? ? 1L. multiscissa Djibouti, Africa ? ? Tropical ? ? ? ? ? 1

L. nayaritensis E. Pacifi c I & S R Tropical Crowd Dull U PSH D,E,M,P 2,20

L. nilita Mediterranean, ? ? Subtropical ? Dull ? PSH E,M 1,21 E. Atlantic L. olavoi Azores and 135– 360 ? Tropical ? Dull ? PSH? M 1,6,28 Savage Is. L. pederseni Caribbean S S Tropical Groups Dull U PSH D,E,M,P 22,27L. philippinensis Philippines 267 ? Tropical ? ? ? ? ? 1L. porteri Juan Fernandez, 0– 12 R Subtropical, ? ? ? ? ? 1

 E. Pacifi c temperateL. rafa Caribbean I & S R Tropical Groups Dull U PSH D,E,M 22,27L. rathbunae Caribbean 13– 119 ? Tropical ? Dull ? PSH? M,P 1,3,23

continued

06_Baeza_095-110_Lang.indd 104 6_Baeza_095-110_Lang.indd 104 9/24/09 9:23/24/09 9:23
NUMBER 38 

• 105

L. seticaudata Mediterranean, I,S R,S Subtropical Crowd Dull U PSH D,E,M,P 1,21,24 E. Atlantic,  Black SeaL. stenolepsis Cape Verde 150– 275 ? Tropical ? ? ? ? ? 1,7

L. striata Caribbean I R,M Tropical Crowd Dull U PSH D,E,M,P 1,25,27L. splendida Indo-Pacifi c 6– 35 W,C Tropical ? Brilliant ? ? ? 12

L. ternatensis Djibouti, 62 Sa Tropical ? Dull ? ? ? 1 Indonesia L. trisetacea Red Sea, New 0– 150 R,C Tropical ? ? ? ? ? 1,2

 ZealandL. uncicornis NW Africa 4– 5 R Subtropical ? Dull ? ? ? 1,8

L. vittata Indo-Pacifi c, 0– 54 A Tropical ? ? ? ? ? 1,5

 Australia, E. AfricaL. wurdemanni Caribbean, 0– 30 R,J Subtropical Crowd Dull U PSH D,E,M,P 1,3,26,27

 E. Atlantic,  Gulf of MexicoL. zacae Indo-Pacifi c ? ? ? ? ? ? ? ? 1

a I  intertidal; S  subtidal; numbers refer to depth in meters.b A  associated with algae; S  symbiont (with moray eels in the case of L. californica and L. seticaudata); Sa  coarse sand; R  rocky bottoms and/or rubble; C  among corals; F  fossilized coral terraces; 

J  jetties; M  mud; W  caverns, on reef roof walls.

c S  specialized; U  unspecialized.d PSH  protandric simultaneous hermaphroditism.e D  dissections; E  experiments; M  morphology; P  population structure.f References: 1, Chace, 1997; 2, Wicksten, 2000; 3, Chace, 1972; 4, Williams, 1984; 5, Kemp, 1914; 6, Fransen, 1991; 7, Crosnier and Forest, 1973; 8, Holthuis and Maurin, 1952; 9, Rathbun, 1906; 

10, Holthuis, 1948; 11, Bruce, 1983; 12, Burukovsky, 2000; 13, Kagwade, 1982; 14, Braga et al., 2009; 15, Fiedler, 1998; 16, Baeza, 2008b; 17, Bauer and Newman, 2004; 18, Wirtz, 1997; 19, Baeza and 

Anker, 2008; 20, Baeza et al., 2008; 21, d’Udekem d’Acoz, 2002; 22, Rhyne and Anker, 2007; 23, Rhyne and Lin, 2006; 24, Dohrn and Holthuis, 1950; 25, Anker et al., unpublished; 26, Bauer, 2000; 

27, unpublished observations; 28, Fransen, personal communication; 29, this study.

06_Baeza_095-110_Lang.indd 105 6_Baeza_095-110_Lang.indd 1059/24/09 9:23/24/09 9:23
106 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

DISCUSSION

The present study suggests that the sexual system in 

shrimps from the genus Lysmata (including Exhippolysmata) represents a fi xed trait. Anatomical observations, 

behavioral experiments, and fi eld samples demonstrated 

that the 2 species studied here are protandric simultaneous hermaphrodites, as reported for all other Lysmata species (Table 1). Size– frequency distributions and additional 

but limited anatomical observations of museum specimens 

further suggest that at least 9 other species are protandric 

simultaneous hermaphrodites. Including the information 

generated in the present study, PSH has been reported for 

a total of 22 species, or 54% of the 41 species described 

worldwide.

The well-conserved sexual system in Lysmata contrasts with that reported for other genera from the closely 

related family Hippolytidae. For instance, two different 

genera of Hippolytidae shrimps, Thor and Hippolyte, are 

known to contain both gonochoric and strict sequentially 

hermaphroditic species (Espinosa-Fuenzalida et al., 2008, 

and references therein). The reasons for PSH to be fi xed 

in Lysmata are not clear, especially when considering 

the diversity of environments inhabited by these species 

(see Table 1). Different habitats with varying degrees of 

structural complexity, seasonality, and predation regimes 

should favor different sexual systems. For instance, the 

rather heterogeneous environment (i.e., seagrass beds, seaweed meadows) in which the gregarious L. boggessi and 

L. wurdemanni occur is expected to favor sequential hermaphroditism over PSH. In these complex environments, 

male mating success most likely decreases with increasing 

body size because small body size is expected to increase 

searching ability and, ultimately, male mating success 

when encounter rate among conspecifi cs is high (Baeza 

and Thiel, 2007). This small-male advantage together 

with the well-reported exponential relationship between 

fecundity and body size in female shrimps is expected to 

favor strict protandry over simultaneous hermaphroditism 

in these species (Charnov, 1982).

On the other hand, hermaphroditic shrimps are known 

to experience brooding constraints (e.g., L. wurdemanni; 

Baeza, 2007c), a condition that theoretically favors simultaneous hermaphroditism (see Charnov, 1982, and references therein). Similarly, in socially monogamous Lysmata

(e.g., L. grabhami; Wirtz, 1997), infrequent encounter 

rates among conspecifi cs should be favoring strict simultaneous hermaphroditism over PSH. It should pay (in term 

of fi tness) for each individual in a pair to reproduce both 

as male and female as soon as possible during their lifetime because this strategy increases reproductive success 

through both sperm donation to the partner and female 

reproduction. Thus, an early male phase in these socially 

monogamous species should not be adaptive. On the other 

hand, differing costs between the sex functions might explain the existence of an early male phase before the simultaneously hermaphroditic phase in these monogamous 

species. The relatively large energetic and temporal costs 

of producing ova might delay maturation of the female 

function, resulting in a functional adolescent male phase 

previous to the simultaneously hermaphroditic phase (see 

Baeza, 2006). Additional studies in gregarious and socially 

monogamous cleaner shrimp species should improve our 

understanding about the conditions favoring PSH under a 

social monogamous mating system in Lysmata.

The literature review conducted herein indicates that 

the diversity of lifestyles in the genus is greater than previously recognized. Initial studies reported a distribution 

for the genus restricted to tropical-subtropical waters. 

The present review suggests that shrimps also inhabit cold 

temperate environments. Lysmata porteri is reported from 

southern Chile, and L. morelandi inhabits New Zealand 

(see Table 1). Because Exhippolysmata spp. represents a 

derived group of Lysmata, the deep water environment 

represents another environment colonized by the species 

in this group (see Baeza et al., 2009). Also, the dichotomy 

in social organization (“Crowd” versus “Pair” species) 

noted in initial studies (Bauer, 2000) is not supported. In 

addition to tropical pair-living and temperate gregarious 

species, the present review indicates other species forming 

swarms (extremely large aggregations) in temperate deep 

water soft-bottom environments (i.e., E. oplophoroides) or 

living in small groups in the tropical or subtropical intertidal 

that might or not associate with sea anemones (L. ankeri; 

Table 1). The possibility of an adaptive radiation in this 

group of shrimps is currently being explored. The rather 

unusual sex allocation pattern of this shrimps might represent the key innovation allowing species in these two genera to colonize and persist in environments where species 

with conventional sexual systems might fail.

The ancestral character state reconstruction analysis 

conducted in this study provides partial support for Bauer’s (2000) hypothesis about the evolution of PSH in Lysmata. The analysis suggested that the ancestral Lysmata

shrimp lived as socially monogamous pairs either facultatively associated to other macroinvertebrates or featuring 

a strictly symbiotic lifestyle (with sea anemones, for example). The free-living condition of several species pertaining 

to the cosmopolitan and neotropical clades is likely to be 

derived according to the present analysis. PSH might have 

06_Baeza_095-110_Lang.indd 106 6_Baeza_095-110_Lang.indd 106 9/24/09 9:23/24/09 9:23
NUMBER 38 

• 107

FIGURE 4. A 50% majority-rule consensus tree obtained using Bayesian inference phylogenetic methods showing the posterior densities of the reconstructed ancestral states 

(symbiosis and group size) at different nodes. For each node, the posterior probability for group size (left tree) and symbiosis (right tree) obtained when reconstructing the ancestral state of the most recent common ancestor to different clades in each tree is shown.

06_Baeza_095-110_Lang.indd 107 6_Baeza_095-110_Lang.indd 1079/24/09 9:23/24/09 9:23
108 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

evolved in the tropics from an ancestral protandric species 

of Lysmata that became a specialized fi sh cleaner, as suggested by Bauer (2000). Restricted mobility of individuals 

resulting from their association with the host, and, hence, 

the reduced probability of encountering mating partners, 

would have favored PSH (Bauer, 2000) (see foregoing for 

further details about this hypothesis). Nonetheless, the inferences about ancestral character states from the present 

analysis need to be considered with caution. Indeed, the 

present analysis did not support an ancestral symbiotic 

condition as signifi cantly more likely than a free-living 

condition. Also, several internal nodes in the phylogenetic 

tree were not well supported by the Bayesian analysis of 

phylogenetic inference (see Baeza et al., 2009). This low 

support for internal nodes, together with the breadth of 

the posterior distributions of the character inferred for 

these nodes, means that other alternative routes to the 

evolution and maintenance of this peculiar sexual system 

in Lysmata cannot be ruled out.

Among alternative historical scenarios (to that proposed by Bauer, 2000), PSH might well have evolved 

from a strict simultaneous hermaphrodite or even from 

a strict gonochoric free-living ancestor inhabiting tropical environments. The evolution of PSH from an ancestral strictly simultaneous hermaphroditic condition has 

been reported previously for the worm Ophryotrocha diadema, one of the few other marine invertebrates in which 

PSH has been demonstrated (Dahlgren et al., 2001). Acting together with the conditions favoring simultaneous 

hermaphroditism (i.e., low abundance), sex-dependent 

energetic costs might have favored an early maturation 

of the male reproductive function compared to that of 

the female function in the ancestral free-living shrimp (regardless of its sexual system), ultimately resulting in the 

evolution of PSH as we observe it today in Lysmata (and 

Exhippolysmata). Similarly, brooding constraints experienced by hermaphroditic shrimps might have favored the 

retention of the male function later in life. If the space 

for brooding embryos in the abdomen becomes saturated, 

allocation of energy to sperm production is expected to 

maximize fi tness. This argument is similar to that of Ghiselin (1987) to explain apparent protogynous simultaneous hermaphroditism in chitons. In some species of polyplacophorans, individuals brood eggs along the side of 

the body. Early in life, they reproduce strictly as females 

until they reach a size at which the space in which they 

brood is saturated. At that point, the same individuals 

start producing sperm while they are brooding. Brooding 

constraints have been previously reported for at least one 

species of Lysmata (L. wurdemanni; Baeza, 2006). New 

studies are needed to confi rm whether brood constraints 

are common in the genus.

In the scenarios depicted here, we should expect 

that, in a phylogeny of the group, “tropical– low abundance” species would have a more basal position than 

the “Pair” and “Crowd” species (“Pair” and “Crowd” 

sensu Bauer, 2000). The rather complex mating system 

(social monogamy) and specialized fi sh-cleaning behavior of the “Pair” species most probably evolved from 

“tropical– low abundance” species without complex 

cleaning behavior and with rather simple mating systems 

(i.e., without long-lasting associations between mating 

partners), as appears to be the case for most shrimps 

from the closely related family Hippolytidae. The unresolved position of the different natural clades with respect to each other in the current phylogeny (see also 

Baeza et al., 2009) constrain testing this last hypothesis 

against Bauer’s (2000) ideas. Future studies attempting to resolve the natural relationships among species 

of Lysmata, Exhippolysmata, and other related taxa together with the detailed examination of their sexual system should allow explaining the origin of simultaneous 

hermaphroditism in shrimps from the genus Lysmata.

Last, it is worth mentioning one of the main assumptions of the present analysis. PSH was treated as a singular innovation only originating in the genus Lysmata

(which contains Exhippolysmata), as initially suggested 

by Bauer (2000). To the best of my knowledge, shrimps 

from the genus Merguia, apparently the sister group 

to Lysmata, seem to have a gonochoric sexual system. 

However, this observation needs experimental confi rmation. Most importantly, future studies need to test for 

the existence of protandric simultaneous hermaphroditism in members from other closely related genera (i.e., 

Mimocaris, Parahippolyte, Merguia, Merhippolyte). 

These studies might reveal that PSH is not a singularity. 

Indeed, PSH has independently evolved in the past at 

least four other times outside the Caridea. In addition to 

Lysmata shrimps, PSH has been confi rmed in the polychaete worm Ophryotrocha diadema (Premoli and Sella, 

1995), the land snail Achatina fulica (Tomiyama, 1996), 

the tunicate Pyura chilensis (Manríquez and Castilla, 

2005), and the symbiotic barnacle Chelonibia patula

(Crisp, 1983). If simultaneous hermaphroditism turns 

out not to be a singularity in shrimps from the families 

Hippolytidae and Lysmatidae, then it should be possible 

to explore the environmental conditions that favor this 

unique sexual system in shrimps.

06_Baeza_095-110_Lang.indd 108 6_Baeza_095-110_Lang.indd 108 9/24/09 9:23/24/09 9:23
NUMBER 38 • 109

ACKNOWLEDGMENTS

I appreciate the support from the Smithsonian Tropical Research Institute (STRI, Panama City and Bocas del 

Toro, Panama) Marine Fellowship and the Smithsonian 

Marine Station at Fort Pierce (Fort Pierce, Florida, USA) 

Fellowship. I thank Dr. Rachel Collin for inviting me to 

join the 2007 Research Cruise to La Coiba Island and Las 

Perlas Archipelago, off the Pacifi c coast of Panama, aboard 

the R/V Urraca (STRI), during which a portion of this 

study was conducted. I thank Dr. Klaus Ruetzler (National 

Museum of Natural History, Smithsonian Institution), Dr. 

Anson (Tuck) Hines (SERC) and Dr. Valerie Paul (SMSFP) 

for funding various research visits to Carrie Bow, Belize, 

during which a major portion of this manuscript was completed. I also thank Paula Rodgers and Rafael Lemaitre for 

their support during my visit to the National Museum of 

Natural History. The comments by two anonymous referees substantially improved this manuscript. This work is 

contribution number 776 of the Smithsonian Marine Station at Fort Pierce and contribution number 840 of the Caribbean Coral Reef Ecosystems Program (CCRE), Smithsonian Institution, and supported in part by the Hunterdon 

Oceanographic Research Fund. This study was partially 

funded by a National Geographic Research Grant from the 

National Geographic Society, USA.

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Reconciling Genetic Lineages with Species 

in Western Atlantic Coryphopterus

(Teleostei: Gobiidae)

Carole C. Baldwin, Lee A. Weigt, David G. 

Smith, and Julie H. Mounts

ABSTRACT. Species identifi cation of western Atlantic Coryphopterus can be problematic because some of the species are morphologically similar, there is confusing morphological variation within some species, no taxonomic key includes all currently recognized 

species, and the validity of some species is questionable. The most recently published keys 

do not include Coryphopterus tortugae or C. venezuelae, the validity of which as distinct from C. glaucofraenum has been questioned. Neighbor-joining trees derived from 

mitochondrial cytochrome c oxidase I (COI) sequences (DNA barcoding) were used to 

determine the number of genetically distinct lineages of Coryphopterus from collections 

made off Belize, Curacao, and Florida. Additional specimens for genetic and morphological analysis were obtained from Panama, Venezuela, and the Bahamas. Subsequent 

comparative analysis of preserved voucher specimens from which DNA was extracted 

and digital color photographs of those specimens taken before preservation yielded, in 

most cases, suffi cient morphological information to separate the genetic lineages. Species 

identifi cation of the lineages was then determined based on review of original and subsequent descriptions of Coryphopterus species and examination of museum specimens, 

including some type material. Many museum specimens are misidentifi ed. Twelve species 

of Coryphopterus are herein recognized in the western Atlantic and Caribbean: C. alloides, C. dicrus, C. eidolon, C. glaucofraenum, C. hyalinus, C. kuna, C. lipernes, C. personatus, C. punctipectophorus, C. thrix, C. tortugae, and C. venezuelae. Coryphopterus 

bol Victor, 2008 is a synonym of C. venezuelae (Cervigón, 1966). Although genetically 

distinct, C. glaucofraenum and some specimens of C. venezuelae are extremely similar 

and cannot be separated on the basis of morphology 100% of the time. Comments on 

the identifi cation of each Coryphopterus species and a revised key to western Atlantic 

species are provided.

INTRODUCTION

To provide specifi c identifi cations of larvae of Caribbean reef fi shes at Carrie Bow Cay, Belize, a small coral-fringed island on the Belizean Barrier Reef 

(16°48.5N, 88°05W), we have been matching larvae to adults through DNA 

barcoding (mitochondrial cytochrome c oxidase I [COI] sequences). In addition 

to greatly increasing our success rate of identifying larvae, DNA barcoding is 

also providing a method of checking existing species-level classifi cations by revealing the numbers of distinct genetic lineages within genera.

Carole C. Baldwin, Lee A. Weigt, David G. Smith, 

and Julie H. Mounts, National Museum of Natural 

History, Smithsonian Institution, P.O. Box 37012, 

Washington, D.C. 20013– 7012, USA. Corresponding author: C. Baldwin (baldwinc@si.edu). Received 

13 May 2008; accepted 20 April 2009.

07_Baldwin_111-138_Lang.indd 111 7_Baldwin_111-138_Lang.indd 111 9/24/09 9:36/24/09 9:36
112 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Attempts to identify Belizean Coryphopterus species using the most recently published keys (Böhlke and 

Robins, 1960, 1962; Böhlke and Chaplin, 1968; Murdy, 

2002) proved problematic for certain species. None of 

those keys includes C. tortugae (Jordan) or C. venezuelae Cervigón, presumably because the validity of both 

species as distinct from C. glaucofraenum Gill has been 

questioned (e.g., Böhlke and Robins, 1960; Cervigón, 

1966; Thacker and Cole, 2002). Longley and Hildebrand (1941) and Böhlke and Robins (1960) considered C. tortugae (Jordan; type locality, Dry Tortugas, 

Florida) a synonym of C. glaucofraenum Gill. GarzónFerreira and Acero (1990) redescribed C. tortugae as 

distinct based on new collections from the Colombian 

Caribbean. Thacker and Cole (2002) acknowledged the 

latter work but did not recognize C. tortugae in their 

phylogenetic analysis of Coryphopterus species. Victor 

(2008) recognized C. tortugae as distinct from C. glaucofraenum and identifi ed what he considered a cryptic 

new species within Garzón-Ferreira and Acero’s (1990) 

C. tortugae, which he named Coryphopterus bol. Cervigón (1994) elevated C. venezuelae from a subspecies 

of C. glaucofraenum to a distinct species, but it was not 

included in Murdy’s (2002) key or Thacker and Cole’s 

(2002) and Victor’s (2008) molecular phylogenies of Coryphopterus species.

Another problem with identifi cation of western Caribbean Coryphopterus is that stated distributions of 

many species are confl icting, and some do not include 

the western Caribbean. Greenfi eld and Johnson (1999) 

identifi ed nine species of Coryphopterus from Belize (all 

of the 12 recognized herein except for C. venezuelae, C. 

punctipectophorus, and the recently described C. kuna

(Victor, 2007)). Murdy (2002) listed only C. alloides, 

C. dicrus, C. glaucofraenum, C. hyalinus, C. lipernes, 

and C. personatus as having ranges that include Central 

America, western Caribbean, or Caribbean. A search 

for reef- associated species in Belize in FishBase (www

.fi shbase.org) returned only C. alloides, C. eidolon, C. 

glaucofraenum, and C. personatus.

The purposes of this paper are to assess the number 

of valid Coryphopterus species known from the western 

Atlantic and to provide comments on the identifi cation 

of, and a revised key to, those species based on results 

of DNA barcoding, subsequent examination of voucher 

specimens and color photographs of them, examination 

of museum specimens, and reference to original and other 

descriptions of the species. A neotype for C. glaucofraenum is designated because the location of Gill’s (1863) 

holotype is unknown.

METHODS

Depending on the locality, fi sh specimens were collected using the fi sh anesthetic quinaldine sulfate or rotenone. Specimens were measured to the nearest 0.5 mm, 

photographed with a Fujifi lm FinePix 3 digital camera 

to record color patterns, sampled for genetic analysis, 

and then preserved as vouchers. Tissue sampling for molecular work involved removing a muscle biopsy, eye, or 

caudal body portion (depending on size) and storage in 

saturated salt buffer (Seutin et al., 1990). Genomic DNA 

was extracted from up to approximately 20 mg minced 

preserved tissue via an automated phenol:chloroform 

extraction on the Autogenprep965 (Autogen, Holliston, 

MA) using the mouse tail tissue protocol with a fi nal 

elution volume of 50 L. For polymerase chain reaction 

(PCR), 1 L of this genomic DNA is used in a 10 L reaction with 0.5 U Bioline (BioLine USA, Boston, MA) Taq 

polymerase, 0.4 L 50 mM MgCl2, 1 L 10 buffer, 0.5 

L 10 mM deoxyribonucleotide triphosphate (dNTP), 

and 0.3 L 10 M each primer FISH-BCL (5-TCAACYAATCAYAAAGATATYGGCAC) and FISH-BCH (5-

TAAACTTCAGGGTGACCAAAAAATCA). The thermal 

cycler program for PCR was 1 cycle of 5 min at 95°C; 35 

cycles of 30 s at 95°C, 30 s at 52°C, and 45 s at 72°C; 

1 cycle of 5 min at 72°C; and a hold at 10°C. The PCR 

products were purifi ed with Exosap-IT (USB, Cleveland, 

OH) using 2 L 0.2 enzyme and incubated for 30 min 

at 37°C. The reaction was then inactivated for 20 min at 

80°C. Sequencing reactions were performed using 1 L of 

this purifi ed PCR product in a 10 L reaction containing 

0.5 L primer, 1.75 L BigDye buffer, and 0.5 L BigDye 

(ABI, Foster City, CA) and run in the thermal cycler for 

30 cycles of 30 s at 95°C, 30 s at 50°C, 4 min at 60°C, 

and then held at 10°C. These sequencing reactions were 

purifi ed using Millipore Sephadex plates (MAHVN-4550; 

Millipore, Billerica, MA) per manufacturer’s instructions 

and stored dry until analyzed. Sequencing reactions were 

analyzed on an ABI 3730XL automated DNA sequencer, 

and sequence trace fi les were exported into Sequencher 4.7 

(GeneCodes, Ann Arbor, MI). Using the Sequencher program, ends were trimmed from the raw sequences until 

the fi rst and last 10 bases contained fewer than 5 base 

calls with a confi dence score (phred score) lower than 30. 

After trimming, forward and reverse sequences for each 

specimen were assembled, each assembled contig was 

examined and edited by hand, and each sequence was 

checked for stop codons. Finally the consensus sequence 

from each contig was aligned and exported in a nexus format. Neighbor-joining trees (Saitou and Nei, 1987) and 

07_Baldwin_111-138_Lang.indd 112 7_Baldwin_111-138_Lang.indd 112 9/24/09 9:36/24/09 9:36
NUMBER 38 • 113

distance matrices were generated using Paup*4.1 (Swofford, 2002) on an analysis of Kimura 2-parameter (K2P) 

distances (Kimura, 1980).

MATERIAL

The Coryphopterus material examined is listed in the 

Appendix (Table A.1). This table includes the voucher 

specimens represented in the neighbor-joining tree (Figure 1), as well as non-voucher specimens collected as 

part of this or other projects. Most specimens examined genetically for this chapter are juveniles or adults, 

except those of C. kuna; that species is represented in 

our samples only by larvae. For most specimens analyzed genetically, a digital color photograph of the specimen taken before dissection and preservation is housed 

at the Smithsonian Institution. Cytochrome c oxidase I 

(COI) sequences for specimens analyzed genetically are 

deposited in GenBank (accession numbers GQ367306–

GQ367475). Genetic information for several specimens 

collected in the Bahamas was not available in time for 

inclusion in the neighbor-joining tree, but identifi cations 

of those specimens based on that information are discussed in the text.

RESULTS

Twelve distinct genetic lineages of Coryphopterus

are present in our material (see Figure 1). One of those 

lineages, a single specimen identifi ed as C. alloides from 

Curacao is under additional investigation and is not discussed further here. Tissue samples of C. punctipectophorus were not available for genetic analysis. The other 

lineages, from top to bottom in Figure 1, are C. lipernes, 

C. hyalinus, C. personatus, C. tortugae, C. glaucofraenum, C. venezuelae, C. dicrus, C. thrix, C. eidolon, C. alloides, and C. kuna. Comments on the identifi cation of 

each lineage, as well as C. punctipectophorus, are provided below. The COI sequence of Coryphopterus bol

Victor, 2008 (PR SIO0869, fi g. 1 [SIO  Scripps Institution of Oceanography]) is part of the C. venezuelae clade, 

and the synonymy of that species is discussed below. 

Intra- and interspecifi c differences in percent sequence 

divergence for COI for all species are provided in Table 

1. We have not plotted distribution maps of Coryphopterus species because our samples are from a limited 

number of locations, and historical confusion about the 

identifi cation of some species precluded our relying on 

geographic information based on museum catalogues. 

Based on extensive recent collecting throughout the 

Caribbean, Ross Robertson (Smithsonian Tropical Research Institute, personal communication, 8 June 2009) 

and James Van Tassell are providing distribution maps of 

Coryphopterus species in their Shorefi shes of the Greater 

Caribbean CD, expected to be released in 2009.

Coryphopterus lipernes Böhlke and Robins, 

1962

FIGURE 2

Our specimens of C. lipernes from Belize and Curacao form a close genetic clade. Identifi cation of C. lipernes presents no problems: It is distinguished from all Coryphopterus species except C. hyalinus and C. personatus

by the presence of black pigment surrounding the anus; 

from C. hyalinus by the presence of a single (vs. two) anterior interorbital pore; and from C. personatus by color 

pattern (see Figure 2). We did not make fi n-ray counts for 

C. lipernes, but according to Böhlke and Robins (1962), 

C. lipernes also differs from C. personatus in having 10 

(vs. 11) second dorsal- and anal-fi n elements. Murdy 

(2002) distinguished C. lipernes and C. personatus from 

C. hyalinus by the presence of two pores between the eyes 

(vs. three), but as noted by Böhlke and Robins (1962), 

there is one anterior interorbital pore in C. lipernes and 

C. personatus and two in C. hyalinus.

Coryphopterus hyalinus Böhlke and Robins, 

1962

FIGURE 2

The validity of C. hyalinus as distinct from C. personatus has been questioned (e.g., Smith et al., 2003), but 

the two are genetically distinct (see Figure 1, Table 1). 

Of the Coryphopterus gobies with a black ring of pigment around the anus (C. hyalinus, C. personatus, and 

C. lipernes), C. hyalinus is the only one with two anterior 

interorbital pores (Böhlke and Robins, 1962; Böhlke and 

Chaplin, 1968). Because head pores can be diffi cult to see 

in fresh material (considerably easier to see in preserved 

specimens), separation of C. hyalinus and C. personatus

in the fi eld can be diffi cult. We have observed no consistent differences in pigmentation in fresh or preserved 

specimens of the two species, but we often collect C. hyalinus in deeper water than C. personatus.

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Coryphopterus personatus (Jordan 

and Thompson, 1905)

FIGURE 2

Identifi cation of C. personatus also presents no problems using published keys. It can be distinguished from 

C. hyalinus by the presence of a single interorbital pore 

and from C. lipernes by pigment pattern (see Figure 2). 

According to Böhlke and Robins (1962), C. personatus

also can be separated from C. lipernes by having 11 (vs. 

10) total elements in the second dorsal and anal fi ns.

Coryphopterus tortugae (Jordan, 1904)

FIGURE 3

Longley and Hildebrand (1941) and Böhlke and 

Robins (1960) considered C. tortugae (Jordan: type locality, Dry Tortugas, Florida) to be a synonym of C. glaucofraenum Gill. Garzón-Ferreira and Acero (1990) redescribed C. tortugae as distinct based on new collections 

from the Colombian Caribbean. Victor (2008) concurred 

with Garzón-Ferreira and Acero’s (1990) recognition of 

C. tortugae but noted that their Santa Marta specimens 

constitute a distinct species, which he described as C. bol. 

As noted below (see “Synonymy of Coryphopterus bol”), 

C. bol appears to be a synonym of C. venezuelae.

We had initially identifi ed all specimens of the C. tortugae, C. glaucofraenum, and C. venezuelae clades as C. 

glaucofraenum using published keys (Böhlke and Robins, 

1960; Böhlke and Chaplin, 1968; Murdy, 2002). However, those specimens separate into three well-defi ned lineages based on COI sequences. Specimens in one of those 

lineages are usually paler than those of the other two and 

almost always have a central bar of basicaudal pigment 

(vs. usually two spots or a dumbbell- or C-shaped marking), characters described by Garzón-Ferreira and Acero 

(1990) as diagnostic for C. tortugae. Böhlke and Robins 

(1960), who considered C. tortugae to be a pallid form of 

C. glaucofraenum, noted that the pigment markings along 

the side of the body are round (upper row) or vertically 

elongate (lower row) versus X-shaped as in C. glaucofraenum, usually a consistent feature in our specimens of 

C. tortugae. The pigment spots in the lower row of markings along the side of the body in C. tortugae are usually 

vertically elongate (crescents or some part of an X), but 

they are rarely distinct X-shaped markings. If some of the 

anterior markings do resemble X’s (Figure 3D), the height 

of each X is considerably smaller than the height of the X’s 

in C. glaucofraenum and, when present, in C. venezuelae

(half or less of eye diameter in C. tortugae, approximately 

three-quarters of or equal to eye diameter in the other two 

species). The pigment spots in the lower row also are not 

rounded, as they are in pale specimens of C. venezuelae.

We have not found the basicaudal pigment to be a 

reliable character for separating C. tortugae from C. glaucofraenum and C. venezuelae, as all three species may 

have a central bar of pigment; however, C. tortugae does 

not have two distinct spots in any of our material, so if 

that feature is present in a specimen, it is not C. tortugae. 

Coryphopterus tortugae shares with C. glaucofraenum

and C. venezuelae the presence of a distinct dark blotch 

or triangle behind the eye above the opercle and with C. 

glaucofraenum the absence of a pigment spot on the lower 

portion of the pectoral-fi n base. Garzón-Ferreira and Acero’s (1990) redescription of C. tortugae did not mention 

the absence of this spot, presumably because the Santa 

Marta specimens included in their description do have the 

spot and appear to be C. venezuelae (see “Synonymy of 

Coryphopterus bol,” below). Our investigations indicate 

that the absence of this pigment spot on the pectoral-fi n 

base, along with the presence of vertically elongate versus 

round pigment spots in the lower row of markings on the 

body, is signifi cant in separating C. tortugae from pale 

specimens of C. venezuelae. Examination of photographs 

of the holotype of Ctenogobius tortugae (SU 8363) confi rms that there is no pigment on the lower portion of the 

pectoral-fi n base.

Coryphopterus tortugae is most easily separated from 

all other Coryphopterus by the following combination of 

characters: a dark blotch or triangle of pigment above the 

opercle is present; large X-shape markings on the side of 

the body and a spot on the lower pectoral-fi n base are 

absent; at least some of the pigment markings in the lower 

row along the side of the body are vertically elongate or 

crescent shaped; and the overall coloring is pale.

Coryphopterus glaucofraenum Gill, 1864

FIGURE 4

The location of the single type specimen upon which 

Gill described C. glaucofraenum is unknown (Eschmeyer, 

2008). Böhlke and Robins (1960:108– 109) described 

FIGURE 1. (facing page) Neighbor-joining tree derived from cytochrome c oxidase I sequences showing genetically distinct lineages 

of western Atlantic Coryphopterus.

NUMBER 38 • 115

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TABLE 1. Average (and range) Kimura two-parameter distance summary for Coryphopterus species based on cytochrome c oxidase I (COI) sequences of individuals represented in the 

neighbor-joining tree in Figure 1. Intraspecifi c averages are shown in bold; n/a  data not available.Coryphopterus lipernes hyalinus personatus tortugae glaucofraenum venezuelae dicrus thrix eidolon alloides alloides kunasp. (n 7) (n 11) (n  10) (n 21) (n 29) (n 33) (n 22) (n 7) (n  19) 1 (n 3) 2 (n 1) (n 5)

lipernes 0.13% ––––––––––– 

(0.00– 0.35)

hyalinus 14.88% 0.06% –––––––––– 

(14.21– 15.40) (0.00– 0.31)

personatus 15.66% 7.14% 0.14% ––––––––– 

(15.10– 16.03) (6.79– 7.65) (0.00– 0.46)

tortugae 19.60% 21.14% 20.08% 0.20% ––––––––  (18.65– 20.23) (20.64– 21.82) (19.46– 21.02) (0.00– 0.61) glaucofraenum 20.71% 21.68% 21.50% 12.07% 0.19% –––––––  (19.49– 21.20) (20.61– 22.44) (20.48– 22.30) (11.07– 12.99) (0.00– 0.92) venezuelae 21.37% 20.86% 20.12% 9.84% 9.51% 0.53% ––––––  (19.27– 22.13) (19.59– 21.69) (18.58– 21.18) (8.10– 10.77) (8.59– 10.21) (0.00– 1.24) 

dicrus 21.72% 19.68% 19.03% 17.53% 20.65% 18.28% 0.61% –––––  (20.10– 22.56) (18.61– 20.37) (18.30– 19.94) (16.59– 18.07) (19.82– 21.32) (16.46– 19.00) (0.00– 2.82) thrix 21.86% 21.10% 19.70% 19.00% 21.03% 19.30% 21.30% 0.11% ––––  (20.85– 22.69) (20.11– 22.44) (19.19– 20.48) (18.43– 19.63) (20.30– 21.54) (17.61– 20.12) (20.74-21.84) (0.00– 0.48) 

eidolon 25.16% 19.19% 17.92% 19.74% 23.17% 18.72% 19.39% 19.54% 0.24% ––– 

 (24.45– 26.19) (18.19– 20.11) (17.12– 18.82) (18.34– 21.42) (21.98– 25.04) (16.75– 20.36) (18.69– 20.87) (18.96– 20.41) (0.00– 0.99) 

alloides 1 22.13% 17.90% 18.16% 19.44% 21.69% 18.62% 18.15% 20.39% 18.06% 0.21% –– 

 (21.53– 22.53) (17.09– 18.64) (17.69– 18.93) (18.79– 20.14) (20.98– 22.48) (17.67– 19.70) (17.52– 19.03) (19.91– 21.18) (17.28– 19.08) (0.16– 0.31) alloides 2 21.15 17.75% 19.27% 21.73% 21.30% 19.68% 17.11% 19.16% 19.34% 9.68% n/a – 

 (21.02– 21.68) (17.62– 17.96) (19.04– 19.94) (21.38– 22.18) (21.04– 21.81) (18.58– 20.23) (16.70– 17.80) (19.10– 19.38) (18.82– 19.90) (9.48– 9.88) n/a kuna 26.41 23.22% 25.70% 25.51% 27.87% 25.78% 24.91% 25.63% 25.54% 23.30% 23.97% 0.57%

 (25.59– 27.00) (22.62– 23.65) (24.86– 26.37) (24.58– 26.27) (26.79– 28.53) (24.48– 26.64) (23.36– 25.57) (24.96– 26.27) (24.61– 26.20) (22.77– 23.65) (23.59– 24.30) (0.15– 1.24)

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FIGURE 2. Coryphopterus lipernes: A, Curacao, 20 mm SL, DNA 8326, USNM 394896; B, Curacao, 21 mm SL, DNA 

8051, USNM 394895. Coryphopterus hyalinus: C, Curacao, 20 mm SL, DNA 8044, USNM 394890; D, Curacao, 17 

mm SL, DNA 8265, USNM 294889. Coryphopterus personatus: E, Curacao, 21 mm SL, DNA 8045, USNM 294897; 

F, Belize, 15 mm SL, DNA 7163, USNM 394742.

NUMBER 38 • 117

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FIGURE 3. Coryphopterus tortugae: A, Belize, 25 mm SL, DNA 7333, USNM 394744; B, Belize, 34 mm SL, DNA 5237, USNM 

394743; C, Belize, 36 mm SL, DNA 7107, USNM 394733; D, Belize, 40 mm SL, DNA 4530, USNM 394730; E, Belize, 40 mm SL, 

DNA 4530, USNM 394730, preserved; F, Venezuela, 37 mm SL, DNA 7736 4, AMNH 247340, alcohol preserved.

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two forms of C. glaucofraenum: “[D]ark inshore form 

(typical glaucofraenum)” and”[P]allid white-sand form.” 

Specimens in our genetic clade identifi ed as C. glaucofraenum match the Böhlke and Robins (1960) “typical 

glaucofraenum,” an identifi cation supported by the fact 

that the pallid form is now recognized as C. tortugae. 

Below (see “Designation of Neotype for Coryphopterus 

glaucofraenum”) we select a neotype for C. glaucofraenum Gill.

In our material, adult C. glaucofraenum can always 

be separated from C. tortugae by having at least some 

large, well-formed X-shaped markings along the side of 

the body. It can almost always be separated from C. venezuelae by lacking a prominent dark marking on the lower 

portion of the pectoral-fi n base and sometimes by having 

10 total anal-fi n elements. Rarely, C. glaucofraenum has a 

dark pectoral-fi n base that includes pigment on the lower 

portion (Figure 4G), and C. venezuelae may have 9– 11 

anal-fi n elements, 10 being the typical count in our material (Table 2). Coryphopterus glaucofraenum usually can 

be separated from both C. tortugae and C. venezuelae by 

the shape of the pigment marking above the opercle: a 

two-peaked blotch in C. glaucofraenum, and a triangular 

or rounded blotch in C. tortugae and C. venezuelae.

If a specimen has a two-peaked blotch of pigment 

above the opercle, has at least some large (height approximately three-quarters of or equal to diameter of 

eye) X-shaped markings along the side of the body, has 

10 anal-fi n elements, and lacks pigment on the lower 

portion of the pectoral-fi n base, it is unquestionably 

C. glaucofraenum.

Coryphopterus venezuelae (Cervigón, 1966)

FIGURE 5

The most recent keys to western Atlantic Coryphopterus (Böhlke and Robins, 1960, 1962; Böhlke and 

Chaplin, 1968; Murdy 2002) do not include C. venezuelae, originally described as a subspecies of C. glaucofraenum by Cervigón (1966), but recognized as a separate 

species by Cervigón (1994) and known at the time only 

from Venezuela. In the Coryphopterus material from the 

northeast coast of Venezuela that we examined are specimens that are clearly C. venezuelae based on Cervigón’s 

(1966, 1994) descriptions: most notably the presence of 

11 second dorsal- and anal-fi n elements, a dark blotch of 

pigment on the lower portion of the pectoral-fi n base, and 

two dark spots on the base of the caudal fi n (e.g., Figure 

5D herein). However, those Venezuelan specimens are part 

of a clade based on COI analysis (see Figure 1) that includes specimens from Venezuela, Curacao, Panama, Belize, 

Puerto Rico, and the Bahamas (the last not shown on the 

tree) that usually have 10 second dorsal- and anal-fi n elements and various patterns of pigment on the base of the 

caudal fi n, including a central bar, two spots joined by a 

bar, and a C-shaped blotch (Figure 5A– C,E). The Venezuelan specimens on the tree (Figure 1), including two that 

have 10 second dorsal- and anal-fi n elements (VEN 7733 

1 and VEN JV12), cluster within the C. venezuelae clade, 

but the genetic distance between the Venezuelan specimens 

and other members of the clade is only 0.41% to 0.85%. 

This distance is extremely small relative to the genetic 

distance between the C. venezuelae clade and other species on the tree (9.51%– 20.86%; see Table 1), suggesting that the individuals in this clade represent a single 

species. Corroborating the identifi cation of the clade as 

Cervigón’s C. venezuelae is the presence in all individuals in the clade of a dark spot on the lower portion of the 

pectoral-fi n base. Among western Atlantic Coryphopterus, 

only C. punctipectophorus and C. dicrus have a prominent pigment spot on the lower portion of the pectoral-fi n 

base: C. punctipectophorus is not known from the Caribbean, and it differs morphologically from C. venezuelae

in, among other features, lacking a dark blotch of pigment 

behind the eye above the opercle; in C. dicrus, there is also 

a prominent spot of equal size on the dorsal portion of the 

pectoral base that is lacking in C. venezuelae (which may 

have a slash of pigment but never a well-defi ned dorsal 

spot equal in size and intensity to the lower spot); C. dicrus also lacks the dark pigment behind the eye above 

the opercle and lacks a pelvic frenum (both present in 

C. venezuelae).

Our data thus suggest that C. venezuelae is a much 

more widespread species than previously recognized, and 

fi n-ray counts alone are not suffi cient in diagnosing the 

species. Cervigón (1994) believed that the presence of 10 

second dorsal- and anal-fi n elements in C. glaucofraenum

distinguished it from C. venezuelae. In his material of the 

latter, all specimens had 11 second dorsal-fi n elements and 

most had 11 anal-fi n elements (two had 10). Most of our 

specimens of C. glaucofraenum have 10 second dorsaland anal-fi n elements, but two specimens have 11 second 

dorsal-fi n elements, and two have 9 anal-fi n elements (see 

Table 2). Both 10 and 11 second dorsal- and anal-fi n elements are common in specimens in our C. venezuelae clade 

(Table 3), although we found 11 in both fi ns only in some 

of our material from Venezuela. It is signifi cant that one 

of the C. venezuelae specimens from Venezuela that has 

10 elements in both fi ns was caught in the same sample as 

NUMBER 38 • 119

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FIGURE 4. Coryphopterus glaucofraenum: A, Belize, 44 mm SL, DNA 6367; B, Belize, 25 mm SL, DNA 7352, 

USNM 394354; C, Belize, 35 mm SL, DNA 7351, USNM 394353, preserved; D, Venezuela, 31 mm SL, DNA 7744 

2, AMNH 247339, alcohol preserved; E, Venezuela, 27 mm SL, DNA 7744 3, AMNH 247339, alcohol preserved; 

F, Panama, 34 mm SL, DNA 7712 2, AMNH 247335, alcohol preserved; G, Panama, 37 mm SL, DNA 7701 1, 

AMNH 247334, alcohol preserved.

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NUMBER 38 • 121

several with 11 in both fi ns. There is thus more variability 

in numbers of second dorsal- and anal-fi n elements than 

Cervigón indicated, and those fi n-ray counts are of value 

in separating C. glaucofraenum and C. venezuelae only 

when 11 elements are present in both fi ns— a condition we 

have not observed in C. glaucofraenum, which may have 

11 second dorsal-fi n elements but no more than 10 analfi n elements (see Table 2).

If a specimen has a dark blotch or triangle of pigment 

above the opercle, 11 second dorsal-fi n and 11 anal-fi n 

elements, and a prominent pigment spot on the lower portion of the pectoral-fi n base, it is C. venezuelae.

If a specimen has those features and has 10 second 

dorsal- and anal-fi n elements, it is usually C. venezuelae

but could be C. glaucofraenum: as noted under “Coryphopterus glaucofraenum,” rarely specimens of that 

species may have pigment on the ventral portion of the 

pectoral-fi n base. The shape of the pigment marking 

above the opercle (with two peaks in C. glaucofraenum, 

a single triangular or rounded blotch in C. venezuelae; 

see “Coryphopterus glaucofraenum”) will frequently resolve the species identifi cation.

There are two distinct forms of C. venezuelae in 

terms of body pigment: one has at least some large Xshaped markings in the ventral row of markings similar 

to those of C. glaucofraenum (Figure 5B,D,E); the other 

is a much paler form, and the ventral pigment markings along the side of the body are usually fairly small, 

somewhat circular blotches (Figure 5A,C). Both forms, 

including the palest specimens, have a pigment spot on the 

lower pectoral-fi n base, but this spot may be composed 

primarily of yellow chromatophores versus melanophores 

in pale specimens. The less-pigmented form is most easily 

confused with C. tortugae, but some of the pigment spots 

in the ventral row of C. venezuelae are usually more circular than the vertically elongate ones of C. tortugae. Additionally, none of our specimens of C. tortugae has a 

spot of pigment (yellow or black) on the ventral portion 

of the pectoral-fi n base. Although unusually divergent 

intraspecifi cally in patterns of pigmentation (see Figure 

5) relative to, for example, the very similar patterns between species such as C. personatus and C. hyalinus, the 

two forms of C. venezuelae form a tight genetic clade 

(intraspecifi c variation, 0.53%; see Figure 1, Table 1). 

The different pigment patterns do not correspond to different fi n-ray counts, as we have observed 10 and 11 

second dorsal- and anal-fi n elements in both forms. For 

example, note the similar patterns of pigmentation in a 

specimen of C. venezuelae from Venezuela (Figure 5D) 

that has 11 second dorsal- and anal-fi n elements and 

a specimen of C. venezuelae from Panama (Figure 5E) 

that has 10 second dorsal- and anal-fi n elements. Furthermore, the differences are not attributable to sexual 

dimorphism or geography, but they could refl ect differences in local habitat. Some specimens of C. venezuelae

collected in mangrove areas tend to be dark, and those 

collected in reef areas pale, although we note that a dark 

form was collected on a reef off Panama (Figure 5E).

There is some correlation with size: the pale form 

of C. venezuelae is more common among small specimens (30 mm standard length [SL]), and the form with 

prominent X-shaped markings is more common among 

larger specimens (40 mm SL). Adults of the pale form 

of C. venezuelae (e.g., Figure 5A) look remarkably similar to juveniles (e.g., see Figure 7C). There is also a trend 

toward increasing depth of the head and anterior body in 

larger specimens. Similar differences in body shape and 

pigment with increasing size are evident in C. glaucofraenum (compare the juvenile in Figure 7B with adults in 

Figure 4). Possibly in C. venezuelae, growth is not always 

accompanied by a transformation in pigment and body 

depth, and adults retain more of the juvenile features. 

More investigation is needed to determine the relationships in C. venezuelae among pigment pattern, body 

shape, size, maturity, and local habitat. Cervigón (1966, 

1994) did not illustrate any of his type specimens of C. 

venezuelae, but we obtained digital photographs of two 

of his paratypes (MOBR-P-0867 [Museo Oceanológico 

Hermano Benigno Román, Venezuela]; one is shown in 

Figure 6). The holotype is not in good condition (J. C. 

Capelo, MOBR, personal communication, 4 July 2008). 

The pigment of the paratypes most closely resembles that 

in Figure 5D herein: a triangular to rounded mark above 

the opercle, a roughly circular dark spot on the ventral 

pectoral-fi n base, and two basicaudal spots joined by 

a light dusky bar. There is some evidence of X-shaped 

markings on the side of the body, but the body pigment is 

mostly faded. Cervigón (1966, 1994) did not mention Xshaped markings in his descriptions; rather, he noted that 

there are three longitudinal rows of dark spots.

TABLE 2. Frequency distributions of numbers of second dorsalfi n and anal-fi n elements in two species of Coryphopterus.

 No. of second No. of

 dorsal-fi n elements anal-fi n elements

Species 10 11 9 10 11

C. glaucofraenum 22 2 2 20 — 

C. venezuelae 20 13 1 22 11

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FIGURE 5. Coryphopterus venezuelae: A, Curacao, 29 mm SL, DNA 8260, USNM 394740; B, Venezuela, 54.4 mm SL, 

no DNA, Photo No. 1907 VT-05-530, photo by J. V. Tassell and D. R. Robertson; C, Belize, 35 mm SL, DNA 7248, 

USNM 394736; D, Venezuela, 50 mm SL, DNA JV15, AMNH 247345, alcohol preserved; E, Panama, 42.5 mm SL, 

DNA 7725-1, AMNH 247341, alcohol preserved.

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NUMBER 38 • 123

Synonymy of Coryphopterus bol

Victor (2008) described Coryphopterus bol as a species that heretofore had been masquerading under C. tortugae (e.g., Garzón-Ferreira and Acero 1990:107, fi g. 1A, 

Santa Marta specimens). We believe that Victor (2008) 

was correct in recognizing that the Santa Marta specimens 

are not C. tortugae, but our investigation indicates that 

they are C. venezuelae. The COI sequence that Victor 

(2008) provided for the new species (from the holotype 

from Puerto Rico) places it solidly with our C. venezuelae

clade (PR SIO 0869, fi g. 1). The average genetic distance 

between C. bol and individuals of C. venezuelae is 0.38% 

(range, 0.00%– 0.85%) and, for comparison, the average genetic distance between the holotype of C. bol and 

the next most closely related clade (C. tortugae) is more 

than 20-fold greater, or 8.47% (range, 8.10%– 9.21%). 

Diagnostic features of Victor’s (2008:4) C. bol include 

10 second dorsal- and anal-fi n elements; 19 pectoral-fi n 

rays; pelvic fi ns fully joined and with a distinct frenum; a 

prominent, dark, upward-pointed triangular marking on 

the stripe behind the eye; a discrete blotch of small melanophores on the lower third of the pectoral fi n base; and a 

basicaudal marking that resembles a thick “C.” The combination of the triangular marking on the stripe behind 

the eye above the opercle, the pigment blotch on the lower 

portion of the pectoral-fi n base, and 10 second dorsal- and 

anal-fi n elements matches most of our C. venezuelae specimens. Victor (2008) distinguished his new species from C. 

venezuelae based on the presence of 11 second dorsal- and 

anal-fi n elements in C. venezuelae, but, as noted above 

(also see Table 2), specimens matching Cervigón’s C. venezuelae based on the pre-pectoral pigment may have 10 or 

11 second dorsal- and anal-fi n elements.

Coryphopterus bol also matches C. venezuelae in 

number of pectoral-fi n rays (19 in C. bol, 61% of specimens with 19 in Cervigón’s [1994] C. venezuelae material), pelvic-fi n morphology, and other pigment. For 

example, the basicaudal mark in C. venezuelae may be 

C-shaped, but it ranges in our material from two separate spots to a central bar of pigment (some examples 

are shown in Figure 5). The basicaudal pigment is also 

somewhat variable in the type material of C. bol (Victor, 

2008:fi g. 1). Two of the type specimens of C. bol most 

closely resemble the pale form of C. venezuelae; that is, 

the form with round spots on a relatively slender body 

(holotype and a 32.1-mm SL paratype). Two paratypes 

(24.5 and 29 mm SL) are darker and have at least some 

X-shaped markings. None of Victor’s type material is 

larger than 32 mm SL, and, as noted under C. venezuelae, above, most of our dark, deeper-bodied specimens of 

C. venezuelae are 40 mm SL.

In summary, one cannot distinguish C. bol and C. venezuelae on the basis of numbers of second dorsal- and 

anal-fi n elements because there is more variation in those 

counts than previously reported. One might argue that 

specimens from Venezuela that have 11 elements in both 

the second dorsal and anal fi ns and heavy pigment with 

X-shape markings are C. venezuelae and that everything 

else in our C. venezuelae clade is C. bol. However, some 

specimens with those features, except with 10 elements in 

the second dorsal and anal fi ns, were taken in the same 

station off Venezuela as those with 11 elements (AMNH 

247345 [American Museum of Natural History]), so 

would one identify the former as C. venezuelae or C. bol? 

Species identifi cation of specimens with 11/10 or 10/11 

second dorsal-/anal-fi n elements also would be nebulous, 

as would species identifi cation of dark forms with 10/10 

but otherwise virtually identical to those with 11/11 (e.g., 

Figure 5D,E). Variation in COI among all specimens in the 

C. venezuelae clade is well within typical intraspecifi c levels for the genus. However, even if COI is masking recent 

divergence within the clade, there is a diagnostic morphological feature for the clade: a conspicuous spot or blotch 

of pigment on the lower pectoral-fi n base; in combination 

with a triangular or circular blotch of pigment behind the 

eye above the opercle, this character is unique to C. venezuelae. The more common presence of 11 second dorsal- and anal-fi n elements in some Venezuelan specimens 

may best be interpreted as regional variation. Known 

currently from Belize, Panama, Curacao, Venezuela, the 

Bahamas, the U.S. Virgin Islands, Puerto Rico, Saba, and 

Brazil, C. venezuelae appears to be a widespread species. 

It is misidentifi ed in the USNM (U.S. National Museum; 

TABLE 3. Frequency distributions of the combinations of second 

dorsal-fi n and anal-fi n elements in Coryphopterus venezuelae by 

country.

 No. of second dorsal-fi n elements / anal-fi n elements

Country 10/9 10/10 10/11 11/10 11/11

Belize —2 ——— 

Curacao 1 11 1 1 — 

Panama —6 1 —— 

Venezuela —2 —1 9

Puerto Rico — 1a ——— 

a Holotype of Coryphopterus bol.

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124 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 6. Paratype of Coryphopterus venezuelae, MOBR-P-0867, 42 mm SL (length estimated from 

ruler included with original photograph; this is likely Cervigón’s 41.2 mm SL paratype).

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NUMBER 38 • 125

i.e., National Museum of Natural History, Smithsonian 

Institution)— and likely other museum collections— as 

C. glaucofraenum or C. tortugae.

Key Notes for C. tortugae, C. glaucofraenum, 

and C. venezuelae

Juveniles (Figure 7), and occasionally adults, of C. tortugae, C. glaucofraenum, and C. venezuelae may lack the 

black marking or triangle above the opercle, or it is not as 

dark as other pigment in the stripe posterior to the eye. As 

we have used this feature in the “Revised Key to Western 

Atlantic Coryphopterus” (see below) to separate C. tortugae, C. glaucofraenum, and C. venezuelae from other 

species, absence of this feature in specimens of any of those 

species could present identifi cation problems. If there are 

well-defi ned X’s of pigment along the sides of the body (C. 

glaucofraenum and some C. venezuelae) or the basicaudal 

pigment comprises two spots or a dumbbell-shaped marking (most C. glaucofraenum and some C. venezuelae), users 

of the key should follow the option in the couplet that indicates the dark marking is present above the opercle (4b). If 

a specimen lacks the dark pigment spot above the opercle, 

has 11 second dorsal- and anal-fi n rays, and has a prominent dark blotch on the lower portion of the pectoral-fi n 

base, it can only be C. venezuelae. Coryphopterus punctipectophorus is similar in lacking the pigment spot above 

the opercle and having 11 second dorsal-fi n elements, but 

it has 10 anal-fi n elements (Springer, 1960). Furthermore, 

geography will currently separate those two species: C. 

venezuelae occurs in the Caribbean, and C. punctipectophorus is known only from the Gulf of Mexico and off the 

southeastern USA.

Coryphopterus dicrus Böhlke and Robins, 1960

FIGURE 8

Numerous features, in combination, separate C. dicrus

from other western Atlantic Coryphopterus, including the 

following: no black ring of pigment around anus; no distinct dark spot behind eye above opercle; anal-fi n elements 

10; pelvic frenum absent; pectoral-fi n base with two prominent dark spots of equal intensity, one above the other; and 

sides of body freckled with scattered large and smaller pigment blotches. The last two characters are the quickest way 

to make the identifi cation. The only other species that usually have pigment dorsally and ventrally on the pectoral-fi n 

base are C. venezuelae and C. thrix, but the dorsal pigment 

on the pectoral-fi n base in C. venezuelae, when present, is a 

slash versus a spot, and the dorsal pigment on the pectoralfi n base in C. thrix is usually much more pronounced than 

the ventral marking. Additionally, both species have a pelvic 

frenum, which is lacking in C. dicrus.

Coryphopterus thrix Böhlke and Robins, 1960

FIGURE 8

Coryphopterus thrix is the only western Atlantic species of Coryphopterus that lacks black pigment around the 

anus and has the second dorsal-fi n spine elongated into a 

fi lament. If the spine is broken, however, the species is still 

identifi able by the combination of features presented in 

the key, most notably the absence of a distinctive pigment 

blotch above the opercle, presence of a conspicuous dark 

blotch on the dorsal portion of the pectoral-fi n base, and 

presence of a pelvic frenum.

Coryphopterus alloides Böhlke and Robins, 

1960

FIGURE 9

Distinguishing features of C. alloides include having a 

low anal-fi n count (8– 9 total elements), a dark blotch of pigment on the lower portion of the membrane between the 

second and third dorsal spines, and the pelvic fi ns almost 

completely separate. Only C. kuna, among the Coryphopterus species lacking a black ring of pigment around the 

anus, has as few as 9 anal-fi n elements, but that species has 9 

second dorsal-fi n elements and 15 pectoral rays (vs. usually 

10 and 16– 17, respectively, in C. alloides). Coryphopterus 

kuna may have a stripe and distal fl ag of pigment on the fi rst 

dorsal fi n, but it never has the pigment blotch on the lower 

portion of the fi rst dorsal fi n characteristic of C. alloides. 

The living color pattern of C. alloides is also distinctive: the 

head and anterior portion of the body bear a considerable 

amount of orange pigment, whereas the posterior portion 

of the body is yellow. An apparently cryptic species related 

to but genetically distinct from C. alloides and known only 

from Curacao is currently under investigation.

Key Note

In some preserved specimens of C. alloides, there are 

melanophores above the opercle that may lead the user 

of the key to select “4b. Distinct black blotch or triangle 

behind eye above opercle . . .” However, this pigment is 

never as consolidated and prominent in C. alloides as in 

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126 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 7. Coryphopterus juveniles: A, C. tortugae, Belize, 20 mm SL, DNA 7693, USNM 394800; B, C. glaucofraenum, 

Belize, 17 mm SL, DNA 7769, USNM 394793; C, Coryphopterus venezuelae, Belize, 17 mm SL, DNA 7728, USNM 394881, 

D, Coryphopterus thrix, Curacao, 16 mm SL, DNA 8261, USNM 394760; E, Coryphopterus dicrus, Belize, 13 mm SL, DNA 

6110, USNM 394779. F, Coryphopterus eidolon, Belize, 18 mm SL, DNA 6223, USNM 394788.

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NUMBER 38 • 127

FIGURE 8. Coryphopterus dicrus: A, Florida, 38 mm SL, DNA 7348, USNM 394345; B, Curacao, 30 mm SL, DNA 8135, 

USNM 394747; C, Belize, 13 mm SL, DNA 6110, USNM 394779. Coryphopterus thrix: D, Belize, 23.5 mm SL, DNA 7816, 

USNM 394914; E, Curacao, 23 mm SL, DNA 8426, USNM 394761; F, Venezuela, AMNH 244983, 26 mm SL, alcohol preserved, no DNA.

07_Baldwin_111-138_Lang.indd 127 7_Baldwin_111-138_Lang.indd 127 9/24/09 9:38/24/09 9:38
FIGURE 9. Coryphopterus alloides: A, Belize, 24 mm SL, DNA 7233, USNM 394754; B, Belize, 19 mm SL, DNA 7264, USNM 

394755; C, Belize, 24 mm SL, preserved, DNA 7233, USNM 394754. C. eidolon: D, Curacao, 38 mm SL, DNA 8050, USNM 

394885; E, Belize, 34 mm SL, DNA 7109, USNM 394752; F, Belize, 33 mm SL, preserved, DNA 5070, USNM 394750.

128 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

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NUMBER 38 • 129

C. tortugae, C. glaucofraenum, and C. venezuelae; furthermore, C. alloides lacks a pelvic frenum, a conspicuous 

feature in the other three species.

Coryphopterus eidolon Böhlke and Robins, 

1960

FIGURE 9

Pigment, except for basicaudal and scattered small 

body melanophores, is yellow, which disappears during 

preservation, typically rendering this a very pale goby. In 

life there is a yellow stripe behind the eye bordered by 

small melanophores that remain in preserved specimens after the color fades. There are no dark markings above the 

opercle, on the pectoral-fi n base, or on the fi rst dorsal fi n. 

The absence of distinctive markings (other than the basicaudal mark) is the easiest way to recognize C. eidolon, a 

very abundant species in many of our samples, particularly 

from Belize and Curacao.

Coryphopterus kuna Victor, 2007

FIGURE 10

Baldwin and Smith (2003) described Coryphopterus B 

larvae from Belize as likely belonging to an unidentifi ed 

species based on the low second dorsal- and anal-fi n counts 

(9 in both fi ns) and low pectoral-fi n count (15). Victor 

(2007) described C. kuna, which has the low fi n-ray counts 

of the Coryphopterus B larvae, as a new species from off 

Panama. Incorporation of the COI sequence published in 

the original description of C. kuna into our analysis revealed that Coryphopterus B larvae are C. kuna. This species is distinctive in typically having 9 second dorsal- and 

anal-fi n elements, as well as a low pectoral-ray count of 15 

(found elsewhere only in C. personatus and C. hyalinus). 

Apparently a small fi sh— the adult male holotype is 17.1 

mm SL— C. kuna has little dark pigment: numerous small 

spots on the pelvic fi n of the holotype, a few scattered small 

spots on the sides of the body, no markings on the pectoralfi n base, and no basicaudal spot. It lacks a pelvic frenum.

Coryphopterus punctipectophorus Springer, 

1960

FIGURE 10

Coryphopterus punctipectophorus is similar to C. tortugae, C. glaucofraenum, and C. venezuelae in having 

three rows of pigment spots along the side of the body, but 

it differs from those species in lacking a dark blotch or triangle behind the head above the opercle. It is most similar 

to C. venezuelae in having a prominent dark spot on the 

lower portion of the pectoral-fi n base, and juvenile (and 

occasionally adult) specimens of C. venezuelae that lack 

the pigment blotch above the opercle will typically key to 

C. punctipectophorus based on the ventral pigment spot 

on the pectoral-fi n base. Like C. venezuelae, C. punctipectophorus was originally described as having 11 second 

dorsal-fi n elements, but as noted above (see C. venezuelae), the former has 10 or 11 second dorsal elements. The 

“dusky light buff” pigment spots along the dorsal contour 

and “coral pink” spots along the sides of the body in fresh 

material of C. punctipectophorus (Springer, 1960:240; see 

Figure 10B,E herein) apparently fade in preserved material 

(see Figure 10D). The known distribution of C. punctipectophorus includes both coasts of Florida, the Gulf of 

Mexico (including the southern Gulf where it meets the Caribbean), and South Carolina. It apparently inhabits deeper 

water than some Coryphopterus species: the type material 

was collected at 62 and 120 feet. It has not been reported 

from the Caribbean. We have not collected C. punctipectophorus, and fresh material of the species was not available for inclusion in our genetic analysis. Thacker and 

Cole’s (2002) C. punctipectophorus from Belize (GenBank 

Accession No. AF391396) is C. dicrus, based on incorporation of their COI sequence into our data set.

REVISED KEY TO THE WESTERN ATLANTIC SPECIES OF CORYPHOPTERUS

 1a. Black ring of pigment surrounding anus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .2

 1b. Black ring around anus absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .4

 2a. One interorbital pore anteriorly . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .3

 2b. Two interorbital pores anteriorly . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Coryphopterus hyalinus

 3a. Second dorsal and anal fi ns each typically with 11 total elements; head with some orange pigment in life; body translucent, with several squares or rectangles of pale orange pigment internally; preserved specimens lacking conspicuous 

postorbital stripes of melanophores but with “mask” of pigment around eye . . . . . . . . . . . . Coryphopterus personatus

(continued on p. 130)

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REVISED KEY TO THE WESTERN ATLANTIC SPECIES OF CORYPHOPTERUS (continued)

 3b. Second dorsal and anal fi ns typically with 10 total elements; head and body predominantly yellow in life; a dusky internal stripe along posterior section of vertebral column; preserved specimens with postorbital stripes of melanophores and 

scattered spots over entire body . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Coryphopterus lipernes

 4a. No distinct black blotch behind eye above opercle in adults; pigment above opercle, if present, no larger or darker than 

other markings behind eye; pelvic frenum present or absent (see “Key Note” for C. alloides in text). . . . . . . . . . . . . . .5

 4b. Distinct black blotch or triangle behind eye above opercle in adults, blotch usually larger and darker than other pigment in stripe behind eye; pelvic frenum present (see “Key Notes for C. tortugae, C. glaucofraenum, and C. venezuelae” in text) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .10

 5a. Anal-fi n elements 8– 9 (usually 9), pectoral-fi n rays 15– 17, pelvic frenum absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .6

 5b. Anal-fi n elements 10– 11, pectoral-fi n rays 17– 20, pelvic frenum present or absent . . . . . . . . . . . . . . . . . . . . . . . . . . . .7

 6a. Second dorsal and anal fi ns each with 9 elements; pectoral-fi n rays 15; pelvic fi ns fully joined; fi rst dorsal fi n with stripe 

of black pigment; in life, head and body with orange spots and blotches and sometimes with fl ag of dark pigment on 

1st– 3rd dorsal spines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Coryphopterus kuna

 6b. Second dorsal fi n with 10 elements, anal fi n with 9 (rarely 8); pectoral-fi n rays 16– 17; pelvic fi ns almost completely separate; black blotch or bar between 2nd and 3rd dorsal spines; head and anterior body mottled orange in freshly caught 

specimens, posterior body mottled yellow . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Coryphopterus alloides

 7a. Pectoral-fi n base with two prominent dark spots of equal intensity, one dorsally and one ventrally; upper spot usually with swath of melanophores extending posteriorly onto pectoral-fi n rays; sides of body freckled with scattered 

large and smaller blotches of melanophores (blotches associated with coral, tan, yellow pigment in life); pelvic 

frenum absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Coryphopterus dicrus

 7b. Pectoral-fi n base not with two prominent dark spots (or, if two spots present, upper spot more intense); sides of body 

with few dark markings (with few to many yellow spots in life) or with three rows of light markings (coral pink/orange 

in life); pelvic frenum present . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .8

 8a. Pectoral-fi n base without prominent dark markings but sometimes with a few to many scattered melanophores; sides of 

body with few if any dark markings (with yellow spots in life) except for basicaudal spot. . . . . .Coryphopterus eidolon

 8b. Pectoral-fi n base with prominent markings; sides of body with or without numerous dark markings . . . . . . . . . . . . . .9

 9a. Pectoral-fi n base with distinct pigment spot dorsally, spot usually dark above, diffuse below, often with dots trailing 

ventrally; ventral dots coalescing into a separate spot in some specimens (ventral spot, if present, less intense than dorsal 

spot); second dorsal-fi n elements 9– 10; second dorsal spine fi lamentous . . . . . . . . . . . . . . . . . . . . .Coryphopterus thrix

 9b. Pectoral-fi n base with prominent dark spot or blotch only on ventral portion; second dorsal-fi n elements 11; second 

dorsal spine not fi lamentous. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Coryphopterus punctipectophorus

 10a. Body usually pale, pigment primarily comprising three rows of markings on side of body; lower row comprising small, 

mostly vertically elongate markings, some of which may be crescent shaped or some part of an X-shape but rarely welldefi ned X’s; if X-shaped markings present, their height is considerably shorter than eye diameter; pigment marking above 

opercle usually a triangle, and basicaudal pigment usually a central bar . . . . . . . . . . . . . . . . . . Coryphopterus tortugae

 10b. Body heavily pigmented or pale but without vertically elongate or crescent-shaped markings in ventral row of pigment 

on side of body; height of X-shaped markings, if present, three-quarters of or equal to diameter of eye; pigment marking 

above opercle triangular, rounded, or with two peaks; basicaudal pigment comprising two separate spots, two spots connected by a line of pigment and resembling a dumbbell, a central bar, or a C-shaped marking . . . . . . . . . . . . . . . . . . .11

 11a. Pigment on pectoral-fi n base variable but always with dark spot or rectangular-shaped blotch ventrally (may be 

associated with bright yellow pigment in life); one or two additional bars, blotches, or concentrations of pigment 

sometimes present dorsally; three rows of dark markings on side of body, some in lower row large, X-shaped markings in heavily pigmented specimens, small, circular blotches in paler specimens; pigment marking above the opercle 

triangular or round . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Coryphopterus venezuelae

 11b. Pectoral-fi n base rarely with prominent dark marking ventrally, although melanophores may form one to three light to 

moderate concentrations on base; body with three rows of dark markings, most of those in the lower row large, distinctive X-shaped markings; pigment marking above opercle usually with two well-defi ned peaks . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Coryphopterus glaucofraenum

130 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

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NUMBER 38 • 131

FIGURE 10. A, Coryphopterus kuna, San Andres, Colombian Caribbean (photo by Keri Wilk, ReefNet Inc.); B, Coryphopterus punctipectophorus, Holbox Island, Mexico (photo by Hilario Itriago); C, Coryphopterus kuna, Panama, 

17.1 mm SL, holotype, SIO-07-5, preserved, DNA GB EF55021 (reproduced from B. Victor, 2007, fi g. 1A, Zootaxa

1526:53); D, Coryphopterus punctipectophorus, South Carolina, 28 mm SL, USNM 315530, preserved, no DNA; E, 

Coryphopterus punctipectophorus, Florida, Gulf of Mexico, 42 mm SL, holotype, ANSP 90103, preserved, no DNA.

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132 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Designation of Neotype for 

Coryphopterus glaucofraenum

FIGURE 11

Eschmeyer (2008) noted the need for designating a 

neotype for Coryphopterus glaucofraenum Gill, because 

the whereabouts of the holotype are unknown. He also 

noted that four MCZ specimens assumed to be syntypes do 

not constitute type material because Gill’s (1863) description was clearly based on a single specimen. Because of the 

historical confusion regarding the validity of C. tortugae

and C. venezuelae as distinct from C. glaucofraenum, and 

because the three species can be diffi cult to separate, we 

have elected to designate a neotype for C. glaucofraenum

from which we have successfully obtained a COI sequence 

that places the specimen in the C. glaucofraenum clade. 

We hereby make the following type designation:

Neotype

Coryphopterus glaucofraenum Gill, USNM 393907, 

44 mm SL, DNA 6367, Twin Cays, Belize, mangrove 

edge on interior channel, 0– 6 ft. (GenBank accession no. 

GQ367355.)

SUMMARY AND FUTURE WORK

Cytochrome c oxidase I sequences (DNA barcoding) 

were useful in determining the number of distinct genetic 

lineages within Caribbean Coryphopterus. We used the 

neighbor-joining tree (see Figure 1) derived from those sequences to assemble voucher specimens (and color photographs of them taken before preservation) into clades and 

then compared the morphology of specimens among those 

clades. Assigning clades to species was relatively easy based 

FIGURE 11. Coryphopterus glaucofraenum, neotype, USNM 393907, Belize, 44 mm SL, DNA 6367: A, 

fresh; B, preserved.

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NUMBER 38 • 133

on review of original literature and examination of some 

type specimens (or photographs of them). Resolving the 

identities of many Caribbean Coryphopterus in the absence 

of the DNA data would have been extremely diffi cult.

We are continuing to expand our geographic coverage 

of Coryphopterus sampling and will continue sequencing 

COI, and ultimately other genes, from specimens from a 

diversity of locations. The precise geographic distributions 

of most western Atlantic Coryphopterus are not known, 

and our genetic analyses have revealed the presence of one 

or more additional cryptic species. Additionally, the existence of two morphological forms within the genetic clade 

identifi ed as C. venezuelae warrants further investigation. 

Ultimately, our multi-locus data set will enable us to reanalyze phylogenetic relationships among Coryphopterus

species, from which we can investigate patterns of speciation and morphological divergence. Finally, testing of the 

species identifi cations of Coryphopterus larvae proposed 

by Baldwin and Smith (2003) based on morphology is currently in progress based on COI sequences of larvae collected as part of this study.

ACKNOWLEDGMENTS

Cody Payne contributed to the organization of our Belizean Coryphopterus material, made radiographs and counts 

of numerous specimens, helped distinguish C. tortugae from 

C. glaucofraenum, and provided data helpful in developing the revised species key. James Van Tassell contributed 

numerous specimens, tissue samples, and photographs of 

Venezuelan and Panamanian Coryphopterus and engaged 

in many helpful discussions about Coryphopterus with the 

fi rst author. Amy Driskell and Andrea Ormos provided laboratory and logistical assistance. Jon Fong provided images 

of the holotype of Ctenogobius tortugae. Victor Springer, 

Lisa Palmer, and Hilario Itriago provided images of Coryphopterus punctipectophorus. Benjamin Victor provided 

the photograph of the holotype of C. kuna, and Zhi-Qiang 

Zhang, Chief Editor of Zootaxa, allowed us to reproduce 

this image. Keri Wilk provided the in situ image of C. kuna. 

Annemarie Kramer allowed us to include her sequences 

of C. tortugae from Curacao in our analysis. Oscar M. 

Lasso-Alcala, Juan C. Capelo, and Ramon Varela provided 

digital images of two paratypes of C. venezuelae. Michael 

Carpenter, Zachary Foltz, Amy Driskell, and Justin Bagley 

provided fi eld assistance in Belize and Florida. Research in 

Florida was conducted pursuant to Special Activity License 

07SR-1024. Amos Gazit, Kate Wilson, and Maureen Kunen 

made it possible for us to collect fi sh samples through the 

CARMABI laboratory in Curacao. Fieldwork in the Bahamas was conducted under the auspices of the Perry Institute 

of Marine Science, with logistical assistance from Brenda 

Gadd. Fourteen members of the fi rst author’s family contributed to the fi eldwork in the Bahamas, and a portion of that 

work was funded by a generous donation from Christine B. 

Lang in memory of David E. Baldwin and Richard A. Lang. 

The Smithsonian Marine Science Network provided most of 

the funding for fi eldwork, and the Smithsonian DNA Barcoding Initiative provided funding for molecular analyses. 

This is contribution number 837 of the Caribbean Coral 

Reef Ecosystems Program (CCRE), Smithsonian Institution, 

supported in part by the Hunterdon Oceanographic Research Fund, and Smithsonian Marine Station at Fort Pierce 

(SMSFP) Contribution No. 756.

LITERATURE CITED

Baldwin, C. C., and D. G. Smith. 2003. Larval Gobiidae (Teleostei: Perciformes) of Carrie Bow Cay, Belize, Central America. Bulletin of 

Marine Science, 72:639– 674.

Böhlke, J. E., and C. G. Chaplin. 1968. Fishes of the Bahamas and Adjacent Tropical Waters. Wynnewood, Pa.: Livingston Publishing 

Company.

Böhlke, J. E., and C. R. Robins. 1960. A Revision of the Gobioid Fish 

Genus Coryphopterus. Proceedings of the Academy of Natural Sciences of Philadelphia, 112(5):103– 128.

— — — . 1962. The Taxonomic Position of the West Atlantic Goby, 

Eviota personata, with Descriptions of Two New Related Species. 

Proceedings of the Academy of Natural Sciences of Philadelphia, 

114(5):175– 189.

Cervigón, F. 1966. Los Peces Marinos de Venezuela. Volume II. Caracas: 

Estacion de Investigaciones Marinas de Margarita Fundacion La 

Salle de Ciencias Naturales.

— — — . 1994. Los Peces Marinos de Venezuela. Volume III. Caracas: 

Fundación Cientifi ca Los Roques.

Eschmeyer, W. N., ed. 2008. Catalog of Fishes: Electronic Version (updated 

23 April 2008), http://www.calacademy.org/research/ichthyology/

catalog/fi shcatsearch.html (accessed January 2008).

Garzón-Ferreira, J., and A. P. Acero. 1990. Redescription of Coryphopterus tortugae (Jordan) (Osteichthyes: Gobiidae), a Valid Species of Goby from the Western Atlantic. Northeast Gulf Science, 

11(2):105– 112.

Gill, T. N. 1863. Descriptions of the Gobioid Genera of the Western 

Coast of Temperate North America. Proceedings of the Academy of 

Natural Sciences of Philadelphia, 15:262– 267.

Greenfi eld, D. W., and R. K. Johnson. 1999. Assemblage Structure and 

Habitat Associations of Western Caribbean Gobies (Teleostei: Gobiidae). Copeia, 1999(2):251– 266.

Jordan, D. S. 1904. Notes on the Fishes Collected in the Tortugas 

Archipelago. Bulletin of the U.S. Fish Commission, 22(1902):

539– 544.

Jordan, D. S., and J. C. Thompson. 1905. The Fish Fauna of the Tortugas 

Archipelago. Bulletin of the Bureau of Fisheries, 24:229– 256.

Kimura, M. 1980. A Simple Method for Estimating Evolutionary Rates 

of Base Substitutions Through Comparative Studies of Nucleotide 

Sequences. Journal of Molecular Evolution, 16:111– 120.

07_Baldwin_111-138_Lang.indd 133 7_Baldwin_111-138_Lang.indd 133 9/24/09 9:39/24/09 9:39
134 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Longley, W. H., and F. Hildebrand. 1941. Systematic Catalogue of the 

Fishes of Tortugas, Florida: With Observations on Color, Habits, 

and Local Distribution. Washington, D.C.: Carnegie Institution of 

Washington.

Murdy, E. O. 2002. “Gobiidae.” In The Living Marine Resources of the 

Western Central Atlantic. Volume 3: Bony Fishes, Part 2 (Opistognathidae to Molidae), Sea Turtles and Marine Mammals, ed. K. E. 

Carpenter, pp. 1375– 2127. Rome: The Food and Agriculture Organization of the United Nations.

Saitou, N., and M. Nei. 1987. The Neighbor-Joining Method: A New 

Method for Reconstructing Phylogenetic Trees. Molecular Biology 

and Evolution, 4:406– 425.

Seutin, G., B. N. White, and P. T. Boag. 1990. Preservation of Avian 

Blood and Tissue Samples for DNA Analysis. Canadian Journal of 

Zoology, 69:82– 90.

Smith, C. L., J. C. Tyler, W. P. Davis, R. S. Jones, D. G. Smith, and C. C. 

Baldwin. 2003. Fishes of the Pelican Cays, Belize. Atoll Research 

Bulletin, No. 497. Washington, D.C.: National Museum of Natural 

History, Smithsonian Institution.

Springer, V. G. 1960. A New Gobiid Fish from the Eastern Gulf of Mexico. 

Bulletin of Marine Science of the Gulf and Caribbean, 10(2):237– 240.

Swofford, D. L. 2002. PAUP*: Phylogenetic Analysis Using Parsimony 

(and Other Methods). Version 4, Beta 10 (CD-Rom). Sunderland, 

Mass.: Sinauer Associates.

Thacker, C. E., and K. S. Cole. 2002. Phylogeny and Evolution of the Gobiid 

Genus Coryphopterus. Bulletin of Marine Science, 70(3):837– 850.

Victor, B. C. 2007. Coryphopterus kuna, a New Goby (Perciformes: Gobiidae: Gobiinae) from the Western Caribbean, with the Identifi cation of the Late Larval Stage and an Estimate of the Pelagic Larval 

Duration. Zootaxa, 1526:51– 61.

— — — . 2008. Redescription of Coryphopterus tortugae (Jordan) and a 

New Allied Species Coryphopterus bol (Perciformes: Gobiidae: Gobiinae) from the Tropical Western Atlantic Ocean. Journal of the 

Ocean Science Foundation, 1:1– 19.

TABLE A.1. Coryphopterus material. A number in the DNA column indicates that the specimen was analyzed for cytochrome c oxidase 

1. An asterisk beside this number indicates the entry appears in the neighbor-joining tree in Figure 1; because of space constraints, not 

all specimens for which DNA was successfully sequenced are included in Figure 1. Extracting DNA was not attempted on formalin-fi xed 

specimens. If the specimen was not sampled for DNA, “no DNA” is recorded in this column; BZE, Belize; FLA, Florida; CUR, Curacao; 

BAH, Bahamas; PAN, Panama; VEN, Venezuela.

Species DNA Standard Specimen Photo voucher

 length (mm) voucher a at NMNH

C. lipernes BZE 4067* —No voucher No

BZE 4082* 23 No voucher No

BZE 4083* 21 No voucher No

BZE 7729* 18 USNM 394796 Yes

CUR 8051* 21 USNM 394895 Yes

CUR 8326* 20 USNM 394896 Yes

CUR 8327* 17 USNM 394894 Yes

C. hyalinus BZE 4511* 15 No voucher No

BZE 4512* 15 No voucher No

BZE 5066* 13 No voucher Yes

BZE 6221* 13.5 USNM 394795 Yes

BZE 6222* 14.5 USNM 394794 Yes

BZE 7760* 7 No voucher Yes

CUR 8044* 20 USNM 394890 Yes

CUR 8046* 19.5 USNM 394891 Yes

CUR 8264* 19 USNM 394893 Yes

CUR 8265* 17 USNM 394889 Yes

CUR 8266* 16.5 USNM 394892 Yes

C. personatus BZE 4014* —No voucher No

BZE 4079* 19 No voucher Yes

BZE 4307* 24 USNM 394756 Yes

BZE 4308* 21 USNM 394757 Yes

BZE 4309* 18 USNM 394758 Yes

 BZE 5067* 19 USNM 394913 Yes

BZE 7163* 15 USNM 394742 Yes

CUR 8045* 19.5 USNM 394897 Yes

APPENDIX

07_Baldwin_111-138_Lang.indd 134 7_Baldwin_111-138_Lang.indd 134 9/24/09 9:39/24/09 9:39
NUMBER 38 • 135

Species DNA Standard Specimen Photo voucher

 length (mm) voucher a at NMNH

BAH 8263 23 USNM 394904 Yes

BAH 8264* 22 USNM 394905 Yes

PAN 7712-1* 22 AMNH 247346 No

PAN 7712-5* 22 AMNH 247346 No

C. tortugae BZE 4016* 28 No voucher Yes

BZE 4530* 40 USNM 394730 Yes

BZE 5237* 34 USNM 394743 Yes

BZE 5238* 30 USNM 394731 Yes

BZE 7106* 20 USNM 394732 Yes

BZE 7107* 36 USNM 394733 Yes

BZE 7333* 25 USNM 394744 Yes

BZE 7677* 31 USNM 394801 Yes

BZE 7690 37 USNM 394878 Yes

BZE 7691* 29 USNM 394802 Yes

BZE 7692* 36 USNM 394879 Yes

BZE 7693* 20 USNM 394800 Yes

BZE 7708* 33 USNM 394877 Yes

BZE 7709* 29 USNM 394798 Yes

BZE 7734* 26 USNM 394799 Yes

BZE (no DNA) 40 USNM 329834 No

BZE (no DNA) 33 USNM 334838 No

CUR CG25* — No voucher No

CUR CG26* —No voucher No

PAN 7725-6* 36 AMNH 247347 No

VEN (no DNA) 45 USNM 194103 No

VEN 7736-1* 33 AMNH 247340 No

VEN 7736-4* 37 AMNH 247340 No

VEN 7736-6* 46 AMNH 247340 No

Bermuda (no DNA) 9 (15– 31) USNM 330023 No

FLA (no DNA, photo —SU 08363 No

 of holotype)

C. glaucofraenum BZE 6037* 35 USNM 394347 Yes

BZE 6367* 44 USNM 393907 Yes

BZE 7343* 6 No voucher Yes

BZE 7351* 35 USNM 394353 Yes

BZE 7352* 25 USNM 394354 Yes

BZE 7353* 17.5 USNM 394355 Yes

BZE 7733* 25 USNM 394748 Yes

BZE 7768* 22 USNM 394792 Yes

BZE 7769* 17 USNM 394793 Yes

BZE 7796* 8.5 No voucher Yes

BZE 7798* 8.5 No voucher Yes

FLA 7341 49 USNM 394348 Yes

FLA 7342 42 USNM 394349 Yes

FLA 7343* 35 USNM 394350 Yes

FLA 7344 36 USNM 394351 Yes

FLA 7345 30 USNM 394352 Yes

FLA 7674 49 USNM 394356 Yes

FLA 7675 44 USNM 394357 Yes

FLA 7676 38 USNM 394358 Yes

 FLA 7677 32 USNM 394729 Yes

 PAN 7701-1* 39 AMNH 247334 No

 PAN 7701-2* 40.5 AMNH 247334 No

 PAN 7701-3* 32 AMNH 247334 No

 PAN 7701-4* 26.5 AMNH 247334 No

 PAN 7701-5* 33 AMNH 247334 No

 PAN 7712-2* 35 AMNH 247335 No

continued

07_Baldwin_111-138_Lang.indd 135 7_Baldwin_111-138_Lang.indd 135 9/24/09 9:39/24/09 9:39
136 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

TABLE A.1. continued

Species DNA Standard Specimen Photo voucher

 length (mm) voucher a at NMNH

 VEN 7729-1* 31 AMNH 247336 No

 VEN 7729-2* 30 AMNH 247336 No

 VEN 7729-3* 31 AMNH 247336 No

 VEN 7736-2* 37.5 AMNH 247337 No

 VEN 7738-1* 38 AMNH 247338 No

 VEN 7738-2* 36 AMNH 247338 No

 VEN 7738-3* 39 AMNH 247338 No

 VEN 7744-2* 32 AMNH 247339 No

 VEN 7744-3* 27 AMNH 247339 No

 VEN 7744-4* 28.5 AMNH 247339 No

 Bahamas (no DNA) 31 USNM 386863 No

 Bahamas (no DNA) 2 (30– 32) USNM 386955 No

 Bermuda (no DNA) 4 (27– 35) USNM 178908 No

 Bermuda (no DNA) 2 (45– 46) USNM 178555 No

C. venezuelae BZE 5099* 16 USNM 394735 Yes

 BZE 5319* 8.5 No voucher Yes

 BZE 7248* 35 USNM 394736 Yes

 BZE 7362* 7.5 No voucher Yes

 BZE 7704* 20 USNM 394880 Yes

 BZE 7728* 17 USNM 394881 Yes

 BZE 7797* 8.5 No voucher Yes

 CUR 8052* 30.5 USNM 394737 Yes

 CUR 8053* 30 USNM 394764 Yes

 CUR 8054* 26.5 USNM 39475 Yes

 CUR 8055 28 USNM 394766 Yes

 CUR 8208* 31.5 USNM 394738 Yes

 CUR 8259* 29 USNM 394739 Yes

 CUR 8260* 29 USNM 394740 Yes

 CUR 8427* 35 USNM 394741 Yes

 BAH 8048* 43 USNM 394908 Yes

 BAH 8049* 42 USNM 394906 Yes

BAH 8262* 39 USNM 394909 Yes

PAN 7725-1* 42.5 AMNH 247341 No

PAN 7725-2* 38 AMNH 247341 No

PAN 7725-3* 33 AMNH 247341 No

PAN 7725-4* 39 AMNH 247341 No

PAN 7725-5* 42.5 AMNH 247341 No

VEN 6670-3* 41 AMNH 247342 No

VEN 6670-4* 45 AMNH 247342 No

VEN 7733-1* 29 AMNH 247343 No

VEN JV07* 20 AMNH 247344 No

VEN JV08* 29.5 AMNH 247344 No

VEN JV09* 36 AMNH 247345 No

VEN JV10* 29 AMNH 247345 No

VEN JV11* 29 AMNH 247345 No

VEN JV12* 52 AMNH 247345 No

VEN JV13* 50 AMNH 247345 No

VEN JV14* 50 AMNH 247345 No

VEN JV15* 50 AMNH 247345 No

VEN JV16* 29 AMNH 247345 No

VEN (no DNA; photo ~42 MOBR-P-0867 No

 of paratype)

Puerto Rico; holotype 26.8 SIO 0869 No

 of C. bol* (DNA 

 from Victor, 2008)

Saba (no DNA) 15 USNM 387726 No

07_Baldwin_111-138_Lang.indd 136 7_Baldwin_111-138_Lang.indd 136 9/24/09 9:39/24/09 9:39
NUMBER 38 • 137

Species DNA Standard Specimen Photo voucher

 length (mm) voucher a at NMNH

Brazil 4 (2– 39) USNM 357709 No

C. dicrus BZE 4213* 22 USNM 394337 Yes

 BZE 5239* 27 USNM 394763 Yes

 BZE 6274* 25 USNM 394774 Yes

 BZE 6110* 13 USNM 394779 Yes

 BZE 7238 29 USNM 294338 Yes

 BZE 7266 24 USNM 294339 Yes

 BZE 7354* 22 USNM 394745 Yes

 BZE 7410 27 USNM 394746 Yes

 BZE 7700* 19 USNM 394778 Yes

 BZE 7701* 17 USNM 394776 Yes

 BZE 7707* 21 USNM 394777 Yes

 BZE 7745* 23 USNM 394780 Yes

 BZE 7818* 22 USNM 394775 Yes

 FLA 7346* 43 USNM 394343 Yes

 FLA 7347* 41 USNM 394344 Yes

 FLA 7348* 38 USNM 394345 Yes

 FLA 7680 39 USNM 394340 Yes

 FLA 7681 42 USNM 394341 Yes

 FLA 7682 44 USNM 394342 Yes

 CUR 8135* 30 USNM 394747 Yes

 BAH 8134* 43 USNM 394900 Yes

 BAH 8135* 38 USNM 394898 Yes

 BAH 8232 36 USNM 394899 Yes

 VEN 7736-3* 35 AMNH 247332 No

 VEN JV01* 33 AMNH 247333 No

 VEN JV02* 35 AMNH 247333 No

 VEN JV03* 36 AMNH 247333 No

 VEN JV04* 20.5 AMNH 247333 No

 VEN JV05* 21 AMNH 247333 No

 VEN JV06* 20 AMNH 247333 No

 Saba (no DNA) 4 (25– 28) USNM 388525 No

 Tobago (no DNA) 35 USNM 318808 No

 Tobago (no DNA) 3 (23– 25) USNM 318818 No

 Dominica (no DNA) 11 (13– 27) USNM 325165 No

C. thrix BZE 6111* 15 USNM 394797 Yes

 BZE 7265* 10 USNM 394734 Yes

 BZE 7267* 30 USNM 394759 Yes

 BZE 7816* 23 USNM 394914 Yes

 BZE 7817* 22 USNM 394915 Yes

 BZE (no DNA) 3 (20– 28.5) USNM 328240 No

 CUR 8261* 16 USNM 394760 Yes

 CUR 8426* 23 USNM 394761 Yes

 Venezuela (no DNA) 26 AMNH 244983 No

 Navassa (no DNA) 31 USNM 359403 No

 Tobago (no DNA) 32 USNM 318811 No

 Tobago (no DNA) 2 (23– 24) USNM 317133 No

C. eidolon BZE 4017* 31 USNM 394749 Yes

 BZE 4080* 20 USNM Yes

 BZE 4081* 29 No voucher No

 BZE 4089* –No voucher No

 BZE 5070* 33 USNM 394750 Yes

 BZE 5099 16 No voucher Yes

 BZE 6223* 18 USNM 394788 Yes

 BZE 6224* 24 USNM 394789 Yes

 BZE 6246* 25 USNM 394787 Yes

 BZE 6268* 23.5 USNM 394790 Yes

 BZE 6302* 33 USNM 394751 Yes

continued

07_Baldwin_111-138_Lang.indd 137 7_Baldwin_111-138_Lang.indd 137 9/24/09 9:39/24/09 9:39
138 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

TABLE A.1. continued

Species DNA Standard Specimen Photo voucher

 length (mm) voucher a at NMNH

 BZE 7108 21 USNM 394785 Yes

 BZE 7109* 34 USNM 394752 Yes

 BZE 7152 19 USNM 394346 Yes

 BZE 7232* 31 USNM 394762 Yes

 BZE 7350* 36 USNM 394753 Yes

 BZE 7671* 28 USNM 394786 Yes

 BZE 7672 24 USNM 394784 Yes

 BZE 7673* 22 USNM 394781 Yes

 BZE 7702 31 USNM 394783 Yes

 BZE 7703* 26 USNM 394782 Yes

 BZE 7726 24 USNM 394912 Yes

 BZE 7727 17 USNM 394911 Yes

 BZE 7735 23 USNM 394791 Yes

 CUR 8047 37 USNM 394886 Yes

 CUR 8048* 39 USNM 394884 Yes

 CUR 8049 33 USNM 394883 Yes

 CUR 8050* 38 USNM 394885 Yes

 CUR 8262* 24 USNM 394887 Yes

 CUR 8263 33 USNM 394888 Yes

 BAH 8046* 41 USNM 394903 Yes

 BAH 8047* 37 USNM 394902 Yes

 Navassa (no DNA) 3 (32– 33) USNM 360458 No

C. alloides BZE 7233* 24 USNM 394754 Yes

 BZE 7264* 19 USNM 394755 Yes

 BZE 7761* 12 USNM 394910 Yes

 BZE (no DNA) 21 USNM 267843 No

 CUR 8325* 18 USNM 394882 Yes

C. kuna BZE 4586* 6 No voucher No

 BZE 5134* 7.5 No voucher Yes

 BZE 6049* 7 No voucher Yes

 BZE 6387* 7.5 No voucher Yes

 PAN; holotype* DNA 17.1 SIO-07-5 No

 from GenBank

C. punctipectophorus FLA; paratype 28 USNM 179307 No

 (no DNA)

 South Carolina 28 USNM 315530 No

 (no DNA)

a USNM  U.S. National Museum (National Museum of Natural History), Smithsonian Institution; AMNH  American Museum of Natural History; MOBR  Museo 

Oceanológico Hermano Benigno Román, Venezuela; SIO  Scripps Institution of Oceanography.

07_Baldwin_111-138_Lang.indd 138 7_Baldwin_111-138_Lang.indd 138 9/24/09 9:39/24/09 9:39
Recent Insights into Cnidarian Phylogeny

Allen G. Collins

ABSTRACT. With representatives of more than 10,000 species from diverse clades scattered throughout the world’s oceans, Cnidaria is a moderately diverse phylum of Metazoa. As such, various taxa within Cnidaria have been the subjects of recent phylogenetic 

analyses. Because of its diversity, it has not yet been possible to conduct any extensive 

phylum-level phylogenetic analyses. In addition, new information suggests that the large 

group of parasites known as Myxozoa is part of Cnidaria. The present contribution summarizes recent fi ndings to create a picture of a current working hypothesis of cnidarian 

phylogeny. This summary, which treats the relationships among taxa down to the approximate level of order, likely provides a suboptimal estimation of cnidarian phylogeny 

as compared to a detailed phylogenetic analysis of data sampled densely from all the 

Cnidaria component clades. Nevertheless, it should provide points of comparison for 

upcoming efforts to more comprehensively assess cnidarian phylogeny. Even at the basic 

level of order, many taxa are thought to be polyphyletic. Understandably, current classifi cations are not fully refl ective of recent phylogenetic advances.

INTRODUCTION

Early in the history of Metazoa, the nematocyst evolved. This capsular organelle encloses venom and a tightly coiled, hollow, dart-like thread that is discharged at incredibly rapid accelerations of up to 5 million g (Nüchter et al., 

2006). This explosive discharge can be achieved because of extreme osmotic 

pressures (Holstein and Tardent, 1984; Weber, 1989) within the highly stable 

nematocyst wall, the molecular structure and function of which are becoming ever clearer (e.g., Meier et al., 2007). Cnida is the more general term for 

this organelle, the nematocyst being just one type. However, it is reasonably 

clear, based on the distribution across cnidarian taxa, that the ancestral form 

of the cnida was as a nematocyst (Marques and Collins, 2004). The lineage in 

which the nematocyst originated gave rise to the moderately diverse phylum 

Cnidaria, most likely during the Ediacaran period (Peterson and Butterfi eld, 

2005; Cartwright and Collins, 2007). Since this time, cnidarians have evolved 

an enormous variety of forms and a great diversity of life history strategies. 

Representative cnidarians build reefs, fi sh the depths, and parasitize other species. Extant valid species number a bit more than 11,000 (Daly et al., 2007), 

Allen G. Collins, National Marine Fisheries Service Systematics Laboratory, National Museum 

of Natural History, Smithsonian Institution, P.O. 

Box 37012, MRC-153, Washington, D.C. 20013-

7012, USA (collinsa@si.edu). Manuscript received 

29 August 2008; accepted 20 April 2009. 

08_CollinsA_139-150_Lang.indd 139 8_CollinsA_139-150_Lang.indd 139 9/24/09 9:35/24/09 9:35
140 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

or more than 13,000 when roughly 2,200 myxozoan species (Lom and Dyková, 2006) are included (see following), and can be found living in all marine environments. 

Many myxozoans infect freshwater taxa, but just a small 

number of other cnidarian species live in freshwater 

(Jankowski et al., 2008).

Daly et al. (2007), in honor of the 300th anniversary 

of the birth of Linnaeus, recently provided a summary 

of phylogenetic knowledge about currently recognized 

cnidarian taxa (exclusive of Myxozoa) typically ranked 

at ordinal and family levels in current classifi cations. I 

aim to provide a summary of recent insights into cnidarian phylogeny focusing on relationships among the different cnidarian orders. No phylum-level analyses of the 

evolutionary relationships among these taxa have been 

carried out, although attempts have been made to assess 

phylogenetic hypotheses for large subclades of Cnidaria; 

i.e., Anthozoa (Berntson et al., 1999; Won et al., 2001), 

Hexacorallia (Daly et al., 2003; Brugler and France, 

2007), Octocorallia (Bertnson et al., 2001; McFadden et 

al., 2006); Medusozoa (Collins, 2002; Marques and Collins, 2004; Collins et al., 2006a; Van Iten et al., 2006), 

and Myxozoa (Kent et al., 2001; Fiala, 2006). In addition, several recent studies have assessed the phylogenetic 

affi nities of taxa that have been problematic (Collins et 

al., 2006b; Van Iten et al., 2006; Dyková et al., 2007; 

Jiménez-Guri et al., 2007). The approach taken here is 

to cobble together results from these various analyses to 

provide a reasonable picture of our present understanding of cnidarian relationships (Figure 1). Representative 

cnidarians are illustrated in Figures 2 and 3.

As it concentrates on recent insights, the present paper does not provide a thorough review of the history 

of ideas about relationships among cnidarian orders, nor 

does it attempt to summarize what recent phylogenetic 

results tell us about cnidarian character evolution. For 

that type of information, one should consult the studies 

referenced herein. The working hypothesis of cnidarian 

relationships (see Figure 1), as well as the summary provided by Daly et al. (2007), should provide points of comparison for phylum-wide analyses of cnidarian phylogeny, 

which will soon be attempted by researchers engaged in 

the cnidarian tree of life project (http://CnidToL.com). 

Because it is a representation of a hypothetical history 

of Cnidaria, every node in Figure 1 is uncertain and is 

subject to change in light of new information. In a couple 

of instances, question marks are inserted on the working 

hypothesis to indicate relationships that are particularly 

tentative at present.

A WORKING HYPOTHESIS 

OF CNIDARIAN PHYLOGENY

Cnidaria is one of the earliest diverging clades within 

Metazoa, and surprisingly its precise position within the 

early diverging animal lineages— Porifera, Placozoa, Bilateria, Ctenophora, and Cnidaria— has remained elusive 

(Collins et al., 2005b; Dunn et al., 2008). That said, it 

has become ever clearer that Cnidaria is more closely related to Bilateria than is Ctenophora, a fi nding based on 

a synthetic consideration of morphology (Salvini-Plawen, 

1978), later supported by 18S rDNA data (Wainright et al., 

1993; Collins, 1998), and most recently confi rmed by a 

large analysis of many sequences of data from expressed 

gene transcripts (derived from large-scale sequencing of 

messenger RNA; known as expressed sequence tags, or 

ESTs) (Dunn et al., 2008; although note that the analyses published therein suggest that Ctenophora is the earliest diverging extant metazoan lineage, which is either 

a radical new fi nding or an indication of bias in the results). Ribosomal data, both 18S (e.g., Collins, 1998) 

and combined 18S and 28S (Medina et al., 2001; Cartwright and Collins, 2007), strongly suggest that Cnidaria 

forms a clade with Bilateria and the little-known phylum 

Placozoa, and that Cnidaria may be the sister group of 

either taxon or both together. More recently, phylogenetic 

analyses using entire genomes (unfortunately without any 

representatives of Ctenophora) found Placozoa to be the 

sister group of a clade composed of Cnidaria plus Bilateria (Srivastava et al., 2008).

Myxozoa is an interesting group of parasites that very 

well may be part of Cnidaria. Although some early workers suggested that they are cnidarians, based on the similarity between nematocysts and myxozoan polar capsules 

(Weill, 1938), they were mainly considered as protists 

throughout the twentieth century. In 1995, an analysis of 

18S and morphological data suggesting that myxozoans 

were derived from within Cnidaria was published (Siddall 

et al., 1995). However, this conclusion was doubted by 

many because the 18S gene of myxozoans appears to have 

evolved very quickly relative to that of most other metazoans, and different analyses involving different sets of taxa 

came to confl icting conclusions about the precise position 

of Myxozoa within Metazoa (Smothers et al., 1994; Siddall et al., 1995; Hanelt et al., 1996; Siddall and Whiting, 

1999; Kim et al., 1999; Zrzavý and Hypsa, 2003). This 

uncertainty was claimed to have been resolved when it 

was discovered that an unusual worm-shaped animal 

known as Buddenbrockia was a myxozoan (Okamura 

08_CollinsA_139-150_Lang.indd 140 8_CollinsA_139-150_Lang.indd 140 9/24/09 9:35/24/09 9:35
FIGURE 1. Working hypothesis of evolutionary relationships among extant cnidarian taxa usually classifi ed at or near the rank of order. 

NUMBER 38 • 141

08_CollinsA_139-150_Lang.indd 141 8_CollinsA_139-150_Lang.indd 1419/24/09 9:35/24/09 9:35
142 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 2. Representative cnidarians: Anthozoa, Staurozoa, and Polypodiozoa. A, Octocorallia, Holaxonia, Plaxaura from St. John, U.S. 

Virgin Islands; B, Octocorallia, Alcyonacea (part of the unnamed clade including Holaxonia), Dendronephthya from Shirahama, Japan; C, 

Octocorallia, Alcyonacea, Briareum from St. John, U.S. Virgin Islands; D, Hexacorallia, Scleractinia, Acropora from St. John, U.S. Virgin 

Islands; E, Hexacorallia, Actiniaria, Thalassianthus from Shirahama, Japan; F, Hexacorallia, Zoanthidea, Palythoa from St. John, U.S. Virgin Islands; G, Staurozoa, Eleutherocarpida, Haliclystus from Hokkaido, Japan; H, Staurozoa, Cleistocarpida, Manania from Hokkaido, 

Japan. I, Polypodiozoa, Polypodium (photographed by N. Evans).

et al., 2002; Okamura and Canning, 2003). Okamura and 

colleagues showed that the morphology and DNA of Buddenbrockia fi rmly placed it within Myxozoa. However, 

they also argued that the presence of four muscles located 

between the endoderm and ectoderm of Buddenbrockia

indicated that it, and by extension Myxozoa as a whole, 

was a close relative of nematodes and fi rmly derived from 

within Bilateria. Most recently, this hypothesis was falsifi ed by analyses of EST data taken from Buddenbrockia

and other metazoans indicating that Myxozoa is part of 

Cnidaria (Jiménez-Guri et al., 2007), as suggested by earlier workers (Weill, 1938; Siddall et al., 1995).

08_CollinsA_139-150_Lang.indd 142 8_CollinsA_139-150_Lang.indd 142 9/24/09 9:35/24/09 9:35
NUMBER 38 • 143

Myxozoa as the sister lineage of Medusozoa, as indicated by 

the EST results, but the branch also includes a question mark 

because of the small number of taxa included in the analysis 

by Jiménez-Guri et al. (2007). Knowing whether myxozoans 

possess linear or the typical circular mitochondrial genomes 

could help place Myxozoa within Cnidaria, as this is a major distinction between Anthozoa and Medusozoa (Bridge 

et al., 1992, 1995; see following).

The inclusion of Myxozoa’s 2,200 species (Lom and 

Dyková, 2006) within Cnidaria increases the richness of 

Not surprisingly, given the type of data analyzed, taxon 

sampling for the EST analysis was rather limited, with just 

two anthozoans, two hydrozoans, and one scyphozoan 

included. The myxozoan was shown to fall as the earliest 

diverging lineage in a clade including the two hydrozoans 

and the scyphozoan (Jiménez-Guri et al., 2007). In contrast, 

even more recent analyses of rDNA data with excellent 

taxon sampling resulted in best trees in which Myxozoa was 

the sister group of Bilateria, a result thought to be biased by 

long-branch attraction (Evans et al., 2008). Figure 1 shows 

FIGURE 3. Representative cnidarians: Hydrozoa, Cubozoa, Scyphozoa, and Myxozoa. A, Hydroidolina, Leptothecata, Lytocarpia from Shirahama, Japan; B, Hydroidolina, other Capitata, Cladonema from Hokkaido, Japan; C, Trachylina, Actinulida, Halammohydra from Bocas 

del Toro, Panama (still taken from video by J. Norenburg); D, Trachylina, Limnomedusae, Gonionemus from Hokkaido, Japan; E, Cubozoa, 

Carybdeida, Carybdea from Bocas del Toro, Panama; F, Cubozoa, Chirodropida, Chironex from Southern Japan (photographed in Enoshima 

Aquarium); G, Scyphozoa, Semaeostomeae, Chrysaora from Bocas del Toro, Panama; H, Scyphozoa, Rhizostomeae, Cassiopea from St. John, 

U.S. Virgin Islands; I, Myxozoa, Myxosporea, Bivalvulida, actinospore stage of Myxobolus (photographed by A. Nawrocki and N. Evans).

08_CollinsA_139-150_Lang.indd 143 8_CollinsA_139-150_Lang.indd 143 9/24/09 9:35/24/09 9:35
144 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

the phylum signifi cantly. As parasites with complex life 

cycles involving multiple hosts, the diversity of Cnidaria 

is substantially enriched as well. In recent years, relationships within Myxozoa have mainly been addressed using 

18S rDNA data. These data give a strong signal that species parasitic of freshwater bryozoans in the class Malacosporea (order Malacovalvulida) form a small clade (just 

three species are known) that is sister to the remaining 

myxozoans classifi ed in the class Myxosporea (Canning 

et al., 2000; Kent et al., 2001). Recent classifi cations of 

Myxosporea break the class into two orders, Bivalvulida 

and Multivalvulida. While neither taxon as traditionally 

recognized is monophyletic, including one aberrant bivalvulidid member in Multivalvulida renders Bivalvulida 

paraphyletic and Multivalvulida monophyletic (as shown 

in Figure 1; Kent et al., 2001; Whipps et al., 2004; Fiala, 

2006; Lom and Dyková, 2006). The great majority of 

myxosporeans appear to fall into two large clades, one 

dominated by species inhabiting freshwater hosts, and 

the other including Multivalvulida and other species that 

primarily infect marine hosts (Kent et al., 2001; Holzer et 

al., 2004). Examples of reversals in freshwater and marine 

habits continue to accumulate, and a third smaller clade 

has been identifi ed (Fiala, 2006). Considerable diversity of 

Myxozoa remains to be sampled, but existing studies indicate that many myxozoan taxa, even genera, are polyphyletic. Continued efforts to identify morphological features 

refl ecting shared ancestry, which could be used to improve 

the existing classifi cation, are necessary (Fiala, 2006).

In analyses of Cnidaria (exclusive of Myxozoa), it has 

generally become accepted that Anthozoa is the sister clade 

of Medusozoa, a hypothesis that is buttressed by morphology (Salvini-Plawen, 1978; Bridge et al., 1995), mitochondrial genome structure (Bridge et al., 1992), and rDNA 

sequences (e.g., Berntson et al., 1999; Kim et al., 1999; 

Medina et al., 2001; Won et al., 2001; Collins, 2002). One 

recent exception is a study by Kayal and Lavrov (2008) 

based on complete mitochondrial genome sequences, which 

found Medusozoa (just two representatives) derived from 

within Anthozoa as the sister group of three sampled representatives of Octocorallia. Although certainly worthy of 

consideration and future testing, limitations in taxon sampling in the Kayal and Lavrov (2008) analysis cast some 

doubt on the veracity of this fi nding. Similar arrangements 

were also presented in early rDNA analyses that similarly 

suffered from poor taxon sampling, as shown by pioneering work of Bridge et al. (1995). As indicated in Figure 1, 

Anthozoa is hypothesized to consist of two well-supported 

sister clades with diverse representatives, Octocorallia and 

Hexacorallia. Anthozoa is usually considered to be a class 

within the phylum (e.g., Daly et al., 2007), but making it 

a subphylum, with Hexacorallia and Octocorallia as its 

classes, would go some way toward balancing the classifi -

cation of Anthozoa with that of Medusozoa.

The phylogeny of Octocorallia has posed some of the 

most troublesome questions in recent cnidarian systematics because of a relatively dramatic incongruence between 

traditional taxonomy and molecular-based hypotheses of 

relationships (Berntson et al., 2001). Nevertheless, consistent progress has been made; many of the alliances fi rst 

suggested by the rDNA analyses of Berntson et al. (2001) 

have been confi rmed, and some morphological synapomorphies of recently recognized clades have been identifi ed 

(McFadden et al., 2006). It has been premature, given the 

great diversity of Octocorallia remaining to be sampled, to 

erect a new classifi cation for the group, but some patterns 

are emerging. There appear to be two major clades and a 

minor clade or grade that branched early in the history of 

Octocorallia (McFadden et al., 2006). One of the three 

octocoral orders, Alcyonacea (soft corals and sea fans), 

which is by far the most diverse and least distinctive, is 

clearly paraphyletic. The other two orders, Pennatulacea 

(sea pens) and Helioporacea (blue corals), are monophyletic, and each appears to be independently descended 

from a paraphyletic Calcoxonia (one group of sea fans), a 

suborder of Alcyonacea (McFadden et al., 2006). Another 

group of sea fans known as Holaxonia all appear in one of 

the major clades, along with other alcyonaceans, but there 

is no strong evidence for holaxonian monophyly.

In contrast to Octocorallia, the overall picture of the 

phylogeny of Hexacorallia has been relatively clear. Of the 

six hexacorallian orders, several lines of evidence indicate 

that Ceriantharia (tube anemones) is the earliest diverging 

lineage (Berntson et al., 2001; Won et al., 2001; Daly et 

al., 2002, 2003; Brugler and France, 2007). Similarly, this 

same set of studies all concur in fi nding a close relationship 

between Scleractinia (stony corals) and Corallimorpharia. 

However, there has been some confusion about whether 

Corallimorpharia might be derived from within Scleractinia, that is, one version of the “naked coral hypothesis,” which posits that one or more hexacorallian groups 

without skeletons are derived from stony coral ancestors. 

Abundant evidence refutes the idea that Actiniaria (true 

anemones) or Zonanthidea are derived from scleractinian 

ancestors (Berntson et al., 2001; Won et al., 2001; Daly 

et al., 2002, 2003; Brugler and France, 2007), but several 

analyses of mitochondrial genes, including whole mitochondrial genomes, have found corallimorpharians to be 

derived from within Scleractinia (France et al., 1996; Romano and Cairns, 2000; Medina et al., 2006). In contrast, 

08_CollinsA_139-150_Lang.indd 144 8_CollinsA_139-150_Lang.indd 144 9/24/09 9:35/24/09 9:35
NUMBER 38 • 145

however, better taxon sampling of mitochondrial genomes 

(Brugler and France, 2007) and analyses of other genes 

with better taxon sampling (Fukami et al., 2008) favor 

the hypothesis that Corallimorpharia and Scleractinia are 

monophyletic sister groups. No clear picture of the relationships between this clade, Actiniaria, Antipatharia 

(black corals), and Zoanthidea has emerged from recent 

work, as different data sets or analytical approaches 

have yielded confl icting results (Berntson et al., 2001; 

Won et al., 2001; Daly et al., 2002, 2003; Brugler and 

France, 2007).

In present classifi cations, Medusozoa is usually presented as including four classes: Cubozoa, Hydrozoa, 

Scyphozoa, and Staurozoa. As mentioned earlier, a recent 

analysis of EST data suggested that Myxozoa is derived 

from within Cnidaria, as the sister group of the three medusozoans included in the analysis (Jiménez-Guri et al., 

2007). Another taxon, Polypodiozoa, which is sometimes 

considered a class because of the unusual nature of the parasitic species within its single genus, Polypodium (Raikova, 

1988), has also recently been hypothesized to fall within 

Medusozoa, most likely as a close relative of Hydrozoa 

(Evans et al., 2008). Thus, Medusozoa may have as many 

as six classes representing rather distinct, evolutionarily 

independent lineages. Evidence for the monophyly of Medusozoa, albeit with the exclusion of Myxozoa and Polypodoizoa, comes from rDNA data (Collins, 1998, 2002; 

Medina et al., 2001; Collins et al., 2006a) and observations of morphology (Werner, 1973; Salvini-Plawen, 1978; 

Schuchert, 1993; Bridge et al., 1995).

Attempts to incorporate data from Myxozoa and 

Polypodiozoa in analyses of cnidarian phylogeny have 

been complicated by the relatively rapid rate of molecular 

evolution in these two taxa. In many analyses of rDNA, 

representatives of these two groups appear to be artifi -

cially attracted to bilaterian examplars and end up forming sister group relationships with Bilateria (Siddall et al., 

1995; Kim et al., 1999; Zrzavý and Hypsa, 2003). In a 

recent study of 18S and 28S data, dense taxon sampling 

of medusozoans appears to have overcome some of this 

long-branch attraction problem, at least so far as Polypodiozoa is concerned (Evans et al., 2008). Although the optimal trees of Evans et al. (2008) had Myxozoa branching 

as the sister group of Bilateria, perhaps because the 28S 

marker was only partially sampled for the myxozoans, 

Polypodiozoa consistently fell within Medusozoa, as one 

would expect based on its morphology (Raikova, 1980, 

1994). Unfortunately, however, the exact position of Polypodiozoa within Medusozoa was shown to be dependent 

upon method of analysis and the inclusion or exclusion of 

myxozoan representatives (Evans et al., 2008), prompting 

the question mark shown in Figure 1.

Among the taxa more traditionally considered as part 

of Medusozoa, Staurozoa (or Stauromedusae) may possibly be the earliest diverging lineage, a result obtained 

through the analysis of both molecular and morphological data (Collins, 2002; Dawson, 2004; Collins and Daly, 

2005; Collins et al., 2006a; Van Iten et al., 2006). As benthic, so-called stalked medusae, the fi nding that Staurozoa 

might branch early in the history of Medusozoa was of 

some interest because it very clearly implied that the pelagic medusa stage was a feature derived within this clade. 

However, Collins et al. (2006a) noted that some methodological choices in their phylogenetic analyses impacted 

the position of Staurozoa. Further, although not specifi -

cally addressed, the position of Staurozoa was not stable 

in the analyses of Evans et al. (2008). Thus far, no strong 

evidence has been published suggesting that Staurozoa 

is not an early diverging lineage of Medusozoa. Within 

Staurozoa, there are two main taxa, Cleistocarpida and 

Eleutherocarpida, neither of which appears to be monophyletic despite the fact that taxon sampling was relatively 

limited (Collins and Daly, 2005).

Another small class of Medusozoa is Cubozoa (box 

jellyfi shes). Although 18S data provide no clear signal 

about the precise position of Cubozoa within Cnidaria 

(Collins, 2002; Evans et al., 2008), 28S data strongly suggest that Cubozoa is the sister group of Scyphozoa (true 

jellyfi shes), together forming the clade Acraspeda (Collins et al., 2006a; Evans et al., 2008). Both 18S and 28S 

strongly support cubozoan monophyly, as well as that 

of its two main subtaxa, Carydeida and Chirodropida 

(Collins, 2002; Collins et al., 2006a). Similarly, there is 

relatively strong and stable evidence concerning the evolutionary relationships among the scyphozoan orders 

Coronatae, Rhizostomeae, and Semaeostomeae, although 

it should be noted that taxon sampling has been sparse. 

The earliest diverging lineage is Coronatae, and Rhizostomeae is a well-supported clade that is derived from within 

Semaeostomeae (Collins, 2002; Collins et al., 2006a).

The largest and most diverse class within Medusozoa 

is Hydrozoa. As indicated in Figure 1, an ancient divergence within Hydrozoa divides the group into two clades, 

Trachylina and Hydroidolina (Collins, 2002; Marques and 

Collins, 2004; Collins et al., 2006a). Each clade has been 

the subject of recent papers aimed at bringing increased 

taxon and genetic marker sampling to bear on the evolutionary relationships among their respective component 

groups (Cartwright et al., 2008; Collins et al., 2008). As 

Figure 1 shows, relationships among the major lineages of 

08_CollinsA_139-150_Lang.indd 145 8_CollinsA_139-150_Lang.indd 145 9/24/09 9:35/24/09 9:35
146 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Hydroidolina are uncertain (Collins et al., 2006a; Cartwright et al., 2008). In terms of taxonomy, the clade includes Leptothecata (thecate hydroids and leptomedusae) 

and Siphonophora (colonial siphonophores including the 

Portuguese man o’ war), two groups with ample evidence 

for monophyly (Collins, 2002; Collins et al., 2006a; Cartwright et al., 2008). Hydroidolina also includes the large and 

diverse taxon Anthoathecata (athecate hydroids and anthomedusae), which is typically subdivided into Capitata and 

Filifera. There is no evidence supporting the monophyly of 

Capitata, Filfera, or Anthoathecata (Collins, 2002; Collins et 

al., 2006a; Cartwright et al., 2008). Despite the diffi culty in 

working out the relationships among hydroidolinan clades, 

some advances have been made in identifying large clades 

that had not been previously recognized. For instance, Capitata appears to be composed of two well-supported clades, 

one dubbed Aplanulata (includes the well-known model 

organisms of Hydra) in reference to the group’s lack of a 

ciliated planula stage (Collins et al., 2005a, 2006a) and the 

other consisting of all the other capitate groups (Cartwright 

et al., 2008). The name Capitata has recently been applied 

to this more restrictive clade (Cartwright et al., 2008). Similarly, within Filifera, a previously unrecognized alliance of 

species that bear gonophores, but not on their hydranth 

bodies, has been given the name Gonoproxima. There is no 

support for the monophyly of the remaining fi liferans.

Trachylina is composed of four orders: Actinulida, 

Limnomedusae, Narcomedusae, and Trachymedusae. The 

monophyly of Narcomedusae seems to be relatively certain (Collins, 2002; Collins et al., 2006a, 2006b, 2008), 

whereas the monophyly of Actinulida has yet to be tested 

because just a single representative has been included in 

any phylogenetic analysis (Collins et al., 2008). Trachymedusae, a group of pelagic species that lack polyp stages, 

appears to be polyphyletic. One family (Geryonidae) has a 

close relationship with a subgroup of Limnomedusae (Collins et al., 2006a, 2008), whereas another (Rhopalonematidae) may have given rise to the interstitial Actinulida 

(Collins et al., 2008). Limnomedusae appears to represent 

a grade at the base of Trachylina (Collins, 2002; Collins et 

al., 2006a, 2006b, 2008). As with many cnidarian groups, 

the classifi cation of Trachylina requires refi nement to better refl ect our phylogenetic knowledge.

CONCLUSION AND CLASSIFICATION

The working hypothesis of cnidarian phylogeny 

presented here (see Figure 1), as do all others, requires 

continued testing and refi nement. Many of the studies 

behind it have limitations, especially in taxon sampling, 

and the original papers should be consulted for more 

detailed assessments of strengths and weaknesses of the 

analyses that they report. As the working hypothesis 

results from no single analysis and was instead put together from numerous sources, some of my biases, in 

the form of judgments, have had an impact on the fi nal 

form of the working hypothesis. This effect is certainly a 

weakness in such an exercise and demonstrates why it is 

less preferable than an analysis that relies on data sampled from diverse representatives across Cnidaria. When 

such an analysis is conducted, the working hypothesis 

presented here may provide a helpful reference point for 

comparison.

Figure 1 makes it clear that the current classifi cation of Cnidaria, even at the basic level of order, has 

not kept up with phylogenetic advances. A new classifi cation using taxa hypothesized to be monophyletic is 

not feasible until more thorough and robust phylogenetic analyses are conducted. Confl icting results from 

different phylogenetic studies create one hindrance to 

advances in classifi cation, but this is not really new, as 

different taxonomists have always offered different classifi cations to refl ect their changing perceptions of taxa. 

More detrimental to progress in classifi cation is the lack 

of completeness in existing phylogenetic analyses. With 

molecular data, individuals are sampled, and assessments of the phyletic status (monophyletic, paraphyletic, 

or polyphyletic) of larger taxa are not very strong until 

large numbers of component species are included in an 

analysis. Moreover, the relevant morphological features 

that distinguish any particular clade (especially if not 

corresponding to a traditional taxon) are not easily discerned without thorough sampling and examination of 

its members.

Nevertheless, classifi cations are made to enhance 

communication. Therefore, it may be prudent to attempt 

classifi cations that better refl ect ongoing advances in phylogenetics. Below I present one such attempt for Cnidaria. 

It is not meant to be adopted, as this author has little expertise in non-medusozoan cnidarians. Instead, it is presented to illustrate one possible system for classifying traditional taxa in light of ongoing phylogenetic advances. It 

relies on annotation indicating whether a given taxon is 

likely to be monophyletic, paraphyletic, or polyphyletic. 

Taxa for which reasonable evidence suggests monophyly 

are followed by a superscript M. Taxa thought to be paraphyletic are followed by superscript P and a list of taxa [in 

brackets] hypothesized to be derived from it. Taxa that are 

likely polyphyletic are placed in quotation marks. Finally, 

08_CollinsA_139-150_Lang.indd 146 8_CollinsA_139-150_Lang.indd 146 9/24/09 9:35/24/09 9:35
NUMBER 38 • 147

taxa whose phyletic status is essentially unknown are left 

with no annotation.

Phylum CnidariaM

 Subphylum AnthozoaM

 Class HexacoralliaM

 Order ActiniariaM

 Order AntipthariaM

 Order CerianthariaM

 Order CorallimorphariaM

 Order ScleractiniaM

 Order ZoanthidaM

 Class OctocoralliaM

 Oder “Alcyonacea”P [Calcoxonia, Helio-

 poracea, Holaxonia, Pennatulacea]

 Order CalcoxoniaP [Helioporacea, Pen-

 atulacea]

 Order HelioporaceaM

 Order Holaxonia

 Order PennatulaceaM

 Subphylum MedusozoaM

 Class CubozoaM

 Order CarybdeidaM

 Order ChirodropidaM

 Class HydrozoaM

 Subclass HydroidolinaM

 Order AplanulataM

 Order CapitataM (excluding Aplanulata)

 Order Filifera (excluding Gonoproxima)

 Order GonoproximaM

 Order LeptothecataM

 Order SiphonophoraM

 Subclass TrachylinaM

 Order Actinulida

 Order Limnomedusae (including Ger-

 yonidae)

 Order NarcomedusaeM

 Order TrachymedusaeP [Actinulida, Nar-

 comedusae]

 Class PolypodiozoaM

 Genus Polypodium

 Class ScyphozoaM

 Order CoronataeM

 Subclass DiscomedusaeM

 Order RhizostomeaeM

 Order SemaeostomeaeP [Rhizostomeae]

 Class StaurozoaM

 Order “Cleistocarpida”

 Order “Eleutherocarpida”

 Subphylum MyxozoaM

 Class MalacosporeaM

 Order MalacovalvulidaM

 Class MyxosporeaM

 Order BivalvulidaP, [Multivalvulida]

 Order MultivalvulidaM

ACKNOWLEDGMENTS

I thank Michael Lang for organizing the Smithsonian 

Marine Science Symposium and for inviting me to participate. I also thank the Smithsonian Institution Marine 

Science Network, which has supported me and other colleagues in collection activities from Smithsonian marine 

laboratories. Many of these specimens yielded critical data 

that were used in several of the papers referenced within 

this manuscript. Finally, thanks are owed to three reviewers, including Antonio Carlos Marques, whose comments 

improved an earlier version of the manuscript. This work 

was supported by “Assembling the Tree of Life” Grant no. 

0531779 from the National Science Foundation.

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Biodiversity and Abundance of Sponges 

in Caribbean Mangrove: Indicators 

of Environmental Quality

Maria Cristina Diaz and Klaus Rützler

ABSTRACT. We have long been fascinated by the lush biological diversity seen on subtidal substrates in Caribbean saltwater mangroves. Several groups of plants and sessile 

invertebrates fl ourish on the submerged prop roots of red mangrove (Rhizophora mangle), competing for space and tolerating a stressful range of ecological variables (temperature, salinity, nutrients, sedimentation) that is quite different from the more stable climate 

on nearby coral reefs. To test the limits of tolerance, we monitored populations of these 

organisms, the abundant sponges in particular, at environmentally and geographically 

dissimilar locations in Panama and Belize. We used relative abundance estimates and 

frequency counts of major ecologically functional groups and common sponge species to 

establish baselines, and we repeated our surveys over long time spans (months to years) 

to fi nd correlations between community and environmental changes. Both study locations demonstrated environmental quality decline during the time of observation, mainly 

through mangrove clear-cutting, followed by increase of suspended fi ne sediments from 

dredging reef sands and fi lling in intertidal land, and elevation of nutrient levels from 

terrestrial inputs. Although our methods are still in a stage of refi nement, our data are 

leading the way to responsible monitoring of our most precious coastal resources in the 

tropics. We fi nd that photosynthetic organisms (cyanobacteria, algae) and fi lter-feeding 

invertebrates (sponges, ascidians, bivalves, bryozoans) count among the “canaries in the 

coal mine” as effective indicators of environmental change.

INTRODUCTION

Red mangrove trees, Rhizophora mangle, grow along thousands of kilometers of Caribbean shorelines, protecting them from storm erosion and offering habitat to many organisms (Rützler and Feller, 1988, 1996; de Lacerda 

et al., 2002). Caribbean mangroves harbor from a handful to more than 100 

sponge species at any one particular site (Table 1). Available data indicate that 

sponges may make up 10% to 70% of epiphytic species diversity on submerged 

mangrove roots. The best studied mangrove sponge faunas are described from 

islands off southern Belize, with species richness reported between 50 and 147 

species (Rützler et al., 2000; Wulff, 2000; Diaz et al., 2004), followed by faunas 

from a few islands in the Bocas del Toro Archipelago, Panama, with 65 species (Diaz, 2005), from various mainland and island sites off Venezuela with 

62 species (Sutherland, 1980; Diaz et al. 1985; Orihuela et al., 1991; Pauls, 

Maria Cristina Diaz, Museo Marino de Margarita, 

Blvd. El Paseo, Boca del Río, Margarita, Edo. Nueva 

Esparta, Venezuela. Klaus Ruetzler, Department of 

Invertebrate Zoology, National Museum of Natural 

History, Smithsonian Institution, Washington, D.C. 

20560-0163, USA. Corresponding author: M. C. 

Diaz (taxochica@gmail.com). Manuscript received 

9 June 2008; accepted 20 April 2009.

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152 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

1998, 2003; Ramirez, 2002; Diaz et al., 2003; Pérez, 

2007), and various mangrove sites in Cuba, with 41 species (Alcolado, unpublished data). Other reports are from 

Colombia, with 26 species (Zea, 1987; S. Zea, National 

University of Colombia, personal communication, 2006); 

Jamaica, with 18 species (Hechtel, 1965; Lehnert and van 

Soest, 1998); and Trinidad and Guadalupe, with 6 species 

(Toffart, 1983) (clearly representing only a portion of the 

mangrove sponge diversity there).

Most of the mangrove systems in the Caribbean remain unexplored, leaving a large void in biodiversity information. Most studies just cited show that the more 

closely these communities are investigated, the more new 

species are being discovered. An example is the research 

by the Caribbean Coral Reef Ecosystems Program in Belize during the past 25 years (Rützler et al., 2000, 2004). 

In particular, specialists on certain sponge taxa discovered and described numerous species in the families 

Suberitidae (order Hadromerida) (Rützler and Smith, 

1993), Chalinidae (order Haplosclerida) (de Weerdt et 

al., 1991) and Mycalidae (order Poecilosclerida) (Hadju 

and Rützler, 1998). A recent revision of Caribbean Lissodendoryx allowed the reinterpretation of L. isodyctyalis (Carter, 1882) and seven other species, four of 

them new to science (Rützler et al., 2007). Similarly, two 

unique haplosclerids were found in Belizean and Panamanian mangroves: a thin, erect, and fragile undescribed 

species of Haliclona from Twin Cays, and Xestospongia 

bocatorensis, a thin crust occurring in Bocas del Toro 

mangroves and reefs. Both are in an endosymbiotic relationship with fi lamentous Cyanobacteria, a very unusual 

occurrence in this order of sponges (Diaz et al., 2007, 

Thacker at al., 2007).

Besides the importance of sponges species richness, 

they may be one of the most abundant animal groups 

in mangrove habitats. In Belize, for instance, on the leeward sides of islands, sponges cover 10% to 50% of the 

root surfaces, followed in importance by sea anemones, 

ascidians, and algae (Farnsworth and Ellison, 1996; Diaz 

et al., 2004). In the Caribbean, epibiont mangrove communities have been interpreted as highly heterogeneous 

(Rützler, 1969; Sutherland, 1980; Alcolado, 1985; Alvarez, 1989; Calder, 1991a; Bingham, 1992; Diaz et al., 

2004) as a result of low recruitment rates (Zea, 1993; 

Maldonado and Young, 1996), low and fragmented 

available space (Jackson and Buss, 1975; Sutherland, 

1980), and stochastic processes in the long term (Bingham and Young, 1995; Ellison et al., 1996). Abundance 

and distribution for sponges and algae in these communities have been related to environmental factors, such 

as light intensity, tides, wave impact, air exposure, and 

sedimentation (Rütz ler, 1995), and to biological factors, 

such as larval supply (Farnsworth and Ellison, 1996), 

root abundance, competition, and predation (Calder, 

1991b; Littler et al., 1985; Taylor et al., 1986; Ellison 

and Farnsworth, 1992; Rützler, 1995; Rützler et al., 

2000; Wulff, 2000). Algae abound on the shallow, welllit parts of stilt roots, and their abundance and species 

composition are highly susceptible to the presence of 

grazers. Sponges are most abundant on the lower subtidal portions of the stilt roots and dominate peat bank 

walls and undercuts.

TABLE 1. Number of species of Porifera and other epifaunal taxa reported from Caribbean mangroves (n.a. no data available).

Country Locality Porifera Other taxa Author

Antilles Guadalupe, Trinidad, Puerto Rico 4–10 32–70 Toffart (1983)

Bahamas Bimini 13 n.a. Rützler (1969)

Belize Four cays 24 59 Farnsworth and Ellison (1996)

 Twin Cays 54 n.a. Rützler et al. (2000)

 Pelican Cays 147 217 See Macintyre and Rützler (2000)

Cuba n.a. 48 n.a. Alcolado (unpublished data)

Panama Bocas del Toro 60 n.a. Diaz (2005)

USA Indian River, Florida 3 25 Bingham and Young (1995)

Venezuela Buche Bay 16 32 Sutherland (1980)

 Morrocoy National Park 23 n.a. Diaz et al. (1985)

 Turiamo Bay 10 n.a. Pauls (2003)

 Cienaga Bay 26 n.a. Pauls (1998)

 La Restinga National Park 18 35 Orihuela et al. (1991)

 La Restinga National Park 40 n.a. Diaz et al. (2003)

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NUMBER 38 • 153

The major physical and biological processes are modulated by competitive abilities, such as growth rates and 

chemical defenses against predation (Wulff, 2000, 2004, 

2005; Engel and Pawlik, 2005). Short-term epibiont abundances are likely to be determined by interspecifi c competitive interactions and predation, while long-term abundances are limited by seasonal environmental changes, 

such as freshwater inputs during periods of rain, strong 

tidal currents, waves, and stochastic processes that make 

these communities unstable (Bingham and Young, 1995; 

Ellison et al., 1996). Despite important generalizations 

about mangrove benthos ecology, we lack understanding 

of the temporal or spatial variation within most epibiont 

groups and knowledge about species occurrence, abundance, dominance, and interactions. For example, we do 

not know which species are generally abundant in these 

communities, how the hierarchy changes with the year’s 

seasons, and if there are predictable succession patterns. 

Our current lack of knowledge prevents us from discerning 

between natural variations, for instance, seasonal or yearly 

dynamics, and artifi cial disturbances caused by humans.

The present work pursues the overall goal of a better 

understanding of diversity, biogeography, and ecological dynamics and their causes among the sponges in Caribbean 

mangroves. It encompasses two major aspects: evaluation 

of our current knowledge of epiphytic sponge taxa and the 

contribution of new data on causes for species richness, distribution, abundance, and dynamics, particularly from the 

examples of mangrove in Panama and Belize. The survey 

carried out in Bocas del Toro (Panama) intends to follow 

short-term changes (over one year) in the epiphytic fauna of 

mangrove roots, whereas the study in Belize will clarify shifts 

in distribution of taxa over a longer period (four years).

METHODS

SPONGE SPECIES DISTRIBUTION IN CARIBBEAN MANGROVES

The distribution of species in Caribbean mangroves was 

determined from currently published data or unpublished 

data provided to the authors. Faunas from different regions 

were compared by using a cluster analysis with the Bray– 

Curtis dissimilarity coeffi cient, which is part of the Multivariate Statistical Package (MVSP 3.1) (van Soest, 1993).

SPONGE IDENTIFICATION

Specimens were identifi ed in situ or, when necessary, 

briefl y characterized and photographed, with a sample 

preserved in ethanol. In the laboratory, routine microscope 

preparations were made by cleaning spicules in household 

bleach and hand-cutting perpendicular and tangential sections, which were dehydrated and mounted in Permount 

and examined under the light microscope.

PHYSICOCHEMICAL VARIABLES

Temperature and salinity were measured at 0 and 50 

cm depth at the Belize sites (January and August 2004), 

and in Bocas del Toro (February, June, and September 

2004). Sedimentation rates were estimated from accumulations in buried sediment traps (plastic pipes, 10 

cm diameter, 50 cm length) left in place for 210 days in 

Belize and 150 days in Panama. The trapped sediment 

was oven-dried (50°C), and its composition was determined as percentage of mud (including the very fi ne clay 

fraction) (0.002– 0.05 mm) and sand (0.05– 2 mm). 

Approximate values of calcium carbonate content were 

determined from weight loss after exposure to changes 

of dilute hydrochloric acid, and sediment deposition 

rates were calculated (g/m2/day). Seawater samples (500 

mL each) were taken in Belize (September 2003) and at 

Bocas del Toro (September 2004) at low and high tide, 

fi ltered (0.2 m, GF/F fi lter) and frozen for nutrient 

analysis (Astor, 1996). Nutrient values were determined 

by spectrophotometric technique using the procedure 

described earlier (Diaz and Ward, 1997). Qualitative 

observations about habitat types surrounding the mangrove fringe were recorded, as well as an estimate of the 

level of human disturbance.

SURVEY SITES, BOCAS DEL TORO, PANAMA

Four sites within a perimeter of 10 km were selected 

and surveyed during 2004 (Figures 1, 2): (1) STRI Point: 

location of the Smithsonian Tropical Research Institute’s 

laboratory, several mangrove stands close to reef patches 

in the southwest of Colon Island, and near a welldeveloped area with a housing complex that is part of 

the station; (2) Solarte In: a protected lagoon in the east 

of Solarte Island, site of a modest housing development; 

(3) Solarte Out: a pristine mangrove island close to reef 

patches to the west side of Solarte Island; and (4) Big 

Bight: a pristine, mangrove-lined lagoon surrounded by a 

well-developed terrestrial forest on Colon Island, less than 

5 km northwest of STRI Point. General physicochemical 

characterization and geographic location of the sites are 

presented in Table 2 and the nutrient regime in Table 3. 

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154 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Mangrove prop roots (25 per site) were haphazardly selected within a 30 m length of the mangrove fringe. The 

front side (facing the channel) of each selected root was 

photographed along its entire length and set to scale by 

tying a transparent measuring tape to the high-tide water 

mark. The tape was prevented from fl oating by attaching 

a metal weight to its lower end. Three to seven photographs were taken, depending on the root length. Roots 

were rephotographed four times during the year (February 2004, June 2004, September 2004, and February 

2005). From these images, abundance values of epifauna 

were estimated by measuring the projected area of each 

species using the CPCe program. The area (cm2) covered 

by each taxon was divided by the root length (m), so that 

the relative abundance values are related to a measure 

of available substrate. Cover of each taxon is reported 

as the sum of its abundances (cm2/m root) on all roots 

at a particular site. Eight categories of epiphytes were 

distinguished: cyanobacterial mats (monospecifi c stands 

of cyanobacteria), green algae, red algae (including both 

crustose calcareous and fl eshy species), turf (mixture of 

densely packed red, green, and cyanobacterial fi laments), 

sponges, hydroids, bivalves, and ascidians; the ninth category was “empty” (spaces not occupied by macrofauna 

or macroalgae). When small organisms were found overgrowing a large one (such as Spongia tubulifera, Hyrtios 

proteus) the projected area of both species was included. 

The number of roots fi nally analyzed per studied site was 

reduced to 14– 22 because there was some accidental loss 

of photographic data.

SURVEY SITES, TWIN CAYS AND PELICAN CAYS, BELIZE

Three sites at Twin Cays and one in the Pelican Cays 

were surveyed in August 2003 and four years later in August 2007 (Figures 3, 4; see Tables 2, 3). Two of the Twin 

Cays sites, the Lair Channel and Hidden Creek, are deep 

creeks that branch off the Main Channel; Sponge Haven 

FIGURE 1. Map of research area at Bocas del Toro, Panama (STRI Smithsonian Tropical Research 

Institute).

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NUMBER 38 • 155

is a bay in the southwest of the Main Channel. The Pelican Cays site was in the northern part of the lagoon of 

Manatee Cay. Transects (30 m long) were placed along 

the red mangrove fringe at each site, with number of roots 

ranging between 52 and 143. In all, the presence of the 

six most conspicuous epiphyte categories was recorded 

on each root within each transect: cyanobacterial mats, 

macroalgae, sponges, sea anemones (Aiptasia pallida), bivalves, and ascidians.

RESULTS

CARIBBEAN MANGROVE SPONGE SPECIES

RICHNESS AND DISTRIBUTION

The distribution of 177 sponge species currently reported from Caribbean mangroves is presented in Table 4. 

A cluster analysis (Figure 5) of the best studied sites (Belize, 

Cuba, Panama, Venezuela) shows the highest similarity 

between Venezuela (62 species) and Panama (65 species). 

FIGURE 2. Views of research locations at Bocas del Toro, Panama. Top row from left: STRI Point looking south, where the transect was 

located in the right foreground; Solarte Island, with transect location Solarte In near the center. Bottom row from left: mangrove fringe at 

Solarte In; underwater view of mangrove prop roots showing a specimen of sponge, Chalinula molitba; mangrove roots covered by the encrusting sponge Halisarca sp. (undescribed; note scale in centimeters [cm] to the left), along with bivalves, algae, bryozoans, ascidians, and 

other fouling invertebrates.

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156 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

These faunas were paired with Twin Cays (54 species) and 

Cuba (48 species). The most dissimilar fauna in the analyses resulted from comparison with the Pelican Cays mangroves (147 species).

MANGROVE SURVEYS AT BOCAS DEL TORO, PANAMA

Changes in Abundance of Major Epifaunal Taxa

The relative abundance of major taxa at each of the 

four localities studied between February 2004 and February 2005 is shown in Figure 6. In terms of the hierarchy of major taxa, sponges were fi rst or second in abundance on mangrove roots at all sites, followed by algal 

turfs. An exception to this pattern was found in Solarte 

In (see Figure 1), where large mats of green algae, mostly 

Caulerpa verticillata and Halimeda spp., dominated over 

the sponges in February 2004 and 2005. Bivalves were the 

third most abundant group, followed closely by unoccupied (empty) spaces.

The abundance of the two most dominant groups, 

sponges and algae/cyanobacteria, showed a considerable 

decrease at STRI Point and Solarte In by the end of the 

TABLE 2. Characterization of study sites in Panama and Belize.

Sedimentation

Country and Habitat a Human Temperature Salinity CaCO3 Rate 

locality (depth, m) impact b range (°C) range (ppm) Type (% dry wt) (g/m2/day) Turbidity b Coordinates

Panama

 STRI Point PR  26– 29 29– 34 Mud 14– 23 34– 41 / 09°2129.1N,

 (1.5– 2) 82°1628.9W

 Solarte In SG / 26– 29 27– 32 Sand 4– 24 28– 58  09°1705.0N,

 (2– 2.5) 82°1003.3W

 Solarte Out PR  27– 29 29– 33 Sand 80– 98 88– 248  09°1735.6N,

 (1) 82°1208.3W

 Big Bight SG / 27– 29 27– 34 Mud/ 25 40 / 09°2231.1N,

 (1.5– 2) sand 82°1738.3W

Belize

 Sponge Haven SG  26– 32 33– 35 Mud 48.75 25  16°4940.5N,

 (1– 1.8) 88°0616.5W

 Hidden Creek TC / 25.5– 33 32– 36 n.a. n.a. n.a.  16°4940.5N,

 (2– 2.5) 88°0616.5W

 Lair Channel TC  25.3– 33 32– 36 Mud 25.9 44  16°4933.7N,

 (1.5– 1.8) 88°0611.6W

 Manatee Lagoon PR/SG  c/ d 25.5– 32 35– 36 Mud 38.9 45  16°4003.3N,

 (1– 2) 88°1132.4W

a Habitat abbreviations: PR mangrove prop roots; SG seagrass (Thalassia); TC tidal creek with peat walls and undercuts.

b Human impact and turbidity designations: , high; , medium; , low. c Survey of 2003.

d Survey of 2007.

TABLE 3. Ranges of nutrient concentrations (low tide to high 

tide) at the study sites: Panama samples taken in September 2004 

and Belize samples taken in September 2003.

Country and Phosphate Ammonium Nitrate

locality (mol/L) (mol/L) (mol/L)

Panama

 STRI Point 0– 0.048 1.32– 0.988 0.26– 0.253

 Solarte In 0.02– 0.85 0.845– 0.88 0.264– 0.23

 Solarte Out 0.024– 0.048 0.096– 0.071 0.345– 0.276

 Big Bight 0.048– 0.048 1.55– 1.100 0.345– 0.230

Belize

 Sponge Heaven 0.528– 0.624 4.79– 1.88 0.5– 0.41

 Hidden Creek 0.336– 0.786 3.19– 2.35 1.1– 0.39

 Lair Channel 0.384– 0.672 2.72– 1.59 1.06– 1.24

 Manatee Lagoon a 0.576 1.41 0.32

a Only one sample taken, at intermediate tide.

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study (February 2005), whereas abundance of both groups 

increased or stayed at similar levels at the other two sites.

Sponge Species Abundances per Site

Because of the high level of heterogeneity in sponge 

composition and dominance among sites, the relative 

abundance of the most conspicuous epiphytic sponge species is presented separately, by sites.

STRI Point

Sixteen of a total of 23 species found at this site comprise 99% of total sponge abundance. Most of them (13 

species) belong to the order Haplosclerida, specifi cally the 

family Chalinidae, and to the order Poecilosclerida. Tedania 

ignis was the most abundant, followed by Clathria schoenus, Spongia tubulifera, Mycale microsigmatosa, Chalinula 

molitba, Haliclona manglaris, and H. tubifera. Figure 7a 

shows the relative abundance of the six most common species at this site, which added up to 87% of the total sponge 

abundance. It is interesting to note that the presence of both 

T. ignis and Clathria schoenus had decreased considerably 

by February 2005, whereas S. tubulifera remained with 

similar abundance throughout the year. Chalinula molitba

shows a considerable increase (	200%) for June 2004 and 

a decrease to its initial values by February 2005.

Solarte In

Eight of 14 species found at this site constituted 99% 

of the total sponge abundance. Figure 7b demonstrates 

FIGURE 3. Map of research areas at Twin Cays and Pelican Cays, Belize.

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FIGURE 4. (facing page) Views of research locations at Twin Cays and Pelican Cays, Belize. Top left, aerial view of Twin Cays looking south, 

where transect locations were in the Lair channel (branching from the Main Channel center toward the left), in Sponge Haven (the small 

bay at the top right), and Hidden Creek (a narrow, deep tidal channel hidden by mangrove canopy, connecting the Main Channel in the far 

right background with Hidden Lake in the center background); top right, aerial view of Manatee Cay where a transect was placed in the 

large lagoon to the left (Cat Cay is in the background); middle left, mangrove fringe at Sponge Haven; middle right, red mangrove prop roots 

hanging free near the Pelican Cays site and covered mainly by the ropy sponge Iotrochota birotulata; bottom left, close-up of Tedania ignis

and Tedania sp. (probably T. klausi Wulff, a species described after this survey was made), both red, attached to exposed roots in the main 

channel of Twin Cays; bottom right, close-up of purple ascidian (Clavelina puertosecensis) with sponges (turquoise Haliclona curacaoensis, 

primarily) on root at Manatee Cay lagoon.

TABLE 4. Distribution of sponge species reported from Caribbean mangrove localities by various researchers (X presence). Localities are abbreviated as follows: BEL, Belize; TC, Twin Cays; PC, Pelican Cays; PAN, Panama; COL, Colombia; VEN, Venezuela; TRI,

Trinidad; GUA, Guadalupe; JAM, Jamaica; and CUB, Cuba. Data sources are given in table footnotes.

 BEL b

Species a TC PC PAN c COL d VEN e TRI f GUA f JAM g CUB h

Plakina jamaicensis —X ——————— 

Plakinastrella onkodes —X ——————— 

Plakortis halichondriodes X X ——————— 

Plakortis angulospiculatus ——X ————— X

Oscarella sp. 1 (purple) X X X —————— 

Oscarella sp. 2 (drab) —X X —————— 

Cinachyrella apion X X X —X ———— 

Ecionemia dominicana —X ——————— 

Myriastra kallitetilla X ——————X X

Erylus formosus —X ——————— 

Geodia gibberosa —X ——X —X X X

Geodia papyracea X X X —X ——X — 

Dercitus sp. —X ——————— 

Chondrilla caribensis X X X —X ——— X

Chondrosia collectrix —X X ————— X

Cervicornia cuspidifera —X ——————— 

Cliona caribbaea —X ——————— 

Cliona raphida ————X ———— 

Cliona varians X X —————— X

Cliona sp. —X ——————— 

Placospongia intermedia —X X —X ———— 

Diplastrella megastellata —X ——————— 

Spirastrella coccinea —X ——————— 

Spirastrella hartmani —X ——————— 

Spirastrella mollis X X X —————— 

Aaptos duchassaingi —X ——————— 

Aaptos lithophaga ———————— X

Terpios fugax —X —————— X

Terpios manglaris X X X —X ———— 

Prosuberites laughlini ——X —X ——X — 

Suberites aurantiaca —X ——X ——X — 

Tethya actinia X X X —X ——— X

Tethya aff. seychellensis ——X —X ——X — 

Discodermia dissoluta ——X —————— 

Paratimea ? sp. X ———————— 

Timea unistellata —X ——————— 

Agela conifera —X ——————— 

continued

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TABLE 4. continued

 BEL b

Species a TC PC PAN c COL d VEN e TRI f GUA f JAM g CUB h

Phorbas amaranthus —X ——————— 

Coelosphaera raphidifera —X ——————— 

Lissodendoryx colombiensis —X X —————— 

Lissodendoryx isodictyalis X X X —X —X — X

Lissodendoryx sigmata X ———————— 

Monanchora arbuscula —X ——X ———— 

Desmapsamma anchorata —X X —X ———— 

Biemna caribea X —X —X ——— X

Desmacella janiae —X ——————— 

Desmacella meliorata —X ——X ———— 

Neofi bularia nolitangere —X ——————— 

Hymedesmia sp. —X ——————— 

Acarnus sp. —X ——————— 

Artemisina melana —X X —X ———— 

Clathria affi nis —X ——————— 

Clathria cf. ferrea ——X —X ———— 

Clathria microchela —X ——X ———— 

Clathria schoenus X —X —X ——— X

Clathria aff. schoenus X ———————— 

Clathria spinosa —X ——————— 

Clathria venosa X X X —X ———— 

Clathria virgultosa X ———————— 

Mycale cf. americana ————X ———— 

Mycale angulosa ————X ———— 

Mycale arenaria ————————— 

Mycale arndti —X ——————— 

Mycale carmigropila X X X —X ———— 

Mycale citrina X ———X ———— 

Mycale escarlatei ——————— — 

Mycale laevis X ——————X — 

Mycale laxissima X X —X X —— — 

Mycale magniraphidifera X X X —X —— X

Mycale aff. magniraphidifera X X X ———— — 

Mycale microsigmatosa X X X X X X —X X

Mycale aff. microsigmatosa —X ——————— 

Mycale paresperella —X X —————— 

Iotrochota birotulata —X X —X ———— 

Strongylacidon sp. —X ——————— 

Ectyoplasia ferox —X ——X ———— 

Eurypon laughlini —X X —X ———— 

Tedania ignis X X X —X ——X X

Tedania aff. ignis —X ——————— 

Dragmacidon reticulata —X ——————— 

Pseudaxinella ? sp. —X ——————— 

Ptilocaulis walpersi —X ——————— 

Dictyonella sp. X X ——————— 

Scopalina hispida —X ——X ——X X

Scopalina ruetzleri X X X X X ——— X

Scopalina ? sp. —X ——————— 

Ulosa funicularis —X ——————— 

Amorphinopsis sp. 1 —X ——X ———— 

Amorphinopsis sp. 2 —X ——————— 

Ciocalypta ? sp. —X ——————— 

Halichondria corrugata ———————— X

Halichondria magniconulosa ? X X X — X X X — X

Halichondria melanadocia X X X X X ——X X

Halichondria poa ? X X ——————— 

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 BEL b

Species a TC PC PAN c COL d VEN e TRI f GUA f JAM g CUB h

Hymeniacidon caerulea —X ——————— 

Myrmekioderma rea —X ——————— 

Topsentia ophiraphidites —X ——————— 

Callyspongia arcesiosa ————X ———— 

Callyspongia fallax —X X ————— X

Callyspongia pallida —X X —————— 

Callyspongia vaginalis —X ——————— 

Haliclona caerulea —X X —X —X X — 

Haliclona curacaoensis X X X —X ——— X

Haliclona aff. curacaoensis —X ——————— 

Haliclona implexiformis X X X X X ——— X

Haliclona aff. implexiformis —X —————— X

Haliclona magnifi ca X X X —X ———— 

Haliclona manglaris X X X —X ——— X

Haliclona mucifi brosa X X X —————— 

Haliclona picadaerensis X X X —X ———— 

Haliclona tubifera X X X X X ——— X

Haliclona aff. tubifera —X ——————— 

Haliclona twincayensis X X X —X ———— 

Haliclona vermeuleni X X X —————— 

Chalinula molitba X X X —X ——X X

Chalinula zeae ——X —————— 

Amphimedon compressa —X ——X ——X — 

Amphimedon erina X X —X X ———— 

Amphimedon aff. erina —X ——————— 

Amphimedon viridis ———————— X

Niphates caicedoi —X X —————— 

Niphates digitalis —X ——————— 

Niphates erecta —X X —X ———— 

Niphates sp. —X ——————— 

Petrosia pellasarca —X ——————— 

Petrosia weinbergi —X ——————— 

Strongylophora davilai —X ——————— 

Xestospongia carbonaria —X ——————— 

Xestospongia muta —X ——————— 

Xestospongia proxima —X ——————— 

Xestospongia subtriangularis —X ——X ———— 

Aka coralliphaga —X ——————— 

Aka siphona —X ——————— 

Aka sp. —X ——————— 

Calyx podatypa X X X —————— 

Oceanapia nodosa ——X —X ———— 

Oceanapia oleracea ——X —————— 

Cacospongia sp. —X —————— X

Fasciospongia? sp. —X ——————— 

Hyrtios proteus X X X —X ——— X

Hyrtios sp. X X ——————— 

Smenospongia aurea —X ——————— 

Ircinia campana —X X —————— 

Ircinia felix X X X X X ——X X

Ircinia strobilina X X ——X ——— X

Spongia pertusa X X X —X —X — X

Spongia tubulifera X X X X X ——— X

Dysidea etheria X X X X X —X — X

Dysidea fragilis ———————X — 

Dysidea janiae —X —————— X

Aplysilla glacialis X X X —X ———— 

Chelonaplysilla aff. erecta —X X X X ——— X

Darwinella rosacea —X ——X ——X X

continued

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162 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

the relative abundance of the six most common species, 

which comprised 96% of all sponges. Tedania ignis and 

Mycale microsigmatosa were among the top species; Halisarca sp. (a species so far undescribed) and Mycale carmigropila appeared to be among the major components. 

Similar to STRI Point, most of the dominant species decreased in abundance or disappeared by the end of the 

study, while Halisarca remained steady in abundance 

throughout the study period. Three of the common species at this site (Dysidea etheria, Haliclona curacaoensis, 

and Mycale carmigropila) show an increase of sponge 

growth in the warmer periods (either June or September 

2004), followed by a decrease in size during cooler periods (February 2005).

Solarte Out

Six of nine species found at this site made up 99% 

of total sponge abundance (Figure 7c). Tedania ignis continues to dominate, followed by three species not seen in 

the previously discussed sites: Spirastrella mollis, Haliclona vermeuleni, and H. caerulea. It is notable that the 

(projected) area coverage of the dominant species is much 

lower here than that at the other sites (most values are less 

than 500 cm2/m).

TABLE 4. continued

 BEL b

Species a TC PC PAN c COL d VEN e TRI f GUA f JAM g CUB h

Halisarca caerulea —X ——————— 

Halisarca sp. (white) X X X —X ———— 

Aiolochroia crassa —X ——————— 

Aplysina archeri —X ——————— 

Aplysina fi stularis —X ——X ——— X

Aplysina insularis —X ——————— 

Aplysina fulva —X —————— X

Aplysina lacunosa —X ——————— 

Verongula rigida —X ——————— 

Clathrina primordialis X X —————— X

Sycon sp. X —X —X ———— 

Leucandra aspera ——X —X ———— 

a Species are listed in taxonomic order according to class, order, and family.

b Rützler et al., 2000.

c Diaz, 2005; Lehnert and van Soest, 1998.

d Zea, 1987; unpublished data.

e Sutherland, 1980; Diaz et al., 1985; Orihuela et al., 1991; Pauls, 1998, 2003; Ramirez, 2002; Diaz et al., 2003; Perez, 2007.

f Toffart, 1983.

g Hechtel, 1965.

h Alcolado, unpublished data.

FIGURE 5. Similarities of mangrove sponge faunas from Belize, 

Panama, Venezuela, and Cuba. The dendrogram is built from a binary matrix (presence or absence) of species distribution using an 

unweighted pair-group method with arithmetic mean (UPGMA) 

clustal analysis program, with the Bray– Curtis distance index.

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Big Bight

Twelve of 17 species found at Big Bight comprised 

99% of the total sponge abundance; 6 of these amounted 

to 90% (Figure 7d). The most abundant species— Tedania ignis, Mycale microsigmatosa, and Haliclona manglaris— increased in size throughout the year, whereas 

Lissodendoryx colombiensis and Dysidea etheria gained 

in size up to September 2004 but disappeared altogether 

in February 2005. It is worth pointing out the large values for area coverage, as compared to the other locations. The September 2004 data from this site were accidentally lost.

Sponge Species Ranks

The most common sponges at each site amount to 21 

species, from a total of 40 distinguished in the studied areas. Abundance ranks from each site are listed in Table 

5. Only one species, Tedania ignis, maintained the same 

rank at all sites, as the most abundant species. The second 

and third most abundant species were Clathria schoenus

and Spongia tubulifera at STRI Point, Mycale microsigmatosa and Halisarca sp. at Solarte In, Spirastrella mollis

and Haliclona manglaris at Solarte Out, and M. microsigmatosa and H. manglaris in Big Bight. Seven of these 21 

common sponges were only found at one site.

FIGURE 6. Relative abundance of major functional groups growing on mangrove roots (expressed as projected area [cm2] per length [m] 

of root) at four Bocas del Toro sites, between February 2004 and 2005: a, STRI Point; b, Solarte In; c, Solarte Out; d, Big Bight. (ASC 

ascidians; BIV bivalves; CYA Cyanobacteria; EMP empty space; GRN green algae; HYD hydroids; POR sponges [Porifera]; 

RED red algae; TUR algal– cyanobacterial turf.)

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MANGROVE SURVEYS IN BELIZE

Changes in Frequency of Occurrence 

of Major Functional Groups

We determined the frequency of occurrence of important functional groups growing on mangrove roots to be 

able to assess changes over time (Figure 8). The six compound groups recorded in our surveys were cyanobacteria, 

algae, sponges, sea anemones, bivalves, and ascidians. In 

terms of the hierarchy, sponges were fi rst or second at all 

sites, followed by colonial ascidians, macroalgae, and cyanobacteria. Only at Manatee Cay had sponge occurrence 

on roots decreased since 2003, whereas at the other three 

sites it either increased or stayed nearly the same. Ascidian occurrence decreased considerably (10%– 26%) at all 

sites between 2003 and 2007. These changes in sponge 

and ascidian populations were accompanied by cyanobacterial blooms at three sites (Lair Channel, Hidden Creek, 

and Manatee Cay), where increases of 10% to 57% of 

these organisms were recorded. One of the less abundant 

FIGURE 7. Relative abundance of most common sponge species growing on mangrove roots (expressed as projected area [cm2] per length 

[m] of root) at four Bocas del Toro sites between February 2004 and 2005: a, STRI Point; b, Solarte In; c, Solarte Out; d, Big Bight. (Cmol 

Chalinula molitba; Csch Clathria schoenus; Deth Dysidea etheria; Hasp Halicarca sp.; Hcae Haliclona caerulea; Hcur H. 

curacaoensis; Hman H. manglaris; Hpro Hyrtios proteus; Htub Haliclona tubifera; Hver H. vermeulei; Lcol Lissodendoryx colombiensis; Mcar Mycale carmigropila; Mmic M. microsigmatosa; Nere Niphates erecta; Smol Spirastrella mollis; Stub Spongia 

tubulifera; Tign Tedania ignis).

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NUMBER 38 • 165

groups, the sea anemone Aiptasia pallida (Cnidaria), is 

worth mentioning for its striking change in occurrence at 

the Twin Cays sites. Although the population remained 

steady at Hidden Creek (8%), it doubled in Lair Channel 

(10%– 24% of roots occupied), but it apparently disappeared from Sponge Haven where it had been present on 

20% of the roots in 2003. The number of roots available 

for settlement per site increased considerably at Sponge 

Haven and Manatee Cay lagoon, although it decreased in 

Hidden Creek and Lair Channel.

Sponge Species Frequencies per Site

The distinctive species composition and richness at 

each site warrant separate presentations.

Sponge Haven

Most mangrove-specifi c species, such as Halichondria 

magniconulosa, Haliclona curacaoensis, H. manglaris, H. 

implexiformis, Hyrtios proteus, Lissodendoryx isodyctialis, and Spongia tubulifera, remained the most common 

among sponges, and some even increased in frequency between 2003 and 2007 (Figure 9a).

Lair Channel

In this mangrove channel most species remained in 

place between survey periods; some increased in root occurrence (Tedania ignis, Haliclona manglaris, H. tubifera, 

Dysidea etheria) and a few decreased (Haliclona curacaoensis, H. implexiformis, Hyrtios proteus) (Figure 9b). 

Overall, this change was accompanied by a slight decrease 

in root numbers (from 105 to 91) and an increase in all 

non-sponge groups except ascidians.

Hidden Creek

This tidal channel site is opposed to Sponge Haven in 

its changes between 2003 and 2007 (Figure 9c). Ten of the 

12 sponge species found on the transect decreased considerably in occurrence on roots; only the opportunistic 

TABLE 5. Ranking of the most common sponge species according to their abundance at each studied site in the Bocas del Toro region, 

2004– 2005.

 Rank in abundance

Species STRI Point Solarte In Solarte Out Big Bight

Spirastrella mollis 0 0 2 0

Lissodendoryx colombiensis 0 0 0 5

Lissodendoryx isodicyialis 11 0 0 11

Clathria schoenus 2 0 0 12

Mycale carmigrophila 16 4 6 16

Mycale microsigmatosa 5 2 0 2

Iotrochota birotulata 7 0 0 0

Tedania ignis 1 1 1 1

Haliclona caerulea 0 0 5 0

Haliclona curacaoensis 13 5 0 0

Haliclona implexiformis 10 0 0 0

Haliclona manglaris 6 7 3 3

Haliclona tubifera 8 0 0 0

Haliclona vermeuleni 0 0 4 0

Chalinula molitba 4 0 0 10

Amphimedon sp. 0 0 0 8

Niphates erecta 0 0 0 4

Hyrtios proteus 15 0 0 6

Spongia tubulifera 3 8 0 13

Dysidea etheria 0 6 0 7

Halisarca sp. 0 3 0 18

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166 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

generalist Tedania ignis and Lissodendoryx isodictyalis

increased slightly.

Manatee Cay

At this lagoon site, abundance of most typical mangrove sponge species decreased considerably during the 

survey period while two common opportunistic species 

(Tedania ignis, Clathria schoenus) experienced a considerable boost in their populations (Figure 9d). This trend 

coincided with a major increase in root numbers (from 89 

to 123), similar to that which took place at Sponge Haven 

during the same time span.

DISCUSSION

BIOGEOGRAPHY OF CARIBBEAN MANGROVE SPONGES

Available reports describing sponge species distribution 

in Caribbean mangroves suggest the importance of geographic vicinity, with high similarities between the faunas of 

Panama and Venezuela. On the other hand, this geographic 

concept is upset by the incongruence of faunas encountered 

at two nearby sites in Belize (Twin Cays and the Pelican 

Cays). This dissimilarity is caused mostly by the presence 

of several unique or usually coral reef-associated species in 

the mangroves of Manatee Lagoon, an environment of particular geomorphological structure and prevailing ecologiFIGURE 8. Frequency of occurrence (% of roots occupied) of major functional groups growing on mangrove roots at four sites in Belize: a,

Sponge Heaven, Twin Cays; b, Lair Channel, Twin Cays; c, Hidden Creek, Twin Cays; d, Manatee Lagoon, Pelican Cays. (ALG algae; ANE 

sea anemones [Aiptasia pallida]; ASC ascidians; BIV bivalves; CYA cyanobacteria; POR sponges [Porifera]).

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NUMBER 38 • 167

cal conditions in the Pelican Archipelago (Macintyre and 

Rützler, 2000; Rützler et al., 2000; Wulff, 2000).

SHORT-TERM DYNAMICS OF MANGROVE

EPIFAUNA IN PANAMA

Major Functional Groups

As previously reported, mangrove-root epiphytic 

communities in Bocas del Toro are dominated either by 

sponges or by algae/cyanobacteria (Farnsworth and Ellison, 1996; Diaz et al., 2004; Peréz, 2007). Elsewhere in 

the Caribbean, other groups, such as bivalves, anemones, 

or ascidians, may rival these taxa in abundance (Sutherland, 1980; Toffart, 1983; Bingham, 1992). The dominance 

of macroalgae at the protected lagoon of “Solarte In” might 

be a consequence of the eastward orientation of this site 

(as opposed to the westward orientation of the other three 

sites), which would expose the mangrove fringe to sunlight 

FIGURE 9. Frequency of occurrence (% of roots occupied) of sponge species growing on mangrove roots at four sites in Belize: a, Sponge 

Heaven, Twin Cays; b, Lair Channel, Twin Cays; c, Hidden Creek, Twin Cays, d, Manatee Lagoon, Pelican Cays. (Aatl Amorphinopsis 

atlantica; Aeri Amphimedon erina; Bcar Biemna caribbea; Ccar Chondrilla caribensis; Cmic Clathria microchela; Cpri Clathrina 

primigenia; Csch Clathria schoenus; Cven Clathria venosa; Deth Dysidea etheria; Hasp Halisarca sp.; Hcur Haliclona curacaoensis; 

Himp H. implexiformis; Hmag Halichondria magniconulosa; Hman Haliclona manglaris; Hpro Hyrtios proteus; Htub Haliclona 

tubifera; Ifel Ircinia felix; Liso Lissodendoryx isodictyalis; Mlae Mycale laevis; Mmag M. magniraphidifera; Mmic M. microsigmatosa; Stub Spongia tubulifera; Tign Tedania ignis.)

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for longer periods, thus promoting the growth of typical 

shallow-water algal species. However, further studies are 

required to sustain this hypothesis. There were no observations of seasonal changes in the composition of epiphytic 

taxa from one sampling period to the other at any site. The 

decrease in abundance (20%– 35%) found for the most 

dominant groups at two sites (STRI Point and Solarte In) 

coincides with housing developments that occurred since 

the study started in 2004. Increases in suspended sediments 

and incidences of sponges covered by silt, which were observed at STRI Point during September and February 2005, 

may have impacted the community. In contrast, at the more 

pristine sites (Solarte Out and Big Bight), these same organisms demonstrated considerable quantitative increases.

Sponge Species

The six most common species at each site constitute from 87% to 99% of the total root area covered by 

sponges. These dominant species differed between sites, 

bringing the number of the most abundant sponges to 21, 

of a total diversity of 40 species. Only Tedania ignis was 

the most common species at all sites. At Solarte In the second most common species was a thin crust of the genus 

Halisarca, whereas at STRI Point it was Clathria schoenus, a species with a highly variable growth form (thick 

crusts to branching), supporting the common observation 

that mangrove fauna can be highly heterogeneous within 

one biogeographic region. It is interesting to note that 5 

species that ranked near the top at the four sites were encrusting sponges (Mycale microsigmatosa, Dysidea etheria, Haliclona manglaris, Halisarca sp., Clathria schoenus, 

and Spirastrella mollis). This result suggests that, at least 

in Bocas del Toro, encrusting species are highly successful competitors. The dominance of Tedania ignis was also 

reported from other Caribbean locations (Toffart, 1983; 

Sutherland, 1980; Wulff, 2004; Diaz et al., 2004) and is 

probably related to its high and nearly year-around production of larvae (Ruetzler, unpublished data) and rapid 

growth rate (Wulff, 2005).

Dominant species were not always consistent in 

abundance at all sites. For example, during the observation time Tedania ignis decreased considerably at STRI 

Point and Solarte In but increased at Solarte Out and Big 

Bight. Furthermore, increase or decrease in abundance 

was not necessarily restricted to certain species or localities. Certain locality trends, however, were observed. At 

STRI Point, where T. ignis and Clathria schoenus decreased or disappeared entirely from the roots, the few 

large specimens of Spongia tubulifera remained with 

only slight size changes throughout the year. At least at 

one location, Solarte In, deterioration of sponges appeared to be coinciding with the aforementioned housing 

development, which caused an increase in suspended and 

deposited sediment.

An interesting trend is the predominance of large 

sponges at Big Bight versus the much smaller sizes at 

So larte Out. Solarte Out is a shallow habitat in an exposed position and subjected to strong wave action and 

scouring by predominantly sandy sediments (see Table 2). 

These parameters must impede the growth of large individuals, with the result that small and better adapted 

forms, such as Haliclona vermeuleni, H. caerulea, and 

Spirastrella mollis, become very abundant. Even an opportunistic species such as Tedania ignis, common and largegrowing elsewhere, tends to be considerably restricted 

in size there. On the other hand, Big Bight sponges were 

found to have rapid growth rates that can be attributed to 

high nutrient concentrations measured at this site, possibly 

related to runoff from the dense forest that surrounds this 

lagoon (see Table 3). The high variability of sponge species 

composition between contiguous sites corroborates previous reports that the mangrove sponge fauna is rather heterogeneous in species distribution and dominance within 

relatively small geographic areas (Farnsworth and Ellison, 

1996; Rützler et al., 2000; Diaz et al., 2004). This characteristic is probably the result of low recruitment rate in 

most species studied and, in some cases, selective physicochemical variables, such as those described for Solarte 

Out. A third aspect that became evident in this study is 

the intrinsic growth dynamics of species over time, high 

in species such as Tedania ignis and Chalinula molitba, 

and low or barely noticeable in Hyrtios proteus and Spongia spp. It must be recognized that species have different 

lifespans, growth rates, growth periods, and frequency of 

reproduction. Understanding these processes is essential to 

the interpretation of community dynamics.

LONG-TERM DYNAMICS OF MANGROVE EPIFAUNA IN BELIZE

Major Functional Groups

The distribution of the four primary components of 

mangrove-root ephiphytic communities in Belize— cyanobacteria, macroalgae, sponges, and ascidians— varied differently at each of the four studied sites between August 

2003 and 2007. Sponges were the most frequent occupants 

at all four locations in 2003; by 2007, the population had 

either increased (Sponge Heaven, The Lair), decreased 

(Manatee Lagoon), or remained steady. The decrease at 

Manatee Cay seemed to be related to macroalgal blooms 

09_DiazRutzler_151-172_Lang.indd168 168 9_DiazRutzler_151-172_Lang.indd168 168 9/24/09 9:21/24/09 9:21
NUMBER 38 • 169

that coincided with the recent clear-cutting of the mangrove adjacent to this lagoon and to dredging for land-fi ll 

that released large quantities of fi ne sediments. Ascidian 

occurrence followed a similar pattern, indicating that all 

fi lter feeders are impacted by environmental events such 

as increase of sedimentation and blockage of vents by cyanobacterial blooms. The effect of changing root numbers 

seems to be obscured by the environmental factors, because there was no obvious relationship between changes 

in root number and frequency of any of the major taxa in 

the community.

Sponge Species

Comparing species composition and frequency at 

the four study sites in Belize, we found that they varied 

considerably during the four years between observation 

periods. The most obvious parameters affecting sponge 

populations were space competitors (cyanobacteria, macroalgae), number of roots available for settlement, and 

anthropogenic destructive events. The considerable decrease in cyanobacteria and macroalgae and increase in 

root numbers (from 99 to 143) in Sponge Haven may be 

related to the strong increase of mangrove-specifi c sponges 

because important competitors were no longer present 

and new substrata became available. In contrast, at Hidden Creek, the increase of fi lamentous cyanobacteria (to 

57% of substrate area) and decrease in root numbers 

(from 59 to 52) must have caused the dramatic reduction 

of most mangrove-specifi c sponge species. In Manatee Cay 

Lagoon, mangrove-specifi c species lost in frequency while 

opportunistic species (Tedania ignis, Clathria schoenus) 

gained. Overall, however, there was a reduction of sponge 

populations despite an addition in root numbers. This 

trend can be explained by increased algal competition and 

an artifi cial incursion, the clear-cutting of mangrove trees 

and dredging of fi ll material for a housing development 

sometime before the 2007 survey. The dredge operation 

in particular can be blamed in the short term as it causes 

suspension of fi ne sediment, affecting the delicate fi ltration system of the sponges. A shift of species toward more 

robust opportunists rather than typical mangrove forms is 

therefore not surprising.

COMMENTS ON METHODS FOR EVALUATING MANGROVE

PROP-ROOT COMMUNITIES

Two criteria were used in the present study to evaluate 

epiphytic communities on mangrove roots. To determine 

short-term dynamics (within one year; Bocas del Toro), 

it was expected that specimen size rather than numbers 

would change. Therefore, a photographic record was made 

of a specifi c number of roots (25) along their entire lengths 

(the side facing the open water), and planimetry was used 

to measure projected area cover of the fouling organisms. 

From these values and the record of root length, an index 

of species abundance could be calculated. Area cover has 

been extensively used to compare the abundances of plant 

and sessile animal communities, and it has been proven a 

most practical and reliable method for reef surveys (Weinberg, 1981). Considering that in mangroves substrate 

availability is quite low, measuring area cover gives a good 

indication of how important an organism is in this community. The limitation of this method applies mostly to 

stoloniferous organisms for which cover may underestimate their importance. The photo-transect method proved 

to be most useful in areas where visibility was very good, 

but it was problematic in locations with high freshwater 

or sediment input. Such conditions caused whole sets of 

photographs to be impossible to interpret. This method is 

also time consuming, both the work underwater and that 

during photo analysis in the lab. For this reason there was 

a limit to the root numbers that could be included in each 

survey. Usually, to complete a survey of 25 roots in one site 

it was necessary to visit twice, and evaluation of all (3– 8) 

photos for one root took from 30 to 60 min. In the end, 

after excluding useless images, the data set was reduced to 

only 14 to 22 recorded roots, depending on the site.

Alternatively, in Belize we used data on the presence or 

absence of taxa on each root and thus were able to survey a 

much larger number of roots (50– 150), from which we determined the frequency of occurrence of major taxonomic 

groups and species of sponges. These data allowed monitoring the presence of each group or species and change 

in distributions over time. This type of survey follows the 

fate of the community rather than fl uctuations in biomass. 

The method also aids detection of a species or community 

reaction to particular environmental disturbances. In terms 

of time investment, it takes only 2 to 5 h to obtain frequency 

data from a 30 m transect along the mangrove fringe. The 

data were in hard copy once the fi eldwork was completed 

and were independent of visibility conditions and other 

variables that may ruin photographic data.

CONCLUSIONS

Many more Caribbean mangroves must be studied before we can expect a full understanding of the biodiversity 

and the biogeographic relationships of their unique and 

09_DiazRutzler_151-172_Lang.indd169 169 9_DiazRutzler_151-172_Lang.indd169 169 9/24/09 9:21/24/09 9:21
170 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

fascinating prop-root fouling communities, particularly 

the sponges. The rather disjunct pattern of sponge species 

distribution found in the Panama and Belize study sites 

suggests that biodiversity is better evaluated by surveying 

extended stretches of mangrove fringe at numerous sites in 

any region rather than short lengths of transects. Interpretation of species composition and interactions can be based 

on smaller-scale levels of inquiry. The most abundant organisms in the studied sites were sponges, macroalgae, cyanobacteria, ascidians, and bivalves. The hierarchical ranking of these groups showed great variability on spatial and 

temporal scales, making generalization and prediction of 

structure and dynamics of communities very diffi cult.

The one-year study of four sites in the Bocas del Toro 

region, Panama, showed various important aspects of 

abundance changes in these fouling communities. First, a 

few sponge species contribute most of the abundance; second, the identity of major community components varies 

within a small geographic scale; third, species have adopted distinct life strategies (in growth potential, recruitment rates, and asexual reproduction capabilities) that 

allow for adaptations to resist stressful environmental 

variables; and fourth, the combination of the factors of 

large sediment grain size and energy from wave or current 

action limits species habitat access, survival, and growth, 

as demonstrated by the increase in turbidity from landfi lling and development in some areas.

The four-year observations in Belize made it evident that the frequency of occurrence of sponge species 

and other taxa, such as cyanobacterial and macroalgal 

blooms, is a relatively simple and fast measure to detect 

major environmental changes. Even if sponge frequency 

on the roots is not much affected by algal blooms, the 

presence of mangrove-specifi c species certainly shows a 

decline; only a couple of generalist species seem to profi t 

from such stressful events. The degree of disappearance 

of ascidians at all four sites in Belize suggests that these 

organisms may be even more sensitive to algal and cyanobacterial competition, as well as suspended fi ne sediments, 

than sponges. We fi nd, both in Belize and in Panama, that 

two sponge growth forms are highly successful among 

sponge root occupiers: encrusting and irregularly massive. 

This observation is in contrast to open reef environments 

where tubular and ramose forms predominate.

Close monitoring of the abundance and frequencies of 

key mangrove benthos at specifi c sites and their correlation 

with short-term or long-lasting environmental impacts and 

stress will be a useful tool for assessing mangrove health 

throughout the Caribbean region in the future.

ACKNOWLEDGMENTS

We thank Mike Carpenter, Kathleen Smith, Estrella 

Villamizar, and Martha Nicholas for support of fi eldwork 

based at Carrie Bow Cay, Belize; likewise, we thank Gabriel Jacome and Plinio Gondola for assistance with logistics at the Smithsonian Bocas del Toro fi eld station, Panama. Molly Kelly Ryan designed the maps and rendered 

the graphs in fi nal form; Carla Piantoni prepared the color 

fi gures and helped with editorial tasks. We acknowledge 

the National Coral Reef Institute for lending us the CPCe 

(Coral Point Count with Excel extensions) program for 

area calculations. Photographs for this paper were taken 

by the following Smithsonian staff or associates: Cristina 

Diaz, Ilka Feller, Diane Littler, Elisabeth McLean, Tony 

Rath, and Klaus Ruetzler. This is contribution number 

855 of the Caribbean Coral Reef Ecosystems Program 

(CCRE), Smithsonian Institution, supported in part by the 

Hunterdon Oceanographic Research Fund.

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09_DiazRutzler_151-172_Lang.indd172 172 9_DiazRutzler_151-172_Lang.indd172 172 9/24/09 9:21/24/09 9:21
Internal Transcribed Spacer 2 (ITS2) 

Variation in the Gorgonian Coral 

Pseudopterogorgia bipinnata in Belize 

and Panama

Daniel Dorado and Juan A. Sánchez

ABSTRACT. One of the most intriguing aspects of molecular evolution is the concerted 

evolution of ribosomal genes, yet the presence of intragenomic rDNA variants is still not 

well understood. We studied the intragenomic variation of the internal transcribed spacer 

2 (ITS2, rDNA) in the gorgonian coral Pseudopterogorgia bipinnata (Gorgoniidae: Octocorallia) using a combined approach of denaturing gradient gel electrophoresis (DGGE), 

DNA sequencing, and RNA secondary structure prediction. We examined intragenomic 

variants of colonies from Carrie Bow Cay (Belize) and Bocas del Toro (Panama). Despite 

frequent intragenomic ITS2 variation in P. bipinnata, predicted RNA secondary structures exhibited no signs of including pseudogenes and comprised functional copies. Given 

the low divergence among the ITS2 sequences recovered from DGGE gels, intragenomic 

variation was restricted to a few mutations that did not compromise the functionality of 

the ITS2 secondary structure. The presence of common ITS2 intragenomic variants at 

two distant populations raises new questions such as whether sharing similar copies can 

be the product of gene fl ow. Regardless of the limited number of individuals analyzed in 

this study, the method used here, excising bands from DGGE gels for further amplifi cation and sequencing, examined the reliability of the technique to separate intragenomic 

variants with up to one nucleotide difference. Studying the intragenomic variation of 

ITS2 has potential to provide us with information on recent population events such as 

introgressive hybridization.

INTRODUCTION

Ribosomal DNA (rDNA) intragenomic variation has puzzled molecular systematists and ecologists during the past few years. The rDNA is a multigene 

family arranged in tandem repeats, frequently achieving several hundreds of 

repetitions per chromosome. Each repetition is composed of three ribosomal 

subunits (18s, 5.8s, and 28s), separated by two internal transcribed spacers 

(ITS1 and ITS2, or ITSs), an external transcribed spacer (ETS), and the nontranscribed intergenic spacers, IGS. The ITS1 and ITS2 spacers form secondary 

structures that are crucial for ribosomal maturation as well as important for 

the maturation of the rRNA (Coté and Peculis, 2001). The ITSs are known to 

have conserved core structures throughout the metazoans (see reviews in Coleman, 2003; Schultz et al., 2005). Changes in the ITS secondary structure are 

known to produce inhibition of the maturation of rRNA as a consequence of 

Daniel Dorado and Juan A. Sánchez, Departamento de Ciencias Biológicas– Facultad de Ciencias, Laboratorio de Biología Molecular Marina– 

BIOMMAR, Universidad de los Andes, P.O. Box 

4976, Bogotá, Colombia. Corresponding author: 

J. Sánchez (juansanc@uniandes.edu.co). Manuscript 

received 9 June 2008; accepted 20 April 2009.

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174 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

coevolution between RNA secondary structures and the 

processing molecular machinery responsible for its removal (Van Nues et al., 1995). As multicopy genes, the 

rDNA is assumed to evolve via concerted evolution, resulting in the homogenization of the sequences throughout 

the genome (Harris and Crandall, 2000; Hillis and Davis, 

1988), that is, homogenization of copies through unequal 

crossing-over and gene conversion processes (Liao, 2000). 

However, variations within individuals have been reported 

primarily as a result of slow concerted evolution (Harris 

and Crandall, 2000; Coté and Peculis, 2001), hybridization, or the presence of pseudogenes (Marquez et al., 

2003; Harpke and Peterson, 2006). The latter can appear 

because of the presence of highly divergent rDNA types 

in different chromosomes (Arnheim et al., 1980), which 

retain ancestral rDNA polymorphisms for long periods of 

time (Marquez et al., 2003). Hybridization phenomena 

between species per se could increase the rDNA diversity 

in an individual, but as an additional consequence could 

result in silencing some rDNA loci by chromatin modifi cations in a nucleolar dominance process (Chen et al., 1998; 

Frieman et al., 1999; Muir et al., 2001), which can drive 

some rDNA loci by neutral selection toward pseudogenes 

(Muir et al., 2001). However, the presence of ITS2 intragenomic variants is a phenomenon that we do not clearly 

understand.

Pseudopterogorgia bipinnata Pallas is one of the most 

abundant shallow-water gorgonian corals in the Caribbean Sea (Bayer, 1961; Sánchez et al., 1997). This species 

has two particular characteristics: it exhibits large phenotypic plasticity along the depth– wave exposure gradient, 

and it presents clear intragenomic variation in the ITS2 

sequence (Sánchez et al., 2007). Consequently, P. bipinnata constitutes an appropriate model species to study the 

nature and genetics of ribosomal intragenomic variation. 

In this study we had two main objectives: (1) to isolate 

sequences of intragenomic ITS2 variants in P. bipinnata

from populations at Belize and Panama and (2) to examine if intragenomic ITS2 variants were functional copies 

using predicted RNA secondary structures.

MATERIALS AND METHODS

Samples from Pseudopterogorgia bipinnata colonies 

were obtained by scuba diving at Carrie Bow Cay (n 27), 

Belize, and Cristobal Island (n 11), Bocas del Toro, 

Panama. A few P. bipinnata from the Bahamas (San Salvador) and Colombia (Bancos de Salmedina, Cartagena), 

as well as a sequence of Gorgonia mariae, were chosen 

as outgroups. However, there was no a priori information on the genetic distance between western and eastern 

Caribbean populations. Total DNA was extracted using a 

cetyltrimethylammonium bromide (CTAB), proteinase K, 

phenol– chloroform– isoamyl alcohol extraction method 

(Coffroth et al., 1992); DNA was resuspended and conserved in TE buffer at 70°C; DNA quality was checked 

in agarose (1%) electrophoresis at 80 V for 30 min. Using the best DNA extraction quality, primers 5.8s 5-

AGCATGTCTGTCTGAGTGTTGG-3 and 28s 5-GGGTAATCTTGCCTGATCTGAG-3, designed by Aguilar and 

Sánchez (2007), were used for the ITS2 amplifi cation. 

Conditions for polymerase chain reaction (PCR) were as 

follows: an initial denaturizing step of 2 min at 94°C; followed by 35 cycles of 30 s at 94°C, 30 s at 56.8°C, and 1 

min at 72°C; and a fi nal extension step of 2 min at 72°C; 

using 1 unit Taq polymerase (Invitrogen), 3.5 mM MgCl2, 

0.2 mM deoxynucleoside triphosphates (dNTPs; Biorad 

Mix), 0.15 M primers (each), and 4 L DNA (dilution 

1/50) in 20 L as the fi nal volume. The amplifi cation was 

standardized with an effi ciency of 95%. PCR reactions were 

screened in denaturing gradient gel electrophoresis (DGGE) 

containing 8% polyacrylamide, 1  TAE buffer, and a linear urea-formamide denaturing gradient from 45% to 80%. 

The gels were pre-run at 60°C and 90 V for 30 min, followed by electrophoresis at 60°C and 90 V for 13 h. Gels 

were stained with ethidium bromide during 15 min and visualized using a BIORAD Chemidoc system. DGGE separates DNA fragments not only by the fragment size but also 

by the DNA sequence, where GC-richer sequences migrate 

further independently of small differences in size (Figure 1). 

All reactions were conducted without a CG-clamp in the 

primers, which is a 40 bp GC-rich sequence added before 

the 5-primer that adds an additional denaturing domain 

allowing further migration of the DNA before denaturing 

(LaJeunesse and Pinzon, 2007). In the case of gorgonian 

corals, there was no need for the GC-clamp owing to the 

great migration in the DGGE of gorgonian ITS2 sequences, 

which avoided the problems involved with PCR reaction 

tailed primers. Bands visualized in the DGGE gel were 

excised using sterilized micropipette tips in the Bio-Rad 

Chemidoc system and placed in 0.5 mL tubes with 100 L 

sterilized double distilled water. The tubes were incubated 

in a shaker at room temperature for 24 h at 150 rpm. Each 

band extract was collected in a 0.5 mL tube and the DNA 

was precipitated with 300 L cold absolute ethanol; tubes 

were placed at 20°C for 24 h and then centrifuged at 

13,000 rpm for 30 min; the supernatant was discarded, 

10_DoradoSanchez_173-180_Lang.in174 174 0_DoradoSanchez_173-180_Lang.in174 174 9/24/09 9:21/24/09 9:21
NUMBER 38 • 175

and the pellet was dried and resuspended in 15 L sterilized double distilled water.

Reamplifi cation of bands was conducted using PCR 

as just described, using the same set of primers, except 

that DNA was used without dilution and the annealing 

temperature was raised a few degrees to increase specifi city. Purifi cation of PCR products for sequencing was performed by the Exo-SAP (Exonuclease 1 and shrimp alkaline phosphatase) method using 1 unit Exonuclease, 0.2 

units shrimp alkaline phosphatase, and 2 L SAP buffer 

10 per 20 L in a 0.2 mL tube. Reactions were held at 

37°C for 1 h and at 80°C for 15 min. Sequencing reactions 

were performed with the BigDye 3.1 system according 

to the manufacturer’s instructions (Applied Biosystems) 

and sequenced in a capillary electrophoresis automated 

sequencer (ABI310). Each sample was sequenced with 

forward and reverse primers. The consensus sequences 

were obtained by assembling the two complementary 

electrophenograms in Sequencer 4.7 software.

Secondary structures of all sequences were obtained 

by reconstructing by comparison via Pairwise Alignment 

(Bioedit) with previously reported structures in octocorals (Aguilar and Sánchez, 2007). The sequences were 

then submitted with a few constraints and restrictions in 

MFOLD at a default temperature of 37°C (Zuker, 2003). 

Constraints force bases to be double stranded whereas 

restrictions cause them to be single stranded, which are 

chosen depending on the sequence homology between the 

sequences with known structure against each problem 

sequence without known structure. A good example for 

a constraint are the two complementary sequences that 

make a stem; an example of a restriction is a string of 

free nucleotides between helices or any kind of loop. The 

structure chosen was the one with the greater negative free 

energy but conserving the ring model known for ITS2. The 

obtained secondary structures were used to construct a 

matrix for cladistic analysis as described by Aguilar and 

Sánchez (2007). Phylogenetic analyses included maximum 

parsimony and maximum likelihood as well a Bayesian inference for a combined sequence-molecular morphometric 

analysis (see details in Grajales et al., 2007).

RESULTS

Denaturing gradient gel electrophoresis (DGGE) analysis revealed that most individuals from Belize and Panama 

contained intragenomic variants of ITS2 (see Figure 1). 

There were as many as three different bands per individual 

that were similar or nearly equal in length because of their 

closeness in the DGGE gel (Figure 2). Some banding patterns were identical for individuals from both Belize and 

Panama, which indicated exact ITS2 copies, although some 

patterns unique to each population were also observed (see 

Figure 1). Great effort was made to obtain sequences from 

most bands, but not all of them were successfully recovered. The sequences had an average GC content of 55.6%, 

which afforded the great migration of intragenomic ITS2 

variants in the DGGE. The sequences from P. bipinnata

had more than 85.6% of sequence similarity, contrasting 

with just 48% with respect to G. mariae.

Predicted secondary structures from all excised bands 

exhibited functional structures with the conserved six helicoidal ring model previously reported for octocorals (Aguilar and Sánchez, 2007), but great variability was observed 

in the length and complexity of each stem and spacer (Figures 2, 3). Intragenomic differences were frequently discrete changes that did not affect the predicted secondary 

FIGURE 1. Runs (2) of internal transcribed spacer 2 (ITS2) denaturing gradient gel electrophoresis (DGGE) banding patterns from 

Pseudopterogorgia bipinnata colonies from Panama (Bocas del Toro; 

stars) and Belize (Carrie Bow Cay; circles). Numbers correspond to 

the sequence size when available. The gels have a common artifact 

in the form of a “smile” (more accentuated in the upper gel), where 

lateral wells tend to migrate slightly further because of the pressure 

acting on the gel edges.

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176 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

structures (see Figure 2). The ITS2 in P. bipinnata from 

Panama and Belize varied from 212 to 224 nucleotides 

(Figure 3). In general, the stems 2, 3, and 6 were shorter 

than the stems 4 and 5, with stem 5 being the longest. 

Multiple internal loops were frequent in stems 3, 4, and 

5, with more nucleotides (nt) on stem 5, where up to six 

internal loops were observed (Figure 3). The spacers were 

often short, ranging from 1 to 4 nt. Spacer ‘1i’ showed a 

conserved sequence, UG, with little variation across individuals, while spacer ‘4i’ was the longest, with 4 to 12 nt 

and a conserved core sequence (AGUNCAGC) observed in 

most of individuals (Figure 3). Phylogenetic results from 

sequence and alignments or combined data sets, including 

11 excised bands from individuals from Belize and 3 from 

Panama, showed little divergence between Panama and Belize despite the long distance with respect to a few individuals from Bahamas and Colombia (Figure 4). Very modest 

support was found within individuals from Panama or Belize, and no particular grouping could be discerned (data 

not shown). In addition, no particular features of the ITS2 

secondary structure as seen with helix 5, which showed the 

largest number of characters, were supporting any particular clade or group of individuals (Figure 4).

DISCUSSION

The intragenomic ITS2 variation in Pseudopterogorgia bipinnata individuals involved functional copies, as 

corroborated by reconstructing their predicted RNA secondary structures. Given the low divergence among the 

ITS2 sequences recovered from DGGE gels, intragenomic 

variation was restricted to a few mutations that did not 

compromise the functionality of the ITS2 secondary structure. Despite frequent intragenomic ITS2 variation in P. bipinnata, predicted RNA secondary structures exhibited no 

signs of including pseudogenes or structural degeneration. 

Having in mind that the ITS2 secondary structure has a 

major role in the maturation of the ribosomal RNA (Coté 

and Peculis, 2001), little tolerance of changes is expected 

as a result of the restrictions imposed by the ITS2 splicing 

machinery (Van Nues et al., 1995; Coleman, 2003); this 

means purifying selection is acting on secondary structural 

constraints (Coté and Peculis, 2001) or concerted evolution mechanisms are acting similarly (Liao, 2000; but 

see Nei and Rooney, 2005; Harpke and Peterson, 2006). 

Similarly, compensatory base changes (CBC), occurring at 

the stem regions, are very unlikely to occur at the intraspecifi c level (Müller et al., 2007). Thus, it is expected that 

only variants or alleles carrying only minor changes occur, 

which was evident with the functionality of co-occurring 

secondary structures found at the intraspecifi c level.

ITS intragenomic variation has been also observed 

in scleractinian corals. Van Oppen et al. (2001) examined diverse nuclear and mitochondrial DNA sequences, 

concluding that paraphyly from intragenomic ITS copies 

could be explained by extensive introgressive hybridization 

and reticulate evolution. Similarly, Marquez et al. (2003) 

found the presence of ribosomal pseudogenes as a possible consequence of multiple hybridization events. However, Vollmer and Palumbi (2004) examined the multiple 

copies of the Caribbean Acropora species and concluded 

that there is no proper way to evaluate if the intragenomic 

shared variation of genes such as ITS1 and ITS2 was the 

result of incomplete lineage sorting or recent hybridization processes. Nonetheless, all the studies mentioned 

studied the intragenomic variation of ITS using the DGGE 

technique, and it is clear that traditional cloning methods 

overestimate the intragenomic diversity (LaJeunesse and 

Pinzon, 2007).

Regardless of the limited number of individuals analyzed in this study, the method used here, excising bands 

from DGGE gels for further amplifi cation and sequencing, probed its reliability to separate intragenomic variants 

up to one nucleotide difference (see Figure 2). DGGE is a 

FIGURE 2. Two different intragenomic ITS2 variants from an individual colony of Pseudopterogorgia bipinnata from Belize. The 

variants were excised from the two bands indicated by arrows in 

the DGGE gel above, reamplifi ed, and sequenced. The arrows below show the differences between the two predicted RNA secondary 

structures corresponding to one INDEL (insertion or deletion) only.

10_DoradoSanchez_173-180_Lang.in176 176 0_DoradoSanchez_173-180_Lang.in176 176 9/24/09 9:22/24/09 9:22
NUMBER 38 • 177

method useful to detect the most prevalent intragenomic 

variants of ribosomal genes, whereas traditional methods 

to screen intragenomic variation such as cloning miscalculate the codominance of the different copies (LaJeunesse 

and Pinzon, 2007; Thornhill et al., 2007). There are two 

main approaches for depicting the nature of intragenomic 

ITS2 variants in octocorals. One method is to study in detail the genetics of the different ITS2 variants by crossing 

individuals with different intragenomic patterns, which 

can provide inheritance information and linkage disequilibrium confi gurations. An alternative method includes 

techniques such as reverse transcription (RT)-PCR and 

quantitative real-time PCR, which can offer more accurate information on the functionality of the different intragenomic ITS2 copies. The RT-PCR technique can fi lter 

copies that are not expressed in the cell, and quantitative 

PCR can quantify the amount of ITS transcripts from each 

particular copy. These methods could also test if the intensity of bands in DGGE actually corresponds to the number 

of copies of a particular intragenomic variant.

ACKNOWLEDGMENTS

This study was partially funded by Facultad de Ciencias [Department of Biological Sciences], Universidad 

de los Andes, COLCIENCIAS (Grant 120409– 16825; 

funding to J. A. Sánchez); a Smithsonian postdoctoral 

fellowship (NMNH); the MSN Invertebrate Workshop 

(2003) at Bocas Research Station, Bocas del Toro, Panama (STRI); and the Smithsonian Marine Science Network. We are grateful to Rachel Collin, Gabriel Jácome, 

Howard Lasker, Klaus Ruetzler, Michael Lang, Stephen 

FIGURE 3. Predicted ITS2 RNA secondary structures in Pseudopterogorgia (P.) bipinnata. The upper 

right structure shows the characters for the molecular morphometrics analysis used in the combined Bayesian inference analysis. The number within the ring structure refers to the total number of nucleotides at 

each structure.

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178 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Cairns, BIOMMAR colleagues, and the Smithsonian 

Station at Carrie Bow Cay, Belize. The Minister of Environment, Household and Territorial Development of 

Colombia granted access to genetic resources to JAS for 

the DNA analyses included in this paper (Contract 007, 

resolution 634; 14 March 2007). This work is contribution number 841 of the Caribbean Coral Reef Ecosystems 

Program (CCRE), Smithsonian Institution, supported in 

part by the Hunterdon Oceanographic Research Fund.

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/24/09 9:22
Obvious Invaders and Overlooked Infauna: 

Unexpected Constituents of the Decapod 

Crustacean Fauna at Twin Cays, Belize

Darryl L. Felder, Peter C. Dworschak, Rafael 

Robles, Heather D. Bracken, Amanda M. Windsor, 

Jennifer M. Felder, and Rafael Lemaitre

ABSTRACT. Decapod crustaceans in the vicinity of Carrie Bow Cay and Twin Cays, 

Belize, have been under study for more than 25 years. Large collections have been assembled, and new species have been discovered. The effort has included photographic 

documentation of coloration, yielding characters of value in identifi cation of problematic 

tropical taxa. Measurements of diversity have been markedly enhanced by extraction 

corer (yabby pump) sampling in shallow subtidal sediments, especially at Twin Cays. 

This technique revealed species, genera, and families of thalassinidean decapods not previously known from the region. Studies continue on the ecological roles of these burrowers, dominant bioturbators in seagrass beds where they produce conspicuous mounds 

of sediment and constitute a major infaunal biomass at Twin Cays. By contrast, familiar large reptant decapods typically dominate shallow rocky substrates. Within the past 

four years, however, the nonindigenous portunid crab Charybdis hellerii has extensively 

invaded large portions of hard substrates at Twin Cays. In 2007, it was found to dominate cavities under coral heads in survey areas along the northeastern and southwestern 

shorelines, possibly displacing populations of large Mithrax, Menippe, Callinectes, and 

Panulirus previously found there in abundance.

INTRODUCTION

Fieldwork centered on Carrie Bow Cay and surrounding habitats, including 

a variety of settings at Twin Cays. The effort continues work by the fi rst author 

in collaboration with the late Ray Manning in 1983, as well as work by the late 

Brian Kensley during the 1980s and early 1990s (Kensley, 1981, 1996). Early 

efforts produced abundant grass-bed and reef-crest species generally identifi able 

with known Caribbean taxa, along with small cryptic forms obtained by cutting 

open sponges, breaking rubble, poisoning in situ, or using several narcotants to 

drive out small decapods from rubble isolated in containers. Rich collections 

that have accumulated in the the Smithsonian Institution’s National Museum of 

Natural History were fi xed in formalin, limiting their value in genetic analyses. 

Efforts in 2002 and 2007 shifted emphasis to varied intertidal and subtidal habitats of Twin Cays and to resampling the regional fauna to obtain alcohol-fi xed 

materials for molecular genetic analyses.

Darryl L. Felder, Rafael Robles, Heather D. 

Bracken, Amanda M. Windsor, and Jennifer M. 

Felder, Department of Biology and Laboratory 

for Crustacean Research, University of Louisiana 

at Lafayette, Lafayette, Louisiana 70504-2451, 

USA. Peter C. Dworschak, Naturhistorisches 

Museum in Wien, Burgring 7, A-1014 Wien, Austria. Rafael Lemaitre, Department of Invertebrate 

Zoology, National Museum of Natural History, 

MRC 163, Smithsonian Institution, Washington, 

D.C. 20013-7012, USA. Corresponding author: 

D. Felder (dlf4517@louisiana.edu). Manuscript 

received 13 May 2008; accepted 20 April 2009.

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182 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Concerted effort has been made to photographically 

document coloration of fresh specimens, given the value 

of color in the identifi cations of tropical species and the 

long-term goal of producing a guidebook for the regional 

decapod fauna (DLF and RL, in progress). More than 260 

decapod species have been enumerated in our collections 

from the Carrie Bow Cay region, some yet to be named. 

Under U.S. National Science Foundation AToL “Decapod Tree of Life” support, molecular and morphological 

systematic studies are under way concerning alpheid and 

other caridean shrimps, paguroid hermit crabs, thalassinidean shrimps, and panopeid, portunid, grapsoid, pinnotherid, and majoid crabs, as well as family-level relationships 

among all major decapod groups. Work incorporating 

porcelain crab collections from the region has been published (Rodríguez et al., 2005, 2006) as has work by other 

investigators on some alpheid shrimp groups (Duffy, 1996; 

Duffy and Macdonald, 1999; Duffy et al., 2000, 2002; 

Macdonald et al., 2006; Ríos and Duffy, 2007). Previous 

collections of upogebiid thalassinidean shrimp from Belize were included in Williams (1993). Several descriptions 

of new species from our Belize collections have also appeared (Goy and Felder, 1988; Manning and Felder, 1996; 

Felder and Manning, 1997), but many species remain to 

be described. The second author has been involved in 

several ecological studies of the infaunal decapods of the 

region (Dworschak and Ott, 1993; Abed-Navandi and 

Dworschak, 2005; Dworschak et al., 2006).

Our protracted fi eld sampling program has in some 

cases allowed us to observe apparent changes in community composition. In a striking example, shallow subtidal habitats at Twin Cays have been recently invaded 

by the nonindigenous swimming crab Charybdis hellerii

(A. Milne-Edwards, 1867), previously unreported from 

Belize. Recurrent trips have also provided opportunities 

for shallow subtidal sampling and burrow-casting of fossorial infauna in turtle grass (Thalassia) beds along shorelines of Twin Cays, revealing unexpected thalassinidean 

diversity. A brief account of these latest efforts is our present focus, preliminary to more comprehensive treatment 

of the full decapod assemblage.

MATERIALS AND METHODS

Sampling included the breaking of dead coral and 

conch shell rubble, netting, extraction of sediments, and 

sorting through hard-surface fouling organisms, but sampling of large crabs such as Charybdis hellerii (Brachyura) 

and its macrocrustacean associates was a targeted effort. 

These decapods were captured from under pieces of dead 

subtidal coral and debris that were lifted while snorkeling 

over and adjacent to seagrass (Thalassia) beds in water 1– 2 

m deep. Sampling of most thalassinideans and related decapod burrowers was accomplished with a suction extractor (yabby pump) and bag-sieve while wading, snorkeling, 

or SCUBA diving in water 0.5– 4 m deep. In addition to 

collections of Glypturus acanthochirus (Callianassidae) 

by suction extractor, some specimens of this species were 

obtained with “weighted line” traps (de Vaugelas, 1985). 

Specimens of Axiopsis serratifrons (Axiidae) were obtained by baiting animals to the apertures of their burrows, 

where they were captured by cutting off the burrow or by 

spearing the specimens. Casts of burrows were made as 

described by Dworschak and Ott (1993). Specimens were 

immobilized by immersion in chilled seawater or by narcotization with clove oil before photography. Photographs 

of specimens immersed in a pan of seawater were made 

with a Fuji Fine Pix S1Pro digital camera equipped with a 

60 mm macrolens while the subject was lighted by a combination of direct and refl ected sunlight or high-intensity 

5000°K fl uorescent photographic lamps. All specimens 

were subsequently preserved in several exchanges of 95% 

nondenatured ethanol and then stored in 75% nondenatured ethanol. Photographic voucher specimens were archived in the Zoological Collections of the University of 

Louisiana at Lafayette (ULLZ), and most other materials 

were deposited in the Smithsonian Institution– National 

Museum of Natural History (USNM). Some collections 

by the second author (especially thalassinideans) were deposited in the Naturhistorisches Museum in Wien, Austria 

(NHMW) and the Muséum National d’Histoire Naturelle, 

Paris, France (MNHN). For fi gured specimens, size is indicated as carapace width (cw) or carapace length (cl).

RESULTS AND DISCUSSION

INVASION BY CHARYBDIS HELLERII

Large bottom debris (waterlogged wood, discarded 

building materials, dead coral heads) typically provides 

cover for large reptants such as spiny lobsters (Panulirus

spp.), swimming crabs (Callinectes spp.), stone crabs (Menippe spp.), and large spider crabs (Mithrax spp.), especially in shallow well-lighted waters. Sampling of these 

environments at both Carrie Bow Cay and Twin Cays in 

October 2002 revealed no large decapods other than these 

genera. That same year, however, a small specimen of the 

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NUMBER 38 • 183

nonindigenous portunid crab Charybdis hellerii was found 

in an empty conch shell on the inshore side of Carrie Bow 

Cay, the fi rst such occurrence recorded in our sampling 

program.

In April 2007, sampling under large pieces of cover at 

Twin Cays was undertaken to obtain fresh materials of the 

aforementioned resident genera for genetic analyses. Initial 

sampling centered in the vicinity of the “Fisheries Camp” 

on the southeastern end of Twin Cays, where a storm had 

scattered sheets of metal building siding from the shoreline to depths of nearly 2 m. Inspections beneath 20 such 

sheets across this entire range of depths revealed none of 

the target species but at least seven variously sized individuals of the nonindigenous swimming crab C. hellerii.

Sampling was thereafter shifted to dead coral heads 

scattered among turtle grass beds on the northeast side of 

Twin Cays. A crude survey was there undertaken for coral 

heads in 1– 1.5 m depths, each head roughly 0.5– 0.7 m in 

diameter and separated from one another by roughly 6– 15 

m. Of the 25 coral heads inspected, 13 were uninhabited 

by large reptant decapods, 8 harbored large specimens of 

C. hellerii (Figure 1b), and four harbored only Menippe 

nodifrons Stimpson, 1859 (Figure 1a). Large single individuals of C. hellerii were found under 6 of the 25 heads 

that were lifted, a mating pair of C. hellerii was found 

under a single head, and a specimen of C. hellerii together 

with a large specimen of M. nodifrons was found under another head. No specimens of Mithrax spp., Callinectes spp., 

FIGURE 1. a, Stone crab Menippe nodifrons, male, 69.7 mm carapace width (cw), Twin Cays, Belize 10 

April 2007, ULLZ 8991. b, Invasive Indo-Pacifi c swimming crab Charybdis hellerii, male, 75.3 mm cw, Twin 

Cays, Belize, 10 April 2007, ULLZ 8990. c, Callianassid Eucalliax sp., female, 8.3 mm carapace length (cl), 

South Water Cay, 22 October 2002, ULLZ 9230. d, Polyester resin burrow cast from Twin Cays, probably assignable to Axianassa australis, cast length 85 cm, made by PCD, Twin Cays, Belize, August 1989, 

NHMW 24001. e, Laomediid Naushonia sp. female, 5.8 mm cl, Carrie Bow Cay, Belize, 3 April 2007, ULLZ 

8895. ULLZ, University of Louisiana at Lafayette; NHMW, Naturhistorisches Museum Wien. Photographs 

a– c and e by DLF; photograph d by PCD.

11_Felder_181-188_Lang.indd 183 1_Felder_181-188_Lang.indd 183 9/24/09 9:49/24/09 9:49
184 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

or Panulirus spp. were observed, despite these taxa being 

commonly found in such settings during 1983 and 2002.

Small or immature specimens of Charybdis hellerii

are easily confused with Cronius ruber (Lamarck, 1818) 

and to a lesser extent with Achelous tumidulus Stimpson, 

1871, both of which also occur in Belize and adjacent waters of the Caribbean, Gulf of Mexico, and other areas 

of the warm temperate Atlantic. This similarity led us to 

initially question the identity of the single small specimen 

collected in 2002, but it was confi rmed to be Charybdis 

hellerii by 16S mtDNA sequence analysis by comparing to 

other sequence data for the species (Robles et al., 2007; 

Mantelatto et al., 2009). Widely used diagnostic morphological characters that apply well to full-sized adults do 

not readily facilitate identifi cation of juveniles among these 

three species, and records of subadults could easily be in 

error if based on presently limited descriptions. At the very 

least, A. tumidulus differs from both C. ruber and Charybdis hellerii by lacking a striking posterior or posterodistal 

meral spine on the fi fth pereiopod (swimming leg) in all 

crab stages. Cronius ruber and Charybdis hellerii, however, share a strongly spined fi fth pereiopod, albeit with the 

spine usually occupying a relatively more distal position 

and being less posteriorly directed on the merus of Cronius 

ruber. The relative position of the spine is, however, diffi -

cult to distinguish in small juveniles. These two species also 

share the presence of small spinules bordering the posterior 

margin of the fi fth pereiopod propodus, although these spinules are of relatively larger size in Charybdis hellerii. This 

characteristic is readily evident in adults, where setation 

obscures small acute granules along the margins of the propodus in Cronius ruber, which are unlikely to be confused 

with the well-formed adult spinules of Charybdis hellerii

(see Figure 1b). In juveniles of Cronius ruber, microspination of this propodal margin is relatively stronger than in 

adults, and distinction from juveniles of Charybdis hellerii

is somewhat subjective, especially if one lacks comparative 

specimens of similar size. No feature in the carapace of 

early crab stages (Dineen et al., 2001: fi g. 24) appears to 

separate small individuals of these species.

Recent observations have revealed an ongoing invasion of C. hellerii into coastal western Atlantic locations, 

and its documented distribution must now include Belize 

along with Brazil, Venezuela, Colombia, Cuba, the Yucatán shelf of Mexico, both coasts of Florida, and other 

northern Atlantic U.S. coastal habitats through at least 

the Carolinas (Campos and Türkay, 1989; Gómez and 

Martínez-Iglesias, 1990; Hernández and Bolaños, 1995; 

Lemaitre, 1995; Calado, 1996; Mantelatto and Dias, 

1999; Dineen et al., 2001; Mantelatto and Garcia, 2001; 

Mantelatto et al., 2007; Robles et al., 2007; McMillenJackson, 2008; Felder et al., 2009). Clearly, the foregoing 

chronology of reports reveals continued western Atlantic 

range expansion for C. hellerii, although the potential 

trophic impacts of this invader remain poorly documented. The fi rst author has on two occasions observed 

individuals of C. hellerii in the Indian River Lagoon, Florida, feeding (inside shallow cavities of hard substrates 

that they occupied) on soft-shelled, postmolt individuals of native species of large decapods (one Callinectes, 

one Panulirus), and in another instance feeding on small 

mussels. As in the present report, all such observations 

and inferences of this invader’s potential competitive and 

predatory impacts in the western Atlantic remain very 

limited and anecdotal, but they serve to justify a call for 

controlled experimental studies.

THALASSINIDEANS

Our collections of cryptic burrowing thalassinideans 

from various habitats in the vicinity of Carrie Bow and Twin 

Cays, along with the few previously reported records, include 

at least 17 species representing the families Callianassidae, 

Laomediidae, Thomassiniidae, Axianassidae, Axiidae, and 

Upogebiidae. The species of these often overlooked groups 

are presented in the following list, with collection sites indicated as TC (Twin Cays), CB (Carrie Bow Cay), SW (South 

Water Cay), and SL (shorelines near Dangriga); catalogue 

numbers are shown for archived specimens.

INFRAORDER THALASSINIDEA SENSU LATO

Callianassidae (Ghost Shrimps)

Corallianassa longiventris (A. Milne-Edwards, 1870)— TC, 

CB: NHMW 6774, 6775, 15352– 15355; ULLZ 4228– 

4230, 6083, 8997.

Eucalliax sp.— TC, SW: ULLZ 9230.

Glypturus acanthochirus Stimpson, 1866— TC, CB: NHMW 

6765– 6770, 15338– 15342; MNHN Th 1181, Th 1185; 

ULLZ 8993– 8995, 9233; USNM 266241– 266244.

Lepidophthalmus richardi Felder and Manning, 1997— 

SL [near river mouths]: NHMW 15343– 15349: ULLZ 

3577, 5186– 5188, 8992; USNM 277777– 277779.

Neocallichirus grandimana (Gibbes, 1850)— TC, CB, 

SW: NHMW 6796– 6799, 15356– 15367; MNHN Th 

11_Felder_181-188_Lang.indd 184 1_Felder_181-188_Lang.indd 184 9/24/09 9:49/24/09 9:49
NUMBER 38 • 185

1182– 1184; ULLZ 8998, 9235– 9237, 9239– 9241, 

9243, 9244.

Neocallichirus maryae Karasawa, 2004— TC: ULLZ 

9234, 9238.

Laomediidae

Naushonia sp.— CB: ULLZ 8895, 8915.

Axianassidae

Axianassa australis Rodrigues and Shimizu, 1992— TC 

[identifi ed by burrow cast]: NHMW 24001.

Thomassiniidae

Mictaxius thalassicola Kensley and Heard, 1991— TC: 

ULLZ 9246.

Upogebiidae (Mud Shrimps)

Pomatogebia operculata (Schmitt, 1924— CB: ULLZ 9231.

Upogebia acanthura (Coêlho, 1973)— ?CB: USNM 251246.

Upogebia omissa Gomes Corrêa, 1968— TC, SL: ULLZ 

5165.

Upogebia sp.— CB: ULLZ 9232.

Axiidae (Lobster Shrimps)

Axiopsis serratifrons (A. Milne-Edwards, 1873)— CB: 

NHMW 6771– 6773, 15350– 15351: ULLZ 4232, 4233, 

5827, 8996; USNM 18905, 18907, 18908.

Coralaxius nodulosus (Meinert, 1877)— CB: USNM 

170856, 171764– 171766, 243431– 243434.

Paraxiopsis hispida Kensley, 1996— CB: USNM 211462.

Paraxiopsis spinipleura Kensley, 1996— CB: USNM 

211451.

Sediments in lower intertidal to subtidal seagrass beds 

at Twin Cays are densely populated by Neocallichirus 

grandimana, Glypturus acanthochirus, Corallianassa longiventris, Neocallichirus maryae, Mictaxius thalassicola, 

and Eucalliax sp., often burrowing more than 1 m into 

sediments. Dworschak and Ott (1993) previously analyzed 

burrow morphologies and distributions for three of these 

species, as well as for Axiopsis serratifrons and two species of pistol shrimp. Their food sources were investigated 

by stable isotope studies (Abed-Navandi and Dworschak, 

2005). Among the species from Twin Cays, M. thalassicola has not previously been reported from the northern 

Caribbean, and Eucalliax sp. (Figure 1c) represents an undescribed taxon presently known only from Belize.

The newly reported Neocallichirus maryae is a replacement name for the more familiar N. rathbunae (Schmitt, 

1935), which proved to be a junior primary homonym 

of a different fossil species (Karasawa, 2004). Although 

Sakai (2005) placed N. raymanningi Blanco Rambla and 

Lemaitre, 1999, in synonymy with N. rathbunae (Schmitt, 

1935), and N. raymanningi would thus predate recent establishment of N. maryae, we do not accept the presently 

limited evidence for this synonymy.

Ejecta from burrows of these thalassinideans dominates bottom topography in intertidal to shallow subtidal 

seagrass beds of this area, but along intertidal muddy shorelines at Twin Cays, especially those immediately adjacent 

to mangroves, it appears that the axianassid Axianassa 

australis also occurs. As no specimens have been captured, 

this can be deduced only from highly characteristic ejecta 

patterns and spiraled burrow casts (see Dworschak and 

Rodrigues, 1997; Felder, 2001), the latter obtained by the 

second author in 1989 (Figure 1d).

Neocallichirus grandimana appears to be the most 

widely distributed callianassid among sites sampled in the 

vicinity, inhabiting both vegetated and nonvegetated sediments. Together with Eucalliax sp., it densely populates 

sparsely vegetated calcareous sands of shallow shoals bordering South Water Cay in addition to sites at Twin Cays. 

At South Water Cay, upper reaches of its burrows are commonly inhabited by Processa sp. and early juvenile stages 

of Callinectes sp., the latter being uniquely pigmented an 

opaque bluish-black. Glypturus acanthochirus and Corallianassa longiventris range into deeper grass beds, where 

they appear to draw grass blades into their burrows. Distributions of all the collected thalassinideans depend on 

sediment characteristics, depths, vegetation, and water 

quality, whereas characteristic burrow architectures are 

both diagnostic of species and suggestive of ecological adaptations (Dworschak and Ott, 1993, Abed-Navandi and 

Dworschak, 2005; Dworschak et al., 2006). Less conspicuous evidence of sediment ejecta characterizes areas among 

seagrasses that are burrowed primarily by nonthalassinidean 

decapods such as the Alpheus spp. reported by Dworschak 

and Ott (1993). Surface features of these burrows can be all 

11_Felder_181-188_Lang.indd 185 1_Felder_181-188_Lang.indd 185 9/24/09 9:49/24/09 9:49
186 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

but indistinguishable from those made by what appear to 

be several species of Upogebia, including U. omissa.

The assemblage of upogebiids in the Carrie Bow Cay 

region remains poorly understood. It appears that Upogebia omissa ranges widely here, from the shoreline along the 

mainland to offshore cays, and the fi rst author has identifi ed specimens taken as “pests” from commercial penaeid 

shrimp farms on the mainland. General treatment of western Atlantic upogebiids by Williams (1993) included records of U. acanthura from a patch reef southwest of Carrie Bow Cay and U. brasiliensis Holthuis, 1956 from more 

distant shoreline areas of Belize, although our collections 

have produced no additional specimens. Two other species listed by Williams (1993) from nearby coastal environments of Quintana Roo (U. corallifora Williams and 

Scott, 1989 and U. vasquezi Ngoc-Ho, 1989) could also 

be expected in Belize, although we have yet to fi nd them. 

Specimens of this genus from coralline rubble just off the 

reef crest at Carrie Bow Cay (ULLZ 9232) and other uncatalogued specimens from Twin Cays (in areas also burrowed by alpheid shrimp) cannot confi dently be assigned 

to known species and warrant further study. Generally 

found in deeper subtidal habitats (Felder et al., in press), 

the upogebiid Pomatogebia operculata ranges into waters 

as shallow as 2 m depth off Carrie Bow Cay and likely occurs elsewhere between cays in appropriate deeper calcareous rubble habitats; these have been collected by breaking 

open highly eroded pieces of coralline rubble to expose the 

muddy interstices and cavities occupied by this upogebiid.

Axiids are also found in association with rubble and 

reef structures of outer cays, as, for example, at Carrie 

Bow. The widely distributed Coralaxius nodulosus, a 

small-sized species inhabiting cavities in subtidal coralline 

rubble from the fore-reef (see also Kensley, 1994), is routinely found along with the upogebiid Pomatogebia operculata in interstices of broken rubble retrieved from depths 

greater than 2 m. By contrast, the large and strongly armed 

Axiopsis serratifrons is widely distributed between pieces 

of coarse coral rubble in back-reef fl ats of Carrie Bow 

(0.5– 2 m depths), there positioned to ambush prey from 

its somewhat concealed burrow aperture. In addition, two 

new species of Paraxiopsis described by Kensley (1996) 

both range into reef habitats of Carrie Bow Cay. Although 

P. spinipleura was originally found there in shallow (1.5 

m) back-reef rubble, we have not encountered additional 

specimens. We have also not found additional materials 

of P. hispidus, previously collected at the reef drop-off in 

depths greater than 20 m.

A remarkable thalassinidean fi nd at Carrie Bow was 

the April 2007 discovery of a laomediid assignable to 

Naushonia sp. (Figure 1e). Two specimens were captured, both from cavities of empty conch shells in shallow (1.5 m) subtidal waters. These individuals appear 

to also represent an undescribed species of a rarely encountered genus in the northern Caribbean region. To 

date known only from Carrie Bow Cay, they are currently being described.

The thalassinidean fauna of the general region also 

includes an abundant nearshore species, Lepidophthalmus 

richardi, adapted to euryhaline waters and muddy sand 

shorelines of the Stann Creek District (Felder and Manning, 1997). This species has not been found in habitats 

immediately associated with Twin Cays or Carrie Bow 

Cay, despite intensive search.

These collections have allowed us to update and expand the burrow distribution schemes for Belize given by 

Dworschak and Ott (1993). We herewith add additional 

taxa and habitat distributions (Figure 2) to underscore the 

overlooked diversity of infaunal macrocrustaceans, some 

of which are dominant bioturbators.

NOTE ADDED IN PRESS

Additional sampling in Belize was conducted in February 2009. Observations in shallow waters at Twin Cays 

confi rmed that populations of Charybdis helleri remained 

as seen in 2007. Further sampling for thalassinideans supported accounts on the preceding pages, with noteworthy 

additions. Sampling among shoreline mangrove roots at 

Twin Cays produced the fi rst specimens of the Axianassidae, representing new records for Axianassa intermedia Schmitt, 1924. Five such specimens were extracted 

by yabby pump from beneath a surface area of no more 

than 0.25 m2 at low tide, but less productive adjacent 

sampling suggested heterogeneous patterning. Given the 

small size of these specimens, we question whether this 

species accounts for burrows provisionally attributed to 

A. australis on the basis of castings mentioned on the 

preceding pages. From these same habitats at Twin Cays, 

the fi rst specimen of the callianassid Biffarius fragilis

(Biffar, 1970) was captured, along with a specimen of the 

same Naushonia sp. reported from Carrie Bow Cay on 

preceding pages. Finally, the fi rst specimen of the family 

Callianideidae, Callianidea laevicauda Grill, 1959, was 

taken from intertidal rubble of the exposed reef crest at 

Carrie Bow Cay. These latest efforts confi rm presence 

of at least one species of the family Axianassidae, add 

a seventh thalassinidean family to our report, and bring 

the documented number of thalassinidean species in our 

survey to at least 19.

11_Felder_181-188_Lang.indd 186 1_Felder_181-188_Lang.indd 186 9/24/09 9:49/24/09 9:49
NUMBER 38 • 187

ACKNOWLEDGMENTS

We are grateful to the late R. Manning and B. Kensley 

for assistance in fi eld collections. We thank S. De Grave, 

E. Palacios-Theil, and B. Thoma for assistance in recent efforts. Research was supported under several travel grants 

to the authors from the Smithsonian Caribbean Coral Reef 

Ecosystems (CCRE) Program and from National Science 

Foundation grants DEB-0315995 and EF-0531603 to 

the fi rst author. This work is contribution number 825 of 

the Caribbean Coral Reef Ecosystems Program (CCRE), 

Smithsonian Institution, supported in part by the Hunterdon Oceanographic Research Fund.

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Imposex in One of the World’s Busiest 

Shipping Zones

Carter Li and Rachel Collin

ABSTRACT. Tributyltin pollution from antifouling paint is well known to disrupt the endocrine system in female marine gastropods. The masculinization of females, including the 

aberrant growth of a penis and vas deferens and occlusion of the capsule gland, has been 

reported primarily in neogastropods and is particularly well documented in muricids. Compared to temperate areas, few studies of imposex have been undertaken in the tropics, and 

there are few studies in general on non-neogastropods. Here we report a high frequency of 

imposex near the Pacifi c mouth of the Panama Canal in two species of muricids and two 

species of calyptraeids. The frequency of imposex declined rapidly with distance away from 

the canal, and several species appeared to be mostly normal less than 10 km from the entrance. This is the fi rst report of imposex in Acanthais brevidentata, Thaisella kiosquiformis, 

Bostrycapulus calyptraeformis, Crepidula cf. nivea, and Anachis fl uctuata. Because imposex 

has not previously been reported for the Calyptraeidae, a family of protandrous gastropods, 

a laboratory study was conducted to verify that imposex was not simply retention of the 

penis after sex change. The 2007 ratifi cation of the International Maritime Organization’s 

convention on antifouling systems should reduce the levels of TBT worldwide, but the persistence of this compound in sediments suggests that imposex may continue to be a problem at 

the mouth of the canal as routine dredging and large tides frequently resuspend sediment.

INTRODUCTION

Tributyltin (TBT) is well known to be a highly effective antifouling agent, 

used primarily on ship hulls, but it has numerous detrimental effects on a wide 

variety of non-target taxa. Despite having demonstrable effects on molluscan 

shell growth (Alzieu et al., 1981), embryological development of fi sh and marine 

invertebrates (Hano et al., 2007; Inoue et al., 2006), neurulation in ascidians 

(Dolcemascolo et al., 2005), and testosterone metabolism in mysids (Verslycke 

et al., 2003), the most well studied and widespread effect is the disruption of the 

endocrine system in marine gastropods. Exposure to very low levels (as little as 

0.5 ng/L) of TBT causes the masculinization of females, including the aberrant 

growth of a penis and occlusion of the capsule gland (Gibbs and Bryan, 1996). 

This condition is referred to as imposex, and severe cases can lead to reproductive failure. For example, an extreme case of population decline as a result of imposex has been demonstrated for Nucella lapillus in southwest England (Bryan 

et al., 1986; Gibbs and Bryan, 1986).

Carter Li, Department of Biology, McGill University (current address: Department of Surgery, 

Montreal General Hospital). Rachel Collin, Smithsonian Tropical Research Institute, MRC 0580-08, 

Unit 9100, Box 0948, DPO AA 34002, USA. 

Corresponding author: R. Collin (collinr@si.edu). 

Manuscript received 21 July 2008; accepted 20 

April 2009.

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190 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

In a recent review, Shi et al. (2005) reported that 

imposex has been recorded in 170 species of gastropods 

from 28 families. The vast majority, 134 species, are 

neogastropods. Among the non-neogastropod, caenogastropod families, ampullarids, rissioids, cypreaids, cymatids, and tonnids all contain several species for which 

imposex has been reported (Shi et al., 2005). Although 

the taxonomic coverage is wide, much of the basic information on imposex in relation to TBT pollution is 

centered on muricids, buccinids, and conids (Fioroni et 

al., 1991; Shi et al., 2005). On a worldwide scale, it is 

necessary to extend the scope of studies to include more 

tropical forms and locations (Ellis and Pattisina, 1990) 

to get a global picture of the effects of TBT pollution on 

gastropods.

The Panama Canal is one of the world’s busiest shipping zones, and commercial transport through the canal 

represents about 5% of world trade. About 14,000 vessels 

pass through the Canal annually (statistics available from 

the Autoridad del Canal de Panama web site http://www

.pancanal.com/), and the most common shipping route is 

between the east coast of North America and Asia. Most of 

the shipping traffi c is composed of large, oceangoing vessels, which have not previously been subject to restrictions 

on the use of tributyltin antifouling paint. The entrance to 

the Canal, on the Pacifi c coast adjacent to Panama City, 

was the site of Rodman Naval Base (1943– 1999), and 

is currently the site of the container port of Balboa and 

a shipyard. The anchorage for the canal commonly has 

more than 30 vessels waiting to transit the Canal. The substrate in this area is primarily a mix of rocky debris and 

sandy mud in the intertidal and fi ne mud in the subtidal. 

With the consistently high levels of shipping traffi c, frequent dredging, and muddy substrate (which is known to 

retain TBT for years, as reviewed in de Mora, 1996), the 

local levels of TBT and, therefore, imposex are expected 

to be higher around the entrance to the Canal than they 

are along the open coast. We conducted a survey of four 

common intertidal gastropod species around the mouth of 

the canal to document the levels and geographic extent of 

imposex in this area.

MATERIALS AND METHODS

Gastropods were collected between February and 

April 2005 from four sites along the Pacifi c coast of 

Panama at varying distances from the mouth of the Panama Canal (Figure 1). The site closest to the mouth of 

the canal consisted of rocky outcrops near Farfan beach 

(8.93°N, 79.58°W) and the Bridge of the Americas. Progressively further away to the west were Isla Venado 

(8.91°N, 79.63°W), Chumical (8.5°N, 79.66°W), and 

Bique (8.90°N, 79.66°W). In November 2007 additional 

samples were collected from Punta Culebra (8.91°N, 

79.53°W), which faces the entrance to the Canal and is at 

the edge of the Canal anchorage.

We collected four species, which were clearly identifi able and abundant at two or more of the sites. Efforts 

were made to collect the same species from all sites, but 

because of the habitat heterogeneity in the area, we were 

not able to collect suffi cient numbers of females for statistical analyses for several sites. Adequate samples were 

collected for the muricids Acanthais brevidentata (Wood, 

1828) from Farfan and Chumical and Thaisella kiosquiformis (Duclos, 1832) from Farfan and Bique, and the 

calyptraeids Bostrycapulus calyptraeformis (Deshayes, 

1830) and Crepidula cf. nivea from Farfan, Venado, and 

Chumical (Table 1).

Shell length was measured with vernier calipers, 

and live snails were extracted from their shells. The reproductive system was immediately examined under a 

stereomicroscope, and the sex was determined based on 

characteristics of the gonad and presence or absence of 

seminal receptacles and seminar vesicles. If the sex was 

not easily identifi ed, sex was verifi ed by examining gametes from a smear of gonad. The length of the penis (if 

present) was measured using an ocular micrometer on a 

stereomicroscope.

FIGURE 1. Map of the study area at the entrance to the Panama 

Canal. Arrows indicate the sites of sample collection and locations 

mentioned in the text.

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NUMBER 38 • 191

Signifi cant differences in the frequency of imposex between the entrance to the Canal and more distant sites 

were tested for using Fisher’s exact test. Analysis of covariance (ANCOVA) was used to examine the relationship between penis length in male and imposex females, 

with shell length as a covariate for samples collected from 

Venado and Farfan. Because samples from Culebra were 

preserved in ethanol before examination, the penis length 

from these samples could not be directly compared to the 

others that were measured fresh.

Experiments to determine if imposex develops in adult 

snails after exposure to ambient water levels of TBT were 

conducted at STRI’s Naos Marine Laboratories, only a 

few hundred meters from the Culebra site. Anachis fl uctuata (Sowerby, 1832) and Bostrycapulus calyptraeformis

were both collected from Isla Venado, an area with low 

levels of imposex, and maintained in the laboratory. Sixty 

adult Anachis fl uctuata were kept in a 100 L fi berglass 

tank in the outside seawater system and fed frozen commercial clams once a week. After fi ve months the animals 

were killed and levels of imposex were determined as already described. Bostrycapulus calpytraeformis were collected as small males. They were maintained in pairs in the 

laboratory in 350 mL plastic cups. The water was changed 

every other day and the animals were fed 10 mL Isochrysis 

galbana culture every day. Animals were measured every 

four weeks, and their sexual state was recorded on the 

basis of external features. The experiment was terminated 

after 400 days. Both species were cultured using the same 

source of seawater (from the side of Isla Naos away from 

the Canal entrance), and neither was exposed to local sediment other than that which settled out of the seawater.

RESULTS

FIELD COLLECTIONS

Imposex was detected in all four species. In the two 

muricids, the imposex was almost always in the early 

stages with limited penis development and no indication 

of any occlusion of the capsule gland. We never observed 

imposex that was so far advanced that the females were 

found to retain eggs or that an obvious vas deferens had 

developed. Imposex in the calyptraeids was more developed; penes were large in many specimens and could easily 

be confused with a normal male penis. Several imposex females of Bostrycapulus calyptreaformis and Crepidula cf. 

nivea were observed brooding egg capsules, showing that 

imposex females were not sterile. Near the entrance of the 

Canal the frequency of imposex ranged from 25% to 50% 

in muricids and was greater than 80% in calyptraeids. The 

number of females collected for each species at each site and 

the frequency of imposex are given in Table 1. In all cases 

the frequency of imposex was signifi cantly higher near the 

entrance to the Canal than at farther sites (Table 1).

Acanthais brevidentata: Because there were no imposex 

individuals in Bique and because animals from that site 

were signifi cantly larger (mean 28.9 mm) than from 

Farfan (mean 26.9 mm; P  0.001), comparisons of 

imposex females with normal males and females were 

conducted for data collected from Farfan only. Imposex 

females were signifi cantly larger (length 30.1 mm) than 

non-imposex females (length 26.4 mm; P  0.02). 

ANCOVA showed that there were signifi cant effects 

of shell length (P 0.01) and imposex (P  0.001) on 

TABLE 1. Frequency of imposex in four gastropod species at sites arranged here from nearest to furthest from the 

Panama Canal entrance. Frequency at each site was compared to that at Farfan (the site at the entrance to the Canal) 

using a Fisher’s exact test. A one-tailed test was used, but two-tailed results did not differ; * P 0.001; ** P 0.0001; 

*** P  0.0001.

 Site

Species Farfan Culebra Venado Chumical Bique

Muricids 

 Thaisella kiosquiformis 29/53 –––13/52*

 Acanthais brevidentata 8/32 ––0/57** – 

Calyptraeids 

 Bostrycapulus calyptraeformis 60/63 22/43a*** 2/79*** 1/122*** – 

 Crepidula cf. nivea 87/90 19/22 –0/99*** – 

a Signifi cantly different from Venado and Chumical <0.0001.

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192 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

penis length as well as a signifi cant interaction effect 

(P  0.04). Penes of imposex females were smaller than 

those of normal males, and male penis length increased 

with shell length, although imposex penis length was not 

associated with shell length (Figure 2).

Thaisella kiosquiformis: Animals from Bique and Farfan did 

not differ in size, nor did the sexes differ in size. Imposex 

females were also the same size as non-imposex females. 

The average size for all categories was 26– 27 mm. Data 

from Bique and Farfan were combined for the analysis. 

ANCOVA showed that there were signifi cant effects of 

shell length (P  0.0001) and imposex (P  0.0001) 

on penis length as well as a signifi cant interaction effect 

(P 0.003). Penes of imposex females were smaller 

than those of normal males, and penis length increased 

with shell length in both sexes (Figure 2). There was a 

signifi cant incidence of imposex at Bique, despite it being the site furthest from the Canal. We attribute this 

relatively high frequency of imposex to this site’s proxFIGURE 2. Relationship between shell length and penis length for males (white diamonds) and imposex females (black dots) of Acanthais 

brevidentata, Thaisella kiosquiformis, Crepidula cf. nivea, and Bostrycapulus calyptraeformis.

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NUMBER 38 • 193

TABLE 2. Frequency of imposex from fi eld-collected and laboratory-reared snails.

 Fisher’s exact test,

Species Laboratory Venado Chumical P value

Anachis fl uctuata 2/29 1/133 – P 0.091

Bostrycapulus calyptraeformis 10/24 2/79 1/122 P  0.0001,  0.0001

imity to a dry dock facility slightly further to the west 

in Vacamonte.

Crepidula cf. nivea: Calyptraeids are protandrous hermaphrodites (Collin, 2006) and the small animals are almost 

always males; therefore, we did not make as much effort 

to collect the smallest animals as we did in the other species. The size of females differed signifi cantly between 

the sites (16.1 mm for Chumical vs. 19.6 mm for Farfan; 

P  0.0001). Imposex females were larger than nonimposex females. Because all females at Chumical were 

normal and virtually all in Farfan had imposex, this size 

difference cannot be distinguished from a site effect on 

size. An ANCOVA showed that shell length had a signifi cant effect on penis length (P 0.03), that imposex 

females and males did not differ in penis length as there 

was considerable penis growth in the imposex females, 

and that there was no signifi cant interaction between imposex status and shell length (see Figure 2). Although 

there were signifi cant levels of imposex in samples from 

Culebra, in all these cases the penis was very small; they 

were not much more developed than a small bump at 

the base of the tentacle, whereas those from Farfan were 

often as long as or longer than the tentacles.

Bostrycapulus calyptraeformis: The average size of females differed signifi cantly among the three sites (17.5 

mm at Chumical; 16.5 mm at Venado; 20.6 at Farfan; 

P  0.01). Again, because nearly all the females in Farfan had imposex but no imposex was detected in the 

other locations, the larger size of imposex females may 

have been a site effect. ANCOVA analysis of animals 

from Farfan showed that there was a signifi cant effect 

of imposex on penis length (P  0.001), and imposex 

females had smaller penes than males. Shell length and 

the interaction between shell length and imposex had 

no signifi cant effect on penis length. The level of imposex in animals from Culebra was again very rudimentary, with penes little more than a nub at the base 

of the tentacle.

In summary, all four species showed signifi cant higher 

rates of imposex near the entrance of the canal. By 20 km 

away, rates were generally of the order of 1%– 2%. In the 

two muricids and one of the calyptraeids, the penes of 

imposex females were smaller than those of similar-sized 

males. In the two muricids and the other calyptraeid, shell 

length was a signifi cant covariate of penis length, and in 

two species the penis length of imposex females increased 

with shell length.

LABORATORY EXPERIMENTS

After fi ve months in the laboratory, 2 of 29 female 

Anachis fl uctuata had developed penes, indicating that 

this species can develop imposex. However, this was not 

statistically signifi cantly different from the frequency of 

imposex in the fi eld in Venado (P 0.09; Table 2). No 

comparisons to the entrance to the Canal could be made 

because this species could not be found there.

Of the 60 Bostrycapulus calyptraeformis that were 

raised in the laboratory, the largest animals in 6 of the 30 

cups retained penes throughout the experiment and did 

not change to become female. In the remaining 24 cups, 

the larger of the 2 animals lost the penis, indicating sex 

change from male to female. Of these 24 animals, 10 lost 

the penis and then subsequently regained it 1 to 3 months 

after sex change. In many cases the penis was not as long 

or thick as a normal male penis, but they were fairly large, 

and casual observers would be likely to categorize such 

animals as males (Figure 3). The largest animals in the remaining 14 cups underwent transition to normal females 

and did not develop imposex before the end of the experiment. The smaller of the 2 animals in each cup was not 

examined, as they usually remain male in the presence of 

the larger animals (Collin et al., 2005).

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194 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

DISCUSSION

Imposex was found in all snail species examined 

from the mouth of the Panama Canal, and in all cases 

the frequency and severity of imposex declined with distance away from the Canal. The frequency of imposex 

differed among the species examined, with calyptraeids 

more likely to display imposex than the muricids. Calyptraeids showed higher frequencies of imposex at the 

mouth of the Canal, and the penes of imposex females 

were much more fully developed then we ever observed 

in muricids. Species differences in sensitivity both to TBT 

(Wilson et al., 1993; Tan, 1999) and to its bioaccumulation (Liu et al., 1997) have been demonstrated in other 

surveys. Liu et al. (1997) found that imposex was much 

more severe in Thais species than Morula, despite similar 

organotin burdens, and suggested a genus-specifi c susceptibility to organotin pollution with the ranking order of 

Nucella, Thais, and Morula. The differences in habitat 

(high on the intertidal versus low on the intertidal), diet, 

and physiology have been suggested as causes of interspecifi c differences in imposex (Tan, 1999). If TBT were 

primarily waterborne either in solution as bis(tributyltin) 

oxide or adsorbed by suspended solids (de Mora, 1996) at 

our study sites, it is possible that fi lter-feeding calyptraeids 

would be exposed to more TBT, by fi ltering large volumes 

of water, than would other gastropods. Suspended particles may have TBT adhered to them and may be captured 

in the mucous net and ingested during fi lter feeding, thus 

increasing the exposure of calyptraeids relative to the muricids. These scenarios are not in agreement with a number 

of laboratory studies (Bryan et al., 1989; see Gibbs and 

Bryan, 1996, for review) that show that TBT accumulates 

more rapidly from the diet than from the ambient water 

and which suggest that carnivores could accumulate more 

TBT from their diet than would herbivores. However, 

controlled experimental comparisons of bioaccumulation 

between carnivorous and suspension-feeding gastropods 

have not been made, and the effects of suspended solids 

have not been examined.

Another factor that can infl uence the expression of 

imposex is age. Because extended exposure to TBT is necessary to elicit imposex, those species that are longer lived 

or slower growing may be more likely to have high levels of TBT and thus exhibit imposex. Studies have also 

shown that juvenile snails are more sensitive to TBT than 

are adults (Gibbs and Bryan, 1996). Our data for Acanthais brevidentata, showing that females with imposex are 

larger than normal females, are consistent with either increase in imposex development with long-term exposure 

or recent reductions in TBT levels. However, Thaisella 

kiosquiformis did not show this pattern. Few data on the 

FIGURE 3. A, B. Photographs of two individuals with well-developed imposex in Crepidula cf. nivea from 

Farfan, with penis (p) and female genital papilla (fgp) indicated in each image. B. The female genital papilla 

can be confused with the anus (a), which is usually obscured by the gills; brooded eggs are visible as the light 

mass in this image.

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NUMBER 38 • 195

age or lifespans of tropical gastropods are available and so 

this possibility is diffi cult to evaluate. However, Panamanian calyptraeids grown in the laboratory generally reach 

maturity at sizes similar to animals that matured in the 

fi eld, in less than a year (Collin et al., 2005, and personal 

observation), and it seems unlikely that TBT in the sediment, which has a half-life of years, would have changed 

drastically in such a short interval.

Imposex has not been previously reported in calyptraeid gastropods. Because animals normally change from 

males to females and transitional animals may sometimes 

retain a penis while also showing well-developed female reproductive structures, it is possible that imposex individuals 

have previously been misidentifi ed as undergoing the normal transition between the male and females phases. Here 

we found, in sites with low expected TBT exposure, that 

there are virtually no individuals that display both male and 

female characteristics at the same time. In addition, our laboratory studies show that during sex change the penis can 

be reabsorbed and that the penes of imposex individuals 

can grow following this reabsorption. These results show 

that the abundant large females with penes collected at the 

entrance to the Canal are indeed imposex females and not 

transitional individuals that have yet to lose the penis.

Numerous studies have shown a tight relationship between levels of TBT in the environment, levels of 

TBT in gastropod tissues, and the frequency of imposex 

within species (Gibbs et al., 1987; Horiguchi et al., 1994; 

Minchin et al., 1997; Ruiz et al., 1998). However, the relationships between sites, species, and the different types 

of triorganotins are not always simple (Ide et al., 1997). 

Imposex has also been shown to be a more sensitive way 

to detect TBT than many chemical detection methods, and 

imposex has been used as a bio-indicator when TBT levels are too low for easy analytical detection (Gibbs and 

Bryan, 1996). Despite an extensive literature on the relationship between TBT and imposex, one study (Nias et 

al., 1993) indicates imposex could result from exposure 

to paint matrix or copper. However, this result has not 

been pursued or elaborated. Although we could not measure levels of TBT directly at the sites around the Canal, 

it can, in the light of this literature, be inferred with some 

level of confi dence that the exposure of animals to TBT 

is higher at the entrance to the Canal than it is in the surrounding areas. Despite the high levels of shipping and 

presumably high levels of TBT leaching into the surrounding water, the development of imposex was not so severe 

as has been reported for areas with high shipping traffi c 

in Europe and Asia, and TBT does not have an extreme 

impact on reproduction by occluding the pallial oviduct 

or splitting the bursa copulatrix and capsule gland, as has 

been reported from these regions (Oehlmann et al., 1996; 

Shi et al., 2005). Less obvious effects on reproduction were 

not directly evaluated in this study. The high amount of 

fl ushing in the area, from large volumes of discharge from 

the Canal and the 6 m tides, may help to prevent local 

buildup of high concentrations of TBT in this partially enclosed area.

In 2002 the International Maritime Organization 

adopted a Convention on Antifouling Systems (AFS) that 

called for a global prohibition of the application of organotin compounds as biocides in antifouling systems on 

ships by 1 January 2003 and a complete prohibition by 1 

January 2008. However, the prohibition was only to be 

implemented 12 months after 25 states representing 25% 

of the world’s merchant shipping tonnage ratifi ed it. In 

September 2007 this quota was met when Panama ratifi ed the convention, and therefore these regulations went 

into effect in September 2008. As the AFS convention applies to ships fl agged in, operated by, or docking in states 

that have ratifi ed it, the convention should signifi cantly 

reduce the exposure of Panama’s marine habitats to TBT 

pollution in the coming years. This regulation is especially 

important because the planned expansion of the Canal in 

2014 will signifi cantly increase shipping traffi c along both 

the Pacifi c and Caribbean coasts of Panama.

ACKNOWLEDGMENTS

We are grateful to L. Weintraub and M. Salazar for assisting with fi eld collections of animals, M. deMaintenon 

for verifying the identifi cation of the columbellid samples, 

and M. Torchin for sharing his knowledge of gastropod 

reproductive systems. We thank the Autoridad Maritima 

de Panama for providing collecting permits. This project 

was conducted during a McGill University Field Semester 

in Panama.

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Minchin, D., B. Bauer, J. Oehlmann, U. Schulte-Oehlmann, and C. G. 

Duggan. 1997. Biological Indicators Used to Map Organotin Contamination from a Fishing Port, Killybegs, Ireland. Marine Pollution Bulletin, 34:235– 243.

Nias, D. J., S. C. McKillup, and K. S. Edyvane. 1993. Imposex in Lepsiella vinosa from Southern Australia. Marine Pollution Bulletin, 

26:380– 384.

Oehlmann, J., E. Stroben, and P. Fioroni. 1996. “New Facts About Tributyltin-Induced Imposex in Prosobranchs: General Aspects.” In Molluscan Reproduction: Malacological Review, Supplement 6, ed. N. H. 

Runham, W. H. Heard, and J. B. Burch, pp. 149– 156. Ann Arbor, 

Mich.: Society for Experimental and Descriptive Malacology.

Ruiz, J. M., M. Quintela, and R. Barreiro. 1998. Ubiquitous Imposex 

and Organotin Bioaccumulation in the Gastropod Nucella lapillus

from Galicia (NW Spain): A Possible Effect of Nearshore Shipping. 

Marine Ecology Progress Series, 164:237– 244.

Shi, H. H., C. J. Huang, S. X. Zhu, X. J. Yu, and W. Y. Xie. 2005. 

Generalized System of Imposex and Reproductive Failure in Female 

Gastropods of Coastal Waters of Mainland China. Marine Ecology 

Progress Series 304:179– 189.

Tan, K. S. 1999. Imposex in Thais gradata and Chicoreus capucinus

(Mollusca, Neogastropoda, Muricidae) from the Straights of Johor: 

A Case Study Using Penis Length, Area and Weight As Measures of 

Imposex Severity. Marine Pollution Bulletin, 39:295– 303.

Verslycke, T., S. Poelmans, K. De Wasch, J. Vercauteren, C. DeVos, L. 

Moens, P. Sandra, H. De Brabander, and C. Janssen. 2003. Testosterone Metabolism in the Estuarine Mysid Neomysis integer (Crustacea; Mysidacea) Following Tributyltin Exposure. Environmental 

Toxicology and Chemistry, 22:2030– 2036.

Wilson, S. P., M. Ahsanullah, and G. B. Thompson. 1993. Imposex in 

Neogastropods: An Indicator of Tributyltin Contamination in Eastern Australia. Marine Pollution Bulletin, 26:44– 48.

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Shorefi shes of the Tropical Eastern Pacifi c 

Online Information System

D. Ross Robertson

ABSTRACT. Shorefi shes of the Tropical Eastern Pacifi c Online Information System 

(SFTEP) version 1, 2008, provides an online electronic identifi cation guide and information system for the known fauna of shorefi shes found in the Tropical Eastern 

Pacifi c. SFTEP allows users (i) to identify all shorefi shes known from the Tropical 

Eastern Pacifi c (TEP) (1,287 species in version 1) and (ii) to analyze and conduct 

biogeographic research on the composition of that fi sh fauna at varying spatial scales. 

Tools for identifi cation emphasize the use of color photographs, along with descriptive 

text that highlights key morphological features; allow comparison of similar species; 

facilitate identifi cation of unfamiliar species using information on location and fi sh 

morphology (shape, color pattern, and color); and incorporate interactive keys to 

members of two species-rich families (Gobiidae, Sciaenidae) that have many similarlooking species. To accommodate nonspecialist users, scientifi c jargon is minimized; 

the interface is intuitive and user-friendly, and searches for species can be made using 

common names. The Research Engine, which provides information about the composition of local faunas and the regional fauna, allows users to compare geographic 

ranges of multiple taxa, to construct faunal lists of taxonomic and functional groups 

of species for single and paired sites, and, at varying spatial scales, to determine local 

endemism and to display region-wide patterns of species richness of different taxa and 

functional groups of fi shes. The system is accessible online at www.stri.org/sftep.

INTRODUCTION

Shorefi shes of the Tropical Eastern Pacifi c Online Information System 

(SFTEP), version 1, 2008, provides an online electronic identifi cation guide 

and information system for the known fauna of shorefi shes found in the Tropical Eastern Pacifi c (TEP). This version represents the latest iteration of a 

series that began with the 1994 English-language printed identifi cation guide 

of the same name (Allen and Robertson, 1994). That book was followed by a 

Spanish-language printed edition in 1998 (Allen and Robertson, 1998). Both 

these works were succeeded by a dual-language CD-based information system 

in 2002 (Robertson and Allen, 2002), which was revised and expanded in 

2006 (Robertson and Allen, 2006).

D. Ross Robertson, Smithsonian Tropical Research Institute, Unit 0948, APO AA 34002 

(drr@stri.org). Manuscript received 15 August 

2008; accepted 20 April 2009.

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198 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

SYSTEM FEATURES

DUAL LANGUAGE INTERFACES

The system incorporates separate, full-capability English- and Spanish-language interfaces.

AIDS TO VISUAL IMPAIRMENT

The system incorporates two types of aids:

1. Variable map-color formats are available. Users can select various color schemes designed to accommodate 

different patterns of color blindness, including monochrome or color with the ability to select colors.

2. Page layout structure accommodates variation in font 

size. Two page layouts are possible—landscape and 

portrait. Page structure is stable over a threefold range 

in font size.

SYSTEM MODULES

HOME

The home page provides an overview of the capabilities of the system and access to all major modules through 

buttons and/or tabs that act as shortcuts (Figure 1). In addition there are links to several modules not accessible from 

other parts of the system: to the Copyright notice, a switch 

to change between English and Spanish interfaces, and to 

the websites of the Smithsonian Tropical Research Institute

and Coeus, the company that programmed the system.

Each of the authors and major contributors of information directly related to the construction of SFTEP has 

an individual contributor page, accessible from the Contributors button and from a link at the top of any screen.

In addition, the major contributors of information presented on each family are noted on each family page.

GENERAL INFORMATION

General information about Shorefi shes of the Tropical Eastern Pacifi c Online Information System (SFTEP) is 

shown in Figure 2; this module includes three sections.

Introduction

The “Introduction” to the TEP and its shorefi sh fauna 

provides background information on the oceanography of 

the region and its marine habitats (geographic and temporal variation in climate, rainfall and salinity, primary 

production and coastal upwelling systems, ocean current 

systems, infl uences of the El Niño cycle, shoreline habitats 

and rocky and coral reefs in the region); a history of taxonomic fi sh guides, major modern guides, global online resources, systematic ordering of the fi shes, and the scientifi c 

and common names of fi shes); the ecology of TEP shorefi shes (species that occur in the upper 100 m of the water 

column over the continental shelf or within ~50 km of the 

shore), their use of different environments and habitats, 

their depth-distribution patterns, their dietary groupings, 

and their modes of reproduction; and the zoogeography of 

the fauna— studies of the region’s zoogeography, resident 

versus vagrant species, relationships of the fauna to the 

faunas of other areas, distribution of the fauna in different climate zones, the geography of variation in species 

richness and local endemism throughout the region, and 

biogeographic subdivisions of the TEP.

Features & User Guide

The “Features & User Guide” section describes system 

features, providing information available on taxon pages, 

databases on biological and zoogeographic characteristics, 

information used to identify fi shes, an interactive glossary 

of ichthyological terms, the functioning of the zoogeographic research engine (comparison of taxon ranges, assembly of faunal lists, determination of local endemism, 

assembly of maps of species richness and sampling intensity, assembly of lists of species from predefi ned parts of 

the TEP), the functioning of the interactive library, the 

database of images, and credits to contributors.

Acknowledgments

The “Acknowledgments” section recognizes support 

from STRI, funding, government permissions, logistical 

support, assistance collecting fi shes, identifi cation of specimens and reviews of section, databases, Spanish translations, images and illustrations, database management, and 

digital image preparation.

THE FISHES

A Page for Each Species, Genus, and Family

Information on the members of the fauna is provided 

through interlinked species, genus and family pages. Genera and species are ordered alphabetically within each 

family, with families being arranged in “phylogenetic” 

order. “The Fishes” module provides access to Species,

Genera, and Families pages by browsing within each taxo13_Robertson_197-208_Lang.indd 198 3_Robertson_197-208_Lang.indd 198 9/24/09 9:50

/24/09 9:50
NUMBER 38 • 199

nomic level, browsing from within a Systematic Tree (with 

optional alphabetic or systematic ordering, and optional 

use of common or scientifi c names), browsing from within 

a Book Mode (species within genera within families), or 

user-selection of level and taxon from pull-down lists.

Family and genus pages include a brief introduction 

to systematics, biology, global geographic distribution, 

and an estimate of the number of genera and species 

worldwide and present within the TEP; a text description 

of distinguishing morphological features— black text indicates the least distinctive features for identifi cation 

purposes, red text indicates important features, and red 

text with yellow high-lighting shows the most important 

features (see Figure 3); a database map of the taxon’s 

range limits distribution in the TEP (assembled from the 

distributional maps of component species) and a list of 

component genera and species with links to their pages; 

an image of a representative species that has a key feature 

FIGURE 1. Opening screen and “Home” module.

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200 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 2. Opening screen from the “General Information” module.

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FIGURE 3. Example of a species page.

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202 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

overlay indicating diagnostic features of the taxon that distinguish it from similar taxa; and comparisons with similar taxa. To assist in distinguishing look-alike fi shes, each 

taxon page includes a button-link that allows the user to 

compare images (with key feature overlays) of such taxa. 

Each page also includes a list of designated similar fi shes (at 

the same taxonomic level), with links to their taxon pages.

Species data pages are similar to genus and family pages 

but also include multiple images (e.g., juvenile, female, male, 

color morphs, specifi c morphological characteristics) and access to a downloadable list of species zoogeographic and ecological attribute data. For example, the Zoogeography tab 

includes Global endemism, a species global-scale distribution 

and its occurrence outside the TEP; Regional endemism, distributions of species within the TEP, including TEP endemics 

(species that occur only in the region or have the great bulk 

of their distributions within it), temperate eastern Pacifi c endemics (whose distributions are primarily to the north and 

south of the TEP, in the Californian and Peruvian provinces), 

eastern Pacifi c non-endemics (species that have populations 

outside the eastern Pacifi c, for instance circumtropical species). Categories relating to the distributions of species within 

the TEP include the occurrence of endemic and non-endemic 

species at offshore islands and/or the continental shore, 

whether TEP endemics are endemic to the offshore islands 

(and which islands) or to the mainland, and to which of the 

three mainland provinces (or combinations thereof) each 

continental TEP endemic is restricted. Attributes for Climate 

zone and Residency (whether the species appears to be a resident or a vagrant in the region) are also included.

Other species ecological attributes that are presented 

include the following:

• the known maximum total length of each species;

• a species’ maximum and minimum depth of occurrence;

• the salinity of environment(s) in which a species occurs;

• the specifi c habitat(s) a species uses (as well as habitat categories as defi ned by FishBase, see www.FishBase.org);

• whether a species is restricted to inshore waters or occurs in offshore, oceanic conditions;

• the position in the water column at which a species lives 

(e.g., bottom, surface);

• a species’ feeding group (e.g., carnivore);

• items in a species’ diet (e.g., fi shes, pelagic crustaceans, 

microalgae);

• a species’ reproductive mode (e.g., different types of 

eggs, live birth); and

• a species’ CITES and IUCN REDLIST status.

When information is available (e.g., for diet) for a species itself, an “S” is given after the value in the database. In 

cases for which such species-level information is lacking, 

the page displays information for the genus (indicated by 

“G”), or for the family (“F”) if there is no information for 

the genus.

Taxon pages includes direct links to external websites 

concerning the same taxon in the following external online sources: William Eschmeyer’s Catalog of Fishes (www

.calacademy.org/research/icthyology/catalog), which provides comprehensive up-to-date data on the systematics 

of fi shes; FishBase (www.fi shbase.org), which covers a 

variety of aspects of the biology of fi shes; ITIS, the International Taxonomic Information System (http://www.itis

.gov) and WoRMS, the World Register of Marine Species 

(http://www.marinespecies.org), both of which focus on 

scientifi c names of fi shes; and OBIS, the International Biogeographic Information System (http://www.iobis.org), 

which aggregates geo-referenced databases of collection 

records of fi shes.

WHAT FISH IS THAT? 

This module facilitates identifi cation of unknown 

fi shes using four distinct tools (Figure 4).

Find a Fish

This tool allows users who are not scientifi cally 

trained to identify an unfamiliar fi sh by choosing among 

the following in any order or combination, with the ability to back-up steps: Where was it?—select location and 

size of area in question on a database map— and combinations of Body Shape, Color Pattern, and Colors. Each 

step narrows the list of possibilities, with each species on 

the possibilities list linked to its image, and hence to its 

species page.

Identifi cation Keys Search

Illustrated dichotomous keys are provided for the genera 

and species in the two families with the largest number of species: Gobiidae (88 species in 27 genera) and Sciaenidae (82 

species in 26 genera). Search results link to species pages.

Compare Images of Fishes

This function allows simultaneous comparison of images of any two to six families, genera, or species selected. 

The feature enables users to compare “apples” with “oranges,” whereas the comparison of designated similar taxa 

on taxon pages limits users to comparing only “apples.” 

Resultant images are linked to taxon pages.

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FIGURE 4. Screen capture from the “What Fish Is That?” module.

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204 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Common Names Search

Searches can be made for families, genera, and species 

from pull-down lists of common names, with results linked 

to taxon pages. The systematic tree or taxonomic hierarchy 

(see “The Fishes” module) also functions with the use of either common names or scientifi c names. The use of common 

names in this hierarchy helps users who are not scientifi cally 

trained to appreciate the relationships among fi shes.

GLOSSARY

An interactive glossary of taxonomic terms is provided 

that uses a combination of images and text to explain basic terms relating primarily to morphological characteristics 

that are used in the identifi cation of fi shes. In addition the 

usage of scientifi c jargon has been reduced as much as possible throughout the taxon pages by using simple descriptive 

phrases from everyday English to replace technical terms.

RESEARCH ENGINE

This module provides a variety of types of zoogeographical data and the ability to generate maps and sitespecifi c species-lists based on complex queries constructed 

by the user (Figure 5).

Taxon Range Maps

This feature provides overlaid displays of the regional 

ranges of up to three taxa (species, genera, families, or a 

mixture thereof). In addition, maps can be generated of 

the geographic distribution of all species-range centroids 

(both paint and point data) and of all geo-referenced sampling points in the system’s database.

Species Richness Displays

This feature provides maps with color-coded overlays 

of patterns of variation in species richness throughout 

the region. Those patterns include richness of individual 

families and richness of species in specifi ed “functional 

groups” (e.g., species sharing one or more biogeographic 

and ecological attribute). Richness displays can indicate 

either absolute richness (number of species) or relative 

richness (number of species as a percentage of the local 

fauna). A display of relative sampling intensity indicates 

the number of species recorded at minimally one site 

within each unit of area (1° of latitude 1° of longitude) 

as a percentage of the number of species whose ranges 

encompass that unit.

Species –List Assembly

Family and genus lists can be constructed for single locations. Species lists for “functional groups” of fi shes for a 

particular location can be constructed using any combination of biogeographic and ecological attributes. Species lists 

include both single-location lists and lists of species found or 

not found at two locations. The spatial scale of a location in 

such a search varies from a single island to an area of variable shape and size, to the entire TEP or map. Locations are 

defi ned by the user employing a library of approximately 

300 preformed templates that include geographic entities 

(e.g., shoreline, continental shelf, named gulfs), habitat features (e.g., mangroves, rocky shores, upwelling areas), islands (individual and archipelagos), biogeographic entities 

(provinces of the TEP), political areas (Exclusive Economic 

Zones and parts thereof), and marine reserves (individual 

reserves, combine country reserves). In addition, quadrants 

of varying sizes (12 groups ranging from 0.5° latitude 

0.5° longitude to 24° 24°) used by the map of the Find a 

Fish tool in the “What Fish Is That?” module provide approximately 5,000 additional [square] templates.

Unconfi rmed/Confi rmed Occurrences

Single-area species lists indicate both likely occurrences (species whose ranges include the selected area) and 

confi rmed occurrences (species with at least one collection 

record in the same area).

Local Endemism Indicator

This feature provides a list of species found only 

within one or two template areas, and nowhere else on the 

system’s map.

List and Map Exports

Lists and Maps produced by searches are exportable/

printable. Lists may be arranged alphabetically or systematically (genera and species arranged alphabetically within 

families arranged in systematic order).

Species Range Maps and Range Data

A database map on each taxon page incorporates two 

types of data: a two-dimensional painted representation 

of the geographic range based on museum and literature 

records of occurrence and range maps, and our own fi eld 

surveys in Mexico, El Salvador, Costa Rica, Panama, Colombia, Ecuador, the Revillagigedos, Clipperton, Cocos, 

13_Robertson_197-208_Lang.indd 204 3_Robertson_197-208_Lang.indd 204 9/24/09 9:51/24/09 9:51
NUMBER 38 • 205

FIGURE 5. Screen capture from the “Research Engine” module.

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206 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Malpelo, and the Galapagos; and points indicating site 

records from museum collections, the scientifi c literature, 

and our own fi eld surveys. Geographic-range statistics 

derived from these two offsets of data and presented on 

species pages include: latitudinal and longitudinal limits, 

ranges and midpoints based on paint data, and, separately, 

site records; data on range characteristics derived from 

paint data have been adjusted in species that occur in the 

eastern Pacifi c beyond the limits of the system’s base map; 

habitat area, based on number of painted pixels in the species range map; and separate range-area polygons with 

centroids based on painted data and site record data.

Continental Ranges

Comprehensive faunal lists exist for few locations, and 

large sections of the coastline and continental platform of the 

TEP remain poorly sampled, a situation that will not be rectifi ed in the near future. Hence the range of most species on the 

continental shelf is derived from data on the northern and 

southern limits of occurrence. Thus painted areas on taxon 

page maps represent the potential range and potential habitat area, and a species is assumed to be present in appropriate 

habitat anywhere between those limits. Exceptions include 

species that are known to have wide gaps in their distributions, such as some well-known anti-tropical species. Those 

gaps are represented in the range maps of such species.

Habitat Area Calculations

Maps constructed for the determination of habitat areas 

incorporate information on habitat usage and depth range as 

well as the extent of the geographic range. Continental areas 

of range maps were modifi ed to exclude large areas of habitat that was inappropriate for the particular species; for example, shorelines composed primarily of sand and mud were 

excluded from ranges of reef-fi shes and rocky shores were excluded from ranges of fi shes living on beaches or in lagoons 

and mangroves. The depth ranges of individual species were 

also taken into account: ranges of demersal species restricted 

to very shallow water (less than ~20 m depth) are indicated 

by lines that follow coastlines. For habitat area calculations 

of such species, the coastal strip of habitat was taken to be 

1 km wide. Ranges of coastal species found in deeper water 

on the continental and insular shelves are divided into three 

groups: those occurring down to ~60 m have maps that span 

the inner continental shelf; species that are limited to depths 

below ~60 m occur on the outer shelf; and the third group 

has depth ranges (and maps) that span the entire shelf. Maps 

for pelagic species variously include parts of the shelf and/or 

open ocean, depending on the biology of the species.

Mercator Projection Distortions and Adjustments 

to Habitat Area Calculations

Mercator projection maps, such as that used in this 

system, incorporate distortions of both latitude and longitude that affect estimation of habitat area. In such projections lines of longitude are shown as parallel rather than 

converging with increasing latitude, and lines of latitude 

diverge with increasing latitude instead of remaining a 

fi xed distance apart. When calculating the habitat area for 

each species those two distortions were taken into account 

by making appropriate adjustments to the areas of individual pixels in different latitudinal bands. Range polygon 

areas were calculated independently using the GIS (Geographic Information System) ArcInfo system.

Cleanup of the Geo-Referenced Records Database

Both the scientifi c literature and databases from museums inevitably include erroneous records as a consequence 

of misidentifi cation of fi shes and sites, as well as book keeping 

errors. In addition museum specimens of demersal species 

include not only individuals collected in demersal habitats 

but also larvae collected in the open sea far from adult 

habitat, and, in some cases, far from the known adult geographic range (Robertson, 2008). Records from the multisource database of ~67,000 collection site records included 

here that were adjacent to the currently known limits of 

the geographic range were used to adjust (by expanding) 

those ranges. However, we removed from the systems 

database those “suspect” records that were well outside 

the known habitat and geographic ranges of the “adult” 

phase of each species, based on extensive records from 

other sources, the biology of the species, and expert determinations of ranges. This cleanup process reduced the size 

of the database by approximately 6%. Points outside the 

current range were retained for some species that, because 

of overfi shing, have had their historical ranges reduced. 

For example, historically the mackerel Scomberomus concolor, which currently occurs only in the northern Gulf 

of California, occurred throughout that gulf and also off 

California, USA (B. B. Collette, National Marine Fisheries Service Systematics Laboratory, personal communication, 2008).

LIBRARY

The library database (Figure 6) includes 1,143 citations. The citation for its original description is included 

for each species, along with citations of revisions of genera 

and families. Other citations include local and larger scale 

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FIGURE 6. Screen capture from “Library” module.

NUMBER 38 • 207

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208 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

lists of species; identifi cation guides to species; and publications about the biology and zoogeography of species 

inside and outside the TEP. Each citation is linked to the 

species it discusses (and hence to appropriate genera and 

families).

Exportable lists can be generated for:

• Citations linked to individual families, genera, and 

species.

• Species linked to a particular citation.

• Citations linked to a particular author, date, or source 

journal.

• The entire bibliography arranged alphabetically by author name.

RANDOM IMAGES

The image database incorporates 2,927 images. These 

include 2,346 color photographs that cover 83% of the 

fauna (1,068 of 1,237 species). In comparison, the 1994 

book from which this system was developed included color 

images of 683 species and treated only 768 species.

This module presents color images in a randomized 

order.

Digital Manipulation of Images

The user should assume that all illustrations used in 

this system have been digitally manipulated to some extent, to increase their utility as identifi cation aids. Such manipulation includes cropping, image sharpening, changes 

in lighting and contrast relationships of different parts of 

individual subjects, changes of subject-to-background contrast, changes of background to enhance subject visibility, 

the (occasional) combination of multiple images of fi shes 

in a montage to provide examples of variation in color patterns within the same image, and minor repairs to fi n membranes and removal of body blemishes (scratches, minor 

cuts, blood spots) that resulted from capture handling.

Image Credits

All images are accompanied by a relevant ownership 

credit, copyright notice, and usage notice. Each image is 

accompanied by a link to either the owner’s e-mail contact 

or website.

ACKNOWLEDGMENTS

Funding throughout the development of this system 

(1990– 2008) was provided the following Smithsonian Institution (SI) sources: the SI Women’s Committee, the SI 

Seidell Fund, the SI Latino Initiatives Fund, the SI Marine 

Science Network, and the Smithsonian Tropical Research 

Institute.

LITERATURE CITED

Allen, G. R., and D. R. Robertson. 1994. Fishes of the Tropical Eastern 

Pacifi c. Bathurst, Australia: Crawford House Press.

— — — . 1998. Peces del Pacífi co oriental tropical. CONABIO, Mexico.

Robertson, D. R. 2008. Global Biogeographic Data Bases on Marine 

Fishes: Caveat Emptor. Diversity and Distributions 14:891– 892.

Robertson, D. R., and G. R. Allen. 2002. Shorefi shes of the Tropical 

Eastern Pacifi c: An Information System. CD-ROM. Balboa, Panama: Smithsonian Tropical Research Institute.

— — — . 2006. Shorefi shes of the Tropical Eastern Pacifi c: An Information System. Version 2. DVD-ROM. Balboa, Panama: Smithsonian 

Tropical Research Institute.

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Nephasoma pellucidum: A Model 

Species for Sipunculan Development?

Anja Schulze and Mary E. Rice

ABSTRACT. Recent developments in metazoan phylogeny, especially with regard to 

the position of the Sipuncula in the annelid clade, have sparked a renewed interest in 

sipunculan development. If Sipuncula are annelids, they must have secondarily lost segmentation. By comparison with segmented annelids, they could provide important clues 

for the evolution of segmentation. A sipunculan model species is needed to examine 

fundamental developmental processes. Here we describe the development of Nephasoma 

pellucidum and explore its potential as a model species for sipunculan development. 

Like other sipunculans, N. pellucidum produces eggs with a thick, porous, multilayered 

egg envelope. Cleavage in N. pellucidum is spiral, holoblastic, and unequal. The species shows the most common, and likely ancestral, developmental mode in the group. 

Its life cycle includes a lecithotrophic trochophore and a planktotrophic pelagosphera 

larva. The trochophore is enclosed in the egg envelope, with cilia growing through the 

envelope’s pores. The trochophore larva metamorphoses into the pelagosphera larva at 

approximately 60 h. Pelagosphera larvae reached metamorphic competence at about fi ve 

weeks. Metamorphosis to the juvenile was induced by supplying sediment that had been 

inhabited previously by conspecifi c adults. Juveniles were observed for several weeks. 

We conclude that N. pellucidum is a good model species for sipunculan development, 

although rearing conditions in the laboratory still need to be optimized.

INTRODUCTION

During the past two decades, our understanding of metazoan relationships 

has changed radically, starting with the fi rst use of ribosomal RNA sequences 

for phylogenetic analysis (Field et al., 1988). Many taxa for which evolutionary 

origins have long been mysterious or controversial can now be placed with more 

certainty into the metazoan tree of life (Dunn et al., 2008; Halanych, 2004). 

Among those, two groups that were long regarded as distinct phyla have been 

absorbed into the Annelida: the Echiura, or spoon worms, and the Siboglinidae, 

previously called Pogonophora and Vestimentifera (McHugh, 1997; Rouse and 

Fauchald, 1997).

The Sipuncula, commonly known as peanut worms or star worms, have had a 

complex taxonomic history but now appear to be following the same route as the 

echiurans and siboglinids. Nearly 50 years after Hyman (1959) affi rmed phylum 

status for the group, recent authors place them into the annelid clade, based on 

Anja Schulze, Texas A&M University at Galveston, 5007 Avenue U, Galveston, Texas 77551, 

USA. Mary E. Rice, Smithsonian Marine Station 

at Fort Pierce, 701 Seaway Drive, Fort Pierce, 

Florida 34949, USA. Corresponding author: A. 

Schulze (schulzea@tamug.edu). Manuscript received 9 June 2008; accepted 20 April 2009.

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phylogenetic analyses of mitochondrial gene order (Bleidorn et al., 2005; Boore and Staton, 2002), sequence data 

from several genes (Struck et al., 2007), and expressed sequence tags (Dunn et al., 2008). Although there is a growing consensus on the annelid affi nities of sipunculans, it 

remains to be determined which of the incredibly diverse 

annelids is the sister group to the Sipuncula. With a simple 

body, consisting of a trunk and a retractable introvert with 

an array of tentacles at the anterior end, they show little 

similarity to any other polychaete group. In the molecular analyses, support for a sister group relationship with 

any other polychaete taxon is low. The monophyly of the 

Sipuncula is uncontested, and solid hypotheses of withingroup relationships have been published (Maxmen et al., 

2003; Schulze et al., 2005, 2007; Staton, 2003).

Sipuncula are an interesting case in the fi eld of 

“EvoDevo,” or the interface of evolution and development. 

Embryonic and larval characters have often been cited as 

support for phylogenetic hypotheses. Rice (1985) listed several similarities between sipunculan and annelid development, such as the larval prototroch and metatroch and the 

retention of the egg envelope to form the larval cuticle. She 

also noted that in some sipunculan larvae the ventral nervous system develops in paired cords, similar to most polychaetes. On the other hand, Scheltema (1993), comparing 

embryos and larvae of annelids, mollusks, and sipunculans, 

argued that sipunculan development shows more similarity 

with that of mollusks. The development of all three taxa 

includes spirally cleaving embryos and a trochophore larva. 

A long-held view is that annelid and mollusk embryos can 

be distinguished at the 64-cell stage by the arrangement of 

the micromeres around the animal pole: they form either an 

“annelid cross” or a “molluskan cross.” Reproducing Gerould’s (1906) drawing of the embryo of Golfi ngia vulgaris

with a molluskan cross, Scheltema concluded that sipunculans and mollusks were sister groups. However, Maslakova 

et al. (2004) showed that the annelid and molluskan crosses 

are far from universal within the respective taxa and probably hold no phylogenetic signifi cance.

The primary reason why few past researchers have 

recognized sipunculans and echiurans as annelids is that 

adults of both taxa show no sign of segmentation, either 

externally or internally. It took advanced techniques in immunohistochemistry and confocal laser scanning microscopy to demonstrate segmentation in the nervous system 

of echiuran larvae (Hessling and Westheide, 2002). Similar 

techniques initially failed to show segmentation in sipunculan larvae (Wanninger et al., 2005) but a recent study 

showed a segmental mode of neural patterning in the early 

pelagosphera stage (Kristof et al., 2008).

If the Sipuncula fall into the annelids, they must have 

secondarily lost segmentation in the later larval stages and 

the adult. If no morphological segmentation is evident, 

what happened with the molecular pathways responsible 

for segment formation in other annelids? By comparison 

with other species, sipunculans are valuable for the identifi cation of the genetic and cellular basis of segment formation in annelids.

The recent developments in metazoan phylogeny have 

thus sparked a renewed interest in sipunculan development. A model species is needed to study fundamental 

developmental processes. A good model species has to 

be readily available, be easy and inexpensive to maintain 

in the laboratory, lend itself to a variety of examination 

techniques, and be representative for its taxonomic group. 

Here we describe the development of Nephasoma pellucidum and explore its potential as a model species. N. 

pellucidum is a relatively common species that inhabits 

cracks and crevices in hard substrates in shallow warm 

waters. The species exhibits the most common developmental mode within the Sipuncula, which includes a lecithotrophic trochophore stage and a planktotrophic pelagosphera larva (Rice 1967, 1975a, 1975b, 1976, 1989). 

We have accumulated these data between 1972 and 1984 

and, more recently, between 2003 and 2006.

MATERIALS AND METHODS

Specimens of Nephasoma pellucidum were collected 

from numerous localities offshore from Fort Pierce, Florida, extending from Capron Shoal and Pierce Shoal 4 and 

6 miles, respectively, southeast of the Fort Pierce Inlet to 

the Sebastian Pinnacles approximately 32 miles north 

of the Inlet. At the Pinnacles, worms inhabited rubble 

of oculinid coral at depths of 70 to 100 m, whereas on 

the more southern shoals they occurred in depths of 9 to 

15 m in rubble composed of mollusk shells, sand dollar 

tests, and rocks. Occasionally specimens were found in the 

Fort Pierce Inlet in intertidal clumps of oyster shells. The 

worms were carefully removed from the rubble with hammer and chisel. Multiple adults from each collection were 

kept in glass dishes in approximately 200 mL seawater 

at room temperature. Spawning occurred in the lab, generally after changing the water. Whenever eggs were observed in the culture dishes, they were pipetted into a clean 

dish and observed for development. Larval cultures were 

kept until the larvae either died or metamorphosed. Water 

was changed at least every two days. The larvae were periodically fed with unicellular algae or diatoms (Isochrysis, 

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Dunaliella, or Nanochloropsis). To induce metamorphosis, larvae were pipetted into dishes with muddy sediment 

previously inhabited by conspecifi c adults.

For scanning electron microscopy (SEM) and transmission electron microscopy (TEM), specimens were fi xed in 

2.5% glutaraldehyde in Millonig’s phosphate buffer (Millonig, 1964) for at least 1 h and up to several days at 4°C. 

Fixation was followed by three washes in a 1:1 mixture 

of Millonig’s phosphate buffer and 0.6 M sodium chloride and post fi xation in 1% osmium tetroxide (1:1:2 mix 

of 4% OsO4 : Millonig’s buffer : 0.75 M NaCl). Samples 

were then dehydrated in an ethanol series up to 100%. 

For SEM, they were critical point dried and mounted on 

SEM stubs using double-sticky tape and viewed in either 

a Nova Scan or a JEOL 6400 Visions scanning electron 

microscope. Images were either scanned from negatives 

or stored digitally. For TEM, the dehydrated specimens 

were transferred to propylene oxide and subsequently embedded in Epon resin and sectioned. Thin sections were 

stained with uranyl acetate and lead citrate and viewed in 

a JEOL 100CX transmission electron microscope.

RESULTS

GAMETES

The spermatozoan of Nephasoma pellucidum is of the 

primitive type according to Franzén’s classifi cation (Franzén, 1958). The nuclear region is rounded and capped by 

a doughnut-shaped acrosome with a central nipple-like 

protuberance. The head, including nucleus and acrosome, 

measures 1.5 1.7 m. Posterior to the nucleus, four 

mito chondrial spheres are arranged in a circle, from the 

center of which extends the fl agellum (Figure 1A).

The egg at the time of spawning is spherical, measuring 105 m in diameter (Figures 1B, 2A). In direct light 

the surface appears opalescent, and the color is pale gray. 

The egg envelope, up to 6 m in thickness, is multilayered 

and perforated by numerous pores (Figure 3).

SPAWNING

As in most sipunculans, sexes are separate; eggs and 

sperm are spawned freely via the nephridipores into the 

surrounding water where fertilization occurs. From data 

accumulated on spawning in the laboratory, two spawning peaks are evident: one in the spring (April– May) and 

the other in the fall (September– November). Observations 

of spawning were carried out on animals in the laboratory, 

usually for a period of one month after collection from 

the fi eld: 139 spawnings were recorded over a period of 8 

years (1972– 1980), and spawning occurred every month 

of the year except January. Although a few animals were 

observed to spawn after maintenance in the laboratory 

for as long as 18 months, 88% of the spawnings were recorded within 30 days of collection.

CLEAVAGE

The eggs at spawning may be arrested in the fi rst 

meiotic metaphase, or they may possess an intact germinal vesicle. In the latter case, the germinal vesicle breaks 

down soon (within at least 30 min) after spawning, regardless of whether the egg is fertilized. Within 40 min 

after fertilization (23°C), the fi rst polar body is formed 

(Figure 2B), and at 55 min the second polar body makes 

its appearance. The fi rst cleavage, occurring at 90 min, 

is unequal, the CD cell exceeding the AB cell in size (Figure 2C). The next three cleavages occur at approximately 

half-hour intervals, and the 16 cell stage is attained 

within 3 h after fertilization. The third cleavage, from 

4 to 8 cells, is spiral and unequal. The A, B, and C cells, 

all approximately the same size, divide simultaneously, 

preceding the initiation of division of the larger D cell by 

about 1 min and completing their divisions 5 min before 

that of the D cell. In the 8 cell stage, the micromeres 

and macromeres of the A, B, and C quadrants are approximately the same size, the C sometimes being slightly 

larger, but all are smaller than the d cell which, in turn, is 

smaller than the D cell.

After the fi rst few cleavages, the divisions are more 

frequent, and by 7 h after fertilization the egg has developed into an early blastula; cilia from the prototrochal 

cells protrude through the pores of the egg envelope and 

the embryo begins to rotate slowly on the bottom of the 

container. By 16 h the embryos are swimming throughout 

the dish, no longer confi ned to the bottom. At this time the 

stomodaeal invagination is evident, and the embryos show 

the fi rst signs of positive phototropism (Figure 2D).

TROCHOPHORE: MORPHOLOGY AND METAMORPHOSIS

TO THE PELAGOSPHERA

By 48 h the embryo has reached the stage of trochophore. The shape has changed from spherical to oval, as 

a result of a slight posttrochal elongation (see Figure 1C). 

A pair of dorsolateral red eyespots is present in the pretrochal hemisphere. Prototrochal cavities are evident to the 

inner side of the prototroch cells, and the gut is differentiated into three regions: esophagus, stomach, and intestine. 

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212 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 2. (facing page) Light micrographs showing development of Nephasoma pellucidum (scale bar lengths here in parentheses). 

A. Unfertilized egg (20 m). B. Egg with polar body (arrow) (20 m). C. Two-cell stage; note size difference between CD and AB blastomeres (20 m). D. Blastula stage; beginning invagination of stomodaeum (arrow) (20 m). E. Early trochophore; note eyespots at anterior 

end (top) (20 m). F. Trochophore shortly before metamorphosis to pelagosphera (20 m). G. Early pelagosphera in the process of elongation (20 m). H. Fully metamorphosed pelagosphera larva (20 m). I. Feeding pelagosphera, 10 d old (50 m). Abbreviations: bo  buccal 

organ; es  esophagus; in  intestine; lg  lip gland; mt  metatroch; st  stomach; to  terminal organ.

FIGURE 1. Scanning electron micrographs showing development of Nephasoma pellucidum (scale bar lengths here in parentheses). A. Sperm 

on the surface of the egg (5 m). B. Egg with sperm on surface (20 m). C. Trochophore larva; note cilia extending through egg envelope 

(20 m). D. Early pelagosphera larva (20 m). E. Fully formed pelagosphera larva, ventral view (50 m). F. Head of a pelagosphera larva, 

lateral view (20 m). G. Terminal organ of the pelagosphera larva (10 m). H. Metamorphosed juvenile (100 m). I. Tip of juvenile introvert 

with tentacle buds and lobes of nuchal organ (50 m). Abbreviations: at  apical tuft; h  head; ll  lower lip; m  mouth; mc  metatrochal 

collar; mt  metatroch; no  nuchal organ; pt  prototroch; t  tentacles; to  terminal organ; tr  trunk. (Images A, B from Rice, 1989: 

fi g. 4E,F; used with permission)

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214 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

The trochophore is lecithotrophic, being completely enclosed by the egg envelope (Figure 2E,F).

Metamorphosis of the trochophore to the pelagosphera larva occurs at 60 to 65 h (23°C) and extends over 

a period of 6 to 8 h. The body elongates from 140 m to 

250 m, by an increase in the length of the post trochal 

hemisphere. The lumen of the gut is completed, and mouth 

and anus break through the overlying egg envelope (Figures 1D, 2G). The ventral ciliated surfaces of the head and 

the lower lip are formed apparently by an evagination and 

expansion of the anterior stomodaeum. Larval organs of 

the lower lip become functional: the buccal organ is protrusible, and the pore of the lip glands opens (Figure 2H). 

The metatrochal cilia project from a prominent metatrochal collar posterior to the mouth and lower lip. As the 

retractor muscles become functional, the entire pretrochal 

body is retractable into the posterior or posttrochal region of the larva. The coelom is considerably expanded, 

and the posttrochal body is capable of great extension 

and contraction. Whereas the posttrochal egg envelope 

is transformed into the larval cuticle, the pretrochal egg 

envelope is gradually sloughed off, leaving a thin cuticle 

covering the head. The terminal organ appears fi rst as an 

evagination of the posterior extremity of the trunk and 

within a few hours differentiates into a more discrete elongate structure (40 m) that is retractable into the trunk 

and provides a temporary attachment for the larva to the 

substratum (Figure 1G).

PELAGOSPHERA: MORPHOLOGY, BEHAVIOR, AND 

METAMORPHOSIS TO THE JUVENILE

Four regions of the body can be distinguished: head, 

metatrochal collar, trunk, and terminal organ (see Figures 

1E,F, 2H). The terminal organ is well developed with an 

unusually long neck, terminated by a bulbous posterior 

expansion (Figure 1G). The terminal organ of a 10-day 

larva may be extended to a length one-third that of the 

entire larva.

For approximately two weeks after metamorphosis, 

the majority of larvae are attached by their terminal organs; some continue to swim, or else attach and swim 

intermittently. At two weeks there is a high rate of mortality and, in the absence of substratum, most larvae die 

within two months; the maximum survival time of larvae 

reared in culture dishes is 103 days. Surviving larvae of 

one month of age attain a maximum size of 1.2 mm. At 

this age the body proportions have changed, the head being relatively smaller than in the younger stages. The external body wall is smooth, glistening in refl ected light, 

and through the relatively transparent body wall the gut is 

apparent as an elongate dark yellow stomach and a lighter 

yellow recurved intestine, ending at the dorsal anus in the 

anterior trunk. Usually larvae are still attached by the terminal organ at these later stages, although some may lie 

on the bottom, relatively quiescent. Swimming occurs only 

rarely, although metatrochal cilia are still present.

Attached larvae are observed to feed on the substratum 

surrounding their points of attachment (Figure 2I). The 

body may be bent downward so that the ventral surface of 

the head is applied to the bottom of the dish, or the body 

may be stretched out from the point of attachment parallel to the substratum. In culture dishes in which there is 

an algal growth covering the bottom, the area surrounding 

the attached larva is often bare, indicative of larval grazing 

activity. The area of attachment is often marked by clumps 

of feces on which the larva may graze and ingest. Occasionally larvae release themselves from the attachment and 

swim or move along the bottom to a new site. Free larvae 

sometimes move with head applied to the substratum and 

posterior end directed upward, either exploring or feeding 

on the bottom. Frequently the terminal organ is placed in 

or near the mouth. Older larvae detach and move to new 

locations less often than younger larvae. A larval behavior, 

common to all sipunculans but of unknown function, is 

placement of the terminal organ in or near the mouth.

FIGURE 3. Transmission electron micrographs showing egg envelopes 

of Nephasoma pellucidum (scale bars  1 m). A. Section through 

multilayered egg envelope. B. Cilium growing through pore in egg envelope of trochophore larva. Abbreviations: ci  cilium; po  pore.

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NUMBER 38 • 215

Metamorphosis of larvae reared in culture dishes 

could be induced at the age of 5 to 6 weeks by exposure 

to a fi ne, muddy sediment that had been occupied previously by adults. Attempts to induce metamorphosis before 

this age were not successful. Before metamorphosis, larvae 

buried themselves in the sediment and in 3 d underwent 

metamorphic changes to the juvenile stage.

The process of metamorphosis is initiated by the loss 

of the metatrochal cilia, reduction in the size of the lower 

lip, narrowing of the head, and elongation of the pretrochal body. At the end of 3 d, both posttrochal and pretrochal regions of the body are narrowed and elongated, 

the metatrochal collar is reduced, the terminal organ and 

lip are partly regressed, the mouth moves to a terminal 

position, and dorsal to the mouth a pair of developing tentacular lobes is apparent (Figure 1H,I). These morphological modifi cations, along with the behavioral changes of 

initiation of burrowing and cessation of swimming, mark 

the beginning of the juvenile stage. Regions of the body of 

the juvenile are reduced from the four found in the larva 

to two: (1) the broader and longer posterior trunk, formed 

from the posttrochal larva, and (2) the more narrow anterior introvert, which is terminated by mouth and developing tentacles and formed from the pretrochal larva. Similar 

to the pretrochal larval body, the introvert of the juvenile 

is retractable into the trunk.

The most immediate modifi cations are found in the 

head and metatrochal regions. As the mouth becomes terminal, the dorsal surface of the head is foreshortened. The 

ventral lip is lost, but ciliation of the ventral surface of 

the head persists to surround the mouth and the ventral 

surface of the developing dorsal lobes. On the dorsal head 

two heavily ciliated patches that will give rise to the paired 

nuchal organ have moved further anteriorly as the head 

foreshortens. In the 7- to 9-day-old juveniles the buccal 

organ is no longer apparent. One to four rings of simple hooks appear in the region of the former metatrochal 

band. Papillae, already apparent in older larvae, are more 

prominent and numerous. Scattered among the hooks, the 

papillae are dome shaped and, as seen in scanning electron micrographs, have central pores from which several 

cilia protrude. Papillae of similar structure, but somewhat 

larger, cover the entire trunk (Figure 1H). A vestigial terminal organ may persist for one or two weeks. Within two 

to four weeks a second pair of rudimentary tentacles appear ventral to the mouth.

The body wall of the juvenile thickens, losing its 

transparency. Externally circular constrictions, also seen 

in late larval stages, are more prominent. Juveniles of one 

week also show longitudinal “folds” of the body wall, 

resulting in a checkered appearance of the integument in 

some regions.

DISCUSSION

Nephasoma pellucidum is one of the few sipunculan 

species in which the life cycle has been observed from 

spawning to juvenile stage. Other species are Siphonosoma cumanense (Rice, 1988), Thysanocardia nigra

(Rice, 1967), Themiste pyroides (Rice, 1967), Themiste 

lageniformis (Pilger, 1987), Themiste alutacea (Rice, 

1975c), Phascolion strombus (Åkesson, 1958; Wanninger 

et al., 2005), and Phascolion cryptum (Rice, 1975c). Most 

of these species show abbreviated development, either 

omitting both the trochophore and pelagosphera stage, or 

omitting the pelagosphera stage, or having a lecithotrophic pelagosphera (Rice, 1976). The oceanic, planktotrophic pelagosphera larvae of many aspidosiphonid and 

phascolosomatid larvae have been recovered in plankton 

tows; however, their complete life cycles are unknown 

(Rice, 1981; Hall and Scheltema, 1975).

We argue that a model species should show the ancestral developmental mode for the taxon. Cutler (1994) concluded that indirect development with a planktotrophic 

pelagosphera was ancestral in Sipuncula. The most recent 

phylogenetic analyses (Schulze et al., 2007; Schulze and 

Rice, 2009) seem to confi rm this view. The genera Sipunculus and Siphonosoma, which to our present knowledge 

only contain species with planktotrophic pelago sphera 

larvae, represent the two basal clades in both analyses. 

The remaining three major clades have species of Phascolosoma and Apionsoma as their basal branches, two 

additional genera in which abbreviated development is 

unknown.

Of the species listed above, only the life cycle of Siphonosoma cumanense includes a planktotrophic pelagosphera as N. pellucidum does. Siphonosoma cumanense is 

a large, sand-burrowing species. Like other sipunculans, it 

survives well under laboratory conditions, when supplied 

with sediment and adequate aeration. However, its potential for use as a model species is limited by two factors. 

First, even though the species has a wide geographic distribution, it is rarely found in signifi cant numbers, and the 

establishment of a viable population would require major 

efforts. Second, larvae do not seem to be competent to 

metamorphose until about 8 weeks old (Rice, 1988).

Nephasoma pellucidum is geographically widespread, 

mostly in shallow warm waters, although it does not seem 

to be as abundant in most places as at our collecting station 

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216 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

near Fort Pierce, Florida. Collection of a signifi cant number of individuals can be time consuming because they 

have to be carefully removed from the cracks and crevices 

of rubble; the removal process can damage the animals, 

often causing their death. After successful retrieval, however, adults are easy to maintain in laboratory conditions. 

Removed from their shelter, they survive in simple glass 

bowls without aeration or food supplement for at least a 

year, feeding only on the biofi lm at the bottom of the dish. 

We assume that, left in their shelter or in sediment, with 

proper aeration and occasional food supply, they would 

survive for years. This assumption is based on the longevity of other sipunculans: individuals of Apionsoma misakianum have been kept in holding tanks at the Smithsonian 

Marine Station for nearly 30 years.

Nephasoma pellucidum spawns frequently during the 

warmer months of the year. Spawning can be induced by 

changing the seawater in the dish, although this procedure 

does not reliably yield the desired results, leaving some 

uncertainty as to when the spawning occurs. Embryos and 

larvae are easy to observe with different microscopic techniques. Mortality before the fi rst metamorphosis, from 

trochophore to pelagosphera, is minor. The pelagosphera 

larvae are more transparent than other sipunculan larvae, 

facilitating observation by light and confocal laser scanning microscopy. In contrast to the pelagosphera larvae of 

some other sipunculan species, they relax relatively well 

when temporarily cooled to 4°C and treated with menthol, magnesium chloride, or 10% ethanol, leaving their 

head and terminal organ exposed.

The increase in mortality during the prolonged pelagosphera phase presents some diffi culties. By the time metamorphic competence is reached, the percentage of surviving larvae is low. A further reduction in numbers occurs 

at metamorphosis, because not all larvae respond to the 

settlement cue, that is, adult-conditioned sediment. Therefore, postmetamorphic juveniles are only rarely observed. 

Common metamorphosis-inducing agents such as potassium chloride, cesium chloride, gamma-aminobutyric acid, 

3,4-dihydroxy-L-phenylalanine (L-dopa), and isobutylmethylxanthine (Bryan et al., 1997; Morse et al., 1979; Yool 

et al., 1986) seem to have no effect on metamorphosis in 

N. pellucidum.

As a conclusion, among the sipunculans for which development has been studied, N. pellucidum is a good candidate for a model species. Rearing larvae through metamorphosis still presents some diffi culties, and future work 

should focus on optimizing the conditions. Recently the 

cold-water species Phascolosoma agassizii from the Sea 

of Japan, which also has a planktotrophic pelagosphera, 

has been reared through metamorphosis (A. S. Maiorova 

and A. V. Adrianov, Institute of Marine Biology, Far East 

Branch of the Russian Academy of Sciences, Russia, personal communication) and might be another appropriate 

candidate for a model species, even though metamorphosis could never be observed in individuals of the same species collected in the Pacifi c Northwest and reared at the 

University of Washington Friday Harbor Laboratories.

ACKNOWLEDGMENTS

We thank the staff at the Smithsonian Marine Station 

at Fort Pierce for their research support (SMSFP Contribution No. 750). We are particularly grateful to Julie Piraino, Hugh Reichardt, and Woody Lee for their support 

with specimen collection, microscopy, and imaging. Valuable assistance was provided in the earlier phases of this 

study by Douglas Putnam and Cindy Hunter. This work 

was partially supported by a Smithsonian Marine Station 

postdoctoral fellowship granted to AS. We thank the organizers of the Smithsonian Marine Science Symposium for 

the opportunity to present our research.

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Mitochondrial Phylogeography of the 

Intertidal Isopod Excirolana braziliensis

on the Two Sides of the Isthmus of Panama

Renate Sponer and Harilaos A. Lessios

ABSTRACT. The intertidal isopod Excirolana braziliensis Richardson possesses limited 

means of dispersal; there is no larval stage, and adults remain sedentary under the sand. 

It is represented on the two coasts of Panama by three morphs, two in the Pacifi c (P and 

C) and one in the Atlantic (C). Previous work has quantifi ed morphometric differences 

between the morphs, found that there are multiple allozyme differences between them, 

and produced indirect evidence that they are reproductively isolated from each other. 

Here we report comparisons of 345 bp of 12S and 678 bp of cytochrome oxidase I (COI ) 

mitochondrial DNA (mtDNA) from three populations of each morph. The mtDNA sequences from the three morphs are reciprocally monophyletic, strengthening the case for 

recognizing them as separate species. As in morphology and isozymes, the C morph and 

the Cmorph are sister clades, and the P morph is an outgroup. In contrast to what was 

previously supposed, the C and Cmorphs neither are the result of a recent introduction 

from one ocean to the other, nor were separated at the fi nal stages of the completion of 

the Isthmus of Panama three million years ago, but rather are anciently separated sister 

clades that now exist on separate shores. Patterns of mitochondrial gene fl ow between 

populations of the same morph vary. The C and Cmorphs show large genetic differences 

between local populations, as would be expected from an organism with such limited 

vagility. In the P morph, on the other hand, populations from localities 5 km apart are 

identical in mitochondrial DNA, even though they differ in one allozyme locus, suggesting the possibility of sex-biased migration.

INTRODUCTION

Many marine organisms are capable of dispersing over large distances at some 

point of their life cycle. The population genetics of such organisms usually reveal 

a genetic neighborhood size in the order of thousands or tens of thousands of kilometers. Some marine species, however, provide a contrast to this picture of wide 

dispersal in that they lack any means of transferring their genes by either vagile 

adults or free-swimming larvae, yet have wide geographic ranges. How much gene 

fl ow may occur between noncontiguous populations of such species and whether 

species cohesion is maintained in the face of limited vagility is of special interest to 

population genetics. The tropical isopod Excirolana braziliensis is an example of a 

species apparently spread over the tropical seas of Americas, even though it lacks 

the means of maintaining genetic contact between distant populations.

Renate Sponer and Harilaos A. Lessios, Smithsonian Tropical Research Institute, Box 0843-03092, 

Balboa, Panama. Corresponding author: H. Lessios 

(Lessiosh@post.harvard.edu). Manuscript received 

15 August 2008; accepted 20 April 2009.

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220 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Excirolana braziliensis Richardson is a common isopod of intertidal beaches on both sides of the Americas, 

from the Pacifi c coast of Mexico (30°N) to S. Chile (40°S) 

and from the northern Caribbean (31°N) to Uruguay (25°S) 

(Cardoso and Defeo, 2003). It is a small (approximately 

3– 4 mm in length), dioecious species, which reaches its 

highest abundance just above the high-tide mark, where 

it lives buried in the sand during low tide and rises to the 

water column at high tide to feed on live and dead fi shes 

and invertebrates (Brusca and Iverson, 1985). E. braziliensis has very limited means of dispersal. The female carries 

broods of 4 to 17 offspring per reproductive event. Young 

are released directly into the adult habitat (Klapow, 1970). 

The frequency of reproduction is such that a population 

may turn over every four months (Brusca and Iverson, 

1985). In Panama, recruitment occurs throughout the year 

(Dexter, 1977). Dispersal in E. braziliensis may occur as a 

result of feeding events, during which individuals of this 

genus have been observed attached to fi sh or other prey 

items for several minutes (Brusca, 1980). This behavior 

may represent the only means of transport of this organism between beaches because free-swimming individuals 

are likely to be eaten by fi sh.

Weinberg and Starczak (1988, 1989) reported the existence of three morphological variants of E. braziliensis

from Panama. Two similar and presumably closely related 

types, termed C and C, are found on the Caribbean and 

Pacifi c coasts, respectively. The third type (P) is morphologically distinct from C and C; its distribution overlaps 

with that of Cthroughout most of its range (Weinberg 

and Starczak, 1989). In general, Pacifi c beaches contain 

only one of the two morphotypes. Nevertheless, 2 of 43 

beaches sampled by Weinberg and Starczack (1989) were 

found to contain Cand P morphs in approximately equal 

numbers. The geographic patterns of morphotype distribution and genetic composition remain stable over time, 

but there are occasional complete replacements of entire 

beaches by a different morph, presumably as the result of 

extirpation and subsequent recolonization (Lessios et al., 

1994). Morphological and genetic divergence (based on 

allozyme data) between morphs are highly correlated and 

large enough to suggest that the P morph constitutes a distinct species (Lessios and Weinberg, 1994). The allozyme 

data are also consistent with the hypothesis that the C and 

Cmorphotypes are geminate species that resulted from 

the rise of the Panamanian Isthmus three million years ago 

(Lessios and Weinberg, 1994).

Allozyme analyses indicate that the three morphotypes of E. braziliensis are probably reproductively isolated, because they form few hybrids even when they 

co-occur at the same beach. Even within morphotypes, 

gene fl ow between populations from different beaches 

is low, as deduced from the predominance of distinct 

alleles in one or more loci, even among beaches situated 

less than 5 km apart. However, dispersal (as measured 

by individuals homozygous for alleles that otherwise occur on a different beach) is rather high, suggesting that 

some form of reproductive isolation prevents them from 

mating with individuals from the local population (Lessios and Weinberg, 1993).

The purpose of the present study is to investigate the 

phylogenetic and phylogeographic relationships within and 

between the three morphotypes of Excirolana braziliensis

using sequences of mitochondrial DNA (mtDNA). Specifi -

cally, we are addressing the following questions: (1) Does 

mtDNA show patterns of genetic divergence, phylogeny, 

and geographic distribution congruent with those suggested 

by isozymes and morphology? (2) When did the three lineages diverge? (3) What are the patterns of population 

genetic structure? Do mtDNA data show similar levels of 

gene fl ow as isozymes within and between morphotypes? 

(4) What processes can explain mtDNA discrepancies between patterns from mtDNA and allozyme markers?

MATERIALS AND METHODS

SAMPLE COLLECTION

Excirolana braziliensis were obtained from nine locations along the Pacifi c and Caribbean coasts of Panama 

(Figure 1). Each of the three morphotypes was represented 

in our collections by three populations. Isopods were collected on beaches during low tide. The top 10 cm of sand 

at haphazard locations above the high-tide mark were 

sifted through a 500 m sieve, and isopods were placed 

in plastic bags with wet sand. The collected isopods were 

brought alive to the laboratory and frozen at 80°C. The 

majority of samples used in this study were from collections made in 1988, the same collections used to assay 

isozymes (Lessios and Weinberg, 1993, 1994). Additional 

individuals were collected in 1998 from Isla Culebra. 

Specimens of Excirolana mayana were also collected at 

Isla Culebra to be used as outgroups.

DNA EXTRACTION, POLYMERASE CHAIN REACTION, 

AND mtDNA SEQUENCING

Genomic DNA was extracted using a standard phenol/chloroform protocol (Sambrook et al., 1989) with 

ethanol precipitation. For amplifi cation and sequencing 

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NUMBER 38 • 221

of 345 base pairs (bp) of the 12S mtDNA gene, we used 

the universal primers 12Sa and 12Sb (Simon et al., 1994). 

A 678 bp fragment of cytochrome oxidase I (COI ) was 

amplifi ed and sequenced with combinations of the forward primers BWBK (5-GAG CTC CAG ATA TAG CAT 

TCC-3) and ISO-F1 (5-CYC TTT TAT TAG GRA GGG 

GG-3) and the reverse primers BWBJ (5-CAA TAC CTG 

TGA GTC CTC CTA-3) and ISO-R2 (5-ACR GCA ATA 

ATT ATG GTA GC-3). The following conditions were 

used for polymerase chain reaction (PCR): initial denaturation for 2 min at 94°C, then 30 cycles of denaturation for 

30 s at 94°C, annealing for 30 s at 50°– 53°C, extension 

for 1 min at 72°C, and fi nal extension for 10 min at 72°C. 

PCR products were cleaned for sequencing using silica gel 

purifi cation columns. Cycle sequencing was carried out in 

both directions, with the ABI PRISM d-Rhodamine Terminator Cycle Sequencing Ready Reaction Kit (Applied 

Biosystematics). Sequences were obtained on an ABI 377 

automated sequencer and verifi ed and aligned by eye in 

the program Sequencher (Gene Codes Corporation). 12S 

was sequenced in 104 individuals; a subset of 22 individuals was also successfully sampled for COI, whereas the 

rest failed to amplify for this locus.

PHYLOGENETIC ANALYSIS

For phylogenetic analysis, identical haplotypes from 

multiple individuals were collapsed. We applied the program Modeltest 3.0 (Posada and Crandall, 1998) to 

calculate the goodness of fi t of various models of DNA 

evolution. The selected model for the 12S data was that 

of Tamura and Nei (1993), with equal base frequencies, a gamma distribution with a shape parameter of 

0.443, and the following substitution rates: [A— C] 

1.00; [A— G]  6.00; [A— T]  1.00; [C— G]  1.00; 

[C— T]  11.71; and [G— T]  1.00. The selected model 

for the COI sequence was a transversional model (TVM 

 I; Posada and Crandall, 2001), with a proportion of 

0.69 of invariable sites and the following substitution 

rates: [A— C]  8908.76; [A— G]  258211.81; [A— T] 

 26092.37; [C— G]  0.0001; [C— T]  258211.82, and 

[G— T]  1.00. A partition homogeneity test, executed in 

version 4.0b10 of PAUP* (Swofford, 2000), indicated that 

phylogenetic signals in the COI and 12S data were not 

signifi cantly different (P  0.256). The best fi tting model 

for the combined 12S and COI data was HKY (Hasegawa 

et al., 1985) with a transition/transversion ratio of 11.46 

and a gamma distribution shape parameter of 0.782. 

Employing these parameters, we ran phylogenetic analyses for 12S and COI separately and with the two DNA 

regions concatenated. We used the BioNJ algorithm 

(Gascuel, 1997) and heuristic searches in maximum parsimony and maximum likelihood with PAUP* (Swofford, 

2000). Bootstrap confi dence values for distance and likelihood trees were calculated in 5,000 and 500 iterations, 

respectively. Bayesian phylogeny inference was carried 

out in the program MrBayes v.3.04b (Huelsenbeck and 

Ronquist, 2001). Bayesian analyses on the COI and the 

combined data sets were run for 800,000 generations, of 

which the fi rst 20,000 (2,000 trees) were discarded. For 

12S, 2,760,000 generations were run, and 67,500 (6,750 

trees) were discarded. Convergence of chains was determined by average standard deviations of split frequencies less than 0.01 and by potential scale reduction factors approximately equal to 1.0. The trees were rooted 

on sequences of Excirolana mayana. Clock-like evolution 

of sequences was tested with likelihood ratio tests. The 

tests were carried out in PAUP* 4.0b10 by calculating the 

difference in log-likelihood of the neighbor-joining trees 

(see above) with and without the enforcement of a molecular clock and comparing the likelihood ratios to the 

2 distribution.

GEOGRAPHIC DISTRIBUTION OF GENETIC VARIATION

WITHIN MORPHS

Genealogical relationships of haplotypes within species may be better represented by networks than trees, as 

FIGURE 1. Map of Panama, indicating localities in which Excirolana braziliensis was sampled (sample size in parentheses). 1, Bocas 

del Toro (14); 2, Shimmey Beach (10); 3, Maria Chiquita (9); 4, Isla 

Santelmo (18); 5, Isla Adentro (15); 6, Causeway (6); 7, Lab (8); 8, 

Perico (10); 9, Isla Culebra (14).

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222 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

ancestral haplotypes may still be present in the population 

(Crandall and Templeton, 1993; Posada and Crandall, 

2001). We calculated unrooted parsimony haplotype networks based on 12S for each of the three morphotypes 

separately, using the computer program TCS (Clement et 

al., 2000). In this method the parsimony limit (the maximum number of differences among haplotypes as a result 

of single substitutions) is calculated with 95% statistical 

confi dence, and haplotypes are connected in order of increasing number of substitutions. To investigate the population genetic structure within each morphotype, we applied analysis of molecular variance (AMOVA; Excoffi er 

et al., 1992) to the 12S data. Genetic variation for this 

analysis was assessed based on the Kimura (1980) twoparameter distance between haplotypes. The signifi cance 

of fi xation indices was tested by 10,000 rearrangements of 

haplotypes between populations. Calculations were carried out in version 2000 of the computer program ARLEQUIN (Schneider et al., 2000).

RESULTS

DESCRIPTIVE STATISTICS AND PHYLOGENETIC ANALYSIS

Although we sampled many more individuals of Excirolana braziliensis for 12S than for COI, trees based on 

the former DNA region (Figure 2) displayed less resolution than the combined analysis of both genes together. 

Despite this, all analyses of the 12S segment alone resulted in three distinct lineages, which correspond to 

the previously described C, C, and P morphs. The 12S 

sequences of each morph were monophyletic in all analyses. The node joining C and Cwas well supported by 

maximum- parsimony analysis but fairly weakly supported by neighbor-joining, maximum-likelihood, and 

Bayesian analysis. The three main lineages were present in more than one beach, but each beach contained 

representatives of only one lineage. Although Santelmo 

had previously been found to contain a mixture of C

and P morphotypes and the allozymes corresponding 

to these morphs (Weinberg and Starczak, 1989; Lessios 

and Weinberg, 1994), all nineteen 12S sequences from 

Santelmo, differing from each other by a maximum of 

three substitutions, belonged to the Cmorph. The tree 

based on fewer sequences of COI (not shown) and the 

tree based on the combined data (Figure 3) were well resolved and gave strong support to the expected grouping 

of the C and Clineages as sister groups, irrespective of 

the type of phylogenetic algorithm used.

The 12S Tamura and Nei average distances ranged 

between 11% and 18% between morphs (Table 1). 

Within morphs, distances varied between 0% and 2.3%. 

For COI, average distances (TMV) among lineages were 

17.4%– 26.1% and within lineages 0%– 1.5%. There 

were fi ve amino acid changes in the COI fragment, of 

which four were substitutions of nonpolar for nonpolar 

residues (Met/Ileu; Val/Ileu) and one was a nonpolar for 

a polar residue (Ala/Thr). Three of the changes differentiate the C/Cand P lineage; one groups C and P, versus 

C, and one is shared between Cand P, compared to 

C. Likelihood ratio tests failed to reject the hypothesis 

of clock-like evolution of either the 12S or the COI sequences (P  0.05).

GENETIC VARIATION WITHIN MORPHS

Parsimony haplotype networks showed that populations of the C and Cmorphs, but not the P morph, were 

genetically structured (Figure 4). The most common and 

(presumably) ancestral haplotype of the P morph was 

shared by all three populations. Two derived haplotypes 

were also shared, one between all populations and the 

other between two populations. In the Cmorph two haplotypes, including the ancestral one, were shared between 

Santelmo and Isla Culebra. Although Isla Adentro contained three haplotypes not found in any other population, 

the majority of specimens from this island were of a single 

haplotype, leading to a low haplotype diversity compared 

to other populations (H  0.14). The population at Bocas 

del Toro (C morph), was characterized by high nucleotide 

diversity compared to other populations (  0.0077 

0.0045). Haplotypes from Bocas del Toro were differentiated from Maria Chiquita and Shimmey Beach by one 

to eight substitutions whereas the latter two populations 

shared the ancestral haplotype.

In the C morph, AMOVA (Table 2) found that 67.44% 

of genetic variance was partitioned among populations; 

population pairwise FST comparisons (Table 3) showed that 

all populations of this morph were signifi cantly differentiated from each other. In the Cmorph, 35.62% of the 

variance was the result of differences between populations. 

The population at Adentro had signifi cantly high FST values 

when compared to both Santelmo and Culebra, whereas 

the latter two were not signifi cantly different from each 

other (Table 3). In the P morph, all the genetic variance 

was contained within populations, a result in stark contrast 

with high levels of population subdivision seen in the other 

two morphs.

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NUMBER 38 • 223

FIGURE 2. 12S mitochondrial DNA (mtDNA) maximum-likelihood bootstrapped consensus tree relating three morphotypes (C, C, and P) of 

Excirolana braziliensis. Numbers above branches indicate maximum-likelihood bootstrap confi dence values; numbers below branches refer to 

posterior probabilities (Bayesian analysis), neighbor-joining bootstrap support, and maximum-parsimony bootstrap support, respectively, from 

top to bottom. Support values 50% are not shown. Locality codes of specimens: prco  Perico; csw  Causeway; lb  Lab; bca  Bocas 

del Toro; mcq  Maria Chiquita; shmy  Shimmey Beach; ade  Isla Adentro; bs  Isla Culebra; selm  Santelmo; xbs  Isla Culebra (xbs 

specimens were collected in 1998; all other samples were collected in 1988). See Figure 1 for the position of each locality.

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224 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

DISCUSSION

The mtDNA data presented here confi rm the results 

from analysis of both morphology (Weinberg and Starczak, 

1988, 1989; Lessios and Weinberg, 1994) and allozymes 

(Lessios and Weinberg, 1994) that Excirolana braziliensis populations from the Pacifi c and Caribbean coasts of 

Panama consist of three distinct lineages. Allozymes suggest that these lineages are reproductively isolated (Lessios 

and Weinberg, 1993) and should, therefore, be considered 

separate species. Although mtDNA data agree with morphological and allozyme data on the grouping of the C and 

Clineages as sister groups with respect to P, the relative 

magnitude of the measures of differentiation in the three 

sets of characters is different. Mahalanobis generalized 

distance from morphometric characters and Nei’s D from 

allozymes indicate that the P morphotype is three times 

more distant from C and Cthan the latter are from each 

other (Lessios and Weinberg, 1994). Mitochondrial DNA, 

on the other hand, gives a P/(C, C) distance that is only 

1.2 to 1.3 times higher than that between C/C. It is clear 

that each type of character evolves at a different rate.

A review of molecular divergence across the Isthmus 

of Panama in 34 lineages likely to have been separated 

by the fi nal closure of the Isthmus of Panama (Lessios, 

2008) has shown that during 3 million years of independent evolution (Coates and Obando, 1996; Coates et al., 

2005), crustacean COI has accumulated genetic distances 

ranging from 4.1% to 8.7% (Knowlton and Weigt, 1998; 

Schubart et al., 1998; Williams et al., 2001; Morrison et 

al., 2004) and 12S ranging from 2% to 3% (Robles et al., 

2007). Based on these calibrations, and given the differences we determined in COI and 12S, the divergence of 

the P morph from the two C morphs occurred between 9 

and 25 million years ago and that of C from the Cmorph 

between 6 and 17 million years ago. Thus, in contrast to 

what was surmised by Lessios and Weinberg (1994) on the 

basis of isozymes, mtDNA data do not support the idea 

that the C and Cmorphotypes were isolated at the fi nal 

stages of the closure of the Panamanian Isthmus, 3 million 

years ago, but rather that their populations were separated 

well before the fi nal closure. On the basis of molecular 

divergence, this appears to be also the case in 73 other 

amphi-isthmian sister lineages of crustaceans, sea urchins, 

fi shes, and mollusks (Lessios, 2008).

The combination of large mitochondrial differences 

and evidence for reproductive isolation from allozyme data 

(Lessios and Weinberg, 1993, 1994; Lessios, 1998) rules 

out the hypothesis that Cmerely represents a recently 

FIGURE 3. Combined 12S/cytochrome oxidase I (COI) mtDNA 

maximum-likelihood bootstrapped consensus tree relating three 

major lineages (C, C, and P) of Excirolana braziliensis in Panama. 

Numbers above branches indicate maximum-likelihood bootstrap 

confi dence values, numbers below branches refer to posterior probabilities (Bayesian analysis), neighbor-joining bootstrap support, 

and maximum-parsimony bootstrap support, respectively, from top 

to bottom. Localities: BCA  Bocas del Toro; MCQ  Maria Chiquita; SHMY  Shimmey Beach; SELM  Santelmo; LB  Lab; 

PRCO  Perico.

TABLE 1. Genetic distances within (along diagonal) and between 

(below diagonal) morphs of Excirolana braziliensis, for 12S 

(Tamura and Nei, 1993) and cytochrome oxidase I (COI) mitochondrial DNA (mtDNA) (in parentheses; TVM  I [Posada and 

Crandall, 2001]).

Morph C CP

C 2.25 (1.52) –– 

C11.03 (17.38) 1.36 (0.49) – 

P 16.21 (24.32) 17.84 (26.12) 1.19 (0.84)

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FIGURE 4. Parsimony network of 12S mtDNA haplotypes of the three morphs (clades) of Excirolana 

braziliensis. Each large oval represents a unique haplotype, boxes represent ancestral haplotypes, and 

small ovals indicate hypothetical, intermediate haplotypes not observed in the populations. The size of 

each shape represents the frequency of each haplotype. Numbers within each symbol indicate the number of individuals bearing each haplotype. Localities: Prco  Perico; Lab  Lab; CSW  Causeway; 

ADE  Isla Adentro; BS  Isla Culebra; SELM  Santelmo; MCQ  Maria Chiquita; BCT  Bocas 

del Toro; SHMY  Shimmy Beach.

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introduced population of C from the Caribbean into the 

Pacifi c, as had been suggested by Weinberg and Starczak 

(1988, 1989) and strengthens the case that each of the 

three lineages represents a distinct species.

POPULATION STRUCTURE AND DISPERSAL

Populations of the C and Cmorphs were characterized by population subdivision, as illustrated by high FST

estimates (overall values of 0.67 and 0.36, respectively), 

whereas samples from different localities of the P morph 

can be considered as belonging to the same genetic population (FST  0.02). Populations from Isla Adentro (C

morph) and from Bocas del Toro (C morph) stand out for 

their lack of alleles shared with individuals from other localities. Maria Chiquita and Shimmey Beach (C morph) 

also have signifi cantly different allele frequencies, whereas 

the populations at Santelmo and Isla Culebra, as well as 

at Perico, Lab and Causeway, are not signifi cantly differentiated. The two populations most divergent from others in the same morph, Adentro and Bocas del Toro, are 

also the most geographically distant from other localities 

containing individuals of their respective morphs, raising 

the possibility that dispersal to and from these localities is 

restricted as a result of physical distance. With only three 

populations per morph, statistical verifi cation of a correlation between geographic and genetic distances is not 

meaningful.

We observed several differences in the degree of population subdivision when comparing mtDNA and allozyme markers (Lessios and Weinberg, 1994). Based upon 

mtDNA sequence, the populations at Bocas del Toro and 

Shimmey Beach were the most different of all (FST  0.71), 

whereas their allozyme allele frequencies were rather similar (FST  0.097, as calculated from data in Lessios and 

Weinberg, 1993). On the whole, mtDNA data suggest a 

higher divergence between the morphs, but a lesser degree 

of subdivision between populations of the same morph, 

compared to data on allozymes. These results support Lessios and Weinberg’s (1993) fi ndings that dispersal among 

populations is much higher compared to gene fl ow, because even individuals of the same morph show some sort 

of reproductive isolation. According to their estimates, up 

to 2.5% of individuals in a locality consist of new immigrants that do not inject their genes into the host population, indicating that some form of reproductive isolation 

exists between populations of the same morph, even at 

the scale of a few kilometers. The data from Santelmo are 

interesting in this connection: This is the only locality in 

which two morphs, P and C, coexist (Lessios and Weinberg, 1993, 1994). The number of hybrids between them, 

as judged by allozymes, is lower than would be expected 

from random mating (Lessios and Weinberg, 1993), but 

hybrids do exist. However, all 19 mitochondrial haplotypes from this locality belong to the mtDNA clade that 

corresponds to the Cmorph, despite having been sampled 

from the same collections as the allozymes. Barring the 

unlikely possibility of a sampling accident, this fi nding indicates that some individuals with a P nuclear genotype, 

as manifested in morphology and isozymes, actually carry 

TABLE 2. Analysis of molecular variance (AMOVA) of Panamanian populations of Excirolana braziliensis based on 12S 

mtDNA sequences. Partitioning of genetic variance within and 

between populations (beaches) was estimated for each morph 

(clade) separately. The signifi cance of fi xation indices was tested 

by 10,000 permutations.

 Variance (%) 

 Between Within 

Morph populations populations C T P

C 67.44 32.56 0.67 0.001

C35.62 64.38 0.36 0.001

P 2.39 102.39 0.02 0.05

TABLE 3. Excirolana braziliensis population pairwise FST values 

from 12S mtDNA sequences. Bold values are signifi cant at the 

P  0.01 level.

 P Morph

Locality Lab Perico

 Perico 0.02 – 

 Causeway 0.02 0.04

 C Morph

Locality Maria Chiquita Bocas del Toro

 Bocas del Toro 0.69 – 

 Shimmey Beach 0.27 0.71

 CMorph

Locality Isla Adentro Isla Culebra

 Isla Culebra 0.58 – 

 San Telmo 0.50 0.02

226 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

15_SponerLessios_219-228_Lang.in226 226 5_SponerLessios_219-228_Lang.in226 226 9/24/09 9:48/24/09 9:48
NUMBER 38 • 227

a Cmitochondrial DNA. This, in turn, suggests that hybridization between the morphs, when it occurs, is successful in only in one direction, that is, only if the mother 

belongs to the Cclade.

In conclusion, E. braziliensis in Panama consists of 

at least three lineages (C, C, and P), which diverged well 

before the fi nal closure of the Isthmus and warrant separate species status. Populations that are more than 30 

km distant from each other (C, C) are genetically divergent, whereas those at less than 5 km (P) are panmictic 

in mtDNA, even though they are different in at least one 

allozyme locus (Lessios and Weinberg, 1994). It remains 

to be seen whether population structure is a result of isolation by physical factors or whether the three species have 

inherently different dispersal potential, and whether the 

higher degree of gene fl ow in mtDNA relative to isozymes 

is the result of sex-biased migration.

ACKNOWLEDGMENTS

We thank Alison Dwileski, Axel Calderon, and Ligia 

Calderon at Smithsonian Tropical Research Institute 

(STRI) for extensive laboratory work, and Bailey Kessing 

of STRI for expert advice and technical help in this study.

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15_SponerLessios_219-228_Lang.in228 228 5_SponerLessios_219-228_Lang.in228 228 9/24/09 9:48/24/09 9:48
Stability and Change in the Indian River 

Area Bryozoan Fauna over a 

Twenty-Four Year Period

Judith E. Winston

ABSTRACT. Two surveys describe changes and stability in bryozoan assemblages at 

sites in the temperate to tropical transition zone of the Florida Atlantic coast over a 

24-year interval in which seawater temperatures increased. Results of a monthly survey 

of the Indian River Area bryozoan fauna carried out in 1974– 1975 as part of a postdoctoral fellowship at the Smithsonian Marine Station were published in 1982. The existence of this baseline work made it possible to resurvey some of the same areas during 

1998– 1999 to determine whether the bryozoan communities at three of the sites in the 

original study had changed or remained stable. Results showed that most of the species 

that had been abundant at a site still occurred at that site 24 years later, indicating a 

high degree of stability. However, there were some important changes. Temperate species such as Hippoporina verrilli, Cryptosula pallasiana, and Bugula stolonifera, which 

had been abundant in 1974, were rare or absent in 1998. Those species were replaced 

by Caribbean species, such as Exechonella antillea and Caulibugula armata. Although 

local seawater temperatures during the time period were not available, the Fort Pierce air 

temperature records indicated that despite the year-to-year variability in both minimum 

and maximum temperatures over the seasons, mean winter air temperatures maintained 

a slow increase from 1974 to 1999.

INTRODUCTION

Most ecological research projects are carried out over a very short time 

period, the length of a research grant or dissertation project, a few years at 

most, and once the researcher moves on to new studies these research efforts are 

seldom repeated. Long-term studies are essential to document effects of climate 

change in communities over time, but the number of such publications for marine communities is extremely low compared with the number documenting the 

effects of climate change in terrestrial systems (e.g., Richardson and Poloczanska, 2008). This paper describes a repeated survey of coastal and lagoon sites 

conducted 24 years after the original survey was completed.

In 1974 and 1975, as part of my research as a postdoctoral fellow at the 

Smithsonian Marine Station, I carried out monthly surveys of the bryozoan fauna 

at fi ve intertidal sites in the Indian River Lagoon region, both in the lagoon itself 

and on the coasts of North and South Hutchinson Islands. Descriptions of the 

species found at these sites, together with descriptions of species taken in one-time 

Virginia Museum of Natural History, 21 Starling 

Avenue, Martinsville, Virginia 24112, USA (judith

.winston@vmnh.virginia.gov). Manuscript received 

13 May 2008; accepted 20 April 2009.

16_Winston_229-240_Lang.indd 229 6_Winston_229-240_Lang.indd 229 9/24/09 9:47/24/09 9:47
230 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

collections at 18 additional localities in the region and 

notes on their distribution and ecology, were published in 

a taxonomic paper, “Marine Bryozoans (Ectoprocta) of 

the Indian River Area (Florida)” (Winston, 1982). Over 

the years I returned to the area many times to study various aspects of the biology and ecology of the bryozoans 

of the region. The apparent persistence of species at particular sites year after year led me to believe that bryozoan 

communities in the area might be very stable. Yet, the 

patchiness and limited extent of the hard substrata available for settlement, combined with the fact that certain 

species were found consistently at only a single site, made 

me wonder about the potential effect of a man-made or 

natural disturbance. If a site were to be destroyed, would 

that mean the regional extinction of the bryozoan species 

uniquely found there, or did they, in fact, have additional 

refuges at other sites in the area? To begin to answer these 

questions, 24 years after the fi rst study, I resurveyed three 

of the original sites over a one year period in 1998– 1999 

to learn how stable was the species composition and to 

look for additions or losses of species at each site.

STUDY AREA

The Indian River Lagoon system, including Mosquito 

Lagoon, extends along about a third of the Atlantic coast 

of Florida, from Ponce de Leon Inlet to Jupiter Inlet, a 

distance of 295 km. Its western boundary is the Florida 

mainland, while a barrier island complex broached by several inlets forms its eastern boundary. The Indian River 

Lagoon proper is a shallow microtidal lagoon 195 km in 

length. It is believed to have the highest biodiversity of 

any estuarine system in North America, perhaps in part 

because of its location at the transition between two biogeographic provinces, the warm temperate Carolinean 

and the tropical Caribbean (Swain et al., 1995).

METHODS

The samples taken in the original survey had been 

gathered at fi rst only to acquire living colonies of as many 

species as possible for behavioral and morphological studies (Winston, 1978). As I became interested in the life 

histories of the species involved, I began collecting at the 

most convenient and interesting sites in the south central 

part of the Indian River Lagoon area on an approximately 

monthly schedule from the fall of 1974 through the summer of 1975. The sites studied were the inner break water 

at Sebastian Inlet, the Johnson House seagrass bed at 

Harbor Branch Oceanographic Institution at Link Port, 

the North Beach breakwater at Fort Pierce Inlet, Walton 

Rocks, South Hutchinson Island, and Seminole Shores, 

South Hutchinson Island. Collections from those sites 

were taken in all seasons, an important consideration in 

the seasonal environment of the Indian River Lagoon region. For bryozoans, as for many organisms inhabiting 

the area, the highest diversity is achieved and the greatest amount of reproduction, recruitment, and growth 

of colonies of most species take place during the cooler 

months (Winston, 1982, 1995). However, tropical species 

are more apt to be present or active in summer. It was 

not possible to return to Florida monthly in 1998– 1999, 

but for the best comparison to 1974– 1975, the sampling 

dates were selected to span the seasons and thus refl ect the 

known seasonality of the bryozoan fauna.

Collections were made quarterly (in November 1998, 

and February, April, and July 1999) at four sites: two 

within the lagoon and two on the open coast.

SITES SAMPLED

It was not possible to resurvey all the sites sampled 

in the original study, for reasons of time and because 

changes such as the development of some sites into offi cial county or state parks had increased restrictions on 

scientifi c collecting. The coastal sites sampled in the restudy were the North Beach breakwater, Fort Pierce Inlet 

State Park (by special permit), and the Walton Rocks area, 

South Hutchinson Island, plus one site in the Indian River 

Lagoon, the Johnson House seagrass bed. One additional 

site was chosen for the 1998– 1999 survey: the intertidal 

bridge pilings on the east side of the Route A1A causeway 

to the North Beach in Fort Pierce. This site was added 

because it was within the Lagoon, yet was close enough 

to the Fort Pierce Inlet, local marinas, and the commercial 

port in Fort Pierce to be a likely settlement spot for any 

newly arrived bryozoan species.

COLLECTING METHODS

Some bryozoan species have colonies several centimeters or more in size and are recognizable in the fi eld, but 

in many other species the colonies are microscopic and 

cryptic. Therefore collections were made by scraping hard 

surfaces and by gathering encrusted substrata: algae, hydroid stems, rocks, shells, or trash. As in the original study, 

sampling was not quantitative but was thorough. At each 

locality all microhabitats available— crevices of break16_Winston_229-240_Lang.indd 230 6_Winston_229-240_Lang.indd 230 9/24/09 9:47

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NUMBER 38 • 231

waters, surfaces of rocks, shells, wood, algae, hydroids, 

octocorals, sabellariid worm tubes, etc.— were examined 

carefully for bryozoans. In addition, encrusted examples 

of each kind of substratum available were taken back to 

the laboratory and examined alive in seawater; attached 

bryozoans were identifi ed under a dissecting microscope 

at 12– 100. Careful microscopic examination made it 

possible to identify the many tiny and/or uncalcifi ed specimens that could not be identifi ed or even detected in the 

fi eld. The condition of the colonies and the presence of 

reproductive structures and/or embryos were also noted, 

as was the relative abundance of each species at a site. 

Voucher samples for the project are deposited at the Virginia Museum of Natural History.

TEMPERATURE AND SALINITY DATA

Seawater temperatures and salinities were recorded at 

each census in this study. Temperature ranges are given in 

the results for each site. Salinity varied little. All readings 

were in the normal ocean range of the area (35– 37‰). 

The salinity range in the Indian River Lagoon can be more 

variable than that recorded at any of the sites during the 

resurvey, but low salinities are connected with periods of 

heavy rainfall, and 1998– 1999 was a drought year. No 

temperature or salinity data were collected in the original 

study, and no seawater temperature data were available 

for the area that covered the entire time period. Air temperatures for Fort Pierce were available (Figure 1) and are 

summarized in the Discussion section.

RESULTS

NORTH BEACH BREAKWATER, NORTH HUTCHINSON

ISLAND, FORT PIERCE INLET

This site was located at the southern tip of North 

Hutchinson Island. Specimens were collected from the intertidal rocks on the north side of the north breakwater 

that protects Fort Pierce Inlet. Habitats sampled included 

the rocks of the breakwater; sabellariid tubes, hydroids, 

octocorals, and algae attached to the rocks; and driftwood 

and other debris wedged among the rocks. The bryozoan 

diversity at the breakwater is largely dependent on the 

presence of the hydroid Thyroscyphus ramosus Allman, 

1877 and the soft coral Carijoa riisei (Duchassaing and 

Michelloti, 1860), whose colonies provide habitat for 

most of the epifaunal invertebrates at the site. The large 

FIGURE 1. Mean annual (A), high (B), and low (C) air temperatures (in degrees Fahrenheit) for Fort Pierce, 

Florida, from 1974 to 1998. Note: lowest, 54°F  12.2°C; highest, 83.6°F  28.7°C.

16_Winston_229-240_Lang.indd 231 6_Winston_229-240_Lang.indd 231 9/24/09 9:47/24/09 9:47
232 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

mounds produced by the sabellariid worm Phragmatopoma lapidosa Kinberg, 1867 stay clean and unfouled 

when the worms are growing actively but break down as 

they age, the mounds dissolving or becoming riddled with 

holes and channels in which other organisms settle.

At the November census, water temperature was 23.3°C. 

New sabellariid tubes were covering the old eroded sabellariid mounds on many of the rocks. The hydroids Thyroscyphus ramosus and Eudendrium carneum Clarke, 1882 

were in an active phase of growth. The cyclostome Crisia 

elongata Milne-Edwards, 1838 was the most common 

bryozoan found; masses of short young Crisia colonies 

were attached to hydroid roots and branches. Colonies 

of the encrusting cheilostome Watersipora subtorquata

d’Orbigny, 1852 were also common, attached directly to 

the rocks near the low water mark.

At the February census the water temperature was 

23.1°C. Hydroids had proliferated. Thyroscyphus and 

Eudendrium colonies were thriving, and Tubularia sp. 

and Halocordyle disticha (Goldfuss, 1820) were also present along with colonies of the octocoral Carijoa riisei. The 

worm reef was extensive and in healthy condition. Watersipora was abundant, with some small, recently recruited 

colonies present along with large mature colonies. Crisia

was still a dominant, with large mature colonies producing gonozooids containing yellow embryos.

At the April census water temperature was 25.3°C. 

Old fouled colonies of Watersipora were still present, but 

the most abundant encrusting cheilostome was Thalamoporella fl oridana Osburn, 1940, which formed thin whitish crusts and bilaminate expansions around the stems of 

Thyroscyphus. Crisia colonies with gonozooids were still 

abundant.

At the July census the water temperature was 29.2°C. 

The worm reef mounds were crumbling in places but still 

showed areas of active growth. Carijoa was abundant, and 

there were large, well-grown colonies of Thyroscyphus, 

still active, with functional polyps and characteristic garlicky smell. The most abundant bryozoan at this census 

was the primitive cheilostome Aetea sica (Couch, 1844). 

This bryozoan has a runner-like growth form, producing 

uniserial rows of semierect zooids, and an ephemeral life 

history. Species of Aetea occasionally appear in an area 

in large numbers, encrusting almost every substratum. At 

other times they may be rare or absent at the same locality. 

At this census Aetea colonies were attached to sabellariid 

worm tubes, sponges, and Codium species of algae, as well 

as to hydroid stems. Crisia was still abundant, but colonies 

were short and there were very few gonozooids. The other 

species common at this census was the branching ctenostome Amathia distans Busk, 1886, whose colonies form 

limp yellow-speckled clumps. They were attached to various substrata, including the senescent worm reef mounds.

Overall, the North Beach Breakwater site was remarkably stable in its bryozoan fauna over the 24-year 

interval. Thirty species were recorded at the site during 

this study, including 20 of the 31 species originally found 

there (Table 1). The species that were dominant in the 

original survey— Amathia vidovici (Heller, 1867), Beania hirtissima (Heller, 1967), Beania klugei Cook, 1968, 

Celleporina hassalli (Johnston, 1848), Crisia elongata, 

Pasythea tulipifera (Ellis and Solander, 1786), Savignyella 

lafontii (Audouin, 1826), Synnotum aegyptiacum (Audouin, 1826), Thalamoporella fl oridana, and Watersipora 

subtorquata— were still abundant and were present during at least three of the four censuses. In addition, two 

new species were common at this site. Amathia alternata

Lamouroux, 1816 was present at other Indian River sites 

in the past and still occurs at those sites, but it had not 

previously been recorded at the North Beach Break water. 

Caulibugula armata Verrill, 1900 is new to the region 

since the original study was carried out.

WALTON ROCKS

This site is located about 13.7 km south of Fort Pierce 

Inlet on South Hutchinson Island, on the beach just south 

of the Hutchinson Island Nuclear Power Plant (which was 

not yet constructed at the time of the original survey). The 

habitat consists of exposed sandy beach, with intertidal 

beach rock ledges; their upper surfaces are covered yearround by a macroalgal turf and seasonally by mounds of 

sabellariid worm reef. Numerous loose slabs of beach rock 

are present in a sandy trough in the surf zone between the 

ledges and the low water line. The exposed location makes 

collecting at this site diffi cult or impossible under high surf 

or wind conditions, and the full extent of the ledges is revealed only during the lowest tides of the year, and then 

only under calm sea conditions. Encrusting bryozoan species and branching species such as Scrupocellaria regularis

Osburn, 1940 occur on the undersides of both the beach 

rock ledges and loose beach rock slabs and stones. Other 

branching and encrusting species grow on the algae and 

hydroids attached to the ledges.

At the November census the water temperature was 

23.3°C. Most common were the spiny mats of the cheilostome Beania hirtissima, which were found on the underside of almost every piece of beach rock. Also common 

were the beach rock-encrusting species Exechonella antillea (Osburn, 1927), Schizoporella “unicornis,” and 

16_Winston_229-240_Lang.indd 232 6_Winston_229-240_Lang.indd 232 9/24/09 9:47/24/09 9:47
NUMBER 38 • 233

Pourtalesella incrassata (Canu and Bassler, 1928), actively 

growing peach or pink colonies with red embryos present in ovicells, along with the ctenostome Nolella stipata

Gosse, 1855. Nolella zooids are straight mud-covered 

tubes resembling miniature polychaete tubes. They are 

connected by a thin stolon, but at this site zooids were so 

thickly aggregated that the stolons were invisible and the 

colony appeared as a fuzzy mat of tubes.

At the February census the water temperature was 

23.0°C. The wind was strong because of a cold front, 

and the surf was high, making collection diffi cult. The 

macroalgal turf was thriving and mostly unfouled except 

TABLE 1. Bryozoans found () in 1998– 1999 four-season resurvey in comparison with those found in 

original survey at the North Beach Breakwater, North Hutchinson Island, Fort Pierce, Florida. Dominant species are shown in bold type; a dash (– ) indicates species not found during the resurvey.

Species November 1998 February 1999 April 1999 July 1999

Species found in 1974– 1975 survey

Aetea sica ––– 

Aeverrillia armata   –– 

Amathia distans –––– 

Amathia vidovici    – 

Anguinella palmata –––– 

Antropora leucocypha ––  – 

Beania hirtissima    – 

Beania klugei –   

Beania mirabilis –––– 

Bowerbankia imbricata  –– 

Bowerbankia maxima   –– 

Bugula minima –––– 

Bugula turrita –––– 

Celleporina hassalli    

Crisia elongata    

Cryptosula pallasiana –––– 

Exechonella antillea –––– 

Hippoporina verrilli –––– 

Jellyella tuberculata a  ––– 

Nolella stipata  ––– 

Pasythea tulipifera    

Pourtalesella incrassata a –––– 

Savignyella lafontii   – 

Scrupocellaria regularis ––– 

Synnotum aegyptiacum    

Thalamoporella fl oridana    

Valkeria atlantica –––– 

Vittaticella contei   –– 

Vittacella uberrima ––– 

Watersipora subtorquata a    

Zoobotryon verticillatum –––– 

Additional species found, 1998– 1999

Amathia alternata    – 

Caulibugula armata    

Caulibugula pearsei ––  – 

Bifl ustra arborescens a ––– 

Bifl ustra denticulata a –   – 

Bugula neritina –  –– 

Bugula stolonifera –   – 

Parasmittina sp. 3 ––– 

Rhynchozoon sp. ––– 

Schizoporella “unicornis” –  –– 

a Species for which nomenclature has been revised since Winston (1982).

16_Winston_229-240_Lang.indd 233 6_Winston_229-240_Lang.indd 233 9/24/09 9:47/24/09 9:47
234 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

by epiphytic hydroids. There were few branching bryozoans. Loose rock in the trough was almost all buried under 

sand. The colonies of beach rock-encrusting bryozoans 

collected were abraded and bleached in color.

At the April census the water temperature was 23.7°C. 

The algal turf was growing luxuriantly. Many more beach 

rock stones, some freshly broken off the ledges, were uncovered. The undersides of most rocks were completely covered 

by a cryptic community that included zooanthids, didemnid 

ascidians, sponges, anemones, and branching and encrusting 

bryozoans. Beania hirtissima was again dominant, but other 

colonies of encrusting bryozoans, including Schizoporella

“unicornis,” Exechonella antillea, Watersipora subtorquata, 

and Cryptosula pallasiana (Moll, 1803), were brightly colored and healthy. Nolella stipata zooids were clean and 

translucent, less mud-coated than in February. Colonies 

were sexually reproductive, as well; many zooids brooded 

two or three yellow-ochre eggs near their distal ends.

At the July census water temperature was 30.9°C. 

Surf was moderate, sand had fi lled in around ledges again, 

and a considerable amount of detached beach rock ledge 

algae was washed up on the beach. The undersides of large 

beach rock slabs still had a healthy cryptic fauna consisting of zooanthids, ascidians, sponges, and bryozoans on 

their undersides, despite being buried in sand. Dominant 

bryozoans were Exechonella antillea, Bifl ustra denticulata

(Busk, 1856), and Beania hirtissima, as well as Nolella stipata (which was still reproducing), plus two erect branching species, the ctenostome Amathia vidovici and the cyclostome Crisia elongata, both present as large, old, fouled 

colonies.

This site, Walton Rocks, had been the most diverse 

inter tidal site in the original study, with 36 species recorded at that time. Twenty-fi ve of the same species were 

found in 1998– 1999 (Table 2). Of the dominant species in 

the original survey, all were still present in at least two of 

the four censuses, and all but one, Parasmittina betamorphaea Winston, 2005, was present at three of the four.

The biggest change at this site was a decline in abundance of Cryptosula pallasiana and its apparent replacement in beach rock undersurface habitats by Exechonella 

antillea, which in 1974 had been found only once, at the 

North Beach Breakwater, and which had not been collected at Walton Rocks.

JOHNSON HOUSE SEAGRASS BED, INDIAN RIVER LAGOON

This seagrass bed is located about 9.7 km north of Fort 

Pierce Inlet. It lies in a shallow cove just north of the Harbor 

Branch Canal, behind the Johnson residence on the campus 

of Harbor Branch Oceanographic Institution. The grass 

bed has been the site of several studies of seagrass and soft 

substratum communities (e.g., Mook, 1976; Kulczycki et 

al., 1981; Virnstein and Carbonara, 1985; Virnstein and 

Howard, 1987) and was one of the bryozoan sites studied 

monthly in 1974– 1975. The turtle grass, Thalassia testudinum Banks and Soland. ex Koenig, is the most abundant 

seagrass at this site, but manatee grass, Syringodium fi liforme Kuetz., is also common. Drift algae fl oat among the 

grass blades.

At the November census water temperature was 

24.4°C. Collections were made of all substrata: Thalassia, Syringodium, and drift algae. Most drift algae were 

fouled by a colonial ascidian, Lissoclinum fragile (Van 

Name, 1902). The stoloniferous ctenostome Bowerbankia

maxima Winston, 1982, and the encrusting cheilostome 

Conopeum tenuissimum (Canu, 1908) were the dominant 

bryozoans.

At the February census, the water temperature was 

15.2°C, with a strong north wind. Masses of drift algae 

had been cast up on shore. Bowerbankia maxima, Conopeum tenuissimum, and the branching cheilostome Bugula 

neritina (Linnaeus, 1758) were the dominant bryozoans 

on seagrass and drift algae, respectively.

At the April census the water temperature was 23.5°C. 

Drift red algae appeared bleached in color compared with 

their February condition; other algal species appeared to 

be thriving. There had been a new settlement of spirorbid 

polychaetes onto the seagrass since February, and Conopeum had decreased in abundance on Thalassia. However, 

there were larger numbers and larger sexually reproductive colonies of Bugula neritina on the Syringodium, along 

with small recent recruits.

At the July census the water temperature was 29.7°C. 

Thalassia and Syringodium blades were heavily fouled by 

fi lamentous algae and hydroids. Large colonies of Bowerbankia maxima, clean and healthy in appearance, with 

long free-trailing masses of stolons and zooids, occurred 

on the drift algae. Conopeum tenuissimum and Schizoporella fl oridana Osburn, 1914, with recently settled recruits and with embryos in mature colonies, were found 

on the Thalassia.

In the original study nine species of bryozoans were 

recorded from this site. Six of these were collected at 

least once in the re-study (Table 3). The dominant species, Conopeum tenuissimum, Schizoporella fl oridana, 

and Bowerbankia maxima, remained unchanged. Four 

additional species, Aetea sica, Aeverrillia armata (Verrill, 

1873), Hippoporina verrilli Maturo and Schopf, 1968, 

and Scrupocellaria “bertholletii,” not recorded here in 

16_Winston_229-240_Lang.indd 234 6_Winston_229-240_Lang.indd 234 9/24/09 9:47/24/09 9:47
NUMBER 38 • 235

TABLE 2. Bryozoans found () in 1998– 1999 four-season resurvey in comparison with those found in 

original survey at Walton Rocks, South Hutchinson Island, St. Lucie County, Florida. Dominant species 

are shown in bold type; a dash (– ) indicates species not found at this location during the resurvey.

Species November 1998 February 1999 April 1999 July 1999

Species found in 1974– 1975 survey

Aetea sica ––– 

Alcyonidium polypylum    – 

Amathia alternata ––  

Amathia distans ––  

Anguinella palmata –––– 

Antropora leucocypha –  –– 

Beania hirtissima    

Beania klugei –   

Bifl ustra denticulata a ––  

Bowerbankia gracilis –––– 

Bowerbankia imbricata –––– 

Bowerbankia maxima –  –– 

Bugula neritina –  –– 

Bugula stolonifera    – 

Bugula turrita –––– 

Bugula uniserialis –––– 

Caulibugula pearsei –––– 

Celleporella carolinensis ––– 

Crisia elongata    

Cryptosula pallasiana   

Electra bellula –––– 

Jellyella tuberculata a   – 

Microporella umbracula –––– 

Nolella stipata    

Parasmittina betamorphaea a –   – 

Pourtalesella incrassata a   

Savignyella lafontii –––– 

Schizoporella “unicornis”    

Scrupocellaria regularis  –  

Sundanella sibogae  ––– 

Synnotum aegyptiacum –  – 

Thalamoporella fl oridana ––– 

Vittaticella contei –––– 

Vittacella uberrima –––– 

Watersipora subtorquata –   

Zoobotryon verticillatum –––– 

Additional species found, 1998– 1999

Aimulosia spp  –  

Amathia vidovici    

Celleporaria sp. 2   

Escharoides costifer ––– 

Exechonella antillea –   

Bifl ustra arborescens –  – 

Lichenopora sp. ––– 

Parasmittina sp. 2 ––– 

Pasythea tulipifera   –– 

Scrupocellaria “bertholletii” –  –– 

a Species for which nomenclature has been revised since Winston (1982).

16_Winston_229-240_Lang.indd 235 6_Winston_229-240_Lang.indd 235 9/24/09 9:47/24/09 9:47
236 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

1974– 1975, were also found at one or more censuses in 

1998– 1999. The three species not found during the restudy, Amathia distans, Bowerbankia gracilis Leidy, 1855, 

and Electra bellula (Hincks, 1881), were still present in 

the lagoon at other sites.

A1A CAUSEWAY

In addition to the three sites from the original study, 

one new site was also surveyed quarterly. The site is a 

shaded spot under the east end of the Route A1A causeway 

bridge to North Hutchinson Island. This site was chosen 

because of its position in the Indian River Lagoon, about 

3 km north of the mouth of Fort Pierce Inlet, and close to 

Little Jim Island, where in 1989 a Scrupocellaria species 

previously unrecorded in the region had fi rst been collected 

(Winston, 1995). Material was collected from bridge pilings, from drift algae, and from submerged wood.

At the November census water temperature was 

23.3°C. The most abundant species were Bugula neritina, 

Caulibugula armata, Bugula stolonifera Ryland, 1960 (the 

latter two reproductive), and Zoobotryon verticillatum

(Delle Chiaje, 1828). Medium-sized Zoobotryon colonies had some areas of new growth with actively feeding 

polypides.

At the February census the water temperature was 

21.1°C with a cold north wind and turbid water conditions. Bugula neritina was again dominant, with large, 

bright wine red-colored, sexually reproductive colonies. 

Other abundant species were Amathia vidovici (colonies 

mostly mud coated, but with clean actively growing branch 

tips) and long stalks of Caulibugula armata. Zoobotryon 

verticillatum was present only as short, heavily fouled, 

and senescent clumps.

At the April census water temperature was 23.2°C, 

with almost no wind and extremely clear water. Bugula 

neritina was still dominant on bridge pilings, with more 

mature and senescent colonies than in February. Zoobotryon verticillatum was still present, as large colonies drifting among seagrasses and short clumps attached to pilings, 

all of them heavily fouled, but with some young actively 

growing branches. Caulibugula armata was still present, 

with large and unfouled colonies. Amathia vidovici was 

still abundant, but colonies were heavily fouled.

At the July census water temperature was 28.8°C, 

wind calm, with fairly clear water (visibility about 1 m). 

Bugula neritina and Zoobotryon verticillatum were absent. 

Dominant species were Caulibugula armata (old, fouled 

colonies, with many brown bodies in the lower parts of 

branches, but with zooids containing feeding polypides 

and ovicelled zooids containing creamy white embryos 

near branch tips), Savignyella lafontii, a delicate branching cheilostome, Nolella stipata, and Amathia vidovici (as 

small, heavily fouled colonies).

Twelve species were found at this site (Table 4), making it less diverse than the open coast sites but more diverse 

TABLE 3. Bryozoans found () in 1998– 1999 four-season resurvey in comparison with those found 

in original survey at the Johnson House Seagrass Bed, Harbor Branch Oceanographic Institution, Link 

Port, Fort Pierce, Florida. Dominant species are shown in bold type; a dash (– ) indicates species not 

found at this location during the resurvey.

Species November 1998 February 1999 April 1999 July 1999

Species found in 1974– 1975 survey

Amathia distans –––– 

Beania klugei ––  – 

Bugula neritina –   – 

Bowerbankia gracilis –––– 

Bowerbankia maxima    

Conopeum tenuissimum    

Electra bellula –––– 

Nolella stipata –   – 

Schizoporella fl oridana    

Additional species found in resurvey

Aetea sica ––  

Aeverrillia armata  ––– 

Hippoporina verrilli  ––– 

Scrupocellaria “bertholletii ” ––  – 

16_Winston_229-240_Lang.indd 236 6_Winston_229-240_Lang.indd 236 9/24/09 9:47/24/09 9:47
NUMBER 38 • 237

than the Johnson House Seagrass Bed site (10 species) further up the lagoon from Fort Pierce Inlet. Species composition was stable; most species found there were collected in 

at least three of the four censuses. Overall dominants were 

Amathia vidovici, Bugula neritina, Zoobotryon verticillatum, and Caulibugula armata, a species that had not been 

collected in the area until about 1994.

DISCUSSION

In the 1974– 1975 study, 55 species were recorded 

from all lagoon and shallow coastal sites. Forty-nine species were recorded at the three sites later resurveyed. During the 1998– 1999 survey, 39 species were found at those 

three sites. Thus, 80% of the bryozoan species known 

originally from those sites were recollected after a 24-year 

interval, despite a smaller sampling effort (4 versus 12 collections). Seventy percent of the species found originally 

from all inshore sites combined were also found in the 

four-site resurvey, again with a much smaller sampling 

effort involved. There has been remarkable stability in 

species composition of the bryozoan fauna over the time 

period.

Sixteen species had additional localities (that is, they 

were present in the area originally, but occurred at a different site in the second study than that from which they 

had been recorded in the original survey), indicating that 

most species were not restricted to one site and could be 

expected at any or all sites provided the appropriate substratum and environmental conditions were present. Even 

though most of the species involved have nonfeeding, rapidly settling larvae, there is apparently enough dispersal 

and recruitment that disappearance from one site would 

not mean that a species would disappear from the region 

entirely. Only one species, Schizoporella fl oridana, was 

limited to one site, the Johnson Seagrass Bed, and to one 

substratum, Thalassia testudinum, and was not collected 

elsewhere in 1998– 1999.

Species new for inshore intertidal sites, but known from 

offshore hard substrata or algae (Winston and Eisman, 

1980; Winston and Håkansson, 1986), included Aimulosia 

uvulifera (Osburn, 1914), Aimulosia pusilla (Smitt, 1873), 

and Escharoides costifer (Osburn, 1914). Four species 

were newly recorded for the region during the study: two 

species of Parasmittina, a species of Celleporaria, and a 

Lichenopora species.

Although species composition remained very stable, 

species abundances changed considerably, not only from 

season to season but also between the two studies. The 

most notable changes involved the decline in abundance 

of the warm temperate species Bugula stolonifera, Cryptosula pallasiana, and Hippoporina verrilli, all of which 

have western Atlantic distributions extending northward 

to Long Island or Cape Cod. During the original study 

period abundant Bugula stolonifera colonies were found 

attached to the proximal portions of Bugula neritina colonies. In the re-study only a few colonies were found, and 

they were not in association with Bugula neritina. Hippoporina verrilli was a common species on Indian River 

Lagoon panels (Mook, 1976) and on panels and seagrasses 

in 1974– 1975, and it was also found at two coastal sites 

TABLE 4. Bryozoans found () in the 1998– 1999 four-season survey at the AIA Causeway Bridge, 

North Hutchinson Island, Fort Pierce, Florida. Dominant species are shown in bold type; a dash (– ) 

indicates species not found at this location during the resurvey.

Species November 1998 February 1999 April 1999 July 1999

Aetea sica –   – 

Amathia vidovici    

Beania klugei –   

Bowerbankia gracilis ––– 

Bowerbankia maxima    – 

Bugula neritina    – 

Bugula stolonifera  ––– 

Caulibugula armata    

Nolella stipata    – 

Savignyella lafontii    – 

Scrupocellaria “bertholletii” –   – 

Zoobotryon verticillatum  ––– 

16_Winston_229-240_Lang.indd 237 6_Winston_229-240_Lang.indd 237 9/24/09 9:47/24/09 9:47
238 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

at that time. Reproduction and settlement were heaviest in 

the cooler months (October– January). In the re-study only 

a few small colonies were found at the Johnson Seagrass 

Bed. Cryptosula pallasiana is a cosmopolitan temperate 

fouling species. In 1974– 1975 it occurred at four intertidal 

coastal sites. In the re-survey, however, it was found only 

at Walton Rocks where it was much less abundant under 

beach rock stones than originally. Instead, in the underrock habitat the dominant encrusting bryozoans in 1998– 

1999 included Exechonella antillea, a Caribbean species 

which, in the original study, had been collected only one 

time, at the North Beach Breakwater site. That original 

record itself may have indicated a range expansion for the 

species because a distributional survey by Maturo (1968) 

reported the species only from Miami south.

The other new species in the study are similarly 

warm-water species. Caulibugula armata was described 

by Verrill from Bermuda, and it is known from the Tortugas, Puerto Rico, and Brazil, according to Osburn (1940). 

Aimulosia pusilla was described from the Tortugas by 

Smitt (1873) and Aimulosia uvulifera and Escharoides 

costifer from the same locality by Osburn (1914). The 

typical Scrupocellaria bertholletii is a circumtropical species, often associated with coral reefs (Winston, 1986), 

but Indian River and other western Atlantic specimens 

show some morphological differences to those from other 

localities, indicating that Scrupocellaria bertholletii is a 

species complex rather than a single widespread species. It 

was fi rst recorded in the Indian River lagoon in 1989 and 

continues to occur at both coastal and lagoon sites. The 

genera Celleporaria and Parasmittina contain numerous 

species that are extremely successful in both tropical fouling and cryptic coral reef communities (Winston, 1986). 

The addition of species in this group is not surprising.

The increase in warm-water species has continued 

since the re-study was completed. Nellia tenella (Lamarck, 

1816), another circumtropical fouling and reef-associated 

species, was fi rst found in the Indian River area in 1999, 

in intertidal collections in Fort Pierce Inlet. It has been 

found every year since then, although its abundance has 

varied. Hippopodina irregularis, a species described form 

Guanica Harbor, Puerto Rico, by Osburn (1940), was 

fi rst found on Syringodium seagrass in Fort Pierce inlet 

in the summer of 2001. Schizoporella pungens (Canu and 

Bassler, 1928), the massive dark purple, Caribbean– Gulf 

of Mexico Schizoporella, whose colonies are characteristically found on submerged mangrove roots and in harbor 

fouling communities, had been on noted on drift plastic 

items washed ashore in the area for several years, always 

with an associated fauna of small corals and Millepora

species that suggested the debris had been colonized further south, perhaps in the Straits of Florida or the Florida Keys. Schizoporella pungens colonies fi rst recruited 

to panels in Indian River Lagoon (Faber Cove), as well 

as to numerous benthic substrata in Fort Pierce Inlet between July 2002 and July 2003. Celleporaria sherryae

Winston, 2005, another Caribbean fouling and shallow 

reef-associated species, has also appeared at some coastal 

sites (2001) and within the Fort Pierce Inlet (2003).

Reasons for the increase in warm-water species are 

harder to identify. One explanation might be global warming. As noted by many recent studies, the decade of the 

1990s was the warmest on record (Levitus et al., 2000). The 

effects of warming seawater temperatures on marine organisms, including bryozoans (Kelmo et al., 2004), have been 

noted worldwide. In addition to direct effects on growth and 

survival of benthic organisms, changes in water temperature 

also affect food supply (Menge et al., 2008; Richardson, 

2008), as well as producing indirect effects via changes in 

ocean chemistry and circulation (Harley et al., 2006).

For these collecting sites no records of seawater temperature exist for the entire time period of the two studies 

(1974– 1999). However, as these sites are all intertidal, it 

seemed reasonable to make use of the published air temperature data that were available for Fort Pierce as a substitute. Although mean annual temperatures and mean 

annual high temperatures (based on monthly averages) 

showed no discernible statistically signifi cant pattern (Figure 1A,B), there is a suggestion in the data that mean annual low temperatures (Figure 1C) have increased over the 

time period. If warm-water species are more susceptible 

to cold-water shock than high temperatures, as has been 

shown in studies of Florida fi sh kills after freezes in the 

region (Gilmore et al., 1978), warmer winter temperatures 

might be a factor permitting the invasion and survival 

of populations of the more tropical species, as has been 

shown to be the case for some introduced marine invertebrates in other studies (Stachowicz et al., 2002).

However, other factors are involved. The Indian River 

Lagoon is part of the Intracoastal Waterway, a passage 

for boat traffi c moving up and down the Atlantic coast, 

as well as in and out of the Gulf of Mexico and the Caribbean. Fort Pierce has a small commercial port with 

shipping traffi c from the Bahamas (especially Freeport, 

where containers from China and other distant sources 

are transferred for transshipment into the USA), the Gulf 

of Mexico, and the Caribbean, as well as U.S. ports along 

the east coast. Species could be introduced through ballast 

water exchange by larger ships, as well as by hull fouling 

of small and large vessels.

16_Winston_229-240_Lang.indd 238 6_Winston_229-240_Lang.indd 238 9/24/09 9:47/24/09 9:47
NUMBER 38 • 239

Although the stability of the bryozoan fauna over this 

time period gives a positive picture of the health and stability of the lagoon epifauna overall, there is no way to 

predict the long-term impact of these factors. The dependence of many bryozoans on living substrata such as seagrasses, hydroids, and octocorals also makes it clear that 

disturbances affecting substratum organisms would have 

a major impact on the bryozoans and would probably be 

more destructive to their local diversity than the environmental fl uctuations noted so far.

ACKNOWLEDGMENTS

I thank Dr. Mary Rice, Dr. Valerie Paul, and the staff 

at the Smithsonian Marine Station (SMS) for logistical support for this project, as well as for many other projects over 

the years. Special thanks are given to Julie Piraino (also of 

SMS) for SEM and digital camera assistance. I thank Drs. 

Mark and Diane Littler (Department of Botany, National 

Museum of Natural History) for collections of bryozoans 

from offshore algae. I also thank the Florida Department 

of Environmental Protection, Division of Recreation and 

Parks, for the permits (5-98-49 and 5-99-24) to collect 

bryozoans at the Fort Pierce Inlet State Park breakwater. 

This work is Smithsonian Marine Station at Fort Pierce 

(SMSFP) Contribution No. 762.

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The Turtles’ Tale: Flagships and 

Instruments for Marine Research, 

Education, and Conservation

John G. Frazier

ABSTRACT. Marine turtles are classic fl agship species. Their remarkable natural history—large body size, dependence on both terrestrial and oceanic environments, delayed 

maturity requiring decades to reach adulthood, regular migrations that crisscross ocean 

basins, massive reproductive output, mammal-like physiology, and other features—make 

them attractive to researchers and the general public alike. This attraction is further enhanced by the fact that these reptiles are widely recognized as endangered species. They 

are “biomagnets” for people around the world, from various sectors of society; incredible amounts of time, energy, and resources go into diverse types of investigation, public 

education, conservation, and international policy directed specifi cally at these “lowly 

reptiles.” Oceanographers, ecologists, geneticists, marine biologists, and specialists from 

other related disciplines frequently begin basic research projects on marine turtles. These 

activities quickly evolve into large multifaceted programs including conservation activities, community-based approaches, and public education together with other forms of 

development and social projects, and even policy initiatives for promoting regional and 

global cooperation in the conservation of these shared resources and the habitats on 

which they depend. Besides enhancing better understanding of the biology and ecology of 

these animals and nurturing more active and diverse conservation and education initiatives, work on marine turtles also promotes much-needed initiatives in interdisciplinary 

and international cooperation, which are fundamental challenges to marine work in general. This paper provides a summary of the fl agship species concept and gives examples of 

how work focused on marine turtles has promoted diverse initiatives in marine research, 

education, and conservation at multiple scholarly, social, and political levels; it argues 

that this approach serves as a critical integrating force to nurture a wider comprehension 

and appreciation of the scientifi c endeavor and its role in society.

FLAGSHIP SPECIES AND THE INCREASE 

AND DIFFUSION OF KNOWLEDGE

Scientists, educators, and conservationists who specialize on marine organisms and marine environments may all be convinced of the fundamental importance of such things as larval nectophores, pedunculate siphonophores, disappearing zooxanthellae, discharged nematocysts, mitochondrial 

cytochrome oxidase 1, maximum parsimony, and other indicators of “good 

science,” but what of the rest of society? Marine biodiversity is unique yet 

poorly understood or appreciated by the general public or decision makers; 

John G. Frazier, Conservation and Research Center, National Zoological Park, Smithsonian Institution, 1500 Remount Road, Front Royal, Virginia 22630, USA (frazierja@si.edu). Manuscript 

received 9 June 2008; accepted 20 April 2009.

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242 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

and a central question with which we all must contend 

is “How can we promote it?”

Many marine organisms have complex, intriguing life 

histories, and marine turtles, comprising just seven living 

species, are classic examples. These air-breathing reptiles 

are typifi ed by highly complex life cycles: they live with fi sh 

but nest on land, relying on terrestrial, coastal, benthic, 

and pelagic environments during different parts of their 

life cycle; they can occur in extremely dense concentrations both on land and in the sea; they are “highly migratory,” crossing ocean basins; they take a decade or more 

to reach sexual maturity and can live for half a century or 

more; and they have highly specialized morphological and 

dietary adaptations, including mammal-like physiology. A 

single female often lays more than 100 eggs in a nest and 

can lay several nests in a season. Their large body size (up 

to 1 ton), striking coloration, and primeval appearance all 

add to the attractiveness of these marine reptiles. The fact 

that marine turtles are globally recognized as endangered 

species adds a further level of importance. Hence, these 

reptiles are fl agship species: ambassadors of the oceans. 

The attraction has led to not only enormous interest on 

the part of the general public but also disproportionate attention in academic circles (Frazier, 2003a, 2005a, 2005b): 

nearly as much research is conducted on just seven species 

of marine turtles as is carried out for the remaining 300-

some species of chelonians.

In addition, marine turtles are widely valued as sources 

of meat, eggs, oil, skin, and shell, which have been utilized, crafted, and traded for millennia. A global trading 

network that supplied elite urbanites of the Mediterranean 

with raw materials from the shores of the Indian Ocean 

and beyond was well established before the time of Christ, 

and the most frequently mentioned commodity was tortoise shell (the external keratinous scutes of the hawksbill 

turtle, Eretmochelys imbricata Linn.). Intricately fashioned toilet articles, particularly ornamental combs, some 

of which were 85 cm wide, as well as a special style of 

French furniture luxuriously inlaid with tortoise shell and 

metal (“Boulle”), and religious accoutrements have all been 

made famous by the tortoise shell used in their creation. 

In addition to the tremendous diversity of objects crafted 

from turtle parts, these animals have been portrayed for 

millennia on a wide variety of media, from cave walls to 

carved rocks to delicate ceramics to the cylindrical seals 

of ancient Arabia (Frazier, 2003b, 2004a, 2005c). Hence, 

they have had very important cultural, social, and spiritual values in many societies. During contemporary times 

marine turtles have been celebrated in many and diverse 

forms, ranging from symbols of sacred nature and “pristine” environments to evidence of the evils committed by 

modern society on the environment (Campbell, 2003). All 

this conveys upon these animals a wide variety of values, 

from cultural and historic to economic and spiritual.

ACTIVITIES FOCUSED ON MARINE TURTLE 

RESEARCH AND CONSERVATION

The national marine turtle program in Brazil, which 

began as a dedicated study of reproductive biology and 

natural history, has evolved into one of the best known 

long-term programs in South America and the world in 

general, and the attraction of the turtle fl agship over the 

years has resulted in the incorporation of massive efforts 

in public education and community development, including alternate livelihoods for community residents, training, 

and facilitated interactions between different sectors of government and society, not to mention national counsel for 

regional and international policy actions (Marcovaldi et 

al., 2005). Similarly, multiyear programs in Uruguay (Laporta and Miller, 2005), northwestern Mexico (Delgado 

and Nichols, 2005), the Caribbean (Eckert and Hemphill, 

2005), and Nova Scotia (Martin and James, 2005) conduct research on diverse topics such as feeding ecology, 

reproductive biology, genetics, migration, and fi sheries interactions. All this research, as well as the associated educational and conservation activities, has been greatly facilitated—if indeed not made possible—by the attractiveness 

of marine turtles and the ease with which researchers have 

been able to make use of these fl agship species to promote 

interest in collaborating with different research activities. 

It is not uncommon for fi shermen to go out of their way 

not only to inform researchers about sightings and captures of marine turtles but also to take on extra work, 

requiring time, effort, and materials to deliver information and specimens to researchers. Frequently this means 

allowing, or even inviting, researchers to come onboard 

and make free use of the fi shermen’s vessels and materials. 

Swordfi sh fi shermen in Nova Scotia provide their vessels 

as research platforms for the complicated process of capturing, boarding, measuring, instrumenting, and releasing 

turtles of half a ton in body weight or more; researchers 

are very much aware that the success of their work depends on the altruistic behavior of fi shermen (Martin and 

James, 2005). Uruguayan fi shermen, many of whom live 

at a subsistence level, not only invite researchers to make 

use of their boats but are active collaborators in the research, attending meetings and participating in presentations (Laporta and Miller, 2005). A dramatic example of 

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NUMBER 38 • 243

the level of dedication to, and investment in, marine turtle 

projects is Theeram Pakriti Samrakshana Samiti (Coastal 

Ecosystem Protection Committee) in Kolavipalam Village, 

Kerala, India. A group of artisanal fi shermen decided to 

protect nesting turtles and their eggs, formed the committee, built a modest beach station, and now run nightly 

beach patrols, maintain an interpretation center with live 

turtles, and give public education presentations: all these 

activities have been self-organized and self-motivated, 

thanks to the attractive power of the turtles (Shanker and 

Kutty, 2005). This sort of material and moral support is 

diffi cult to evaluate adequately in simple fi nancial terms, 

but it has been absolutely essential in supporting various 

aspects of basic research, education, and conservation activities. Indeed, many of these activities would not only be 

far outside the operational budgets of the organizations 

involved but simply impossible to achieve without the full 

collaboration of the fi shing communities.

Adventure tourism, often referred to as “eco-tourism,” 

has been widely promoted around the world with marine 

turtles as the central attractants; indeed, there is even an 

international travel guidebook that is dedicated specifi -

cally to marine turtle tourism (Devaux and De Wetter, 

2000). In addition to paying their travel costs, it is not 

uncommon for tourists to actually pay for the privilege 

of working as volunteers in turtle research projects, some 

of which have been operating for decades (Campbell and 

Smith, 2005). In this way the fl agship attraction directly 

supports research through both funding and the availability of trained volunteer assistants.

An incredible diversity of outreach and public education has been developed with marine turtles as the centerpiece, a phenomenon common around the world and far 

too diverse to summarize easily (Frazier, 2005d). There are 

national and regional training programs specifi c to marine 

turtle biology and conservation, and some of these have 

been active for more than a decade, during which time they 

have seeded well-trained and enthusiastic researchers, educators, and conservationists throughout vast areas, such 

as India (Shanker and Kutty, 2005), the Caribbean (Eckert 

and Hemphill, 2005), and Latin America (Buitrago et al., 

2008; Marcovaldi et al., 2005). In some cases, the activities and festivals organized by conservationists have been 

appropriated by local people, who have completely taken 

over what were initially devised to “sensitize” and “motivate” them to collaborate with marine turtle projects. One 

of the clearest examples of the rapidly increasing and powerful attraction of marine turtles is the Annual Symposium 

on Sea Turtle Biology and Conservation, an event that is 

attended by about a thousand people, with representation 

from scores of countries and hundreds of presentations 

(Frazier, 2003a). By using the turtles as attractants “to get 

people in the door,” these activities, events, and projects 

clearly transcend the turtles and provide a wide basis of 

information on a diversity of marine organisms and environments, thereby promoting greater interest, research, 

and appreciation for these topics.

There is ample evidence that the fl agship attraction 

can be instrumental for developing popular and political 

support to affect local policy decisions, such as the creation of special protected areas and tourism management 

programs (Tisdell and Wilson, 2005). Moreover, international maritime and fi sheries policies have been directly 

affected by international, regional, and national efforts to 

conserve marine turtles, particularly through such efforts 

as mitigation of fi sheries bycatch (Bache, 2005). In fact, an 

extraordinary amount of attention has been paid to marine turtles in the fi eld of international environmental law 

(Frazier, 2002). At present there are two bilateral agreements, an incipient trilateral agreement, a program under 

a United Nations Environmental Programme (UNEP) Regional Seas convention in the southeast Pacifi c, a memorandum of understanding for the Atlantic coast of Africa, 

and another memorandum of understanding for the Indian Ocean (both under the United Nations Convention 

for Migratory Species), and a “stand-alone” treaty for 

the Western Hemisphere, all focused specifi cally on the 

conservation of marine turtles. Every one of these instruments includes measures of habitat protection, and the 

term “habitat” is even included in the title of one accord. 

Hence, through activities to protect marine turtle habitats 

over vast areas, these instruments have direct relevance 

to a wide range of marine organisms and environments, 

again clearly transcending marine turtles.

In addition to these seven agreements specifi c to marine turtles, there are many other international agreements 

that are relevant to marine turtle research, conservation, 

and education: these include such major global treaties as 

the UN Convention on the Law of the Sea (UNCLOS), 

Convention on International Trade in Endangered Species 

of Wild Fauna and Flora (CITES), Convention on Biological Diversity (CBD), and the Convention on the Conservation of Migratory Species of Wild Animals (CMS) (Wold, 

2002). Moreover, intense concern for the conservation of 

marine turtles has been instrumental in shaping policy and 

management directions in fi sheries and other maritime 

issues (Bache, 2002). For example, the Inter-American 

Tropical Tuna Commission (IATTC), which was constituted nearly 60 years ago to develop regional management of tuna stocks in the Eastern Tropical Pacifi c, has 

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244 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

been dealing specifi cally with accidental capture of marine 

turtles since 2003 and has adopted at least eight resolutions to promote mitigation measures on turtle bycatch. 

Even the United Nations Food and Agriculture Organization (FAO), originally created to enhance the production 

of food, has become intimately involved in marine turtle 

conservation. In March 2004 the “Expert Consultation on 

Interactions between Sea Turtles and Fisheries within an 

Ecosystem Context” was held in Rome (FAO, 2004), followed by a technical consultation at which guidelines for 

mitigating turtle bycatch in fi sheries were proposed (FAO, 

2005). These technical considerations and recommendations were then taken up by the political body, FAO’s 

Committee on Fisheries, where the proposal was adopted 

at a global level (COFI, 2005). The result is a set of recommendations for all States that are members of FAO 

(virtually every country that exists). Some of the specifi c 

actions that States are supposed to carry out include stock 

identifi cation and assessment, tagging and genetic studies, 

testing mitigation techniques, “pay urgent attention . . . to 

collection of statistics,” collect and share information, and 

harmonize conservation and management initiatives.

At an even greater level of political importance was 

a dispute brought before the World Trade Organization 

(WTO), which challenged the right of a Party to the WTO 

to enact unilateral measures that ban certain imports in an 

effort to protect marine turtles from capture and mortality in certain fi sheries operations. After several years of 

contentious debate and the production and exchange of 

thousands of pages of documentation, an WTO Appellate 

Body decision released on 22 October 2001 concluded that 

because marine turtles are endangered species, countries 

can take exceptions to the all-powerful free-trade rules of 

the WTO and—following certain procedures—enact unilateral measures to protect turtles, including trade embargos (Bache and Frazier, 2006; Frazier and Bache, 2002).

COMPLEXITIES OF FLAGSHIP PERCEPTIONS

It is important to point out, however, that the inappropriate use of a fl agship can lead to totally misguided 

policies and activities, counterproductive to both environmental and social needs. For example, easy access to highly 

attractive hatchling marine turtles led to an explosion of 

“sea turtle conservation hatcheries” along the coast of Sri 

Lanka, generously funded by unknowing tourists, despite 

the fact that these establishments were illegal and had negative impacts on hatchling recruitment (Tisdell and Wilson, 2005). Conservation programs that focus refl exively 

on an urgent need to do everything possible to protect marine turtles but ignore local sociopolitical complexities can 

create tremendous confl ict, for different sectors of society 

often have divergent, even confl icting, views on how to 

respond to the fl agship and what it primarily symbolizes 

(Shanker and Kutty, 2005; Frazier, 2008). Although conservationists view marine turtles as indisputable symbols 

of the need for people to cherish and protect the environment, other sectors of society—for example, certain ethnic groups—see the same turtles in very different ways, 

such as symbols of cultural identity and reclamation. This 

divergence in perceptions is true both on Pacifi c islands 

(Kinan and Dalzell, 2005) and on a Greek island in the 

Mediterranean, where contradictions in perceived value of 

the marine turtle fl agship have resulted in violence, death 

threats, and other forms of intense confl ict between different sectors of society (Theodossopoulos, 2005).

SHARED RESOURCES—THE ROOT PROBLEM

Because of their life history characteristics (particularly the long lifespan, dependence on a variety of diverse 

environments, and dispersal and migration across oceanic 

basins), marine turtles provide a classic case of shared resources, or “common property.” Simple, but basic, questions such as “Who owns turtles?” or “Who has rights to 

turtles?” clearly show that many parts of many societies 

have direct impacts, rights, and responsibilities relating to 

these animals (Frazier, 2004b). This contention is easily illustrated by the fact that more than 2 million reproductive turtles were taken from the breeding grounds in Pacifi c 

Mexico between 1964 and 1980 (Frazier et al., 2007). Yet, 

animals from this population migrate widely throughout 

the eastern tropical Pacifi c, living at different times within 

the jurisdiction of different sovereign States or on the high 

seas (Morreale et al., 2007). Who had the right to slaughter 

so many reproductive animals that are part of the fauna of 

a vast region (an action that had enormous implications on 

the status of a shared population)? The same question can 

be asked of people who pollute the oceans with oil spills, 

plastics, or other wastes: What right do they have to contaminate a common resource? Similarly, when endangered 

species of marine wildlife, such as dolphins, whales, seabirds, and marine turtles, are caught and killed in fi shing 

activities, the question arises: “What right does the fi shing 

industry have to be killing (even if it is accidentally) wildlife 

species that are valued by the citizens of many nations?”

Dealing with shared resources is the root issue for 

nearly all questions regarding biological conservation—

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NUMBER 38 • 245

particularly in marine environments. Hence, by highlighting the importance of this central problem, work on 

marine turtles brings even greater attention to this critical 

issue, and because these reptiles are regarded globally as 

endangered species, their importance is further enhanced. 

Investigations on marine turtles that help promote ways to 

resolve intractable issues of common property have implications that go far beyond chelonian biology and natural 

history: they bear on the way modern societies interact 

with the oceans.

CONCLUSIONS: 

PROMOTING MARINE RESEARCH, 

EDUCATION, AND CONSERVATION 

THROUGH FLAGSHIP SPECIES

The attention given to marine turtles spans the entire 

sociopolitical spectrum, from marginalized, politically insignifi cant fi shing communities to the most politically powerful organizations on the planet. From one extreme of the 

political continuum to the other, these animals have been 

given extraordinary importance. These local, national, regional, and global policy decisions have enormous importance in the ways that individuals, governments, and organizations at various levels assign priorities and allocate 

resources. Even if the intent is only to comply superfi cially 

with obligations that are not enforced, the end result is 

resources and personnel allotted to some aspect of marine 

turtle research, education, and conservation.

Although the scientifi c enterprise and its practitioners strive to develop and maintain an objective, unbiased view of the world, there is no escaping the fact that 

both the enterprise and the practitioners are immersed 

within complex social and political systems. The result, 

despite the fi rmest of desires, is that there is close interplay and interaction between scientifi c activities and attitudes that dominate in the surrounding society (Rozzi, 

1999). In fact, an anthropological study of the scientifi c 

establishment shows not that scientists and their practices are unique among humanity, but rather that they 

are immersed in a world of power struggles, politics, and 

myths—little different from the world of the lay public 

that is so often demeaned by the scientifi c community 

(Nader, 1996).

There is no inherent reason that information produced by scientifi c research will be read, understood, 

appreciated, followed, used, or even recognized in the 

halls of power; if practitioners of the scientifi c endeavor 

want their information to impact society outside the ivory 

towers of academia, it is essential that we learn how to 

“package” the information in digestible, understandable, 

interesting, and convincing ways (Frazier, 2005e). Flagship species greatly facilitate this exercise for they have 

values that are attractive to the general society. Used effi -

ciently and appropriately, such species are powerful tools 

for promoting research, education, and conservation of 

countless marine issues.

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Latitudinal Gradients in Recruitment 

and Community Dynamics in Marine 

Epifaunal Communities: Implications 

for Invasion Success

Amy L. Freestone, Richard W. Osman, 

and Robert B. Whitlatch

ABSTRACT. Although the latitudinal diversity gradient, where species diversity peaks 

at low latitudes, is well documented, much less is known about how species life history 

strategies differ among regions and the implications of these differences for community 

development trajectories and particularly for invasion dynamics. As a fi rst step in trying 

to understand these factors, we contrast spatial and temporal variation in recruitment 

rates and resultant community development of epifaunal assemblages in regions along a 

latitudinal gradient from the temperate zone to the tropics. We exposed settlement panels 

in four regions: Long Island Sound (Connecticut), Chesapeake Bay and Virginia’s Eastern 

Shore (Maryland and Virginia), Indian River Lagoon (Florida), and a portion of the Mesoamerican reef in Belize. Panels were deployed for either one to two weeks, to evaluate 

recruitment patterns, or one year, to monitor community development. We found that 

both recruitment and community development rates were inversely correlated with diversity, with the highest rates seen in temperate latitudes and the lowest in tropical Belize. 

Seasonal variability in recruitment also varied latitudinally, with strong summer pulses 

of recruitment in northern latitudes shifting to low and year-round recruitment at low 

latitudes. However, species turnover through time in communities becoming established 

was highest in Belize. We conclude with predictions regarding the implications these patterns may have on invasion dynamics at different latitudes.

INTRODUCTION

Latitudinal patterns in diversity have remained an important theme in ecology 

for more than a century, yet we still continue to debate the relative contributions 

of processes that may cause these patterns (Currie et al., 2004; Mittelbach et al., 

2007). There are many environmental variables that change with latitude, and it 

is easy to correlate species distribution patterns with these factors. Unfortunately, 

it is as easy to fi nd exceptions to these correlations. In addition, with increased 

transport of nonnative species (Ruiz et al., 2000), species distributions continue to 

be altered. Although latitudinal gradients in native species diversity are well documented, studies on terrestrial and freshwater systems suggest latitudinal gradients 

in invasion success occur as well (Sax, 2001). However, little work to date has 

examined this question in marine systems. Therefore, we have been documenting 

latitudinal differences in both the recruitment and the community development of 

Amy L. Freestone and Richard W. Osman, 

Smithsonian Environmental Research Center, 

647 Contees Wharf Road, Edgewater, Maryland 

21037, USA. Robert B. Whitlatch, Department 

of Marine Science, University of Connecticut, 

1080 Shennacossett Road, Groton, Connecticut 

06340, USA. Corresponding author: A. Freestone 

(freestonea@si.edu). Manuscript received 25 July 

2008; accepted 20 April 2009.

18_Freestone_247-258_Lang.indd 247 8_Freestone_247-258_Lang.indd 247 9/24/09 9:53/24/09 9:53
248 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

marine epifaunal invertebrates as a fi rst step in understanding latitudinal differences in species invasions.

The mode by which species successfully invade new 

habitats is a pressing ecological research issue (Rejmanek 

and Richardson, 1996; Williamson and Fitter, 1996; Moyle 

and Light, 1996). Current theory predicting the attributes 

of successful invaders has largely been developed in terrestrial environments and usually stresses the importance of 

life history traits associated with rapid reproduction and 

wide dispersal ability (Rejmanek and Richardson, 1996). 

In the far more open marine environment, ocean currents can disperse larvae and adults of many species for 

great distances over relatively short time periods (Jokiel, 

1984; Scheltema, 1986). Additionally, man inadvertently 

transports countless individuals and species between discrete biogeographic provinces (Ruiz et al., 1997; Carlton, 1999). Given the generally good dispersal abilities of 

marine species, those attributes of new species that allow 

them to coexist with, or even displace, native species will 

be as important as dispersal ability to a species invasion 

potential.

The sessile invertebrate or epifaunal community is an 

excellent system in which to examine rigorously both the 

life history attributes that characterize successful invaders 

as well as those attributes of native communities that govern their susceptibility to invasion. Epifaunal communities 

occur in all coastal habitats and can be found in all biogeographic regions. These communities contain species with a 

variety of life histories, yet their principal species are usually permanently attached as adults and are easy to manipulate. Although the species within these communities differ 

among regions, they function in similar ways. Most have 

planktonic larvae as the main means of dispersal, feed from 

the water column, compete for limited available space, and 

are preyed on by a variety of mobile vertebrate and invertebrate predators. Because epifaunal species are sessile and 

relatively small in size, natural communities can develop 

on small discrete substrates, with larval dispersal and recruitment linking communities within a site or habitat as 

well as within a region. These attributes make them ideal 

systems that can be experimentally manipulated in the fi eld 

to test directly hypothetical relationships while maintaining natural levels of abundance, species composition, and 

diversity.

Among epifaunal communities, a major difference is 

the number of available species that have some reasonable probability of recruiting to a particular site within a 

region. Osman and Dean (1987) found that these regional 

pools of species varied by almost an order of magnitude 

and that both the mean number of species found on individual substrates and the correlated richness at each site 

varied greatly among the study sites within each region, 

with overlap among sites in different regions. These patterns potentially result from (1) the low probability of recruits of many species in the regional species pool actually 

reaching a particular site during the course of investigation and (2) the high probability of local, within-site dispersal of species already present at a particular site. Alternatively, high predation and local extinction rates at some 

sites may prevent certain species in the regional species 

pool from colonizing these sites (Osman and Whitlatch, 

1996, 1998). As a fi rst step in trying to understand factors contributing to the local and regional differences in 

diversity and how these are likely to infl uence species invasions, we have been contrasting temporal variation in 

recruitment rates and resultant community development 

in regions along a latitudinal gradient from tropical to 

temperate regions.

METHODS

We deployed experimental panels in four biogeographic regions along the eastern seaboard of the United 

States and in the Caribbean Sea. These regions were Long 

Island Sound in Connecticut (LIS; 41°N), Maryland and 

Virginia’s Chesapeake Bay and Eastern Shore region (CB; 

37°N), the Indian River Lagoon in Florida (IRL; 27°N), 

and the vicinity of Carrie Bow Cay in Belize (BEL; 16°N). 

Polyvinyl chloride (PVC) panels, 100 cm2, were abraded to 

facilitate settlement of invertebrates and were suspended 

on racks underneath docks. The panels were held horizontal with the experimental surface facing the seafl oor.

RECRUITMENT

To estimate recruitment in all regions, panels were 

sampled either weekly (LIS) or biweekly (CB, IRL, BEL). 

At the beginning of each sampling period, four clean panels were exposed at each of the fi eld sites. After the one- or 

two-week exposure period the panels were collected and 

new panels were deployed. In the laboratory, all panels 

were examined under a dissecting microscope, and all attached invertebrates were identifi ed to the lowest possible 

taxonomic unit (usually species) and counted.

Sample schedules varied by region as necessitated 

by recruitment patterns and destructive storm activity. 

Weekly sampling at the LIS Avery Point (AP) site began 

in 1991 and has continued unabated to the present. In the 

years 1991– 1996 sampling was suspended during the win18_Freestone_247-258_Lang.indd 248 8_Freestone_247-258_Lang.indd 248 9/24/09 9:53

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NUMBER 38 • 249

ter months when almost no settlement occurs. From 1997 

to the present, sampling was conducted continuously with 

biweekly sampling during the winter. The remaining LIS 

sites (Groton Long Point [GLP] and Mystic River [MR]) 

were added in 2001 and have been sampled on the same 

schedule as the AP site. Sampling in CB and IRL was begun 

in 2004 with two sites in each region. The CB sites were at 

the Smithsonian Environmental Research Center (SERC) 

in the upper Bay and at the Virginia Institute of Marine 

Science (VIMS) in the lower Bay. The IRL sites were the 

Smithsonian Marine Station (SMS) and the Ft. Pierce Inlet (Inlet). Sampling at the VIMS site was discontinued in 

2007 after hurricane damage to the dock, and sampling at 

both IRL sites was suspended from September 2004 until 

March 2005 because of the loss of docks as the result of 

two hurricanes. Sampling in BEL began in December 2004 

and continued through February 2006.

DATA ANALYSIS

Recruitment differences among sites within and across 

regions were compared by matching means for each sampling time and using paired t tests to analyze for signifi cant 

differences. Wilcoxon signed-rank tests were also conducted for each pairing to eliminate the possible effects of 

large seasonal differences biasing the results. Because of 

the species differences among regions, analyses were done 

for total recruitment of all species, pooled invasive species, 

and pooled native species. Species identifi ed as cryptogenic 

were included with the native species. The number of sampling periods varied greatly among the regions, and we 

conducted the analysis of each pair of stations using the 

maximum number of sampling periods in common based 

on the year and week of sampling. Data were corrected 

for exposure time to account for the one- and two-week 

sampling periods used in different regions.

COMMUNITY DEVELOPMENT

To measure difference in community development, 

experimental panels (same as above) were deployed for 

at least one year and nondestructively sampled for invertebrate richness. Four panels were deployed at each 

site (three per region) between July and August 2006 to 

a depth of 0.6 m below LLT and at least 0.5 m above the 

bottom. Panels in LIS, CB, and IRL were sampled iteratively 1, 3, and 12 months after deployment. Panels in 

BEL were sampled 3, 6, and 12 months after deployment. 

Panels were sampled with a dissecting microscope, and 

attached invertebrates were identifi ed to the lowest possible taxonomic unit. Taxonomic richness on each panel 

was recorded.

RESULTS

RECRUITMENT

Three types of recruitment patterns are evident. Within 

sites there are temporal patterns, among sites within regions there are fairly consistent relationships, and together 

these produce broader patterns among the regions.

Within-Site Temporal Patterns

Within each site there are temporal patterns in recruitment that result from seasonal cycles in reproduction and 

year-to-year variation in recruitment that can result from a 

variety of causes. Seasonal variability in recruitment is most 

evident in the two northern regions, LIS and CB, which experience large variations in temperature. In both regions 

recruitment is largely absent during the coldest winter 

months. The three sites in LIS are consistent in exhibiting 

peak recruitment in the late summer (Figure 1). Recruitment at the GLP site begins earlier and remains consistently higher than at the other sites throughout the whole 

season. This site is in shallower water and consequently 

experiences lower winter temperatures and higher summer 

temperatures (Osman and Whitlatch, 2007) and warms 

more quickly in the spring. At the CB sites, the majority of recruitment occurs in the spring and early summer, 

with a second, much smaller peak period in the autumn 

(Figure 1). Most dominant species in this region such as 

barnacles, bivalves, and polychaetes are planktotrophic 

with feeding larvae dependent on the spring and autumn 

plankton blooms. Recruitment in the remaining two regions, although temporally variable, exhibits no consistent 

seasonal cycle. Recruitment occurs year round at both IRL 

sites, with the inlet having somewhat higher recruitment 

in the summer (Figure 1). Recruitment at the SMS dock is 

dominated by several species of barnacles and has much 

more sporadic peaks. Finally, BEL recruitment was extremely low and demonstrated no obvious patterns.

Spatial Variability among Sites within Regions

Within the three regions with multiple sites we have 

observed fairly consistent differences among the sites. Based 

on the paired t tests of weekly differences in total recruitment over the period 2001 through 2007, the three sites 

in LIS were signifi cantly different, with GLP AP MR 

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250 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

(Table 1). Native species recruitment at the three sites showed 

the same pattern while the recruitment of invasive species 

was not signifi cantly different among the sites (Table 2).

A similar analysis of the two CB sites for 2004 through 

2006 found that total recruitment at the VIMS site was signifi cantly greater than at the SERC site (Table 1). Recruitment at both sites was dominated by native barnacles, and 

invasive species recruitment was very low. Nevertheless 

both native and invasive species exhibited the same pattern 

as total recruitment (Table 2). Although experiencing similar variability in temperature, these two sites differ greatly 

in their salinity regimes. The SERC site is in the upper, lowsalinity region of CB whereas the VIMS site is in the lower 

CB with higher salinities. In general fewer species recruit at 

the SERC site, and barnacle recruitment is much less.

Similarly, the two IRL sites differed signifi cantly 

(2004– 2006) in total recruitment, with SMS greater than 

Inlet (Table 1). Native and invasive species exhibited the 

same pattern (Table 2). Although there was little difference between the sites in temperature and salinity, they 

did differ in dominant species, which resulted in strong 

differences in total recruitment. Barnacle recruitment (six 

different species) was consistently much higher at the SMS 

site and this contributed greatly to the overall site differences. Most species of bryozoans as well as spirorbid 

worms had higher recruitment at the Inlet site. Figure 2 

illustrates these differences.

The nonparametric paired analyses of the data from 

all three regions were almost identical to those above. The 

only difference was that in LIS invasive species recruitment 

was signifi cantly greater at GLP than at either AP or MR.

Regional Patterns

The regional differences in temporal and spatial patterns in recruitment can be seen in Figure 1. In LIS the strong 

FIGURE 1. Comparison of temporal variation in mean recruitment in the four regions. Individual sites within 

regions are shown. Means were based on 1– 6 years of data depending on region and the periods over which 

recruitment was measured (see Methods). Sampling sites are as follows: New England: AP  Avery Point, 

GLP  Groton Long Point, MR  Mystic River; Chesapeake Bay: SERC  Smithsonian Environmental 

Research Center, VIMS  Virginia Institute of Marine Science; Florida: Inlet  Ft. Pierce Inlet, SMS  Smithsonian Marine Station; Belize: Carrie Bow Cay.

18_Freestone_247-258_Lang.indd 250 8_Freestone_247-258_Lang.indd 250 9/24/09 9:53/24/09 9:53
NUMBER 38 • 251

seasonality produces a relatively normal distribution in recruitment centered on the summer months of peak temperatures. Peak periods are relatively broad, with 1,000 to 2,000 

recruits per panel per week. This overall pattern refl ects the 

concentration of recruitment by most species in the summer 

period. Recruitment in CB is also seasonal but generally 

dominated by a few species, with sharp peaks in recruitment 

of 3,000 to 10,000 individuals per panel. The pattern in IRL 

is more diffuse with recruitment occurring throughout the 

year and several sharp peaks of 2,000 to 3,000 recruits per 

panel (barnacles) over a background of continuous recruitment. Individual species do have peaks in recruitment but 

they do not occur at the same time as in the northern regions. Thus, some species recruit in the winter and others in 

the summer, and this difference is refl ected in the continuous 

total recruitment throughout the year. Finally, recruitment 

at the BEL site was extremely low, despite the much greater 

species diversity in the region.

Given these patterns, we examined whether total annual recruitment was infl uenced by the regional differences 

in variability and peak abundances. Figure 3 shows the total mean annual recruitment for each of the sites; no general pattern is discernible from these data. Except for BEL, 

within-region differences in total annual recruitment are as 

great as, if not greater than, differences among regions. Figure 3 also shows the dominance of barnacle recruitment in 

both the low-diversity CB and high-diversity IRL regions, 

whereas bryozoans and ascidians dominate recruitment in 

LIS. Interregional differences in total recruitment, regardless of strong differences in temporal patterns, exhibited no 

pattern that could be associated with diversity or latitude.

Results from the paired analyses did show some regional 

differences (Tables 1, 2; see Figure 3). For total recruitment 

the VIMS site in CB had signifi cantly greater recruitment 

than all other sites. The GLP in LIS and SMS in IRL were signifi cantly greater than the Inlet IRL, SERC CB, and AP LIS 

TABLE 1. Results of paired analysis of mean recruitment between each pair of sites. Recruitment data were 

paired by sampling time. Mean values are for 2-week sampling periods and vary based on the number of sampling dates in common between any two pairs of sites (df  degrees of freedom;). Signifi cant probabilities (Prob) 

are in bold.

 Total Annual Recruitment

Site 1 a

 Site 2 a df Mean 1 Mean 2 t-ratio Prob 1 ƒ t ƒ One-sided

Avery Point Mystic River 229 474.5 299.2 6.39 ! 0.0001 ! 0.0001

 Groton LP 252 446.6 1000.4 8.60 ! 0.0001 ! 0.0001

 SERC 21 208.4 550.8 1.44 0.16 0.08

 VIMS 21 251.3 2206.2 2.99 0.007 0.004

 SMS 38 638.2 1010.0 2.22 0.03 0.02

 Inlet 36 607.5 607.5 1.37 0.17 0.09

Mystic River Groton LP 234 296.7 996.8 9.63 ! 0.0001 ! 0.0001

 SERC 23 152.3 506.2 1.65 0.11 0.06

 VIMS 23 184.1 2097.8 3.22 0.004 0.002

 SMS 39 425.4 1068.1 4.15 0.0002 0.0001

 Inlet 38 451.2 459.9 0.09 0.93 0.46

Groton LP SERC 21 698.5 550.8 0.52 0.61 0.31

 VIMS 21 761.3 2275.1 2.11 0.05 0.02

 SMS 39 1288.4 1050.5 0.91 0.36 0.18

 Inlet 37 1192.5 471.3 3.60 0.0009 0.0005

SERC VIMS 17 381.6 1519.7 2.11 0.05 0.03

 SMS 10 341.6 685.3 1.18 0.26 0.13

 Inlet 10 341.6 242.1 0.42 0.68 0.34

VIMS SMS 15 2694.9 903.9 2.38 0.03 0.02

 Inlet 15 2694.9 169.6 3.01 0.009 0.004

SMS Inlet 71 1045.5 399.6 7.20 ! 0.0001 ! 0.0001

a Groton LP  Groton Long Point (GLP); SERC  Smithsonian Environmental Research Center; VIMS  Virginia Institute of Marine Science; 

SMS  Smithsonian Marine Station.

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252 

• SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES TABLE 2. Results of paired analysis of mean invasive and native recruitment between each pair of sites. Recruitment data were paired by sampling time. Mean values are for 2-week sampling periods and vary based on the number of sampling dates in common between any two pairs of sites. Signifi cant probabilities (Prob) are in bold. Invasive Native Site 1 a Site 2 a df Mean 1 Mean 2 t-ratio Prob 1 ƒ t ƒ One-sided Mean 1 Mean 2 t-ratio Prob 1 ƒ t ƒ One-sided Avery Point Mystic River 229 144.9 144.9 0.00 0.99 0.50 329.6 154.3 6.69 ! 0.0001 ! 0.0001 Groton LP 252 133.7 145.9 0.67 0.50 0.25 312.9 854.5 8.91 ! 0.0001 ! 0.0001 SERC 21 66.6 1.3 2.18 0.04 0.02 141.8 549.5 1.81 0.08 0.04 VIMS 21 95.8 18.8 1.94 0.07 0.03 155.6 2187.4 3.14 0.005 0.003 SMS 38 218.9 345.5 1.23 0.22 0.11 409.0 666.6 1.84 0.07 0.04 Inlet 36 203.2 191.0 0.39 0.70 0.35 381.3 270.6 1.46 0.15 0.08 Mystic River Groton LP 234 143.3 149.3 0.31 0.75 0.38 153.4 847.5 9.87 ! 0.0001 ! 0.0001 SERC 23 35.8 1.2 2.27 0.03 0.02 116.4 505.0 1.86 0.08 0.04 VIMS 23 28.9 24.0 0.60 0.55 0.28 155.1 2073.8 3.24 0.003 0.002 SMS 39 199.9 355.9 1.85 0.07 0.04 225.4 712.3 4.37 0.0001 !0.0001 Inlet 38 200.4 186.1 0.21 0.83 0.42 250.8 273.8 0.37 0.71 0.36 Groton LP SERC 21 163.7 1.3 2.31 0.03 0.02 534.8 549.5 0.05 0.96 0.48 VIMS 21 220.7 18.8 2.47 0.02 0.01 540.7 2256.3 2.47 0.02 0.01

 SMS 39 218.9 126.6 2.01 0.05 0.03 1069.5 705.0 1.50 0.14 0.07 Inlet 37 203.2 12.2 0.30 0.77 0.38 989.3 280.3 3.55 0.001 0.0005SERC VIMS 17 1.2 25.6 2.11 0.05 0.02 380.3 1494.2 2.05 0.06 0.03 SMS 10 0.4 173.1 3.11 0.01 0.006 341.2 512.2 0.63 0.54 0.27 Inlet 10 0.4 48.7 1.95 0.08 0.04 341.2 193.4 0.61 0.56 0.28VIMS SMS 15 11.0 239.4 3.23 0.006 0.003 2683.9 664.5 2.78 0.01 0.007 Inlet 15 11.0 26.6 2.38 0.03 0.02 2683.9 143.0 3.02 0.009 0.004SMS Inlet 71 374.8 138.7 5.11 ! 0.0001 ! 0.0001 670.7 260.9 5.96 ! 0.0001 ! 0.0001

a R.  River; Inlet  Ft. Pierce Inlet.

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NUMBER 38 • 253

sites, and all were greater than the MR LIS site. Recruitment 

of native species exhibited similar interregional patterns. 

However, for invasive species, recruitment was signifi cantly 

higher in IRL than CB, with the LIS sites intermediate.

COMMUNITY DEVELOPMENT

Spatial and Temporal Variability

The speed of community development varied dramatically with latitude. The primary limiting resource, space, 

was quickly occupied in the temperate and subtropical 

regions by three months, compared to the tropical communities, which took close to a year to attain comparable 

spatial coverage (Figure 4). In the northernmost region, 

LIS, growth rates were particularly high, and at one site 

(AP) panels were completely covered after only one month, 

which is a striking comparison to comparably aged communities in BEL (Figure 5). These productive communities 

in AP were primarily composed of Diplosoma listerianum, 

an invasive colonial tunicate, and Mogula manhattensis, a 

solitary tunicate. These animals quickly became too heavy 

to remain attached to the panel and sloughed off, providing another fl ush of open space to recruiting species. This 

punctuated seasonal pulse of productivity of Diplosoma

and Mogula did not occur at the other two sites in LIS, but 

growth rates remained high throughout the region.

Overall, communities in LIS experienced less temporal 

turnover in species composition than more southerly sites, 

FIGURE 2. Comparison of recruitment at the two sites in Indian River Lagoon, Florida, for the barnacle Balanus improvisus, spirorbid polychaetes (Spirorbis spp.), arborescent bryozoan Bugula neritina, and encrusting bryozoan Hipporina sp.

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254 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

particularly BEL (Figure 6). Communities in LIS were consistently dominated by bryozoans, particularly Bugula turrita, 

and both solitary and colonial tunicates (Figure 7; personal 

observations). This observation is in contrast to the higher 

rates of species turnover that characterized communities in 

tropical BEL (Figure 6; Freestone, unpublished data).

Epifaunal communities in CB had low temporal and spatial variability in species composition compared to other regions. Barnacle recruitment occurred soon after deployment, 

in July 2006. After the fi rst month, all panels had 99% to 

100% cover (see Figure 4) and were almost completely covered with barnacles, with few other coexisting species. After 

three months, community structure still closely resembled 

the one-month communities; however, barnacles began to 

die and other species, such as Mogula, various hydroids, and 

sabellid polychaete worms recruited (see Figure 7). After one 

year, the primary layer of barnacles was less visible, having 

been covered with a thick layer of sediment tubes, mostly 

from amphipods and worms. Anemones were also common 

throughout. Panels deployed at the three sites were also very 

similar. Porifera were least common in CB when compared 

with other regions throughout the experiment.

Overall, communities in IRL retained almost complete phyla representation through time (Figure 7). All 

focal phyla were found on all panels in IRL after three 

months, and only Porifera had a very modest decline by 

one year. Species in these communities coexisted at very 

small spatial scales, with the result that IRL had the most 

diverse invertebrate assemblages at the panel scale after 

FIGURE 3. Comparison of recruitment among regions. Top: Total 

annual recruitment at each of the sites within regions. The contributions in each region of major taxonomic groups are represented by 

colored shading and/or scoring within the histogram bars. Middle: 

Mean recruitment of invasive (blue) and native (red) species by sites 

within region; signifi cant differences are based on paired analyses 

(see Table 2). Bottom: Total mean recruitment by site showing the 

contribution of invasive (Inv) and native species. Dashed lines separate regions in all graphs.

FIGURE 4. Total percent cover of open space on panels in the four 

regions after 3 and 12 months (CT  Connecticut; VA  Virginia; 

FL  Florida; BZ  Belize). In Belize, space occupied by algae was 

included as covered space, so percent cover of invertebrates was even 

lower than shown.

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NUMBER 38 • 255

one year (Freestone, personal observation). More species 

turnover was apparent over the course of the year at IRL 

than in LIS or CB, but not as much as at BEL.

Communities in BEL were characterized by signifi cant 

temporal and spatial variability in species composition. 

Communities developed much more slowly than did more 

northern communities (see Figure 4), and community 

composition clearly changed with time. These communities also varied at very small spatial scales, as panels that 

were deployed within a meter of each other harbored very 

distinct community assemblages with differing amounts 

of open space. In contrast to more northern communities, 

BEL communities were more consistently dominated by 

polychaetes, Cnidaria (sea anemones, hydroids, coral), 

and Porifera. After one year, Porifera clearly dominated 

the panels (Freestone, personal observation). Compared to 

the bushy and common bryozoan colonies that occur in 

LIS, bryozoans in BEL were generally very small, delicate, 

and rare.

Similar to the recruitment study, the largest difference 

in taxonomic composition of developing communities 

across all regions was the presence of barnacles. Barnacles 

were common in temperate and subtropical zones but were 

completely absent in BEL at 3 months. After 12 months, 

their dominance was still seen in CB and IRL, but barnacles 

were less common in LIS. However, only one barnacle on 

one panel was found in BEL. Although barnacles in temperate and subtropical zones are both intertidal and subtidal, barnacles are almost exclusively intertidal in BEL.

DISCUSSION

Based on our preliminary examination of these ongoing studies, it is clear that there are both strong intraregional and interregional patterns in both the recruitment 

and the development of epifaunal communities. Seasonality 

in recruitment clearly varies with latitude. Strong summer 

peaks coupled with the almost complete absence of any 

recruitment in the winter were found for most species in 

the temperate regions (LIS and CB). The strong dominance 

of barnacles in CB resulted in a bimodal pattern generally associated with the spring– fall plankton blooms upon 

which barnacle larvae feed. In IRL there was also a strong 

temporal variability in recruitment but neither a consistent 

seasonal pattern nor any similarity among species. Finally, 

in BEL recruitment was too low to discern any pattern. 

There were also fairly distinct patterns among sites within 

regions. In the temperate regions, sites showed consistent 

differences in numbers of recruits but little difference in the 

species recruiting at any one time or in the relative abundances of these species. In the subtropical IRL, there were 

greater differences between the two sites in the composition of the fauna recruiting at any one time. Based on the 

low recruitment and greater community variability among 

sites in BEL, it would appear that site differences in recruitment in the tropics are likely to be even greater.

The interregional variation in recruitment for native 

species was infl uenced by the variation in barnacle dominance, with the CB and IRL sites showing signifi cantly 

FIGURE 5. Growth rates were higher at northern latitudes, a pattern that is clearly visible in this comparison 

between (a) a 3-week-old community from Carrie Bow Cay, Belize and (b) a 4-week-old community from 

Avery Point, Long Island Sound (100-cm2 panels are shown).

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256 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

higher recruitment than the LIS sites. However, the recruitment of invasive species varied in a similar manner 

to patterns described by Sax (2001). The tropical BEL 

site had little overall recruitment and no recruitment of 

invasive species, the subtropical IRL sites had the highest 

recruitment of invasive species, and the higher latitude 

temperate sites had lower recruitment of invasive species. 

The combined patterns of native and invasive species resulted in invasive species representing a much higher proportion of overall recruitment in IRL than in all other regions. In the low-diversity estuarine CB, invasive species 

contributed a very small proportion of total recruitment 

(see Figure 3).

Finally, even with the strong differences in recruitment 

refl ected in the paired analyses, similarities in total annual 

recruitment were found between some sites in the three 

northern regions. This result suggests that the cumulative 

recruitment in more seasonal regions with strong peaks 

and in regions with little or no seasonality in recruitment 

can be similar.

In BEL, the epifaunal communities were quite spatially 

variable in community composition even at the smallest 

scale of panels at each site. This pattern is consistent with 

the spatial heterogeneity hypothesis for the latitudinal diversity gradient, which states that abiotic variability in tropical 

systems allows more species to coexist (see Davidowitz and 

FIGURE 6. Time-series comparison of community development in (a) Long Island Sound after 1, 3, and 12 

months and (b) Belize after 3, 6, 9, 12, and 20 months (100-cm2 panels are shown). Greater species turnover 

occurred in Belize than in Long Island Sound.

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NUMBER 38 • 257

Rosenzweig, 1998). Interestingly, in contrast to the abiotic 

variation that characterizes other systems, such as terrestrial 

plant– soil relationships, the settlement panels were identical in size and material, so substrate composition was not a 

source of variability. While it is possible that differences in 

subtle small-scale variation in currents or eddies could drive 

community variability, a more parsimonious explanation is 

that propagule supply is very low and sporadic. Community developmental trajectories may therefore be more a result of random recruitment from a limited larval pool rather 

than spatial variability in abiotic conditions.

Another possible explanation that has strong theoretical underpinnings is that biotic interactions, such as predation, are also strong and spatially variable in the tropics 

(Schemske, 2002). Although this hypothesis has not been 

empirically tested in a comprehensive experiment, the idea 

that biotic interactions are stronger in the tropics has received much theoretical attention (Mittelbach et al., 2007). 

Visual observations of the communities in BEL support this 

hypothesis. For example, we commonly observed grazing 

or saw indirect evidence of grazing (i.e., abrasions) on the 

panels from indiscriminate consumers, including gastropods, crabs, and fi sh. While predation undoubtedly occurs 

in temperate environments (Osman and Whitlatch, 1995, 

1998, 2004), overall interaction strengths may be weaker 

and more spatially predictable in northern latitudes. Sporadic and low larval recruitment, spatially variable predation, and low growth rates in areas of low productivity are 

all potential contributors to the spatial and temporal variability of tropical epifaunal community development.

Our main goal has been to document and contrast 

recruitment and community development patterns among 

regions along a latitudinal gradient to ascertain potential 

differences in the ability of nonnative species to invade 

these systems. Except for our sites in BEL, all the regions 

we have been studying have nonnative species present, and 

such species are often dominant within these epifaunal 

communities. In LIS we have found that early recruitment 

of invasive ascidians in years with warm winters (Stachowicz et al., 2002a) and their dominance at harbor sites 

without native predators that prey on their recruits (Osman and Whitlatch, 1995, 1998, 2004) have contributed 

to their successful invasion. The strong and consistent timing of recruitment of native species certainly can create an 

opening for invaders that can recruit outside this window. 

In CB recruitment is even more constrained temporally 

with much higher numbers of recruits, again creating potential temporal windows for invasion. However, as our 

community development data have shown, the communities in both these temperate systems develop rapidly and 

thus quickly limit resources for new species. Studies in LIS 

(Stachowicz et al., 2002b) have shown that as community 

diversity within these systems increases, the communities 

become more resistant to invasions, mostly by increasing 

the likelihood of limiting open space.

In IRL, space was also rapidly occupied and the 

amount of open space remained low after three months. 

In addition, the diversity within this system is higher, and 

some species are recruiting at any time of the year. Based 

on the results of the LIS study (Stachowicz et al., 2002a) 

these factors should increase the resistance of this system 

to invaders. Although we have found several invasive species at our study sites, none of these species appears to be 

particularly abundant or dominant. Finally, in BEL we have 

observed much more diverse and spatially variable communities. Recruitment and the rates of community development are low, and this situation certainly allows spatial 

resource to be available for much longer periods of time, 

which should create a greater window for species invasion. 

However, the extremely high diversity of both epifaunal 

FIGURE 7. Proportion of panels that had listed taxa present at (a) 3 

months and (b) 12 months by region.

18_Freestone_247-258_Lang.indd 257 8_Freestone_247-258_Lang.indd 257 9/24/09 9:54/24/09 9:54
258 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

species and predators may inhibit invasion success. It is 

also likely that, given the spatial variability in communities, invaders will face completely different communities at 

each site as well as temporal variability in communities 

within sites. Although it is much too early in our studies 

to link latitudinal variation in recruitment or community 

development to invasion success, our preliminary results 

do suggest that there is a correlation between decreasing 

invasion success and increasing diversity, increasing community variability, and the reduction in recruitment windows in less seasonal environments, with species varying 

greatly in the timing of recruitment.

ACKNOWLEDGMENTS

We thank the Smithsonian Marine Science Network 

for support for this research. Funding from the National 

Science Foundation (NSF), U.S. Environmental Protection 

Agency (EPA), and Connecticut Sea Grant supported the 

long-term recruitment studies in Long Island Sound (LIS). 

The research at Carrie Bow Cay could not have been done 

without the support of Klaus Ruetzler, Michael Carpenter, and the many extremely helpful station managers. The 

staff of the Smithsonian Marine Station, Sherry Reed in 

particular, was instrumental in the studies being conducted 

in Indian River Lagoon (IRL). None of this research could 

have been done without their generous support. We offer 

special thanks to Gregory Ruiz and Tuck Hines for their 

helpful conversations and ideas. This work is Smithsonian Marine Station at Fort Pierce Contribution number 

786 and contribution number 843 of the Caribbean Coral 

Reef Ecosystems Program (CCRE), Smithsonian Institution, supported in part by the Hunterdon Oceanographic 

Research Fund.

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18_Freestone_247-258_Lang.indd 258 9/29/09 1:56
Ex Situ Culture of Caribbean and Pacifi c 

Coral Larvae Comparing Various 

Flow-Through Chambers

Mary Hagedorn, Virginia L. Carter, Lea 

Hollingsworth, JoAnne C. Leong, Roland 

Kanno, Eric H. Borneman, Dirk Petersen, 

Michael Laterveer, Michael Brittsan, 

and Mark Schick

ABSTRACT. Coral reefs are some of the oldest and most diverse ecosystems on our 

planet, yet throughout their range coral reefs are declining precipitously, mainly as the 

consequence of human activities. In situ conservation practices, such as habitat preservation, are an important way to protect coral reefs. However, reefs now face global 

threats in addition to local impacts. It is therefore critical that ex situ conservation activities are incorporated into conservation practices for coral reefs. Many coral species 

reproduce sexually during a limited yearly breeding season. If the resulting larvae are 

cultured, their husbandry can be very time consuming: time that is often taken away 

from larval research. Three different types of fl ow-through larval rearing systems were 

designed and tested during breeding seasons of the elkhorn coral Acropora palmata, the 

mushroom coral Fungia scutaria, and the caulifl ower coral Pocillopora meandrina. The 

fl ow-through systems were tested against static bowl rearing, and no difference was 

observed in the survival of the larvae in two of the species: P 0.12 for A. palmata

and P 0.99 for F. scutaria. These results suggested that these chambers may result in 

signifi cant savings of limited research time during a coral spawning event. However, 

P. meandrina larval survival was better in bowls than in the fl ow-through chamber (P 

0.03). Rearing the maximum number of larvae possible with minimal maintenance will 

enhance opportunities for larval research, settlement, and growth. This is especially important for species that are now threatened, for which time and information are critical 

during the breeding season.

INTRODUCTION

Coral reefs are some of the oldest and most diverse ecosystems on our 

planet. They are essential nurseries and feeding grounds for fi sh and invertebrates, act as natural storm barriers for coastlines, and are a potential source 

for novel pharmaceuticals (Colin, 1998). Throughout their range, coral reefs 

are declining precipitously, mainly because of human activities. These negative 

infl uences induce stress and can increase diseases in corals. Even in the most 

Mary Hagedorn and Virginia L. Carter, Department of Reproductive Sciences, National Zoological Park, Smithsonian Institution, Washington, D.C. 20008, USA, and Hawaii’ Institute 

of Marine Biology, University of Hawaii, P.O. 

Box 1346, Kaneohe, Hawaii 96744, USA. Lea 

Hollingsworth, JoAnne C. Leong, and Roland 

Kanno, Hawaii’ Institute of Marine Biology, 

University of Hawaii, P.O. Box 1346, Kaneohe, 

Hawaii 96744, USA. Eric H. Borneman, University of Houston, Department of Biology and Biochemistry, Houston, Texas 77204-5001, USA. 

Dirk Petersen and Michael Laterveer, Rotterdam 

Zoo, P.O. Box 532, 3000 AM Rotterdam, The 

Netherlands. Michael Brittsan, Columbus Zoo 

and Aquarium, 990 Riverside Drive, Powell, 

Ohio 43065, USA. Mark Schick, John G. Shedd 

Aquarium, 1200 South Lake Shore Drive, Chicago, Illinois 60605, USA. Corresponding author: 

M. Hagedorn (hagedornm@si.edu). Manuscript 

received 21 July 2008; accepted 20 April 2009.

19_Hagedorn_259-268_Lang.indd 259 9_Hagedorn_259-268_Lang.indd 259 9/24/09 9:47/24/09 9:47
260 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

remote marine bioreserves, such as the northwestern 

Hawaiian Islands (Maragos et al., 2004), human activities are damaging fragile coral ecosystems (Bellwood et al., 

2004). Additionally, other environmental pressures, such 

as El Niño-Southern Oscillation events, result in bleaching and coral mortality (Glynn and D’Croz, 1990; Glynn, 

1996). As greenhouse gases increase, atmospheric and seasurface temperatures and ocean acidifi cation are also expected to increase (Kleypas et al., 1999; Hoegh-Guldberg 

et al., 2007). When these effects are coupled with humaninduced stresses, reefs will remain in crisis, their existence 

worldwide increasingly threatened (Hoegh-Guldberg, 

1999; Hughes et al., 2003).

Scientists speculate that unless committed efforts are 

made to remedy this situation functional coral ecosystems 

may disappear in less than 50 years (World Wildlife Report, 2004; Hoegh-Guldberg et al., 2007). Although all 

the oceans in the world have corals, reef-building corals 

in the Caribbean are showing the greatest signs of diseaserelated mortality, and these corals may have far less than 

50 years left to survive (Hoegh-Guldberg et al., 2007). The 

massive elkhorn coral, Acropora palmata, has historically 

been the most ecologically important reef-building coral 

in the Caribbean, but its populations have declined 90% 

to 99% since the mid-1980s, primarily because of disease 

(Aronson and Precht, 2001). Because of this decline and 

its critical role for Caribbean reefs, A. palmata has been 

one of the fi rst two corals listed as “threatened” under 

the Endangered Species Act (Acropora Biological Review 

Team, 2005). As stony corals continue to die, they are being replaced with sponges, gorgonians, and algae (Hughes, 

1994; McClanahan and Muthiga, 1998), altering the composition of Caribbean ecosystems.

In situ conservation practices, such as establishment 

of marine protected areas, are an important way to protect 

coral reefs. However, reefs now face global rather than just 

local threats. Therefore it is critical that ex situ conservation techniques are incorporated into conservation actions 

for coral reefs. Ex situ conservation techniques, defi ned as 

protecting organisms outside their native habitat, such as 

rearing sexually produced larvae in seminatural enclosures 

for future restoration purposes, hold strong promise for 

improvements in preserving species and genetic diversity 

within ecosystems. This stage is particularly needed to 

help diversify some of the declining endangered populations in Florida where many of the stands of A. palmata

are genetically identical (Baums et al., 2005).

To address the ex situ conservation needs for coral 

reefs, SECORE (www.secore.org) was initiated by the 

Rotterdam Zoo in 2001 with the primary goals of studying sexual coral reproduction, specifi cally developing ex 

situ breeding techniques, disseminating techniques among 

aquarium and research communities through workshops 

and publications, developing a cooperative international 

network of public aquariums and research institutions, 

and establishing breeding programs to help sustain ex situ 

and fi eld populations. In 2006 and 2007 SECORE members representing several national and international institutions held workshops in Puerto Rico with goals to successfully rear elkhorn coral from spawn produced during 

the annual mass spawning at Rincón and Bajo Gallardo 

sites. Gametes were collected and fertilized, producing 

close to a million larvae, of which hundreds of thousands 

were raised in the fi eld laboratory and more than 400,000 

were brought into captivity, resulting in approximately 

2,300 juvenile larval recruits now living in public aquaria 

around the world (Petersen et al., 2007). These larvae 

were the fi rst juveniles of this species ever reared in captivity, constituting a major step that will help with the conservation of their genome and restoration of this species 

in the wild.

Although ex situ conservation practices have yet to be 

applied to coral populations in conjunction with restoration, extensive work has been conducted in the zoological 

community on maintaining gene diversity in populations 

with ex situ techniques (Ballou, 1992; Harnal et al., 2002; 

Pukazhenthi et al., 2006). In particular, the black-footed 

ferret was rescued from the brink of extinction, with only 

18 individuals remaining in the population, using ex situ 

conservation practices in parallel with restoration practices (Howard et al., 2003). Enhancing reproductive success of endangered coral through ex situ practices may 

be key to their future restoration and preservation (Richmond and Hunter, 1990). There are a number of ex situ 

techniques that have enhanced larval survival and settlement. Heyward et al. (2002) used a seminatural enhancement procedure for maintaining acroporid corals in open 

fl oating pools in the ocean. Water was pumped into the 

pools throughout the larval growth period, and then the 

contents were pumped into an enclosed area on the sea 

bottom with conditioned ceramic tiles. Heyward et al. 

started with 10.5  106 larvae/pool and after 144 h postfertilization had 7.5  105 larvae/pool (0.7% survival), 

resulting in 1,500 settled recruits in the best treatments 

versus 0 on the control tiles. Although this settlement rate 

was relatively low, it was far greater than the natural settlement rate and indicated a robust enhancement of recruits 

for this area.

Most current coral larval husbandry practices are 

low-cost efforts, such as bowls or aquaria fi lled with fi l19_Hagedorn_259-268_Lang.indd 260 9_Hagedorn_259-268_Lang.indd 260 9/24/09 9:47

/24/09 9:47
NUMBER 38 • 261

tered seawater, and these methods are very successful at 

rearing larvae (Babcock and Heyward, 1986; Schwartz et 

al., 1999; Petersen et al., 2007). The problem is that these 

time-consuming and labor-intensive husbandry practices 

compete with the limited time available for research during a coral breeding season, especially if the coral species is limited to a single annual breeding, as is Acropora 

palmata. For coral in need of replenishment, rearing the 

maximum number of larvae possible with the least time invested in husbandry would enhance opportunities for larval growth and settlement (Richmond and Hunter, 1990; 

Petersen and Tollrian, 2001; Borneman, 2006). The goal 

of this paper was to design and test simple fl ow-through 

systems in the fi eld that would minimize husbandry and 

yet successfully rear large numbers of coral larvae without compromising survival.

Three species of coral larvae were tested in three different types of rearing chambers. These larvae were selected 

because they represented a good cross section of coral larval types with different buoyancies, swimming behaviors, 

and rates of development that might benefi t from these 

chambers. Acropora palmata are large lipid-fi lled fl oating larvae (Figure 1a) that develop slow swimming ability 

in the water column after 48 h. Fungia scutaria are small 

negatively buoyant larvae containing modest lipid stores. 

These larvae develop rapid swimming behavior in the water column within 12 to 24 h (Figure 1b). Pocillopora meandrina are negatively buoyant larvae with modest lipid 

stores (Figure 1c); these larvae develop slow swimming behavior along the bottom after 24 h. In designing and constructing these low-tech chambers, we made an effort to 

use materials for their components that are affordable and 

available in most hardware stores throughout the world.

MATERIALS AND METHODS

LARVAL COLLECTION AND REARING

Acropora palmata eggs and sperm were collected during the annual spawn from Tres Palmas Reserve (Rincon, 

Puerto Rico) and the offshore submerged bank Bajo Gallardo (Boqueron, Puerto Rico) in August 2007. Egg/sperm 

bundles were collected in the water over the spawning coral 

with 1 L plastic Nalgene bottles attached to fi ne mesh nets. 

The egg/sperm bundles were brought to shore in the plastic 

bottles, separated by gentle agitation, and then combined 

with the eggs and sperm from at least three to four individuals to yield a sperm concentration of approximately 106

cells/mL (fi nal concentration in water). The eggs and sperm 

were gently agitated for 2 h, cleaned with 1 m-fi ltered 

seawater, assessed for fertilization rates, and released into 

rearing chambers for subsequent development.

Fungia scutaria eggs and sperm were collected from 

captive animals held in fl owing seawater tanks from June 

through October 2006 at Coconut Island, Hawaii. Animals were prepared for spawning following the methods 

of Krupp (1983). Briefl y, as a female spawned, these eggs 

were gently moved into a plastic bowl and fertilized with 

150 mL sperm (106 cells/mL, fi nal concentration in water) from four or fi ve males. The embryos, resulting from 

several male and female gametes, were kept in a single plastic bowl (8 L) and left overnight to develop. In the morning 

the developing larvae were cleaned with four changes of 

0.5 m-fi ltered seawater and then released into their rearing chambers for subsequent development.

Egg/sperm bundles were collected from Pocillopora 

meandrina fragments in April and May 2008 from Coconut Island, Hawaii. The eggs and sperm were separated 

FIGURE 1. Three species of coral were reared in this study. a, Acropora palmata, elkhorn coral; inset: larvae at 24 h postfertilization. b, Fungia 

scutaria, mushroom coral; inset: larvae at 96 h postfertilization. c, Pocillopora meandrina, caulifl ower coral; inset: larvae at 96 h postfertilization. All scales 50 m.

19_Hagedorn_259-268_Lang.indd 261 9_Hagedorn_259-268_Lang.indd 261 9/24/09 9:47/24/09 9:47
262 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

by gentle agitation, and then combined with the eggs and 

sperm from at least three or four individuals to yield a 

sperm concentration of approximately 106 cells/mL. The 

eggs and sperm were gently agitated for 0.5 h, cleaned with 

0.5 m-fi ltered seawater, and left overnight to develop. 

The next morning the developing larvae were cleaned with 

0.5 m-fi ltered seawater and released into their rearing 

chambers for subsequent development.

Digital images of the larvae from all three species were 

captured with an Olympus BX41 microscope with an attached digital camera Sony DFWV300, and the major and 

minor axes were measured with NIH Image software.

CONSTRUCTION OF REARING TANKS 

AND MEASUREMENT OF DENSITIES

Larval corals were reared in three different designs 

of fl ow-through chambers (Figures 2– 4), as well as static 

bowls that required daily cleaning and water changes. The 

names of these chambers were chosen to describe the major water movement they provided to the larvae. All developmental times reported throughout the paper are in 

hours postfertilization.

Up-Flowing Tanks

These tanks were made from 20 L heavy-walled plastic 

pans (U.S. Plastics Corp., Lima, Ohio) modifi ed by covering the handles in a buoyant foam and removing four panels from the bottom and replacing them with nylon screening (240 m mesh). A central cross-shaped area was left 

intact to create an inlet for upward-directed water fl ow; 

then additional shear fl ow was added with four additional 

adjustable water inlets around the edges approximately 

16 cm above the bottom, yielding a fi nal volume in the 

chambers of 23 L (see Figure 2). All fl ow was regulated 

by valves to optimize the slow tumbling movement of the 

larvae in the chamber. The fl oating chambers were immersed in large 2,400 L pools to stabilize their temperature 

(28°– 31°C) and mimic natural temperature cycles throughout a 24 h period. To maintain water quality close to that 

which the larvae would experience in open water, the chambers were attached to a fi ltered (1 m) fl ow-through system 

with seawater pumped from the reserve, so that water was 

completely exchanged in the chambers several times each 

day. Flow rates through the chambers were maintained 

at approximately 2 L/min, and the bath of fresh seawater 

surrounding the chambers was turned over about one to 

two times per hour. Salinity, temperature, and pH closely 

mimicked natural conditions without additional effort. 

Approximately 1,000 to 1,500 larvae/L were fertilized in 

50 mL conical plastic tubes, then placed into either the upfl owing tanks (n 2) or static bins. Counts were taken immediately, and then daily for all groups. Bin density began 

at 900 larvae/L, and the two fl ow chambers contained 

either 1,100 or 1,500 larvae/L. The fertilization rate for A. 

palmata spawn used for these tests was 90%.

FIGURE 2. Larval rearing of Acropora palmata larvae. a, Up-fl owing 

tank used to rear the A. palmata larvae. b, There was no signifi -

cant difference in survival between the up-fl owing tanks and static 

bins (ANCOVA, P 0.12). Points show mean counts for each trial. 

Larvae in the upward-fl ow tanks were developing rapidly (28°C) 

while those in the static bins were maintained at a slightly lower temperature (25°C). Larvae in the fl ow chambers were removed from 

the experiment one day earlier than those in the bins to ship them to 

an aquarium for settlement and rearing.

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NUMBER 38 • 263

The static treatments used for comparison with the 

up-fl owing tanks were plastic rectangular bins (length [L] 

 width [W] 51 cm  36 cm) with water depth of 12 

cm, yielding a volume of 22 L. These tanks were maintained in an air-conditioned room; the water was maintained at 25° to 26°C and changed twice daily. To keep 

the fl oating A. palmata larvae from clumping and forming 

an anoxic layer, the water and fl oating larvae were stirred 

every hour with a bubble-wand (2-mm-diameter rigid air 

line attached to a small air pump) throughout the rearing 

period. The previous year, a stocking density of approximately 1,000 A. palmata larvae/L was used successfully in 

each bin and we used this same level for these tests. Larvae 

from the same spawn and bulk fertilization as were used 

in the chambers were placed in the static bins (n 2) 2 h 

after fertilization.

To determine larval survival, the chamber and static 

containers were stirred to suspend the larvae evenly in the 

water column, and fi ve 15 mL samples were taken and 

the number of larvae counted each day. The number of 

larvae/mL was multiplied by 1,000 to determine the density per liter (density/L). The larvae in both systems were 

only allowed to develop for two to three days, and then 

they were packaged for shipment. Approximately 4,000 

larvae were placed into a 2 L Nalgene bottle with fi ltered 

sea water (FSW); the bottles were fi lled to the top with 

FSW and capped leaving no bubbles, taped for security, 

placed horizontally in a cooler (8– 12 bottles were placed 

in a single cooler), and sent by express mail to aquaria 

throughout the USA.

Spiral-Flowing Tanks

Small conical fi berglass tanks (75 L) were fi tted with 

a central standpipe covered with 40 m nylon mesh to rear 

Fungia scutaria larvae (see Figure 3). To maintain the water quality close to that which the larvae would experience 

under natural conditions, the conical tanks were attached 

to a fi ltered (0.5 m) fl ow-through system with seawater 

FIGURE 3. Larval rearing of Fungia scutaria. a, Drawing of assembled spiral-fl owing tank and its fl ow, mixing, and position of dye experiments. Curved lines with arrowheads indicate direction of water 

fl ow spiraling upward from one inlet of a Loc-Line (both inlets had 

fl ow, but for simplicity fl ow from only one is drawn). Double arrows 

indicate water freely fl ows into and back out of the mesh areas on 

the standpipe. Asterisks (*) indicate locations in the water column 

where dye was injected for dye tests. b, Survival rate of F. scutaria

larvae maintained in the spiral-fl owing tank (upper graph, “Flow”) 

and the static bowls (lower graph, “Bowls”) between 24 and 144 h 

postfertilization. Each point shows mean and standard error. There 

was no difference in survival of larvae from fl ow chambers and static 

bowls (ANCOVA, P 0.99).

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264 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

pumped from the reef. Flowing fi ltered seawater entered 

the top of the central tube and moved through nozzles 

at the tank base to produce gentle circular movement 

throughout the water column, and the wastewater exited 

the tank through the mesh-covered outfl ow. The fl ow rate 

was 150 to 300 mL /min, producing a complete turnover 

in the tanks approximately every 4 to 8 h. To test whether 

the conical tank could support the growth and development of F. scutaria, approximately 10,000 larvae/ L were 

stocked in the conical tanks (n 4) tanks. To reduce mortality of the early fragile stages (0– 24 h postfertilization) 

from excessive motion in the fl ow-through chambers, the 

spiral-fl ow tanks were tested with 24 h postfertilization 

larvae. Therefore fertilization rate was not an issue, because all the larvae used for these tests were intact and 

developing. A comparison of the static bowl method (with 

daily cleaning) and the fl ow-through method was then performed to determine survival rate over time (up to 144 h 

postfertilization).

The static treatments used for comparison to the conical tanks were 3 L plastic bowls that had been the standard for successfully rearing F. scutaria larvae for many 

years (Schwarz et al., 1999). At 24 h postfertilization, F. 

scutaria larvae from 10 bowls were combined and evenly 

distributed into 2 larger bowls. Counts (see below) were 

taken for each bowl, and a standard rearing density was 

redistributed into 8 separate smaller bowls at a larval density of 100,000 larvae/L fi ltered seawater.

Fungia scutaria larvae were counted each day by gently stirring to homogeneously suspend them in the water 

column. Ten 1 mL samples were taken midwater from each 

conical fl ow-through tank and placed into a SedgewickRafter counting chamber; the larvae were counted with 

a dissecting microscope and their numbers averaged. In 

addition, 10 samples (20 L each) were taken midwater 

from each bowl, the number of larvae counted under a 

dissecting microscope, and their numbers averaged. These 

smaller 20 L samples were assessed from the F. scutaria

because of their high densities in the chambers.

Down-Flowing Tank

In April 2008 we attempted to rear Pocillopora meandrina larvae in the spiral-fl owing tanks, but because of 

the negatively buoyant nature of the larvae, this method 

resulted in 100% mortality. Therefore, we developed a 

down-fl owing tank for rearing P. meandrina larvae in May 

2008 (see Figure 4). The tank was constructed of a 1.65 L 

glass bowl with a plastic lid. The center of the lid was removed and replaced with 40 m mesh, leaving a 2 cm ring 

around the outside in which a hole was made to insert a 2 

mm plastic rigid air line attached with air-line tubing to a 

manifold for controlling water fl ow. To maintain the water quality close to that which the larvae would experience 

in the open water, the down-fl owing tanks were attached 

to a fi ltered (1 m) fl ow-through system with seawater 

pumped from the reef. Flow to the tanks was maintained 

at 120 mL/min.

The larvae were fertilized in 50 mL tubes, rinsed with 

sterile fi ltered seawater, and placed into two bowls at 

28°C to develop overnight at a density of approximately 

80,000/L. After 24 h postfertilization, larvae were counted 

and then cleaned using a 40 m mesh and 0.5 m-fi ltered 

FIGURE 4. Larval rearing of Pocillopora meandrina. a, Downfl owing tank used to rear P. meandrina. b, Curves for larval survival 

in the static (“Bowl”) and down-fl owing (“Flow”) tanks did not 

have the same slope (ANCOVA, P 0.03); bowl rearing for this 

species produced substantially better survival than the down-fl owing 

tank. Points show mean counts for each trial and standard error of 

the mean.

19_Hagedorn_259-268_Lang.indd 264 9_Hagedorn_259-268_Lang.indd 264 9/24/09 9:47/24/09 9:47
NUMBER 38 • 265

seawater. One group was placed into the downward-fl ow 

chamber at a fl ow rate of 120 mL/min with a 40 m mesh 

top to allow the water to fl ow out. The other bowl remained static. P. meandrina larvae were cleaned (static 

bowl only) and counted daily from the fl ow tanks and 

static bowl (maintained as described for F. scutaria above) 

for comparison.

STATISTICS

To determine the differences between survival in 

fl ow chamber versus static treatment, the data from all 

experiments was normalized and the y-values linearly 

transformed; analysis of covariance (ANCOVA) was then 

performed to determine whether the slopes were signifi -

cantly different, using GraphPad Prism 5 software for the 

Macintosh GraphPad Software (San Diego, CA).

RESULTS

Rearing chambers were designed for three different 

coral species exhibiting different larval swimming behaviors, buoyancy, and sizes.

Up-Flowing Tank

Acropora palmata was the largest of the larvae studied 

(700  500 m depending on the developmental stage) 

and had the slowest rate of development (see Figure 1a). A. 

palmata larvae fl oat at or near the surface of the water approximately 48 to 60 h postfertilization (depending on the 

temperature) until they began swimming. Even once they 

had begun swimming, they swam at or near the surface 

and were considered positively buoyant for most of their 

larval development before metamorphosis and settlement 

(144 h). Clearly, all the larvae must become negatively 

buoyant before settlement; therefore, these categories only 

apply to the early larval periods (up to 120 h, depending 

on the species).

During the fi rst 24 h of development, the larvae developed asymmetrical, small protrusions of cells that could 

have easily be damaged in the up-fl owing tank, but the 

chamber produced normally developed A. palmata larvae 

(as compared to the bins) because it simulated the gentle 

tumbling that the larvae would experience in the natural 

water (see Figure 2). Larval survival in the up-fl owing 

tanks was similar to that in the static bins (P 0.12) (Figure 

2a). However, the up-fl owing tank did not produce viable 

larvae for F. scutaria and P. meandrina. This tank produced 

100% mortality in F. scutaria larvae within 24 h, even if 

the larvae were slightly more developed when placed in 

the chambers.

Spiral-Flowing Tank

Dye injection studies were performed on the spiralfl owing tank, using food coloring to examine the mixing 

properties of the vessel with an inlet fl ow of 150 mL/min. 

Figure 3 illustrates the mixing pattern in the fl ow-through 

vessel. Flow into and out of the system was equal, but the 

open area of the slits in the 10 cm central polyvinyl chloride (PVC) tube dictated the velocity through the screens. 

The nozzles were angled slightly downward to promote 

turbulence at the bottom to keep the larvae well mixed. 

The 180° positions of the nozzles provided rotation within 

the water column and encouraged mixing. Dye studies 

with separate injections were made at positions noted by 

asterisks (*) in Figure 3. At a fl ow of 150 mL/min, full 

vertical mixing occurred within minutes.

Developing F. scutaria larvae were fairly small (200 

 100 m) and fragile during the fi rst 12 h of development and were just negatively buoyant during their early 

embryonic period (0– 12 h postfertilization) (Figure 1b). 

However, once they began swimming, they were evenly 

distributed in the water column, and we considered this 

species to be neutrally buoyant. There was no difference 

in the survival between the spiral-fl owing tank and bowls 

(P 0.99). Both rearing systems produced similar survival 

rates in which the densities remained relatively steady 

through 96 h postfertilization and then dropped off at 120 

to 144 h postfertilization (see Figure 3). This decrease in 

densities may refl ect the complete absorption of stored fats 

(M. Hagedorn, unpublished data), as these larvae did not 

have zooxanthellae. P. meandrina larvae were tested in the 

spiral-fl ow tank, but 100% mortality was observed after 

48 h postfertilization.

Down-Flowing Tank

Pocillopora meandrina larvae were the smallest of the 

larvae tested (120  40 m); they began slow swimming 

at 24 h but were negatively buoyant for the remainder of 

their larval development, remaining on or near the bottom (Figure 1c). Similar to F. scutaria, P. meandrina larvae 

were relatively susceptible to damage within the fi rst 24 

h, so they were reared in 3 L bowls for the fi rst 24 h. The 

down-fl owing tank was used for rearing P. meandrina; 

however, the static bowls appeared superior to the downfl owing tank for this species (P 0.03) (see Figure 4).

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266 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

DISCUSSION

For many years, large numbers of coral larvae have 

been reared successfully using simple husbandry methods 

such as static bowls and tanks. We have demonstrated 

that species of buoyant and neutrally buoyant coral larvae have similar survival in either static or fl ow-through 

chambers (see Figures 2, 3). These devices have proven to 

be very useful in improving culture conditions to reduce 

husbandry labor because neither embryos nor fresh water 

needed to be constantly transferred.

Modifi ed examples of the up-fl owing tank have already been used successfully by coral restoration biologists in the fi eld (Margaret Miller, NOAA Southwest 

Fisheries Center, personal communication). Montastraea 

faveolata and Diploria strigosa were reared successfully 

in the up-fl owing tanks and shipped to Columbus Zoo 

and Aquarium for settlement with 3-month survival as 

high as 65% and 45% for each species, respectively. 

Thus, the up-fl owing tank has proven to be both practical, in that it can be adapted to the researcher’s needs, and 

valuable, because it reduced husbandry time and facilitated restoration science under fi eld conditions.

In weighing the benefi ts of each rearing system, one 

of the biggest factors to consider is time. For species that 

have only a single breeding season consisting of a few days, 

time available for conservation and restoration research 

is precious, and any time savings is a benefi t. Moreover, 

the time remaining for some species that are threatened 

has become critical, and restoration practices need to be 

improved. Acropora palmata (elkhorn coral) and Acropora cervicornis (staghorn coral) were the fi rst corals to 

be listed as threatened species under the U.S. Endangered 

Species Act. These major reef-building species once formed 

dense thickets and stands in the Caribbean. Today, these 

two species are currently at 1% to 20% of their historical 

levels throughout their range (Bruckner, 2003). Here we 

describe only one aspect of an ex situ conservation process, namely improved rearing associated with yielding 

better time management.

However, both the static and fl ow-through methods 

described here have their strengths and weaknesses. The 

static method was inexpensive to set up in terms of equipment and space. For example, 60 bowls can be maintained 

in two double-tiered fl owing water tables taking up only 

about 2.5 m2; however, this method was very expensive in 

terms of labor needed for cleaning (5,000 h year1). The 

fl ow-through system was more costly to set up because 

it required a fi ltered fl ow-through water system and specially constructed rearing chambers. The amount of salary 

needed to pay one person for a season cleaning larvae, 

however, far exceeds the cost of the fi ltered seawater system and rearing chambers. The fl ow-through chambers required more space than the bowls, but each fl ow-through 

vessel could maintain almost three times the density (in 

0.25 m2) than was ordinarily maintained in a static bowl 

and with little maintenance time required.

One of the major issues facing biologists in rearing 

coral larvae is how to keep them cool (28°– 30°C) under 

fi eld conditions. During daylight hours, static bins left 

outside without any cooling mechanism can easily reach 

31° to 33°C, which is lethal for most species. The rearing 

data in Figure 3 refl ect some of these issues. These data 

were not exactly comparable, because they did not have 

the same developmental temperatures. Had the static bins 

been maintained at 28° to 30°C (as were the fl ow chambers), possibly their survival would have been far worse, 

because their water quality would decay so rapidly. Because A. palmata is an endangered species, our goal was to 

produce the most larvae for captive maintenance in public 

zoos and aquaria (Petersen et al., 2007), this required having static “backup” bins maintained at a slightly cooler 

temperature to provide the larvae suffi cient development 

time in transit to reach their respective sites before settlement. However, without an air-conditioned room to cool 

the bins, this would not have been possible, making this 

impractical under some fi eld conditions.

Within the fi rst 24 h of development, many coral larvae are susceptible to fragmentation by mechanical disruption. However, the water movement within the up-fl owing 

tank and potential contact with the walls did not cause 

substantial fragmentation of A. palmata during early development, even when the A. palmata larvae were placed 

in the chambers within the fi rst few hours after fertilization. In contrast, P. meandrina was far more delicate, did 

not develop strong swimming behaviors, and could not 

withstand the water movements in the fl ow chambers. 

F. scutaria larvae are negatively/neutrally buoyant larvae 

that develop strong swimming behaviors within the fi rst 

12 to 24 h, and the spiral-fl ow system shown in Figure 3 

functioned well for them, because the water fl ow is upward and any disintegrating unfertilized oocytes and larvae 

passed through the mesh, allowing for the maintenance of 

excellent water quality in the rearing chambers. However, 

no one type of rearing chamber can be applied universally 

across species. Instead, the type of water fl ow within the 

chamber must be matched with the buoyancy and early 

swimming behavior of the larvae. Regardless, these readily 

built and easily maintained fl ow-through chambers may be 

a substantial aid to coral conservation and restoration.

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NUMBER 38 • 267

ACKNOWLEDGMENTS

This work was supported by NOAA (grant # 

NA07NMF4630109), the Columbus Zoo and Aquarium 

Conservation Fund, the Rotterdam Zoo, the Green Foundation, The Clyde and Connie Woodburn Foundation, the 

Smithsonian Institution, Louisiana State University Agricultural Center, the University of California, the Omaha 

Zoo, Lou Nesslar, and the John G. Shedd Aquarium. We 

thank the anonymous reviewers whose comments have 

greatly improved this paper.

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Worldwide Diving Discoveries 

of Living Fossil Animals from the 

Depths of Anchialine and Marine Caves

Thomas M. Iliffe and Louis S. Kornicker

ABSTRACT. Inland (anchialine) and offshore submarine caves in limestone and volcanic bedrock are extreme environments inhabited by endemic, cave-adapted (typically 

eye- and pigment-reduced) fauna. Specialized cave diving technology is essential for investigating this habitat. A number of new higher taxa are represented herein, including 

closely related species inhabiting caves on opposite sides of the Earth, thus suggesting an 

ancient common ancestry. Because many of these species are known from only a single 

cave, pollution or destruction of caves will result in their extinction.

INTRODUCTION

DEFINITION OF ANCHIALINE AND MARINE CAVES

Anchialine caves are partially or totally submerged caves situated within a 

few kilometers inland from the coast in volcanic or karstic limestone terrain. 

Tidal marine waters in these caves have a long residence time, of months to years. 

Such caves are locally termed “cenotes” in the Yucatan Peninsula of Mexico, 

“blue holes” in the Bahamas and Belize, and “grietas” in the Galapagos Islands. 

The caves typically possess a highly stratifi ed water column, with surface layers 

of freshwater or brackish water, separated by a thermo– chemocline from underlying fully marine waters low in dissolved oxygen (Iliffe, 2000). Animals that 

are restricted to the anchialine habitat and show pronounced morphological, 

physiological, biochemical, and behavioral adaptations are termed stygofauna 

or stygobites. In some areas such as Yucatan, freshwater and marine stygobites 

inhabit their respective water masses within the same caves.

In contrast to anchialine caves, marine caves are located either directly on 

the coastline (e.g., tidal springs) or are wholly submerged beneath the seafl oor 

(e.g., offshore blue holes) and contain marine waters that freely exchange with 

the sea on each tidal cycle. The stygophilic fauna of marine caves can also be 

found in suitable and similar habitats outside of caves (e.g., under rocks or in 

crevices within the reef) and lack specialized adaptations for subterranean life.

Moderate to strong tidal currents are present in many marine caves. As a 

result, encrusting and low-growing, fi lter-feeding animals such as sponges, hydroids, anemones, tube worms, and even some corals may completely cover all 

Thomas M. Iliffe, Department of Marine Biology, 

Texas A&M University at Galveston, Galveston, 

Texas 77553-1675, USA. Louis S. Kornicker, 

Department of Invertebrate Zoology, National 

Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560– 0163, USA. Corresponding author: T. Iliffe (iliffet@tamug.edu). 

Manuscript received 9 June 2008; accepted 20 

April 2009.

20_Illiffe_269-280_Lang.indd 269 0_Illiffe_269-280_Lang.indd 269 9/24/09 9:49/24/09 9:49
270 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

hard surfaces. Other organisms are swept into caves by 

tidal currents but can only survive there for short periods 

of time and are termed accidentals. Some species of fi shes, 

lobster, and mysidaceans seek shelter within marine caves 

but must venture out into open waters to feed and are classifi ed as stygoxenes.

Some extensive marine caves extend far or deep 

enough so that a more or less gradual transition to long 

water residence times takes place and conversion to a 

true anchialine habitat occurs. Similarly, a number of inland anchialine systems have submerged entrances in the 

sea, with signifi cant water exchange occurring in the entrance sections but with a transition to anchialine characteristics and fauna taking place as distance from the 

sea increases and the magnitude and impact of tidally 

exchanging water decline.

Biological Signifi cance

Anchialine caves contain a rich and diverse, endemic 

stygobitic fauna (Sket, 1996; Iliffe, 2000, 2004) but, because of the specialized technological demands and potential dangers of cave diving, are relatively unstudied. These 

habitats serve as refuges to “living fossil” organisms, for 

instance, members of remiped crustaceans, and to animals 

closely related to deep-sea species, such as the galatheid 

crab Munidopsis polymorpha. Such stygobites typically 

possess regressed features including loss of eyes and body 

pigmentation. For reasons that remain unclear, the invertebrate fauna is dominated by crustaceans and includes 

the new class Remipedia, plus three new orders, nine new 

families, more than 75 new genera, and 300 new species. 

This extraordinary degree of novelty qualifi es anchialine 

habitats as uniquely important. Because anchialine species commonly have a highly restricted distribution, often 

being found only in a single cave system on one island, 

pollution or destruction of the caves will result in their 

extinction.

Stygobitic anchialine fauna often have highly disjunct 

biogeographic distributions, inhabiting caves in isolated 

locations on opposite sides of the Atlantic and Pacifi c 

Oceans, as well as in the Mediterranean, and are considered Tethyan relicts. Various hypotheses have been proposed to explain the origin of anchialine fauna. In general, 

these theories invoke either vicariance (geological) or dispersal (biological) processes. Recently initiated molecular 

genetic comparisons of cave populations from distant locations may help provide data for determining the age and 

dispersal sequence of anchialine stygobites (Zakšek et al., 

2007; Hunter et al., 2008).

Lifestyle Adaptations

The extreme environmental conditions in anchialine 

caves, such as the absence of light, hypoxia, and limited 

food reserves, present a unique set of challenges for the 

organisms that reside there. The lack of light precludes 

photosynthetic (primary) production of oxygen and food. 

Without light, organisms receive no visual information for 

orientation or communication and must function without 

diurnal timing mechanisms.

Adaptations to anchialine and marine caves can be 

morphological, behavioral, and physiological (Iliffe and 

Bishop, 2007). As a result of both food scarcity and hypoxia, there is a high selective advantage for economy of 

energy observed in many taxa, with possible adaptations 

including enhanced chemo– mechano-receptors for improved food fi nding capability, starvation resistance, and 

reduction in energy demand via reduced metabolism.

METHODS

Diving Investigations

Because anchialine stygobites are commonly found only 

at signifi cant depths or distances from the water surface, 

cave diving is an essential component of the collection and 

study of anchialine fauna (Iliffe and Bowen, 2001). Cave 

diving requires specialized training, equipment, and techniques because a direct assent to the surface is not possible 

and divers may be hundreds of meters from outside access. 

In case of equipment failure or loss of air supply, cave divers 

must have readily available backups. Special techniques for 

cave diving may include the use of side-mounted, instead of 

back-mounted, scuba tanks to allow divers to pass through 

low bedding plane passages. Closed circuit rebreathers, 

which recycle the diver’s exhaled gases, reduce the amount 

of percolation, that is, of silt dislodged from cave ceiling or 

walls by the exhaust bubbles produced in conventional open 

circuit scuba, and lessen contamination of the cave waters, 

which are low in dissolved oxygen (Figure 1). Rebreathers 

allow for much longer dives and generally less decompression time. Deep dives, depths below 40 m, require the use of 

special breathing gas mixtures that replace part or all of the 

nitrogen with helium to reduce the effect of nitrogen narcosis. As many cave dives are for longer durations and/or to 

deeper depths, they frequently involve long decompression.

Sampling and Fixation

The exceptionally clear waters of anchialine caves 

facilitate visual observation and collection of stygobitic 

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NUMBER 38 • 271

species. Collectors generally lead the dive to have undisturbed water in front of them. As they slowly sweep their 

dive lights back and forth in an arc, observing the water 

column illuminated by the light beam, animals as small as 

a few millimeters can be distinguished as white pinpoints, 

sharply contrasting with the black background of the cave. 

Specimens recognized in this manner can be collected either individually in clear glass vials or plastic tubes or in 

larger numbers using a type of suction device known as the 

“Sket bottle” (Chevaldonné et al., 2008). Plankton nets, 

of 93 m mesh with a 30 cm mouth diameter and 1 m 

length, can be used to collect smaller animals, such as copepods, from the water column. When collecting animals 

from the surface layer of sediments, divers can gently fan 

up the sediments with a hand and then sweep the plankton 

net through the disturbed water. This agitation should be 

done with care so as not to obscure overall visibility, which 

could cause the dive team to lose sight of their guideline 

leading back to the surface. Larger amounts of sediment 

can be collected in sealable plastic bags for later sorting 

in the laboratory. Finally, minnow traps or similar funnelshaped traps made from plastic bottles (Manning, 1986) 

can be baited with a small amount of fi sh, crab, or other 

attractant and left within the cave for 6 to 24 h. If the trap 

is carefully placed inside a sealed plastic bag when it is 

recovered, even small invertebrates can be collected.

If temperatures are kept close to cave temperature after collecting, specimens will remain alive for up to 24 h. 

Photographic documentation of color pattern and natural 

body position in live specimens is highly desirable. Smaller 

animals can be photographed using a phototube attachment on a dissecting microscope and larger specimens with 

the macro setting found on many digital cameras. If animals 

are too active to be photographed easily, they can be chilled 

in a small dish placed in a refrigerator or an ice bath until 

they stop moving. Digital video segments showing swimming and other behaviors can be made in the same manner. 

Specimens are sorted under a dissecting microscope using 

small pipettes to transfer them to individual dishes for each 

taxon. Depending upon the type of animal and its intended 

use, various fi xatives can be used. Most animals are best 

preserved in 70% to 95% pharmaceutical grade ethanol, 

which allows them to be used for either morphological 

or molecular investigations. Specimens for confocal laser 

scanning microscopy can be fi xed in 4% paraformaldehyde 

in phosphate-buffered saline (PBS) buffer (1:1 in seawater), 

while those intended for scanning or transmission electron 

microscopy are fi xed in 2% glutaraldehyde in seawater.

GEOLOGICAL ORIGINS, AGE, AND 

DISTRIBUTION OF ANCHIALINE HABITATS

Anchialine caves occur in both volcanic bedrock and 

karstic limestone. Lava tube caves form during volcanic 

eruptions of basaltic lava. They typically occur close to the 

earth’s surface and are thus relatively short lived (thousands 

to a few tens of thousands of years). Anchialine lava tubes 

may originate on land and extend out under the coastline 

and beneath the seafl oor or can form from submarine eruptions. Anchialine lava tube caves are known from the Canary Islands, Galapagos Islands, Hawaii, and Western Samoa. The longest of these is the Jameos del Agua (Atlantida 

Tunnel) on Lanzarote in the Canary Islands, the submerged 

portion of which extends 1.6 km beyond the coastline, 

reaching a depth of 50 m (Iliffe et al., 2000).

The most extensive of known anchialine habitats 

are solutionally developed limestone caves that typically 

contain both freshwater and marine waters. Such caves 

are sometimes referred to as fl ank margin caves and were 

formed by mixing dissolution in a fresh groundwater lens 

(Mylroie and Carew, 1990). The largest anchialine cave 

is Sistema Ox Bel Ha located on the Caribbean coast of 

the Yucatan Peninsula in Mexico; it contains 180 km of 

FIGURE 1. A diver uses a Megalodon closed-circuit rebreather with 

full face mask to collect a small shrimp, Typhlatya sp., from a cave 

in Yucatan. Rebreathers recycle expired gas so that no bubbles are 

produced.

20_Illiffe_269-280_Lang.indd 271 0_Illiffe_269-280_Lang.indd 271 9/24/09 9:49/24/09 9:49
272 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

surveyed underwater passages interconnecting 130 cenote 

entrances. Extensive anchialine limestone caves are also 

known from the Bahamas, Bermuda, Belize, Dominican 

Republic, and Bonaire in the Caribbean, plus the Balearic 

Islands and Sardinia in the Mediterranean. Smaller anchialine caves are present on many islands in the Indo-South 

Pacifi c and in Western Australia.

Limestone caves last much longer than lava tubes and 

can be hundreds of thousands to many millions of years 

old. Commonly, massive stalactites and stalagmites occur 

underwater to depths in excess of 50 m in coastal limestone caves. Because speleothems form very slowly and 

only in air, these caves must have been dry and fi lled with 

air for long periods of time when glacial sea levels were as 

much as 130 m lower than today. The last low stand of Ice 

Age sea level occurred only 18,000 years ago.

Coastal tectonic faults that extend below sea level 

constitute another form of anchialine habitat. On Santa 

Cruz in the Galapagos Islands, vertical faults in coastal 

volcanic rock are locally called “grietas” (Iliffe, 1991). 

Wedged breakdown blocks have partially roofed over 

submerged portions of grietas so that they are in total 

darkness. Similar faults are present in Iceland. Fault caves 

also occur in uplifted reef limestone on the island of Niue 

in the Central Pacifi c, producing deep chasms containing 

anchialine pools. The Ras Muhammad Crack in the Sinai 

Peninsula consists of a water-fi lled crack in an elevated 

fossil reef formed by a 1968 earthquake (Por and Tsurnamal, 1973). Many of the offshore ocean blue holes of 

the Bahamas consist of submarine faults running parallel 

to the platform edge. Ocean blue holes typically exhibit 

exceptionally strong, reversing tidal currents created by an 

imbalance between tides on opposite sides of the islands.

ANCHIALINE CAVE ECOLOGY

PHYSICAL AND CHEMICAL CHARACTERISTICS

The water column in most anchialine caves is highly 

stratifi ed (Iliffe, 2000). The largest changes in chemical and 

physical parameters typically occur at the halocline where 

freshwater or brackish water is separated from underlying fully marine waters (Figure 2). It is not uncommon for 

caves to possess multiple haloclines. On larger islands and 

in continental regions such as Yucatan and Western Australia, freshwater occurs in the shape of a lens with thickness 

increasing in a direct relationship with distance inland from 

the coast. In Yucatan, the depth of the halocline and corresponding thickness of the freshwater lens increases from 

10 m at 2 km distance inland to 20 m at 10 km inland.

Water temperature in Yucatan caves generally increases with depth, although in the Bahamas the inverse 

occurs and water below the halocline is generally cooler 

than surface water. Warmer waters below the halocline 

could be caused by geothermal heating at depth or evaporative cooling at the surface.

In the lightless interior of caves, there are no plants 

and hence no photosynthetic oxygen production; stable 

and stratifi ed water masses also restrict vertical mixing and 

exchange of oxygen with surface waters. Thus, cave waters 

are typically hypoxic to anoxic. Where deeper, water- fi lled 

vertical shafts extend to the surface, such as in many cenotes and inland blue holes, input of leaves and other organic 

detritus has caused the total depletion of dissolved oxygen 

with resulting anoxia and hydrogen sulfi de production. A 

cloud-like layer of hydrogen sulfi de several meters thick occurs just below the halocline and may reduce under water 

visibility to near zero, but water clarity improves considerably below the H2S layer. In some caves, dissolved oxygen 

levels can recover to 1 mg/L or less and populations of stygobitic animals occur.

A pH minimum generally occurs at the halocline, possibly arising from microbial oxidation of organic matter 

suspended at the density interface and resulting CO2 production. Increased acidity at the halocline may explain the 

dissolution of limestone and the resulting development of 

cave passages at this depth.

TROPHIC RELATIONSHIPS

Determination of stable carbon and nitrogen isotopes 

values from animals, sediments, and other sources of organic matter in Yucatan caves has been used to examine 

the trophic ecology of these systems (Pohlman et al., 1997, 

2000). Four potential sources of organic matter were identifi ed in Yucatan caves: the soil from the surrounding jungle, algae from the cenote pool, chemoautotrophic bacteria, and, to a lesser extent, organic matter originating from 

marine waters. Stable nitrogen isotope data determined 

that the food web comprised 2 to 2.5 trophic levels.

The paucity of food in anchialine caves drives organisms toward a generalist diet. Mysids and isopods tend toward omnivory, while ostracods and thermosbaenaceans 

occupy the roles of detritivores. The thermosbaenacean Tulumella and atyid shrimp Typhlatya have modifi ed appendages that allow them to fi lter out even the tiniest particles. 

Remipedes, fi shes, and some amphipods, operating either 

as top-level predators or as scavengers, feed on ostracods, 

thermosbaenaceans, copepods, isopods, amphipods, and 

shrimps.

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BIODIVERSITY

FISHES

Stygobitic anchialine fi shes (Figure 3a) are represented 

in the families Bythidae (eight species in two genera from 

the Bahamas, Cuba, Yucatan, and Galapagos Islands), Eleotridae (one species from Northwestern Australia), Gobiidae (three species in two genera from the Philippines and 

Japan), and Synbranchidae (two species in one genus from 

Northwestern Australia and Yucatan) (Romero, 2001).

NON-CRUSTACEAN INVERTEBRATES

Although most stygobitic anchialine invertebrates are 

crustaceans, a variety of non-crustacean invertebrate stygofaunal species have been described. Anchialine species include four sponges, one turbellarian, fi ve gastropods, ten 

annelids, four chaetognaths, one tantulocarid, and three 

water mites. Although some of these species are questionable stygobites, several are clearly cave adapted. The polychaetes Gesiella jameensis from the Canary Islands and 

Pelagomacellicephala iliffei from the Caicos Islands and Bahamas (Figure 3b) conserve energy by slowly swimming in 

the cave water column, while the chaetognath Paraspadella 

anops from the Bahamas lacks eyes and pigment.

CRUSTACEANS

Crustaceans are the most abundant and diverse group 

present in both freshwater and anchialine cave habitats. 

Among the anchialine Crustacea, the largest numbers of 

species are represented by amphipods, copepods, decapods, ostracods, isopods, mysids, and thermosbaenaceans, 

approximately in that order.

Remipedia

Remipedes are a class of Crustacea originally described 

from Bahamian caves by Yager (1981). Although their 

multi-segmented trunk and paired swimming appendages

FIGURE 2. Depth profi les of salinity, temperature, dissolved oxygen, and pH from an anchialine cave, Cenote 27 Steps, Akumal, Mexico, 

7 December 2003, recorded with a YSI 600 XLM multiparameter water quality monitor. Individual measurements (diamond symbols) were 

taken at 4 s intervals between the surface and 26 m water depth.

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274 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 3. Characteristic anchialine cave animals include the (a) Yucatan cave fi sh Typhliasina pearsei; (b) polynoid polychaete worm 

Pelagomacellicephala iliffei from the Bahamas; (c) remipede Cryptocorynetes longulus from the Bahamas; (d) thermosbaenacean Tulumella 

unidens from Yucatan; (e) mictacean Mictocaris halope from Bermuda; (f) halocyprid ostracod Spelaeoecia capax from the Bahamas; (g) stygiomysid Stygiomysis sp. from Yucatan; and (h) cirolanid isopod Bahalana caicosana from the Caicos Islands.

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NUMBER 38 • 275

appear primitive, their head and mouth parts are highly 

specialized (Figure 3c). Remipedes have paired hollow 

fangs for capturing prey and are among the top predators in anchialine habitats. They are up to 4.5 cm in 

length, usually colorless and blind, with elongate, centipede-like bodies. Twenty species of remipedes inhabit 

fully marine, oxygen-defi cient waters in caves from the 

Bahamas, Cai cos Islands, Cuba, Yucatan Peninsula, Dominican Republic, Canary Islands, and Western Australia (Koenemann et al., 2008b; Daenekas et al., 2009). 

The recent discovery of free-living, nonfeeding remipede 

larvae promises to yield information on the reproduction 

and development as well as the evolutionary affi nities of 

this enigmatic group (Koenemann et al., 2007, 2009).

Thermosbaenacea

Thermosbaenaceans (Figure 3d) are small (5 mm or 

less), eyeless or eye-reduced, anchialine and freshwater 

peracarid crustaceans with a dorsal brood pouch in females (Wagner, 1994; Jaume, 2008). They include at least 

34 species with a wide distribution in caves and thermal 

springs around the Mediterranean and Caribbean, as well 

as in Australia and Cambodia.

Mictacea

Mictaceans (Figure 3e) are small (3– 3.5 mm), eyeless 

and depigmented, nonpredatory crustaceans. This peracarid 

order is represented by only a single species that inhabits 

anchialine caves in Bermuda (Bowman and Iliffe, 1985).

Bochusacea

Bochusaceans are very small (1.2– 1.6 mm), semitransparent, and eyeless peracarid crustaceans that include two anchialine species from the Bahamas and Cayman Islands, plus two deep-sea species (Gutu and Iliffe, 

1998; Jaume et al., 2006).

Copepoda

Platycopioid, misophrioid, cyclopoid, harpacticoid, 

and calanoid (especially epacteriscid and ridgewayiid) 

copepods inhabit anchialine caves in tropical regions 

around the globe. They are small (typically 1– 2 mm long) 

and have a short, cylindrical body with head and thorax 

fused into a cephalothorax. Most are planktonic fi lter 

feeders, but some, such as the harpacticoids and cyclopoids, are benthic, while epacteriscids are predators on 

other copepods.

Ostracoda

Halocyprid ostracods (Figure 3f) include anchialine 

species with a distribution and co-occurrence similar to 

that of remipedes (Kornicker et al., 2007). Danielopolina

is the most widely distributed stygobitic genus with species 

on opposite sides of both the Atlantic and Pacifi c, inhabiting caves in the Bahamas, Cuba, Yucatan, Jamaica, Canary 

Islands, Galapagos, Western Australia, and Christmas Island. More than 300 species of podocopid ostracods have 

been found in springs, caves, and anchialine habitats.

Mysidacea

Stygobitic mysids are found in freshwater and anchialine habitats in Africa, the Caribbean, Mediterranean, and 

India. Their distribution suggests that they were stranded in 

caves by lowering of the sea level in the Tethys and Mediterranean. Recent molecular phylogenies of the mysids suggest 

that a new order is justifi ed for the stygiomysids (Figure 3g), 

which inhabit caves in the Caribbean and Italy (Meland and 

Willassen, 2007).

Isopoda

Stygobitic isopods (Figure 3h) range from several millimeters to several centimeters in length. Anthurid isopods 

occur in anchialine and freshwater caves in the Canary 

Islands, Caribbean and Indian Ocean islands, Mexico, 

and South America. Asellot isopods inhabit anchialine and 

freshwater caves in the Caribbean, Europe, Galapagos, India, Indonesia, Japan, Malaysia, North and Central America, and Polynesia. Cirolanid isopods have been found in 

freshwater and anchialine caves clustered in Mexico and 

the Caribbean (Iliffe and Botosaneanu, 2006), as well as in 

Europe and the Mediterranean.

Amphipoda

Amphipods occur in freshwater and marine cave habitats. Stygobitic representatives are present in the bogidiellid, crangonyctid, hadziid, and niphargid families of the 

amphipod suborder Gammaridea. They are very widely 

dispersed, with large numbers of species inhabiting caves 

in Central and Southern Europe, the Mediterranean, eastern and southern North America, and the Caribbean.

Decapoda

The anomuran galatheid crab Munidopsis polymorpha inhabits an anchialine lava tube in the Canary Islands 

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276 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

(Wilkens et al., 1990). Brachyuran crabs are widely distributed in caves of the tropics and subtropics. Anchialine 

stygobitic shrimp include representatives from the caridean families Agostocarididae, Alpheidae, Atyidae, Hippolytidae, Palaemonidae, and Procarididae; the stenopodid 

family Macromaxillocarididae; and the thalassinid family 

Laomediidae.

Other Crustacean Stygofauna

One tantulocarid, an exceptionally tiny ectoparasite 

on anchialine harpacticoid copepods, occurs in the Canary 

Islands (Boxshall and Huys, 1989). A species of stygobitic 

nebaliacean inhabits anchialine caves in the Bahamas and 

Caicos Islands (Bowman et al., 1985). Several species of 

cumaceans and tanaidaceans have been collected from anchialine caves in Bermuda and the Bahamas, but it is not 

clear whether they belong to the stygofauna.

BIOGEOGRAPHY

Upon examining the biogeography of anchialine fauna, 

some extraordinary patterns are evident. A number of anchialine genera, including the remipede Lasionectes, ostracod Danielopolina, thermosbaenacean Halosbaena, and 

misophrioid Speleophria, inhabit caves on opposite sides of 

the Earth and are believed to be relicts whose ancestors inhabited the Tethys Sea during the Mesozoic (Humphreys, 

2000). Some anchialine taxa are represented in the Mediterranean, but others, notably remipedes and Halosbaena, are 

absent. The presence of anchialine taxa at all in the Mediterranean is remarkable considering that this basin was completely dry for long periods of time during the Miocene. The 

aytid shrimp Typhlatya shows an especially interesting distribution with 17 known species inhabiting freshwater and 

anchialine caves in the Mediterranean region, Bermuda, Ascension Island, Caribbean locations including Cuba and Yucatan, and the Galapagos Islands (Alvarez et al., 2005). The 

shrimp family Procaridae contains one genus with species in 

the mid-Atlantic and Caribbean, as well as Hawaii.

Based on numbers of stygobitic species, the Bahamian 

archipelago appears to have been a possible center of origin for anchialine fauna. Among the Remipedia, 15 of 

20 described species inhabit caves in the Bahamas (Koenemann et al., 2008b; Daenekas et al., 2009), whereas 

among anchialine halocyprid ostracods, Bahamian species account for 4 of 11 in the genus Danielopolina, 6 of 

11 in Spelaeoecia, and all 8 species of Deeveya (Kornicker 

et al., 2007).

The Bahamas archipelago consists of a series of broad, 

shallow-water, highly karstifi ed, carbonate platforms rising 

abruptly from the deep sea. The islands and cays consist of 

Pleistocene limestone covered by a thin veneer of Holocene 

carbonate reefs and sediments. Underlying these younger 

limestones is a continuous section of Tertiary and Cretaceous 

limestones and dolomites exceeding 11 km in thickness. If 

the position of the tectonic plates before the development of 

the Atlantic Ocean is reconstructed, virtually all the Bahamas overlap the African continent and its continental shelf. 

This fi nding suggests that the Bahama platform developed 

over oceanic crust during the earliest phase of the creation of 

the Atlantic. The extended shallow-water history of the Bahamas, coupled with the cavernous nature of the limestone, 

may help to explain its rich and diverse anchialine fauna.

ORIGINS OF ANCHIALINE BIOTA

A number of theories have been proposed to explain 

the trans-oceanic distribution of many anchialine taxa. The 

vicariance model suggests that plate tectonics served as a 

mechanism for the dispersal of anchialine fauna (Rosen, 

1976; Wiley, 1988). This model mainly describes the Tethyan track of ancient taxa that were rafted on the drifting 

continents to their present positions (Stock, 1993; Jaume 

et al., 2001). However, the existence of anchialine fauna on 

mid-ocean islands such as Bermuda, Ascension, and Hawaii 

that have never been part of or closer to a continent cannot 

be explained by this mechanism (Iliffe, 2000).

The regression model suggests that sea-level regressions, caused by tectonic uplift or eustatic glacial lowering of sea levels, stranded crevicular or interstitial marine 

littoral species that subsequently adapted to brackish or 

freshwater conditions (Stock, 1980). This model is supported by the observed correlation between the distribution patterns of numerous, marine-derived cave organisms 

and the position of shorelines during the Late Mesozoic 

or Tertiary seas. Nevertheless, the presence of anchialine 

fauna in caves that were completely dry and air fi lled (as 

evidenced by their now-submarine speleothems) less than 

10,000 years ago indicates that these animals can migrate 

vertically with raising postglacial sea levels (Iliffe, 2000). 

Also, small islands such as Bermuda offer little chance for 

marine species to be stranded.

A deep-sea origin has been proposed for some anchialine species having close relatives that inhabit bathyal 

depths (Hart et al., 1985). Both caves and the deep sea 

are old, climatically stable, lightless, and nonrigorous environments. Anchialine habitats on islands and continental 

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NUMBER 38 • 277

margins could be connected via a continuum of crevicular 

corridors extending from shallow depths to the deep sea 

(Iliffe, 1990). However, evidence against a deep-sea origin 

of cave faunas includes the questionable ability of deepsea species to cross the oceanic thermocline, the relatively 

recent nature of deep-sea species (resulting from the lack 

of oxygen in Atlantic bathyal waters during the late Oligocene), and phylogenetic analyses of morphological characters supporting independent colonization of deep-sea and 

anchialine habitats (Stock, 1986; Danielopol, 1990).

The active migration model involves the inland dispersal and colonization of subterranean habitats by expansionistic marine species with a high degree of salinity 

tolerance (Rouch and Danielopol, 1987). This process is 

independent of climatological and geological variations.

Passive oceanic dispersal of larval or postlarval stages 

of anchialine species by currents could explain the wide 

distribution of some anchialine shrimp species within the 

Indo-Pacifi c. Rafting on fl oating objects, such as wood, 

algae, kelp, and coconuts, or on mobile and migratory 

animals, for instance, sea turtles, fi shes, and larger arthropods, could disperse anchialine species, even those without 

a free larval stage. However, oceanic dispersal is unlikely 

for many anchialine groups that produce few offspring or 

have narrow physiological tolerances.

ADAPTATION TO LIFE 

IN ANCHIALINE CAVES

BEHAVIORAL ADAPTATIONS

Behavioral adaptations are the most immediate adaptations for survival and colonization in cave systems. Cave 

organisms, in particular amblyopsid cave fi shes, use a glideand-rest technique to conserve energy in their search for 

food. Remipede locomotion is also designed for the economy 

of movement. Remipedes swim slowly, using less energy for 

the same distance than if they swam at higher speeds (Koenemann et al., 2008a). The power stroke produces drag by 

individual legs, but the recovery stroke is completed with the 

legs folded with other legs to reduce water resistance.

The stygobitic galatheid crab Munidopsis polymorpha, inhabiting an anchialine lava tube in the Canary Islands, has a number of specialized behaviors (Parzefall, 

1992, 2000). These small crabs are most abundant in a 

dimly illuminated pool where they hide in rock crevices 

during the day but come out at night to feed on diatoms. 

Because of the large numbers of individuals in this pool, 

they spread in an almost regular pattern determined by the 

length of the second antennae.

Munidopsis crabs remain aggressive throughout the 

year. They detect intruders from water movements and attack with extended chelipeds. Male crabs are attracted by 

a molting hormone released by females. To prevent the 

females from fl eeing, males rhythmically move their chelipeds as they approach, until the female responds by vibrating one of her chelipeds. The male then seems to turn 

the female over on her back to initiate insemination.

MORPHOLOGICAL ADAPTATIONS

Regressive Features

The loss of features that in cave environments no longer 

have a function, such as eyes and pigmentation, is regarded as 

regressive evolution. There are two main theories explaining 

the driving force for regressive evolution. In an environment 

with a depauperate food supply, natural selection should 

favor reallocating energy from developing unused features, 

such as eyes and pigment, to growth and survival. A second 

explanation is that regressive evolution may be the result of 

nonselective processes such as neutral mutation and genetic 

drift. Features such as eyes and pigment that abruptly lose 

their biological function when animals enter caves are free to 

be turned off by now non-lethal mutations.

Unfortunately, the theory of energy economy by character reduction in stygobites is not well tested, especially 

with anchialine stygobites, yet the anchialine environment 

is dominated by blind, depigmented organisms.

Constructive Features

In the case of constructive features, priority is given to 

life history, metabolism, development, and starvation resistance, with sensory development such as mechano- and 

chemoreceptors being subordinate. For troglomorphy to 

occur, two factors must be present: (1) selective pressure 

in favor of the development and (2) genetic, physiological, 

or behavioral ability of the organism to respond to the 

selective pressure. A prerequisite for constructive traits is 

their genetic availability in epigean forms: if traits are not 

present in epigean ancestors, they will not be present in 

hypogean descendants.

There are several areas of the body where constructive 

features occur. In crustaceans, appendages may be elongated, in particular, the antennae, and in fi sh, the head 

may become enlarged or fl attened. Corresponding to the 

morphological changes, there is an increased sensitivity to 

chemical and mechanical stimulants. As a result of compensatory enhancement of extraocular senses, the signalprocessing structures in the brain are altered.

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278 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

PHYSIOLOGICAL ADAPTATIONS

Adaptations to a Food-Poor Environment

Food in the stygobitic environment may be in general 

scarce or at best patchy; therefore, the stygofauna need 

to cope with temporal periodicity of food availability and 

potentially tolerate long periods of starvation. This adaptation occurs through lipid accumulation or energy economy. In comparison with pelagic crustaceans, anchialine 

crustaceans sacrifi ce protein mass for increased lipid stores 

(Iliffe and Bishop, 2007). Lipids provide neutral buoyancy 

without energy expenditure, while also serving as an energy reserve when food is limiting. Anchialine stygobites 

also tend to be smaller than their epigean counterparts. 

Their small size is a mechanism for energy economy.

Adaptation to Hypoxia and Anoxia

As mentioned previously, the anchialine environment, 

especially at or below the halocline, is commonly hypoxic 

or even anoxic. As a result, hypogean organisms tend to 

have substantially lower oxygen consumption rates than 

their epigean relatives (Bishop et al., 2004). Many organisms are capable of obtaining energy when faced with a reduction or absence of oxygen, but few are able to survive 

indefi nitely without a return to oxygen. When the oxygen 

supply becomes inadequate, organisms switch to anaerobiosis to compensate for adenosine triphosphate (ATP) 

demand.

During periods of anaerobiosis, organisms conserve 

their energy stores by a loss in physiological functions 

such as motility, ingestion, and digestion, combined with a 

dramatic depression of their energy (ATP) demand. When 

oxygen is temporarily unavailable, many organisms switch 

to anaerobic glycolysis. Anaerobic glycolysis is, however, a 

fundamentally ineffi cient metabolic strategy and thus not 

an attractive solution for anchialine organisms.

By examining the activities of enzymes critical to metabolism and energy conversion, it is possible to determine the rate at which food is converted to cellular energy 

(Bishop et al., 2004). Citrate synthase (CS) is an indicator 

of an organism’s maximum aerobic potential, or how fast 

an organism can aerobically convert glucose to energy. 

Malate dehydrogenase (MDH) functions in the presence 

as well as absence of oxygen, whereas lactate dehydrogenase (LDH) contributes to both aerobic and anaerobic 

metabolic pathways and serves as an indicator of glycolytic potential.

Anchialine organisms are anaerobically poised with 

both LDH:CS and MDH:LDH ratios tending to be greater 

than one. The higher the MDH:LDH ratio, the greater 

is the tolerance to hypoxia. Such high ratios indicate 

an evolutionary adaptation to the anaerobic anchialine 

environment.

CONSERVATION

Over the past 25 years, more than 400 new species of 

anchialine stygobites have been discovered and described. 

A high percentage of these species are known only from a 

single cave or cave system. Even within caves, species are 

characteristically found only at specifi c depths or locations 

as defi ned by a narrow range of environmental parameters. In many parts of the world, tourism development, 

limestone quarries, and groundwater pollution are either 

destroying or grossly polluting numerous caves, resulting 

in extinction of untold numbers of species.

Anchialine species qualify for inclusion on endangered 

species lists for reasons of their limited distribution and 

the declining environmental quality of their habitat. In 

Bermuda, 25 cave species are on the IUCN (International 

Union for Conservation of Nature) Red List of endangered 

species. Other cave species from the Yucatan Peninsula are 

on the offi cial Mexican list of threatened and endangered 

species.

Maintaining groundwater quality is essential to the 

environmental health of the subterranean environment. 

For example, the small oceanic island of Bermuda is the 

third most densely populated country in the world and has 

the largest number of private cesspits per capita. Disposal 

of sewage and other wastewater into cesspits or by pumping down boreholes is contaminating the ground water 

and cave water with nitrates, detergents, toxic metals, and 

pharmaceuticals; depleting the very limited amounts of 

dissolved oxygen in cave water; and generating toxic levels 

of hydrogen sulfi de.

Some ocean caves such as the Blue Holes of the Bahamas have strong tidal currents sweeping through them for 

very considerable distances. In one such cave, plastic bottles and other trash have been observed littering the fl oor 

of the cave nearly a mile back into previously unexplored 

passages. Far too many caves and sinkholes are viewed as 

preferred locations for the dumping of garbage and other 

waste products.

Another serious environmental problem concerns the 

destruction of caves by limestone quarries or construction 

activities. Half a dozen or more Bermuda caves have been 

totally destroyed by two limestone quarries that produce 

crushed aggregate for construction purposes. Untold other 

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NUMBER 38 • 279

caves have been lost to enormous limestone quarries in the 

Yucatan Peninsula. Many caves have been fi lled in and built 

over by golf courses, hotels, and housing developments in 

Bermuda. Recently, a series of luxury town homes was 

built directly on top of the largest cave lake in Bermuda.

Sometimes even seemingly innocent activities can 

threaten caves and cave animals. Along the Caribbean 

coast of the Yucatan Peninsula, many open water cenote 

pools are inhabited by the freshwater fi sh Astyanax fasciatus. Some of these fi sh frequently follow divers into caves, 

moving in front of the dive team and voraciously darting 

in to consume any cave fi sh or crustaceans that are illuminated by the beam of a dive light. Considering the many 

thousands of cave divers who use these systems each year, 

it is not surprising that the caves most heavily visited by 

tourist divers are now essentially devoid of life.

Even the gas exhaled by divers may have adverse effects on cave animals. Because anchialine cave waters 

typically contain extremely low levels of dissolved oxygen, exhaust bubbles from open circuit scuba could have 

profound effects on the cave ecosystem. Several anchialine 

caves in Western Australia with unique fauna are currently 

off limits to open circuit divers and may only be visited by 

those using rebreathers (Humphreys et al., 1999).

Some anchialine caves in Bermuda, the Canary Islands, 

and Mallorca have been developed into commercial tourist 

attractions. Unfortunately, many of the tourists visiting these 

sites have viewed the deep clear water cave pools as natural 

wishing wells in which to throw a coin or two. Copper coins 

tend to rapidly deteriorate and dissolve in saltwater, producing high levels of toxic copper ions in the cave waters. 

In one such cave in the Canary Islands, the endemic crab 

Munidopsis polymorpha has shown a marked decline in 

abundance during the past decade or longer, probably in 

response to high levels of copper in the cave water.

ACKNOWLEDGMENTS

Investigations of the anchialine cave fauna of the Bahamas were supported by awards DEB-9870219 and DEB0315903 from the U.S. National Science Foundation’s Biodiversity Surveys and Inventories Program and by grants 

from the NOAA Caribbean Marine Research Center to 

T. Iliffe. Collection of specimens was carried out under a 

permit from the Bahamas Department of Fisheries. This research would not have been possible without the generous 

collaboration of numerous scientists, graduate students, 

and cave divers from around the world. Renee Bishop 

(Penn State University at Worthington Scranton) generously provided much useful information on physiological 

adaptations of anchialine stygobites. This is contribution 

number 845 of the Caribbean Coral Reef Ecosystems Program (CCRE), Smithsonian Institution, supported in part 

by the Hunterdon Oceanographic Research Fund.

LITERATURE CITED

Alvarez, F., T. M. Iliffe, and J. L. Villalobos. 2005. New Species of the 

Genus Typhlatya (Decapoda: Atyidae) from Anchialine Caves in 

Mexico, the Bahamas, and Honduras. Journal of Crustacean Biology, 25(1):81– 94.

Bishop, R. E., B. Kakuk, and J. J. Tones. 2004. Life in the Hypoxic and 

Anoxic Zones: Metabolism and Proximate Composition of Caribbean Troglobitic Crustaceans with Observations on the Water 

Chemistry of Two Anchialine Caves. Journal of Crustacean Biology, 24:379– 392.

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Decimating Mangrove Forests 

for Commercial Development 

in the Pelican Cays, Belize: Long-Term 

Ecological Loss for Short-Term Gain?

Ian G. Macintyre, Marguerite A. Toscano,

Ilka C. Feller, and Maria A. Faust

ABSTRACT. The unique, biologically diverse ecosystems of Pelican Cays, Belize, are in 

serious danger from sediment suffocation related to the recent clear-cutting of mangroves 

for commercial development in what is currently designated Southwater Cay Marine 

Reserve. Field observations in the Pelican Cays in March 2007 revealed extensive clearcutting of mangroves and covering of exposed peat surfaces with sediment dredged from 

the adjacent seafl oor to create false sand cays. On Manatee Cay, introduction of dredge 

spoils taken from the nearby seabed resulted in fi ne sediment plumes spilling into the 

adjacent ponds, smothering the attached benthic communities on mangrove roots and 

burying Thalassia bottom communities. In addition, comparative studies of microalgal 

(phytoplankton) assemblages in a Manatee Cay pond before and after mangrove clearing 

indicate a dramatic loss in this group. This change, related to high turbidity observed in 

the water column, signals a serious impact to this aquatic ecosystem. In March 2007, 

clear-cutting, burning, and dredge and fi ll operations were taking place on Fisherman’s 

Cay, with additional survey lines visible on Fisherman’s, Manatee, and Cat Cays. We used 

a series of aerial photographic surveys from 2003 to 2007 to document the extensive loss 

of mangroves on both Manatee and Fisherman’s Cays. To date, additional clearing of 

mangroves has occurred on Northeast Cay, Bird Cays, and Ridge Cay, resulting in a total 

of 15.3 ha or more than 29% of the mangrove community that have been destroyed in 

the Pelican Cays. Furthermore, several survey lines through still-forested areas on these 

islands indicated that additional clearing of mangroves was planned. The Pelican Cays 

ponds contain unique, biologically diverse ecosystems dominated by delicate sessile photosynthetic and fi lter-feeding populations; these rare communities will be lost as a result 

of sediment suffocation caused by the clearing and fi lling of these islands. However, the 

conversion of mangrove ecosystems for residential, tourism, and commercial uses is both 

widespread and accelerating in Belize and throughout the global tropics. This pressure 

is having an adverse effect on the health of coral reefs and the biomass and viability of 

commercial fi sheries, which are essential for both tourism and local livelihoods.

INTRODUCTION

The Pelican Cays group is an oceanic coral reef boundary environment (Macintyre et al., 2000a), containing a network of coral ridges and semi-enclosed or 

enclosed ponds (Figure 1) where shallow mangrove cays are immediately adjacent to channels approximately 20 to 30 m deep. The lagoon-like ponds, which 

Ian G. Macintyre and Marguerite A. Toscano, 

Department of Paleobiology, National Museum 

of Natural History, Smithsonian Institution, 

P.O. Box 37012, MRC 125, Washington, D.C. 

20013-7012, USA. Ilka C. Feller, Smithsonian 

Environmental Research Center, 647 Contees 

Wharf Road, Edgewater, Maryland 21037, USA. 

Maria A. Faust, Department of Botany, National 

Museum of Natural History, Smithsonian Institution, 4210 Silver Hill Road, Suitland, Maryland 

20746, USA. Corresponding author: I. Macintyre 

(macintyr @si.edu). Manuscript received 13 May 

2008; accepted 20 April 2009.

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282 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

may be 10 to 12 m deep, harbor high-diversity, low-energy 

environments dominated by populations of photosynthetic 

and fi lter-feeding organisms. These ponds were formed by 

differential coral accumulations on polygonal karst patterns of the underlying Pleistocene limestone (Macintyre et 

al., 2000b). The scleractinian coral Acropora cervicornis, 

which is capable of rapid accretion in response to sea-level 

rise (catch up), exaggerated the underlying karst topography, resulting in greater relief than that of the antecedent 

karst surface, and created steep-sided ridges that form the 

ponds. Red mangrove (Rhizophora mangle) communities 

have established on the reef ridges of this area, forming 

intertidal cays encircling or partially encircling the ponds. 

The mangrove prop roots extending into the ponds proFIGURE 1. Index map showing the major mangrove islands of the Pelican Cays and their ponds.

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NUMBER 38 • 283

vide substrate for rich communities of sponges, ascidians, 

algae, corals, bryozoans, mollusks, and other organisms 

(Macintyre and Rützler, 2000).

Pelican Cays ponds and associated ridges support a 

very high level of shallow marine biodiversity within the 

Belize Lagoon. Examples include 70 species in 30 genera 

of ascidians (Figure 2A), representing 60% of all known 

shallow-water species in the Caribbean (Goodbody, 2000). 

Ten of 52 species of echinoderms found in the ponds and 

associated space had never been previously reported from 

Belize waters (Hendler and Pawson, 2000). Of 187 sponge 

species (Figure 2B) reported for several mangrove island 

groups along Belize Mesoamerican Barrier Reef, Rützler 

et al. (2000) found the “most diverse sponge fauna” at 

Pelican Cays. Of the 147 sponge species at Pelican Cays, 

45% were new species or variants special to the pond environments. Manatee Cay had 95 species, Cat Cay had 77 

species, and Fisherman’s Cay had 90 species. Wulff (2000) 

attributed sponge community differences to the fact that 

the Pelican Cays’ mangrove roots are embedded in coral 

reefs rather than thick peat sections as at Twin Cays (Macintyre et al., 2004) and Tobacco Range (Macintyre et al., 

1995). The reef substrate may be a preferred environment 

for spongivorous fi shes that determine the distinctive species composition of the Pelican Cays sponge community 

(Wulff, 2000). Richardson (2000) reported a total of 7 

species of epiphytic foraminifera living on turtle grass 

(Thalassia testudinum) blades, of which 2 were new species. Littler et al. (2000) reported 152 species of marine 

macrophytes, of which 148 were algae and 4 were vascular plants. A total of 31 bryozoan species were found 

in the Pelican Cays, forming extensive colonies on the 

mangrove roots (Winston, 2007). Coral species on ridges 

and in deeper or more open areas of the ponds included 

Porites furcata, P. divaricata, P. porites, P. astreoides, Acropora cervicornis, Siderastrea siderea, Agaricia tenuifolia, 

Millepora complanata, and Montastrea annularis (mainly 

at the opening of Pond E, Fisherman’s Cay; see Figure 1). 

Barnacles and mollusks also inhabit the ponds in signifi -

cant numbers.

Faust (2000) identifi ed 110 species in 33 genera of 

planktonic, oceanic, red tide-forming, benthic, and coastal 

dinofl agellate species from six of the Pelican Cays of great 

typological diversity. Approximately 50% of these appeared to be new species. Manatee Cay had 93 species, 

Douglas Cay, 47 species, and Cat Cay, 32 species. Waters 

in the Pelican Cays allow dinofl agellates to proliferate in 

a naturally nutrient-enriched environment, protected from 

prevailing winds by the surrounding mangroves and coral 

ridge (Faust, 2000).

In March 2000, a special issue of the Atoll Research 

Bulletin on the biology and physical characteristics of the 

Pelican Cays ponds was published to assist the efforts of 

the Government of Belize (GOB) to determine if this area 

should be included in the South Water Cay Marine Reserve (SWCMR). It was hoped that by bringing attention 

to the unique characteristics of these fragile communities 

they would be preserved. Based on those studies, the Pelican Cays were incorporated into the SWCMR that extends 

from Tobacco Cay in the north to Cat Cay in the south. 

The SWCMR is part of the Belize Barrier Reef Reserve 

System, which was inscribed on the UNESCO World Heritage List in 1996 (http://whc.unesco.org/). At that time, 

it was recognized by the World Heritage Committee and 

the GOB that, except for privately owned cays and those 

with preexisting leases, the cays of the SWCMR would 

be protected from development. In the Pelican Cays, such 

an exclusion would apply to a small area (1 ha) at the 

southern tip of Northeast Cay. However, since 1996 most 

of the mangrove cays within the SWCMR have been leased 

for proposed resort developments. Based on our recent 

aerial surveys in April 2008, in most of the islands in the 

Pelican Cays archipelago, large sections of the mangrove 

forests have been cut down and covered with dredged marine sediment from the adjacent seafl oor. Runoff of the 

fi ne fraction of the covering sediment has entered the interior ponds and smothered both the prop root-based and 

benthic seagrass communities. The extensive land clearing and fi lling is apparently an attempt to convert these 

mangrove islands into sandy cays in preparation for new 

tourist resorts.

METHODS AND RESULTS

FIELD OBSERVATIONS, MARCH 2007

We visited Manatee Cay (16°39.97N, 88°11.53W) 

in mid-March 2007 to conduct reconnaissance of seagrass 

and prop root-based benthic communities along the perimeter of Pond C. At a point on the southeast side of Pond C 

(see Figure 1), we encountered an area of dead mangrove 

roots and a thick sediment drape covering the steep slope 

into the center of the pond (see Figure 2C). The seagrass 

communities lining the pond slope had been effectively 

buried by the sediment drape. At the top of the slope in 

this area, the ubiquitous submerged mangrove root epibenthos was conspicuously absent. At the surface, we noted 

a fringe of dead red mangrove trees behind which was 

recently cleared land covered in white marine sediment 

containing numerous coral fragments and mollusk shells. 

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284 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 2. Marine communities of the Pelican Cay before (A, B) and after (C– F) dredging operations. A. Pre-dredging example of a rich 

encrusting community on a mangrove root that is dominated by the purple ascidian Clavelina puertosecensis. B. Healthy sponge community 

dominated by Mycale sp. and Scopalina sp. on a root before dredging. C. Spillover sediment surrounding bare dead mangrove roots in Pond 

C, Manatee Cay, after the deposition of dredged lagoonal sediment on clear-cut mangrove peat, March 2007. D. Aerial photograph showing 

the clear-cut sedimented areas of Fisherman’s and Manatee Cays. Note the dredge site in the lagoon at the right of Manatee Cay. E. Dredged 

Thalassia– Porites bottom community in the lagoon east of Manatee Cay. F. Harmful toxic alga Dictyota caribaea overgrowing the seagrass 

Thalassia testudinum at the bottom of Pond C, August 2007.

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NUMBER 38 • 285

At that time, the dredging work on Manatee Cay had 

been completed, but on Fisherman’s Cay (16°40.25N, 

88°11.40W), it appeared to be under way. Here, we observed similar clear-cutting and numerous large-diameter 

plastic pipes laid across the cleared area (Figure 3). The 

pipes are used to spread the sediment– water slurry over 

the mangrove peat and stumps. A dredging vessel was anchored just offshore of Fisherman’s Cay (Figure 4).

Dredged marine sediment covered the exposed mangrove peat substrate and created the illusion of a sandy 

cay. However, the introduction of loose, water-laden sediment over peat resulted in runoff, which smothered and 

killed the mangrove root and lagoonal bottom communities along the edges of the islands. Sediment collected on 

the mud-covered slope in Pond C (see Figure 2C) was very 

fi ne grained (rich in the clay-size fraction), which caused 

turbidity when it washed off the island. Along the outer 

edges of the island, runoff of the sediment slurry carried 

these fi ne sediments into nearshore waters. In one case, it 

smothered shallow-water head coral communities along 

the windward side of Fisherman’s Cay and created a muddy 

plume that extended into the pass between Fisherman’s 

and Manatee Cays. More detailed studies are needed to 

establish the changes that have occurred in the pond communities as a result of the dredging activity. A brief visit in 

August 2007 indicated a marked increase in macroalgae, 

most notably Dictyota caribaea, a bushy and toxic brown 

alga (Littler et al., 2006; see Figure 2F). In addition, further 

studies of the dredged lagoonal seafl oor areas should undertaken to assess the damage. A seagrass– Porites community 

to the east of Manatee Cay had been dredged down to 

2 to 3 m below the shallow surface (Figure 2E). We estimate that such destruction will take decades to recover, as 

indicated by the still bare but shallower seismic line depressions in seagrass beds surveyed in the 1960s between 

Carrie Bow Cay and Twin Cays.

AERIAL PHOTO SURVEYS, APRIL 2007

Aerial photos taken in April 2007 indicated extensive 

clearing of mangroves and dredge-spoil fi lling over the exposed mangrove peat on Manatee and Fisherman’s Cays 

FIGURE 3. Stumps of clear-cut mangroves being covered with lagoonal sediment transported by the black 

pipes (arrow) in the background, March 2007.

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286 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

(see Figure 2D). An area of disturbed, bare seabed (see 

Figure 2E) was visible where the dredge removed the sediment near Manatee Cay. The time series of aerial photos 

since 2003 indicated that Northeast Cay had been partially 

cleared and had buildings on it before March 2003. Manatee, Fisherman’s, Ridge, Bird, and Cat Cays had not yet been 

cleared in March 2003, but clearing had begun on all but 

one of the Bird Cays by April 2006. With the pumping of 

dredge spoil over the exposed mangrove peat and truncated 

roots, sediment spillover and runoff has resulted in extensive nearshore turbidity, which was also visible from the air 

along the edges of the ponds and the outer shorelines.

As of April 2007, approximately 15.4 ha (of 53.3 ha, 

or 29% of the total) of mangrove forests in the Pelican Cays 

had already been cleared, burned, and fi lled. Additional survey lines, which are typically the fi rst evidence of development activity, were visible on both Fisherman and Manatee 

Cays in the aerial photographs taken in April 2007.

PHYTOPLANKTON SAMPLING ALONG 

THE NORTH SIDE OF POND C

In May 2007, we conducted a preliminary survey at 

Manatee Cay to determine the effect of mangrove clearing and dredging in the Pelican Cays on the phytoplankton 

populations dominated by dinofl agellates, which may form 

red tides and visibly discolor the water (Morton and Villareal, 2001). Manatee Cay Pond C (see Figure 1) is large, 

semi-enclosed, separated from open water by coral ridges 

(Figures 1, 2D), and has distinct hydrographic, chemical, 

and biological characteristics. With little water exchange 

from the ocean side, the pond is warmer and more saline 

than the surrounding waters. This environmental setting allows microplankton, fi lter feeders, and corals to proliferate 

(Villareal et al., 2000). We observed that dying mangrove 

trees edged the pond and the water surface was highly turbid. Dinofl agellates and associated microplankton were collected in the center of Pond C via a vertical tow with a 20 

m pore size plankton net. Specimens were examined in the 

laboratory with an Axiophot Carl Zeiss light microscope, 

and dinofl agellate species were identifi ed (Faust, 2000). The 

water sample included a total of 14 species representing six 

genera. Oceanic species included Ceratium (2), Protoperidinium (5), and Pyrophacus (2). Coastal planktonic species 

included Gymnodinium (3) and Peridinium (2). Benthic 

species included Prorocentrum (3) (Table 1).

TABLE 1. Number of species in the dinofl agellate genera recorded in Manatee Cay, Pond C, Pelican Cays, collected in May 

1996 and May 2007.

 Number of species

Dinofl agellate genus 1996 2007

Amphidinium 2 – 

Bepharocysta 1 – 

Bysmatrum 1 – 

Ceratium 10 2

Cochlodinium 1 – 

Coolia 1 – 

Corythodinium 1 – 

Dinophysis 3 – 

Diplopelta 1 – 

Diplopsalis 3 – 

Diplopsalopsis 1 – 

Gambierdiscus 3 – 

Gonyaulax 6 – 

Gymnodinium 3 3

Heteraulacus 1 – 

Lingolidinium 1 – 

Ostreopsis 5 – 

Peridiniella 1 – 

Peridinium 3 2

Phaeopolykrikos 1 – 

Plagodinium 1 – 

Prorocentrum 1 3

Protoceratium 2 – 

Protoperidinium 15 5

Pyrodinium 2 – 

Pyrophacus 2 2

Scrippsiella 2 – 

Zygabikonidium sp. 1 – 

 Total genera: 28 75 17

FIGURE 4. Dredge boat operating off Fisherman’s Cay, March 2007.

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NUMBER 38 • 287

Live dinofl agellate cells were fewer than expected. 

Table 1 provides a comparison of the biodiversity and 

species associations of dinofl agellate assemblages before 

(May 1996) and after (May 2007) the clearing. In 1996, 

dinofl agellates included 28 genera and 83 species. In contrast, in 2007 only 6 genera and 14 species were present, 

and all were reduced in numbers of individuals present.

DISCUSSION

Despite repeated demonstration of their ecological and economic importance, mangroves are one of the 

world’s most threatened ecosystems (Valiela et al., 2001; 

Alongi, 2002; Rivera-Monroy et al., 2004). Overall, 50% 

of the world’s mangrove forests have been lost in the past 

50 years, with at least 35% lost in just the past two decades (Valiela et al., 2001). Duke et al. (2007) predicted 

the current rate of loss would lead to mangrove extinction 

in 100 years. Loss of mangroves is occurring faster in some 

areas. For example, 29% of Guatemala’s mangroves were 

lost in just 6 years between 1992 and 1998 (Abt Associates Inc., 2003). Most of that loss is directly attributed to 

unfettered clear-cutting for shrimp farm aquaculture, agriculture, mining, and development (Alongi, 2002). Based 

on growing evidence from around the world, the clearing 

and fi lling of mangrove forests for waterfront property to 

meet the demands of the leisure and tourism market for 

seaside resorts and retirement homes are also contributing 

signifi cantly to this loss (Ellison and Farns worth, 1996; 

Curran and Cruz, 2002; Barbier and Cox, 2003; Naylor et 

al., 2002; Choong, 2005). In the Gulf of Honduras along 

the Caribbean coast of Central America, mangroves have 

been destroyed to make way for hotels and other tourism 

infrastructure (CZAI, 2000). In these low-lying areas, such 

development requires fi ll material that is dredged from the 

seabed of nearby subtidal habitats. This action not only 

destroys corals and seagrass directly but also causes the 

suspension of sediments (turbidity), reduces light penetration, smothers seagrass and corals, increases nutrient levels, 

and releases contaminants (Rambøll Consulting Engineers, 

2000). In addition, the inadequately disposed solid waste 

and untreated sewage associated with this coastal development enter waterways and increase unwanted nutrients, thus decreasing water quality. Similar building efforts 

have been observed all along the Belize mainland coastline 

where many acres of mangroves have been cut down to 

make room for numerous large private homes and resorts. 

In addition, many acres of mangroves have been removed 

to create extensive areas of shrimp ponds.

Although tourism is the second largest foreign exchange earner for the countries of Belize, Honduras, and 

Guatemala in the region, this type of development is counterproductive because loss of mangroves leads to a reduction in income from tourism and fi sheries, changes in employment, loss of aesthetic value, loss of cultural heritage, 

confl icts between user groups, and loss of recreational opportunities (Abt Associates Inc., 2003).

Although mangrove forests are apparently considered 

of little value, recent studies have demonstrated the vital 

role of mangroves as nursery habitat for several species of 

reef fi sh (Mumby et al., 2004; Mumby, 2006). As stated 

by Mumby et al. (2004; specifi cally concerning Belize 

and Mexico), “Current rates of mangrove deforestation 

are likely to have severe deleterious consequences for the 

ecosystem function, fi sheries productivity and resilience of 

coral reefs.” In particular, the availability of mangroves 

for fi sh nursery habitat (intermediate between seagrass 

beds and coral reefs) is highly correlated to the numbers 

of reproducing adults and even the continued existence 

of certain species. According to these authors, parrotfi sh, 

which are important herbivores on reefs, have become locally extinct as a consequence of mangrove removal. Commercial species biomass has been effectively halved in areas of mangrove removal. Thus, the health of coral reefs 

and of fi sheries, both essential for both tourism and local 

livelihood, are deleteriously affected by mangrove loss.

Despite the legislated restrictions on leasing government-owned lands within the Belize Barrier Reef World 

Heritage Site and the SWCMR, most of these cays have 

been leased or sold to foreign developers since 1996 by 

following standard procedures. These procedures involve 

locating a suitable site and having it surveyed; this requires 

a permit from the Lands & Surveys Offi ce in Belmopan, 

Belize, which has apparently ignored the legal protection 

status afforded areas in marine protected areas. Separate 

permits from government departments are required to 

clear the leased areas delineated by survey lines. After the 

areas have been cleared, a developer must obtain another 

permit from the government to dredge material from the 

adjacent seabed to fi ll the leased areas.

The areas of mangrove clearing and fi lling with lagoonal sediments on Manatee and Fisherman’s Cays (and 

other islands in the group) are extensive, exposing most of 

the available island surfaces. As such, suffi ciently large areas 

have been cleared on these cays to account for potentially 

extensive development of seaside resorts. Disturbingly, the 

thin veneer of sediment laid over mangrove peat, especially 

where the mangroves themselves have been cleared, will 

not prevent signifi cant subsidence as the underlying peat 

21_Macintyre_281-290_Lang.indd 287 1_Macintyre_281-290_Lang.indd 287 9/24/09 10:29/24/09 10:29
288 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

decomposes and compacts. The substrate will then further 

subside because of the pressure of any load placed upon 

it, pilings notwithstanding, which will prove to be a signifi cant long-term problem for construction on mangrove 

substrate.

In addition to these obvious problems, construction 

on and habitation of these islands will ensure perpetual 

pollution of the ponds from continued sediment runoff 

combined with the eventual addition of sewage outfl ow 

and solid waste. Turbidity in the water column from 

runoff of dredge spoil will continue to deleteriously affect marine communities adjacent to the affected islands. 

Along the outer shorelines of Manatee and Fisherman’s 

Cays, numerous nearshore coral heads and patch reefs will 

eventually be smothered by the sediment load noted along 

the shorelines and in the passes between the Cays. In the 

Ponds, the rich benthic communities inhabiting the ridges 

upon which the islands are built and in the seagrass beds 

lining the slopes of the ponds have been locally decimated 

by direct sediment runoff. The water column in Pond C is 

now generally turbid, and it is anticipated that further sediment pumping, runoff, construction waste, and eventually untreated sewage outfall will further impact the pond 

habitats and cause eutrophication of the water column, 

which could lead to further losses of species, particularly 

photosynthetic organisms.

The Pelican Cays, although small in geographic scale, 

are characterized by great topological diversity in coral 

reef– mangrove habitats. Biological communities within 

this system vary markedly from one pond to another. Because of this complexity, some important details about the 

associations of dinofl agellate species in this ecologically 

diverse environment have come to light as a result of longterm studies in Pelican Cays (Faust, 2000). Dinofl agellates 

and microalgae are the primary food source for zooplankton, their primary consumer, including fi lter feeders and 

juvenile fi sh (Frenchel, 1988). Dinofl agellates and zooplankton proliferate in response to their unique physical, 

chemical, and biological needs (Villareal et al., 2000).

Species associations of dinofl agellates is another important indicator of certain stability in mangrove communities 

that are constantly threatened. Studies targeting processes in 

the Caribbean have examined benthic and epiphytic dinofl agellates in the coral reefs of the Virgin Islands (Tindall and 

Morton, 1998). Mangrove detritus, a unique microcosm, 

maintains a reservoir of diverse microalgae and meiofauna at 

Twin Cays, Belize (Faust, 1996). Most species tend to show 

preference for one habitat, either on sessile macroalgae or 

free-fl oating in the water column (Faust, 2004), although 

some species are found in a wide range of habitats.

Microbial communities can be damaged and species 

driven to local extinction by external factors; however, 

the damage is not immediately apparent to the human 

eye. Recent fi eld observations of microscopic microalgae 

and zooplankton signaled signifi cantly altered dinofl agellate populations, dead cells, and a greatly changed microscopic food web in Manatee Cay Pond C (see Table 

1). This is yet another example of the continuing trend 

in the Belizean coral reef– mangrove ecosystem observed 

over 25 years (beginning in 1982) indicating declining 

abundances of dinofl agellate and zooplankton in the 

microbial food web caused by human activities (Faust, 

2004). This fi nding in itself has important implications 

for the ecology and economy of the Belizean Barrier 

Reef, in that dinofl agellate populations are the primary 

food source of zooplankton, including fi sh larvae and 

juvenile fi sh.

CONCLUSIONS

Despite the location of Pelican Cays within the 

SWCMR and the World Heritage Site, development has 

been accomplished by following a sequence of procedures 

involving several separate jurisdictions. Investigations began recently into the process of mangrove cutting, clearing, and fi lling in the Pelican Cays, and it appears that 

some of this activity was illegal (Melanie McField, Smithsonian Marine Station at Fort Pierce, personal communication, April 2008). 

It is highly questionable that the proposed highly vulnerable tourist resort on the Pelican Cays will survive the 

subsidence related to rotting peat or storms. Indeed, these 

sea-level structures will be readily destroyed by severe 

storms, leaving abandoned communities both on land and 

in the sea in an area originally noted for its unique and 

unusually high biological diversity.

The future of the unique ecology of the mangrove 

and seagrass communities in the Pelican Cays appears to 

be very bleak. The dredging barge is no longer operating 

off Fisherman’s Cay, and a Caribbean Island Brokers website is now offering 37 acres of cleared mangrove on this 

cay for US $1,750,000. Given this situation, all mangrove 

islands in this area will be cleared and developed, so that 

the ponds adjacent to cleared areas will likely suffer the same 

fate as Pond C of Manatee Cay, as will nearshore marine 

communities along the outer perimeters of these islands. 

Lack of foresight, which is disrupting the connectivity between mangroves and the health of the nearshore marine 

realm, will result in economic losses following the reduc21_Macintyre_281-290_Lang.indd 288 1_Macintyre_281-290_Lang.indd 288 9/24/09 10:29

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NUMBER 38 • 289

tion of commercial and recreational fi sheries that rely on 

mangroves. Much of this collapse is related to the dramatic 

loss of dinofl agellate assemblages, which provide the base 

of food webs supporting fi sheries in Belize.

Tourism losses will subsequently occur as coral reefs 

decline without mangroves to support the mangrovedependent fi sh species essential to reef herbivory and 

commerce. Thus, the short-term economic gains from 

construction will lead to long-term environmental disruption, ecological degradation, local species extinction, and 

the consequent economic collapse of the tourism and fi shing industries all along the Belizean coast and similarly 

affected areas of Mesoamerican reefs. The government of 

Belize has instituted a mangrove clearing moratorium to 

evaluate the situation.

ACKNOWLEDGMENTS

We thank Gary Peresta for fi eld assistance; LightHawk 

(Michele Gangaware) for providing the plane and pilot for 

aerial surveys; Molly Ryan of the Smithsonian National 

Museum of Natural History (NMNH) for preparing the 

index map; Chip Clark of the Smithsonian NMNH for 

photographs (Figure 2A,B); and fi nally Klaus Rützler, Janet 

Gibson, Isaias Majil, Melanie McField, and John Tschirky 

for providing advice and information for this manuscript. 

This is contribution number 831 of the Caribbean Coral 

Reef Ecosystems Program (CCRE), Smithsonian Institution, supported in part by the Hunterdon Oceanographic 

Research Fund.

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21_Macintyre_281-290_Lang.indd 290 1_Macintyre_281-290_Lang.indd 290 9/24/09 10:29/24/09 10:29
Using the Panama Canal to Test Predictions 

about Tropical Marine Invasions

Gregory M. Ruiz, Mark E. Torchin, 

and Katharine Grant

ABSTRACT. As humans alter the landscape of the Earth and economic globalization 

expands, biological invasions increasingly homogenize the world’s biota. In temperate marine systems, invasions are occurring at a rapid pace, driven by the transfer of 

organisms by vessels and live trade (including aquaculture and fi sheries activities). In 

contrast, little is known about patterns and processes of tropical marine invasions, 

although the same species transfer mechanisms are in operation. This disparity may 

be the result of limited studies of invasions in the tropics relative to temperate regions. 

Alternatively, the tropics may be less susceptible to invasion than temperate regions for 

reasons of environmental unsuitability and biotic interactions. This paper provides a 

brief summary of the current but limited information of marine invasions across latitudes, focusing particular attention on the eastern Pacifi c north of the Equator. Within 

this latitudinal framework, the Panama Canal provides an especially important model 

system for testing predictions about marine invasions in the tropics for reasons of (a) 

the high level of shipping traffi c since the Canal opened in 1914; (b) the permeability 

of the Canal as a conduit for marine invaders, despite the apparent freshwater barrier; 

and (c) the current expansion of the Canal that is expected to increase the size and 

number of ships visiting the region.

INTRODUCTION

Biological invasions are common in coastal marine ecosystems around the 

world (Cohen and Carlton, 1995; Orensanz et al., 2002; Fofonoff et al., 2008). 

In fact, reports of new invasions are increasing exponentially in many wellstudied regions (Cohen and Carlton, 1998; Ruiz et al., 2000; Hewitt et al., 

2004). Although invasions can result from natural dispersal, most contemporary invasions derive from human-mediated transfer associated with a variety 

of activities. As economic globalization continues to expand, creating a high 

degree of connectivity through the movement of commodities and people, opportunities for new invasions also increase. Bays and estuaries have been the 

most invaded marine systems, probably because they are hubs for shipping, 

aquaculture, and other human endeavors known to transfer organisms (Ruiz et 

al., 1997; Wasson et al., 2005).

Gregory M. Ruiz and Katharine Grant, Smithsonian Environmental Research Center, 647 Contees 

Wharf Road, Edgewater, Maryland 21037, USA. 

Mark E. Torchin, Smithsonian Tropical Research 

Institute, Apartado 0843-03092, Balboa, Ancon, 

Panama, Republic of Panama. Corresponding author: G. Ruiz (ruizg@si.edu). Manuscript received 

29 August 2008; accepted 20 April 2009.

22_Ruiz_291-300_Lang.indd 291 2_Ruiz_291-300_Lang.indd 291 9/24/09 10:20/24/09 10:20
292 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

To date, most human-mediated invasions (hereafter 

introduced species) in marine habitats have been reported 

in temperate latitudes (Ruiz and Hewitt, 2008, and references therein). Relatively few introduced species have been 

reported from tropical or polar regions. This difference 

across latitudes may result partly from historical research 

effort and taxonomic knowledge, which are greatest in the 

temperate zone. However, a small but growing literature 

for high latitudes suggests that marine invasions may be 

limited in polar regions by a combination of current low 

temperatures and low propagule supply (Barnes et al., 

2006; Aronson et al., 2007; Ruiz and Hewitt, 2008).

It is evident that marine invasions can occur in tropical 

marine systems (Agard et al., 1992; Guerrero and Franco, 

2008), but the extent to which they occur remains largely 

unexplored. Few studies have evaluated marine invasions 

in the tropics. The exceptions are extensive analyses of 

introduced species on the Hawaiian Islands and Guam 

(Eldredge and Carlton, 2002; Paulay et al., 2002). It is uncertain whether these island ecosystems are broadly representative of the tropics, including especially mainland sites 

that may differ from islands in susceptibility to invasion 

(Elton, 1958; MacArthur and Wilson, 1967; Sax, 2001).

In a preliminary analysis of marine invasion patterns for mainland Australia, Hewitt (2002) reported an 

increase in introduced species richness with increasing 

latitude. The study included four tropical and four temperate sites, spanning 13°– 38°S latitude. Despite a signifi -

cant relationship with latitude, there is uncertainty about 

the taxonomic identifi cation and biogeographic origin of 

many tropical species, resulting from limited information 

and relative lack of study for low latitude biotas. For this 

reason, Hewitt urges some caution and underscores the 

need for further analyses to interpret the observed pattern. 

It is nonetheless intriguing that this preliminary analysis provides results similar to those reported for tropical 

terrestrial systems, where relatively few exotic species of 

birds, mammals, and plants are established (Sax, 2001).

We have begun to explore latitudinal patterns of 

marine invasions for the mainland (continental) habitats 

within the Americas. To date, most of our analyses have 

focused on bays and estuaries within the United States, 

particularly on the Pacifi c Coast. We are currently initiating a research program to compare the number of introduced species, scale of vector operations (propagule 

supply), and ecology of invasions across temperate and 

tropical latitudes. Here, we briefl y review the current state 

of knowledge about invasions and invasion processes 

along the Pacifi c Coast of the Central and North America and discuss the potential signifi cance of Panama as a 

model system to evaluate regional and latitudinal patterns 

of marine invasion.

LATITUDINAL PATTERN OF INVASIONS 

ALONG THE NORTHEASTERN PACIFIC

Outside of the tropics, there is a clear increase in the 

number of nonnative species reported with decreasing 

latitude, from Alaska to California, 61°–32°N (Ruiz et 

al., 2006a). An extensive review and synthesis of the literature indicate that more than 250 nonnative species of 

invertebrates and algae are established in coastal waters 

of California (NEMESIS, 2008). Most of these invasions 

are attributed to commercial shipping and live shipments of organisms, especially oysters and their associated biota (Cohen and Carlton, 1995; Miller, 2000; Ruiz 

et al., unpublished data). Some of the California invasions have spread northward through natural dispersal, 

and other species have been introduced independently to 

the north. However, compared to California, far fewer 

nonnative species are known from Oregon, Washington, 

and Alaska (Cohen et al., 1998; Wonham and Carlton, 

2005; Ruiz et al., 2006a).

Although this latitudinal pattern of invasion could result from reporting biases in the literature, particularly in 

the level of research (search effort) among regions, recent 

surveys suggest that the pattern is robust for sessile invertebrates in hard substrate fouling communities. Using standardized surveys to sample sessile invertebrates, deRivera et 

al. (2005) and Ruiz et al. (2006a) found that the number 

of introduced species increased with decreasing latitude 

from Alaska to southern California. It appears that the 

northern spread of many nonnative species from California may have been limited by dispersal as a result of the 

relatively low level of human activities (and, thus, species 

transfer opportunities) that have been present historically 

(Ruiz and Hewitt, 2008).

Similar analyses are not yet available to extend this 

comparison to lower latitudes along the eastern Pacifi c. 

Although there have been some studies reporting introduced marine species in Central America (Rubinoff and 

Rubinoff, 1969; Lambert and Lambert, 2003; Wysor, 

2004, Roche and Torchin, 2007; Roche et al., 2009; Bastida-Zavala, 2008), standardized, quantitative community-level comparisons are lacking. In particular, synthetic 

studies focused within bays and estuaries of Central America targeting those taxonomic groups for which invasions 

are often most prevalent do not exist. Even where syntheses from the literature have been attempted, the paucity 

22_Ruiz_291-300_Lang.indd 292 2_Ruiz_291-300_Lang.indd 292 9/24/09 10:20/24/09 10:20
NUMBER 38 • 293

of available data limits conclusions about the scope of 

invasions. For example, Cohen (2006) provides a useful 

summary of available information on invasions surrounding the Panama Canal, which has received considerable 

attention for a tropical system. Despite the historical interest on biotic exchange in Panama, Cohen characterizes 

the current state of knowledge as follows: “The Panama 

Canal lies in a region of the world where the marine biota 

is both diverse and relatively poorly known, and there has 

been remarkably little investigation of the effect that the 

Canal has had on the distribution of that biota.”

With a broad goal to evaluate patterns and processes 

in marine invasions using a latitudinal framework, we have 

initiated a research program in Central America (a) to compile available data from the literature on nonnative marine 

species, as part of our database (NEMESIS, 2008), and 

(b) to conduct standardized surveys at multiple sites. Our 

approach will allow direct comparisons with more than 

two dozen sites surveyed on the Pacifi c and Atlantic coasts 

of the USA. Our initial effort is focused primarily on sessile invertebrates (including ascidians, barnacles, bryozoans, hydroids, mussels, and sponges), which comprise a 

large proportion of marine introductions, are relatively 

well studied, and are conducive to standardized, quantitative fi eld surveys.

A preliminary review of the literature for barnacles 

suggests the number of introduced species increases from 

Alaska to Panama (Figure 1A), consistent with an increase 

in the magnitude of shipping (see next section). At least 

four nonnative species of barnacles are reported to occur 

on the Pacifi c coast of Panama, including Amphibalanus 

amphitrite, A. reticulatus, Balanus trigonus, and Fistulobalanus pallidus (Matsui et al., 1964; Jones and Dawson, 

1973; McCosker and Dawson, 1975; Laguna, 1985). 

Three introduced barnacles are known from California: 

Amphibalanus amphitrite, A. eburneus, and A. improvisus (Carlton, 1979; Carlton and Zullo, 1969; Cohen and 

Carlton, 1995; Cohen et al., 2002). Amphibalanus reticulatus has also been detected in recent surveys in southern California, but it is not yet known to be established 

(Ruiz, unpublished data). Only one introduced barnacle, 

A. improvisus, is reported in Oregon and Washington 

(Carlton, 1979; Wonham and Carlton, 2005), and there 

are no introduced barnacles known from Alaska (Ruiz et 

al., 2006a). It is noteworthy that the reported number of 

nonnative barnacle species in Panama exceeds that along 

the western USA, considering the latter is relatively well 

surveyed. Thus, we expect that strength of this inverse 

relationship with latitude may increase with additional 

information.

FIGURE 1. A. Number of nonnative barnacle species established by geographic region. Shown are the numbers of nonnative barnacle species 

reported to be established from Alaska to Panama (see text). B. Number of vessel arrivals by geographic region. Shown are the numbers of commercial vessel arrivals from overseas to different geographic regions, from Alaska to Panama, over a two-year period (2004– 2005). Coastwise 

domestic traffi c is excluded from arrivals to U.S. locations. (Data from Miller et al., 2007; ACP, 2008b.)

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294 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

At the present time, the relationship between introduced species richness and latitude is poorly resolved for 

the northeastern Pacifi c and other global regions. The pattern presented in Figure 1A should be considered as preliminary, and it may change with further research. We also 

caution that these data are restricted to barnacles, a very 

small subset of species present in the fouling community.

PANAMA: A TEST CASE FOR 

TROPICAL MARINE INVASIONS

Panama is a potential hotspot for tropical marine invasions, because of the country’s historic signifi cance as 

a hub of world trade since the fi fteenth century, expanding greatly since construction of the Panama Canal. The 

Canal created a new shipping route between the Atlantic 

and Pacifi c basins, resulting in a large infl ux of commercial 

ships, which have been an important source of introduced 

species in North America (Cohen and Carlton, 1995; Cohen et al., 1998, 2002; Ruiz et al., 2000; Wonham and 

Carlton, 2005; see discussion below). Figure 1B compares 

the magnitude of commercial shipping to several major 

port systems, indicating that ship arrivals to Panama exceed those to major port systems in the western United 

States by a large margin. Over the two-year period 2004– 

2005, nearly twice as many vessels arrived to Panama as 

overseas vessels arrived to California. In fact, Panama receives more ship arrivals than any of the largest ports in 

the United States (Ruiz et al., 2006b; Miller et al., 2007).

Since its opening in 1914, the number of Canal transits increased rapidly, with the exception of a brief interruption during WW II, until reaching capacity in 1970 

(ACP, 2008a; Figure 2). Currently, the Canal is operating at 90% of its theoretical maximum capacity, servicing 12,000 to 14,000 vessels and carrying approximately 

5% of the world’s cargo annually (Reagan, 2007). More 

than 800,000 ocean-going commercial vessels have 

passed through the Canal since its completion (Ruiz et 

al., 2006b).

While the number of transits has leveled off, the average size of ships transiting the Canal has continued to 

increase, allowing for a continued increase in the volume 

of cargo passing through the Canal (ACP, 2008a; see Figure 2). The average tonnage (based on CPSUAB, a universal system of tonnage for the Panama Canal, or Canal 

ton, which is equivalent to approximately 100 cubic feet 

of cargo) per transit has increased from 4,832 in 1955 to 

21,963 in 2005 (ACP, 2008a). This change in cargo capacity refl ects an increase in the size of vessels over time; 

these changes are the topic of a future analysis that will 

characterize changes both in vessel size and in underwater surface area available for colonization by organisms. In recent years, however, the size of vessels has been 

constrained by the lock dimensions and has been relatively 

static, with the Panamax ships designed specifi cally as the 

largest vessels able to transit the locks (see next section).

Likely consequences of the Panama Canal and ports 

located at both entrances are an increase in (a) the global 

transfer of marine organisms, as the canal provides a conduit for worldwide shipping, and (b) regional biological 

invasions in Central America. Commercial shipping is a 

major pathway for the movement of species and appears 

largely responsible for a dramatic increase in the rate of 

known invasions for many regions in recent time (Ruiz 

et al., 2000; Fofonoff et al., 2003; Hewitt et al., 2004). 

Ships move organisms associated primarily with hull 

and sea chest fouling and with ballasted materials, as an 

unintended result of normal operations (Carlton, 1985; 

Minchin and Gollasch, 2003). In general, the likelihood 

of invasions increases with increasing propagule supply, 

including the magnitude and frequency of organisms delivered (Ruiz and Carlton, 2003; Lockwood et al., 2005). 

Thus, the chance of colonization by introduced species 

in Panama is likely to have increased over time with the 

high frequency of vessels arriving to Panama from around 

the globe.

FIGURE 2. Number of commercial vessel transits (black line) 

through the Panama Canal and associated cargo tonnage (gray line); 

CPSUAB is a universal system of tonnage for the Panama Canal, or 

Canal ton, which is equivalent to approximately 100 cubic feet of 

cargo. (Figure modifi ed from ACP, 2008a.)

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NUMBER 38 • 295

Given the high number of vessel arrivals, we might 

also expect the relative magnitude of propagule supply and invasions to be high in Panama. However, this 

remains to be tested, and there are several reasons why 

this may not be the case. First, different ship types and 

operational behaviors vary in their potential to transfer 

marine organisms (Verling et al., 2005; Miller et al., 2007; 

NBIC, 2008). Second, independent of propagule supply, 

some sites are less susceptible to invasion for reasons of 

either environmental conditions or biological interactions 

(Lonsdale, 1999; Ruiz et al., 2000; Roche et al., 2009).

Past studies have certainly highlighted the potential 

signifi cance of vessels as a source of invasions to the Panama Canal and surrounding waters (see Cohen, 2006, 

and references therein for recent review). For example, 

Chesher (1968) discusses the potential importance of 

ballast water. Menzies (1968) considers the capacity of 

vessels to transfer fouling organisms. Hay and Gaines 

(1984) suggest that small pleasure boats may be especially important in the transfer or organisms across the 

Isthmus of Panama. A few studies also test the capacity 

of marine organisms to survive freshwater exposure for 

the duration of a transit through the Canal (Chesher, 

1968; Hay and Gaines, 1984). Despite the long interest and recognition in ship-mediated transfer, the estimates given above are limited to few (if any) data on 

species composition or direct quantitative estimates of 

propagule supply (abundance) on vessels. Surprisingly 

few data exist on biota associated with ballast water 

or hulls of vessels associated with the Canal. Instead, 

there are only coarse data available on general operational aspects of vessels that may affect species transport 

opportunities.

Most commercial ships arriving to Panama will transit the Canal, but some will have considerable time at anchorage before entering the Canal. From 2000 to 2005, 

the average service time (from arrival to complete transit) 

of ships passing through the Canal was 16 hours when 

holding reservations. However, many ships have not had 

reservations, and average service times for these ships can 

reach 57 hours (Table 1). Although the proportion of ships 

holding reservations has increased in recent years, half of 

all ships still experienced some delay. Such increased residence time is likely to also increase the opportunity for reproduction and colonization of organisms associated with 

ships’ hulls (Minchin and Gollasch, 2003; Davidson et 

al., 2008), relative to shorter residence times. It is evident 

that some organisms arrive to Panama on the hulls of vessels (Figure 3). However, a lack of quantitative information on the biota associated with outer surfaces of vessels 

transiting the Panama Canal and surrounding ports limits 

any detailed analyses.

For ballast water, we are not aware of any reliable 

estimates of the historical patterns of ballast water management and discharge of vessels arriving to Panama, including those ships delivering cargo to the terminals and 

those simply transiting the Canal. Even a coarse estimate 

of volume is challenging, given large differences in operations among vessels (Verling et al., 2005; but see Chesher, 

1968). Presumably, ballast water discharge today is rather 

limited because many vessels conduct ballast operations to 

compensate for loading or off-loading cargo. In addition, 

Panama prohibits ballasting operations in the Canal under 

most circumstances (ACP, 2008b).

Despite the limited information available, we surmise 

that propagule supply has been relatively high in Panama, 

compared to many other temperate and tropical sites. Based 

solely on the large number of vessel arrivals and their relatively long residence times (see Figure 2, Table 1), it is likely 

that Panama has received large inocula of nonnative organisms associated with the vessels’ hulls and sea chests, which 

have been historically important sources of invasions in 

TABLE 1. Comparison of service time for ships with and without reservations transiting the Panama 

Canal; n number of ships. (Source: Modifi ed from ACP, 2008a.)

 Mean transit time (hours) through canal

Year Reservation (n) No reservation (n) Could not get reservation (n)

2000 16.7 (1,944) 35.7 (6,864) 42.1 (121)

2001 15.7 (5,008) 26.3 (6,590) 43.7 (306)

2002 16.1 (5,692) 29.0 (5,134) 57.1 (1,062)

2003 16.2 (5,527) 24.9 (4,596) 45.1 (1,361)

2004 16.4 (6,419) 30.5 (3,568) 49.8 (2,531)

2005 16.5 (6,972) 27.3 (3,406) 45.8 (2,270)

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296 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

other regions (Coutts, 1999; Coutts et al., 2003; Coutts 

and Taylor, 2004; Hewitt et al., 2004).

As a result of its shipping history, Panama provides 

a unique opportunity to test hypotheses about patterns 

and processes of invasions to tropical marine systems. If 

propagule supply drives invasion patterns, we predict that 

Panama may be a hotspot for invasions. If tropical systems 

are inherently less susceptible to invasions (Elton, 1958; 

Sax, 2001), we would expect to see low introduced species 

richness despite high historical propagule supply. Our current research seeks to estimate nonnative species richness 

and advance our understanding of historical propagule 

supply in Panama, in the context of a broader latitudinal 

comparison as discussed above.

EVALUATING FUTURE 

CHANGES IN PANAMA

In October 2006, the Republic of Panama passed a 

referendum to expand the capacity of the existing Canal. 

The modernization will include (a) two new sets of locks, 

one at the Pacifi c entrance and one at the Atlantic; (b) two 

new navigational channels to connect the locks to existing 

channels; and (c) deeper and wider shipping lanes (Reagan, 2007). The expansion project is now under way and 

is scheduled to be completed by 2015 (Reagan, 2007).

When the expansion is completed, the Panama Canal 

Authority estimates that Canal transits will most likely 

increase from 12,700 per year in 2005 to approximately 

19,600 in 2025, with an optimistic forecast as high as 

22,100 transits per year (Figure 4). Further, the largest vessels currently capable of transiting the Canal are Panamax 

ships reaching 320 m in length that can carry 65,000 tons 

of cargo. After the completion of the new locks, the Canal 

will accommodate vessels up to 425 m long, carrying about 

twice the amount of cargo of today’s ships (Gawrylewski, 

2007; Reagan, 2007).

While efforts have been made to evaluate potential environmental effects of the Panama Canal expansion (ACP, 

2008a), the possible effects of this expansion on invasion 

dynamics have not received much attention to date. One 

might expect an increase in propagule supply associated 

with the increased number and size of vessels transiting the 

FIGURE 3. Photograph of a vessel hull upon arrival to Panama showing associated biofouling organisms. 

Inset: Close up of bow with barnacles.

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NUMBER 38 • 297

Canal. There may also be shifts in trade routes that could 

expand the species pool associated with ships’ arrivals, resulting from either new markets or previous constraints 

on the size of vessels that could previously use this corridor. Alternatively, the service time of vessels may decrease 

as the capacity to accommodate more transits increases. 

This decrease could reduce the establishment probability 

of organisms attached to the hulls of arriving vessels, as 

residence time and likelihood of invasion are thought to be 

positively correlated (Davidson et al., 2008).

Potential changes in environmental conditions associated with both the ships and the Canal entrances 

could also infl uence future invasions. With the international ban on tributyl tin as an antifouling coating now 

coming into force, some have suggested that biofouling 

of ships’ hulls, and hence ship-mediated propagule supply, may increase (Nehring, 2001). Additionally, changes 

in the salinity regimes will probably occur at both Pacifi c and Atlantic entrances to the Canal, as well as in 

areas within the Canal near the lockages, as a result of 

increased freshwater discharges into the oceans and potential seawater intrusion into the Canal. Such changes 

in salinities could alter the susceptibility to invasion for 

arriving organisms. However, any predictions about directional changes in propagule supply and susceptibility 

are currently speculative at best, as suffi cient information 

presently is not available.

There is also a regional context for the Panama Canal 

that deserves consideration. Although the Canal provides 

a critical corridor across the Isthmus of Panama for global 

trade, Panama’s ports are becoming increasingly important 

hubs for the regional distribution of commodities. More 

specifi cally, cargo that is delivered to Panama’s ports is often transferred secondarily by other vessels to surrounding 

countries in the region. As Panama is a distribution center, 

any increase in introduced species increases the chances for 

ship-mediated dispersal to surrounding ports. Conversely, 

increased commerce with the other countries in the region 

also enhances the opportunity for delivery of organisms to 

Panama. The potential signifi cance of such regional dispersal through this hub-and-spoke system of shipping has 

not been evaluated for the past, present, or future.

We are currently working with the Panama Canal Authority and the University of Panama to evaluate the role of 

the Panama Canal in regional and global marine invasions. 

Although the major focus of our efforts is to evaluate past 

and current levels of invasion, as well as to obtain some 

coarse estimates of propagule supply to the region, we 

hope to provide the baseline needed to forecast and evaluate potential impacts of future changes on invasion risks.

CONCLUSIONS

Panama provides exceptional opportunities to test 

hypotheses about invasions in tropical marine systems. 

The presence of the Canal and the magnitude of shipping 

to the region have undoubtedly increased the supply of 

nonnative species delivered to the shores of Panama. 

While there is limited information on actual propagule 

delivery, the Panama Canal Authority has maintained 

historical records on the number and characteristics of 

transiting vessels. This information provides a unique 

view of the magnitude of shipping and changes through 

time and could be used as an initial coarse proxy for 

propagule supply. We predict that invasions are common 

in Panama relative to surrounding regions as a result of 

the intensity of shipping in the area. If propagule supply 

is positively correlated to introduced species richness, as 

the literature suggests, we predict a relatively high number of invasions have occurred. However, if relatively 

few introduced species are detected in Panama, this suggests that some combination of environmental conditions and biotic resistance may limit invasions in this 

tropical region.

FIGURE 4. Forecast of demand for Canal transits. Solid black line 

probable demand, dashed line high (optimistic) demand, and 

shaded gray line low (pessimistic) forecast demand. In 2005, there 

were 12,647 recorded Canal transits (solid circle). (Figure modifi ed 

from ACP, 2008a.)

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298 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

We have focused attention on Panama as a model system to understand marine invasion dynamics, but a robust 

analysis must also include comparisons to other locations 

that differ in the intensity of shipping and other transfer 

mechanisms. Ideally, such comparisons should be replicated across latitudes. Such a comparative approach is key 

to untangling patterns of marine invasions in tropical and 

temperate regions and, ultimately, in determining the processes that drive these patterns.

ACKNOWLEDGMENTS

We thank Michael Lang for organizing the Smithsonian Marine Science Symposium and for providing us the 

opportunity to participate. For discussions on the topic, 

we thank James Carlton, Ian Davidson, Richard Everett, 

Paul Fofonoff, Chad Hewitt, Anson Hines, Julio Lorda, 

Valentine Lynch, Whitman Miller, Ira Rubinoff, and Mark 

Sytsma. For comments and improvements to the manuscript, we thank James Carlton, Daniel Muschett, John 

Pearse, and Brian Wysor. We also acknowledge assistance 

from the Panama Canal Authority (ACP) and funding from 

the National Sea Grant Program, Smithsonian Institution, 

Secretaría Nacional de Ciencia Tecnología y Innovación 

de Panamá (SENACYT), and the U.S. Coast Guard.

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22_Ruiz_291-300_Lang.indd 300 2_Ruiz_291-300_Lang.indd 300 9/24/09 10:20

/24/09 10:20
Ciguatera Fish Poisoning in the Caribbean

Patricia A. Tester, Rebecca L. Feldman, 

Amy W. Nau, Maria A. Faust, 

and R. Wayne Litaker

ABSTRACT. Ciguatera fi sh poisoning (CFP) is a signifi cant illness in the Caribbean. Local fi shers and natives attempt to avoid CFP by applying traditional knowledge concerning where and when certain fi sh species are likely to be ciguatoxic, but this knowledge 

is incomplete. Evidence gathered over the past decades indicates that CFP events are 

increasing and becoming more unpredictable, thereby posing a greater threat to local 

inhabitants as well as tourists. The current understanding of CFP distribution is from 

studies nearly a decade old and generated largely by self-reported CFP incidents to a 

call-in “hotline” in Miami, Florida. To better guide resource allocation and focus future 

research, an active survey method was used to uniformly query public health professionals and fi sheries offi cials on the occurrence of CFP. Points of contact from each of these 

two groups were compiled for the 24 Caribbean island countries and territories and 9 

mainland countries bordering the Caribbean. An outcome of this project will be to provide public health agencies, resource managers, and others with information they can use 

in developing CFP tracking systems and effective public education programs. The longterm goal of associated efforts is to provide accurate and affordable monitoring tools for 

predicting the onset of CFP events.

PREFACE

Ciguatera fi sh poisoning (CFP) occurs in tropical regions worldwide and is 

globally the most common nonbacterial food-borne illness (Tester, 1994; CDC, 

2007; Figure 1A). The toxic organisms most commonly associated with CFP 

are benthic dinofl agellates reported to produce ciguatoxins or maitotoxins (Yasumoto et al., 1977; Durand-Clement, 1987; Satake, 2007). Ciguatoxins bioconcentrate in the food chain and reach their highest levels in top predators 

such as barracuda or other tropical reef fi sh. These toxins have been found in 

more than 400 fi sh species, including groupers, snappers, jacks, mackerels, triggerfi sh, and surgeonfi sh (Bagnis et al., 1970). Consumption of tainted fi sh can 

lead to gastrointestinal distress followed by neurological (perioral numbness, 

tingling, temperature sensory reversal) and cardiovascular (arrhythmia, bradycardia, tachycardia, reduced blood pressure) symptoms and, in rare cases, death. 

The chronic phase of CFP can persist for weeks, months, or years (Freudenthal, 

1990), and repeated exposure to ciguatoxins exacerbates the symptoms.

Patricia A. Tester, Amy W. Nau, and R. Wayne Litaker, National Ocean Service, NOAA, 101 Pivers Island Road, Beaufort, North Carolina 28516, USA. 

Rebecca L. Feldman, RLF Environmental, 2220 

Sheffl in Court, Baltimore, Maryland 21209, USA. 

Maria A. Faust, Department of Botany, National 

Museum of Natural History, Smithsonian Institution, 4210 Silver Hill Road, Suitland, Maryland 

20746, USA. Corresponding author: P. Tester 

(pat.tester@noaa.gov). Manuscript received 9 June 

2008; accepted 20 April 2009.

23_Tester_301-312_Lang.indd 301 3_Tester_301-312_Lang.indd 301 9/24/09 10:00/24/09 10:00
302 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

This paper provides the justifi cation for and an overview of our recent efforts to conduct an active survey of 

public health offi cials and fi shery management professionals on the incidence of CFP in the Caribbean. We currently lack an accurate picture of CFP in the Caribbean 

because of the diffi culty in diagnosing CFP and the absence of uniform reporting criteria or any entity responsible for maintaining this information. Previous information gathered on the incidence of CFP in the Caribbean 

has relied heavily on self-reporting mechanisms, such as 

calls to a “hot-line” in Miami, Florida. Because people 

living closer to Miami are more likely to know about the 

hot-line, the reported incidence rates could refl ect a geographic bias (Figure 1B). Another important aspect of this 

research has been to focus the joint research efforts of 

the National Oceanic and Atmospheric Administration 

(NOAA) and Smithsonian Institution scientists who are 

working on the molecular and morphological characterization of the toxic dinofl ag ellates responsible for CFP. 

Both groups have strong interests in understanding how 

changes in the distribution and abundance of ciguateraassociated dinofl agellate species relate to the occurrence 

and severity of CFP.

An important outcome of this project will be to provide public health agencies, resource managers, and others with information that they can use in developing CFP 

tracking systems and effective public education programs. 

The long-term goal of associated efforts is to provide accurate and affordable monitoring tools for predicting the 

onset of CFP events.

INTRODUCTION AND BACKGROUND

Ciguatera fi sh poisoning is a common disease in the 

Caribbean, caused by the ingestion of a wide variety of 

fi shes that contain toxins accumulated from the marine 

food web (Lewis and Holmes, 1993) (Figure 1B). The ultimate sources of these toxins (ciguatoxins and maitotoxins) are small benthic microalgae belonging to the dinofl agellate genera Gambierdiscus, Coolia, Ostreopsis, and 

Prorocentrum (Figure 2) (Steidinger and Baden, 1984). Although ciguatera fi sh poisoning (CFP) is a threat to public 

health throughout the Caribbean, it is generally managed 

by local, traditional knowledge of the native fi shers. However, their knowledge of the seasonality of occurrence and 

locations of ciguatoxic reefs may no longer be accurate 

because of changing environmental conditions (Tester, 

1994; Tosteson, 2004). These environmental changes in 

turn alter the distribution and abundance patterns of the 

cells that cause CFP. Some evidence exists that ciguatoxicity may vary seasonally, but not all studies support this 

view (de Fouw et al., 2001). Tosteson (2004) argued that 

seasonality of CFP and the correlation of dinofl agellate 

abundance with CFP intoxications evident before 1990 

FIGURE 1. A, Potential global distribution of ciguatera fi sh poisoning (CFP). Red areas indicate regions with a high CFP prevalence, 

yellow indicates moderate potential exposure, and green indicates 

regions where the dinofl agellates responsible for the disease are 

found and represent a potential problem. This map represents a 

composite of the data obtained from an aquatic biotoxins review by 

Huss et al. (2003), the CFP distribution map maintained by the journal Harmful Algae (WHOI, 2008), and Lewis (2006). B, Potential 

distribution map of CFP in the Caribbean, as modifi ed from Stinn et 

al. (2000), combined with some recent incident reports showing the 

presumed distribution of ciguatera fi sh poisoning in the Caribbean, 

mostly collected by passive means; that is, a self-reporting CFP hotline in Miami (“Cigualine” at 1-888-232-8635). Red areas indicate 

high frequency of CFP reports; yellow indicates regions where CFP 

is reported less frequently; green indicates infrequent reports of CFP. 

These maps may not accurately portray the actual CFP distribution 

because many cases go unreported.

23_Tester_301-312_Lang.indd 302 3_Tester_301-312_Lang.indd 302 9/24/09 10:00/24/09 10:00
NUMBER 38 • 303

was not observed in data from 1990– 2000. He suggested 

these changes appeared to be associated with increasing 

periods of elevated sea-surface temperatures in the Caribbean. Further, the potential for a greater number of people 

to be exposed to CFP has increased because of more intense exploitation of fi sheries and the depersonalization 

of markets (Olsen et al., 1984). Both trends have been accelerated by tourism and rapidly growing resident populations (CIA, 2008).

The average number of tourist days (excluding ships’ 

passengers) in the Caribbean, 174 million, dwarfs the 38.8 

million residents and represents a signifi cant exposure of 

a naive population to CFP. The most common route of 

exposure is through consumption of locally harvested fi sh. 

Currently, the annual total Caribbean fi shery landings exceed 1.6 million metric tons (CRFM, 2008; FAO, 2005, 

2008; WRI, 2007), making a strong argument for focused 

studies on CFP occurrence and on the environmental factors that affect the distribution and abundance of CFPassociated organisms.

As part of its commitment to understand and characterize the diversity, distribution, and abundance of 

organisms throughout the Caribbean, the Smithsonian 

Institution has carried out extensive studies on dinofl agellates over the past 20 years (Faust and Gulledge, 2002). 

Because of this pioneering work, much of the background 

information and expertise needed to characterize the diversity of ciguatera-causing dinofl agellates are already in 

place. During the past fi ve years, NOAA (National Oceanic and Atmospheric Administration) and Smithsonian 

scientists have collaborated to isolate, identify, and genetically characterize the ciguatera-causing dinofl agellates 

FIGURE 2. Scanning electron micrographs of ciguatera-associated dinofl agellates: A, Gambierdiscus; 

B, Coolia; C, Ostreopsis; D, Prorocentrum.

23_Tester_301-312_Lang.indd 303 3_Tester_301-312_Lang.indd 303 9/24/09 10:00/24/09 10:00
304 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of the Caribbean, as well as to develop species-specifi c 

molecular assays for assessing their abundance. As part 

of this work, four new Gambierdiscus species have been 

discovered and are being described (Tester et al., 2008; 

Litaker et al., in press).

We are now in a position to begin systematic studies 

of the incidence of CFP and distribution and abundance 

of CFP-causing dinofl agellates throughout the Caribbean. 

To identify areas of concern from both public health and 

marine resource perspectives, and to focus the effectiveness of environmental sampling, we needed to identify areas where CFP was most common. Consequently, we initiated active surveys of local fi shery managers and public 

health offi cials. By examining the CFP incidences among 

the 24 islands and the 9 mainland countries surrounding 

the Caribbean, additional insights can be gained into factors that govern the spatial and temporal variations in the 

prevalence of CFP.

A second objective of this study was to determine 

how CFP was being monitored and reported throughout 

the Caribbean, where more than 46% of the tourists are 

from the United States (United Nations Statistics Division, 

2004; CTO, 2008; Figure 3) and the average length of 

stay is 8.7 days (United Nations Statistics Division, 2004; 

CTO, 2008; Figure 4). This project represents the fi rst 

steps toward an assessment of community vulnerability by 

the identifi cation of susceptible populations and serves as 

a framework for developing human dimensions research 

as a cross-cutting priority of ecosystem science supporting 

marine resource management (Bauer, 2006).

FIGURE 3. Average percentage of American tourists visiting the Caribbean by country (1996– 2005). Only 

data from Cancun and Cozumel were used for Mexico. On average, 46% of tourists who visited all Caribbean countries came from the United States. On average, not counting visits from passengers on cruise ships, 

tourists spend over 174 million tourist days in this region each year (OAS, 1997; ACS-AEC, 2003; UNSD, 

2004; CIA, 2008; CTO, 2008).

23_Tester_301-312_Lang.indd 304 3_Tester_301-312_Lang.indd 304 9/24/09 10:00/24/09 10:00
NUMBER 38 • 305

Our ultimate goal is a comprehensive assessment of 

the environmental, sociocultural, and economic impacts 

of CFP in the Caribbean and the development of effective detection and monitoring tools to support management decisions and improve inter-island communications 

among public health offi cials, marine resource managers, 

Caribbean residents, and tourists.

METHODS

Based on published cases and self-reporting, it appears that CFP is more prevalent in the eastern Caribbean than the western Caribbean (Stinn et al., 2000; see 

Figure 1B). To assess whether this is the case or whether 

the pattern derives from reporting bias, we used an active method to query public health offi cials and fi sheries 

managers about the occurrence of CFP from 1996 through 

2006 in 24 Caribbean island nations and territories and 

9 mainland countries bordering the Caribbean. Fisheries 

and public health offi cials were contacted separately. One 

or both agencies could be involved in the surveillance of 

and response to CFP, although often within different administrative units. Querying two separate agencies was 

intended to allow corroboration of the data and to measure information-sharing between agencies. The questionnaires used in this study were vetted by a panel of experts 

with experience in designing human health surveys (see 

Acknowledgments).

Initial contact was made with public health and fi sheries department staff persons by telephone. Introductory conversations were conducted in English, Spanish, 

or French, depending on the preference of the offi cial 

FIGURE 4. Average length of stay for all tourists visiting the Caribbean during 1996– 2005, by country. Only 

data from Cancun and Cozumel were used for Mexico. The average length of stay for all tourists was 8.7 

days (OAS, 1997; ACS-AEC, 2003; UNSD, 2004; CIA, 2008; CTO, 2008). ND no data.

23_Tester_301-312_Lang.indd 305 3_Tester_301-312_Lang.indd 305 9/24/09 10:00/24/09 10:00
306 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

contacted. The following preliminary information and 

questions were provided during these telephone calls before sending the survey:

• The focus of the project is to gather information about where 

and how many people are poisoned by eating fi sh contaminated with ciguatera toxin (ciguatoxin) throughout the Caribbean, including in ____________ (name of country). People 

who eat fi sh carrying this toxin can develop ciguatera fi sh 

poisoning, an illness that affects primarily the digestive and 

nervous systems.

• Does your offi ce compile information about fi sh that transmit 

ciguatera or cases of ciguatera fi sh poisoning in ____________

(name of country)?

 (If No) Do you know of another offi ce that does?

 (If Yes) What is the name of that offi ce?

 (If No) Do you know anyone who might be able to help me 

locate an offi ce that compiles information about ciguatera fi sh 

poisoning?

A long-term goal of the research project is to better understand where ciguatera fi sh poisoning occurs, which could improve 

the use of resources to monitor and respond to it. The results of 

our research throughout the Caribbean will be summarized in a 

report, documented in a database, and displayed on maps that 

will be available to you and others interested in the project. We 

will not be collecting names, addresses, or other personal information from people who have ciguatera fi sh poisoning.

• Are you the best person in your offi ce to provide information 

about ciguatera in ____________ (name of country)? 

 (If referred to another person or agency) Do you have any contact information for the person you recommend I speak with?

We are asking for your voluntary assistance with our research.

• Would you be willing to answer a few questions?

 (If Yes) Thank you! I would greatly appreciate being able to 

e-mail you some specifi c questions I have. May I do so?

 (If No) Why not?

Once an appropriate contact was identifi ed, a written copy of the questionnaire was provided in the appropriate language (or languages, as some participants 

received the questionnaire in both Spanish and English 

or French and English). Both questionnaires (the fi sheries department version and the public health department 

version) included the 11 core questions listed in Appendix I, as well as 4 questions that applied to only the fi sheries department (Appendix II) or the public health department (Appendix III). Efforts were made, in designing 

the questionnaire, to allow respondents to qualify how 

confi dent they were of the completeness of the data they 

were providing.

RESULTS AND DISCUSSION

To date, results are preliminary, as not all the questionnaires have been returned. However, some trends 

have begun to emerge, and it is possible to provide a brief 

synopsis of these. One of the most striking results was the 

wide range of concern and knowledge about CFP. Some 

government agencies have simply asserted that CFP cases 

do not occur in their jurisdictions and declined to receive 

or complete the questionnaire. Other agencies acknowledged that a potential problem exists but have been hampered by insuffi cient resources to institute an organized 

monitoring system. Still other governments reported 

making progress toward bringing CFP surveillance programs online, sometimes in response to a recent outbreak 

of CFP cases.

Some countries had a well-developed mandatory 

protocol for reporting CFP, including information on 

the name of the patients, symptoms, and diagnosis. In 

some instances, public health offi cials have a high degree of confi dence that they are fi nding 90% or more 

of the cases, but most public health offi cials who have 

responded to date are less confi dent in their statistics. 

In some countries, when clusters of CFP cases are observed, the health department issues a press release. At 

the same time, the department may do a public service 

announcement for radio and TV about the risk of consuming barracuda.

A wide range of opinions were offered about how 

aware and concerned local populations and fi shers are 

about the risk that eating certain types of locally caught 

fi sh could result in developing CFP. These responses 

ranged from “Not aware” or “Not concerned,” to 

“Somewhat aware” or “Somewhat concerned,” to “Very 

aware” or “Very concerned.” One respondent commented that native-born citizens had a higher level of 

awareness and concern than people who recently moved 

to the region. Perceived levels of risk might depend more 

on being educated about the problem rather than an actual risk of exposure. At least in some regions where CFP 

is well known, most people seem to understand that if 

they feel tingling or prickling on their tongues when they 

are eating fi sh, they should stop eating it to minimize the 

risk of becoming sick.

23_Tester_301-312_Lang.indd 306 3_Tester_301-312_Lang.indd 306 9/24/09 10:00/24/09 10:00
NUMBER 38 • 307

In some countries, the data also suggest a trend toward increasing numbers of CFP cases with time. Public 

health offi cials on a few islands attributed this not to environmental change, but to population growth, in some 

cases as rapid as a doubling of the population in 20 years. 

As the population has grown, so too has the demand for 

fi sh, which could result in an increase in the number of 

people exposed to CFP. It is generally agreed that CFP is 

underreported and that this lack could be attributable to 

a variety of reasons (e.g., because its symptoms resemble 

those of other diseases when the poisoning is mild). This 

apparent increase may also be attributable to increased reporting because of heightened awareness, or it may refl ect 

an actual increase in new cases of CFP.

Several public health departments have compiled and 

reported the months and years when people ate ciguatoxic 

fi sh and were diagnosed with CFP. From these limited data 

it appears that the number of CFP episodes was distributed evenly throughout the year but that the number of 

cases (people diagnosed with CFP) per episode was greater 

in September and October (Figure 5).

Overall, public health and fi sheries offi cials indicated that consumption of contaminated barracuda was 

the most common cause of CFP. Other species frequently 

identifi ed with CFP include jack, grouper, snapper, hogfi sh, and mackerel. Some fi shermen discard barracuda that 

do not “put up a fi ght” when caught, believing that if a 

fi sh does not fi ght, it is sick. However, it should be noted 

that ciguatoxic status cannot be discerned visually; seemingly healthy fi sh can be quite toxic. One positive outcome 

of this research was that some countries provided data indicating geographic locations where ciguatoxic fi sh were 

frequently found. This information will guide future sampling efforts.

CONCLUSIONS

The data currently available from Caribbean countries 

suggest there is wide variability in the amount of attention 

given to CFP. This variability is probably not entirely attributable to how prevalent CFP is in various areas. The 

reasons for this include differences in (1) how signifi cant 

a problem CFP is thought to pose, (2) awareness of the 

risk of CFP, (3) whether central reporting of CFP cases is 

mandatory, and (4) resources available for CFP monitoring and education.

Active surveys, such as the one described in this 

study, can help countries quantify potential risks and 

establish training and monitoring systems for CFP. This 

study also provides unique insights into human dimensions of CFP, including perceptions of how signifi cant the 

risks are in different areas and how frequently health and 

fi sheries departments exchange information concerning 

CFP. The data from this study were also detailed enough, 

in some cases, to suggest specifi c regions in the Caribbean 

where CFP occurrences are elevated or are relatively rare. 

This information will facilitate identifi cation of specifi c 

sampling sites for future investigations of the factors that 

affect the temporal and spatial variability in exposure to 

CFP. The fruitful partnership between the Smithsonian Institution and NOAA continues the Smithsonian’s tradition 

of documenting the diversity of life on earth and NOAA’s 

mission to bring state-of-the-art management tools to the 

marine community.

ACKNOWLEDGMENTS

We thank Drs. Nathalie Valette-Silver, David Johnson, and Michael Dowgiallo and Mr. Joseph Schittone of 

the National Ocean Service (NOS), NOAA, for facilitating this study. Dr. Richard Appledorn, Director of the Caribbean Coral Reef Institute, provided guidance for fi eld 

sampling. Mr. Michael Carpenter, National Museum of 

Natural History (NMNH), kindly provided logistic support. Mr. Scott Whittaker (Head) and Mr. Don Hurlbert 

of the Smithsonian’s NMNH Imaging and Photography 

Department generously gave us technical assistance. We 

FIGURE 5. Ciguatera episodes and cases in the Caribbean by month 

from 1996 to 2007. Episodes indicate multiple cases (usually defi ned 

by zip code) during the same week.

23_Tester_301-312_Lang.indd 307 3_Tester_301-312_Lang.indd 307 9/24/09 10:00/24/09 10:00
308 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

appreciate the guidance from Leonard Young, Public 

Health Scientist, Eastern Research Group; Dr. MaryBeth 

Bauer, NOAA National Centers for Coastal Ocean Science; Dr. Chris Ellis and Ms. Lauren Smith, Human Dimensions Program, NOAA Coastal Services Center; and 

Dr. Janna Shakeroff, Duke University Marine Laboratory, in the development of the questionnaire used in this 

study. We are especially grateful to Dr. Klaus Ruetzler 

and the Caribbean Coral Reef Ecosystem Program and 

the NOS International Program Offi ce for funding. This 

is contribution number 851 of the Caribbean Coral Reef 

Ecosystems Program (CCRE), Smithsonian Institution, 

supported in part by the Hunterdon Oceanographic Research Fund.

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Stinn, J. F., D. P. de Sylva, L. E. Fleming, and E. Hack. 2000. Geographic 

Information Systems and Ciguatera Fish Poisoning in the Tropical 

Western Atlantic Region. Geographic Information Systems in Public Health: Proceedings of the Third National Conference. http://

www.atsdr.cdc.gov/gis/conference98/proceedings/html/stinn.html 

(accessed 17 July 2008).

Tester, P. A. 1994. “Harmful Marine Phytoplankton and Shellfi sh Toxicity: Potential Consequences of Climate Change.” In Disease in Evolution: Global Changes and Emergence of Infectious Diseases, ed. 

M. E. Wilson, R. Levins, and A. Spielman, pp. 65– 70. New York: 

The New York Academy of Sciences.

Tester, P. A., M. A. Faust, M. W. Vandersea, S. R. Kibler, M. Chinain, 

M. Holmes, C. Holland, and R. W. Litaker. 2008. “Gambierdiscus 

toxicus: Does Clonal Type Material Exist?” In 12th International 

Conference on Harmful Algae, ed. Ø. Moestrup, and H. Enevoldson, pp. 269– 271. Paris: IOC of UNESCO.

Tosteson, T. R. 2004. Caribbean Ciguatera: A Changing Paradigm. Revista de Biologia Tropical, 52:109– 113.

United Nations Statistics Division (UNSD). 2004. National Accounts. 

http://unstats.un.org/unsd/nationalaccount/amasample.pdf (accessed 

16 June 2008).

Woods Hole Oceanographic Institute (WHOI). 2008. Maps: Ciguatera 

Fish Poisoning. Harmful Algae, http://www.whoi.edu/redtide/page

.do?pid18103&tid542&cid47588&c3 (accessed 17 July 

2008).

World Resources Institute (WRI). 2007. Coastal and Marine Ecosystems: 

Country Profi les. EarthTrends: The Environmental Information Portal, http://earthtrends.wri.org/country_profi les/index.php?theme1 

(accessed 16 July 2008).

Yasumoto, T., I. Nakajima, Y. Oshima, and R. Bagnis. 1977. A New 

Toxic Dinofl agellate Found in Association with Ciguatera. In Toxic 

Dinofl agellate Blooms, ed. D. L. Taylor, and H. H. Seliger, pp. 65– 70. 

New York: Elsevier.

23_Tester_301-312_Lang.indd 308 3_Tester_301-312_Lang.indd 308 9/24/09 10:00/24/09 10:00
NUMBER 38 • 309

APPENDIX 1

The following core questions were used in both fi sheries and health department questionnaires:

1. a. What information does your offi ce compile about cases of ciguatera fi sh poisoning (for example, number of people 

diagnosed, locations of people diagnosed, locations where fi sh were caught, etc.)?

 b. If your offi ce does not compile such information, is there another governmental offi ce or agency that does, and 

what is its name? ___ Yes ___ No ___ I’m not sure

 Name of other offi ce or agency:

 c. If yes, what types of information do you think that offi ce might have?

 d. Please provide contact information for someone in that offi ce, if possible (contact name, e-mail address, phone 

number, and fax number).

2. If you receive reports of ciguatera fi sh poisoning, from whom do the reports come? (Please check ALL that apply.)

___ Doctors ___ Clinics and Hospitals ___ Fisheries Department [for the health department survey] ___ Fishermen 

___ Health Department [for the fi sheries department survey]/Other Health Agencies [for the health department 

survey] (please specify jurisdiction represented and contact person, if available) ___ Restaurants ___ Hotels 

___ Individual Citizens ___ Other Sources (please list)

3. Please indicate the total number of reported ciguatera fi sh poisoning cases per calendar year from January 1, 1996, 

through December 31, 2006.

 [A table containing one line for each year, a column for the number of cases reported, and a column for any comments was provided here.]

4. To the extent available, please provide the following information for each episode of ciguatera fi sh poisoning. (For 

this study, an episode is defi ned as an occasion when one or more people were poisoned on the same day by one or 

multiple fi sh of the same variety, caught in the same place.)

 a. Number of people poisoned

 b. Date of episode (list season and year if date or month is not known)

 c. Date of diagnosis, if date of poisoning (B) is not known

 d. City where fi sh with ciguatera was eaten

 e. Home city of patient(s), if city where fi sh was eaten (D) is not known

 f. Type of fi sh with ciguatera (common name or scientifi c name)

 g. Describe where fi sh with ciguatera was caught, in as much detail as possible (with latitudes and longitudes, if 

available)

5. At this time, is reporting any information about fi sh transmitting ciguatera or cases of ciguatera fi sh poisoning voluntary or mandatory? ___ Voluntary ___ Mandatory ___ I’m not sure

 If reporting is mandatory:

 a. What information must be reported?

 b. When did it become mandatory?

 c. What agency receives these reports initially?

6. a. What percentage of ciguatera fi sh poisoning cases diagnosed each year in ____________ (name of country or territory) do you think are reported to your offi ce?

 b. How confi dent are you of this estimate? ___ Very confi dent ___ Somewhat confi dent ___ Slightly confi dent 

___ Not at all confi dent ___ I’m not sure

continued

23_Tester_301-312_Lang.indd 309 3_Tester_301-312_Lang.indd 309 9/24/09 10:00/24/09 10:00
310 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Appendix 1 continued

 7. a. To your knowledge, has your agency or another governmental agency issued any advisory warnings related 

to consuming fi sh that might carry ciguatera, such as barracuda or large reef fi sh?

___ Yes ___ No ___ I’m not sure

 b. If yes, please indicate which offi ce issued the advisory.

 c. If applicable, please include or attach the wording of each such advisory and indicate when it was issued. Attach 

additional pages, if necessary.

 d. If your agency has not issued an advisory, who or what agency would be most appropriate to consult for 

information on advisories? (Please list the agency name and the following, if available: a contact name, e-mail 

address, phone number, and fax number.)

 8. How often do your department and fi sheries department offi cials [for the health department survey]/health department offi cials [for the fi sheries department survey] exchange information about episodes of ciguatera fi sh poisoning? 

___ As cases occur ___ Every month ___ Every 3 months ___ Every 6 months ___ Every year ___ Never 

___ Other (please specify):

 9. How aware do you think local citizens are of the risk that eating certain types of fi sh could cause them to develop 

ciguatera fi sh poisoning? ___ Very aware ___ Somewhat aware ___ Not very aware ___ Not aware 

___ I’m not sure

10. To what extent do you think local citizens are concerned about ciguatera fi sh poisoning?

__ Very concerned __ Somewhat concerned __ Slightly concerned __ Not concerned __ I’m not sure

11. Please provide your contact information for future reference. Thanks again for your assistance!

 Government represented:

 Agency and offi ce:

 Name and title of person completing questionnaire:

 Telephone number, with city code:

 Fax number, with city code:

 e-mail address:

 Date information provided:

 Would you like to receive notifi cation of the results of the study? ___ Yes ___ No

APPENDIX 2

The following questions were directed only to offi cials representing fi sheries departments:

1. a. Is information usually communicated to you about where fi sh suspected of carrying ciguatera were caught?

___ Yes ___ No

 b. Is information usually communicated to you about what types of fi sh have carried ciguatera?

___ Yes ___ No

 c. If yes to either (a) or (b), and if you do not have information in the format provided in Question 4, please provide 

any information you have about the types of fi sh, and the locations involved in episodes of ciguatera fi sh poisoning 

reported to you, for the years 1996 to 2006. [A table was provided with the following headings: Year, Common or 

scientifi c names of fi sh reported, Locations of fi sh reported (latitudes/longitudes, if possible, or place names, in as 

much detail as possible).]

23_Tester_301-312_Lang.indd 310 3_Tester_301-312_Lang.indd 310 9/24/09 10:00/24/09 10:00
NUMBER 38 • 311

2. Please provide any information you have on economic losses resulting from ciguatera fi sh poisoning, either quantitative or qualitative (for example, if fi shing had ceased at a particular reef because of the suspected presence of ciguatera toxins, there might be an annual loss of $10,000 to the fi shing industry). Please include the year(s) your data 

refl ects and note your data sources.

3. To what extent do you think fi shermen are aware of the risk of catching certain types of fi sh that could cause people 

to develop ciguatera fi sh poisoning? ___ Very aware ___ Somewhat aware ___ Not very aware 

___ Not aware ___ I’m not sure

4. To what extent do you think fi shermen are concerned about catching certain types of fi sh that could cause ciguatera 

fi sh poisoning? ___ Very concerned ___ Somewhat concerned ___ Slightly concerned ___ Not concerned 

___ I’m not sure

APPENDIX 3

The following questions were directed only to offi cials representing health departments:

1. Is any information available to you on the cost per year to your government of monitoring or documenting the incidence of ciguatera fi sh poisoning? ___ Yes ___No

If yes, please provide the information below and note your data sources.

2. Is any information available to you on the cost per year of medical treatments in ____________ (name of country or 

territory) for ciguatera fi sh poisoning, as an average per person affected by ciguatera fi sh poisoning and/or annually 

for ____________ (name of country or territory)? ___ Yes ___No

If yes, please provide it below, specify whether it refl ects a total or an average per person, and note your data sources.

3. Is any information available to you related to the number of days people have been unable to work due to ciguatera 

fi sh poisoning per year in ____________ (name of country or territory)? ___ Yes ___No

If yes, please provide it below, specify whether it refl ects a total or an average per person, and note your data sources.

4. Would you rank ciguatera fi sh poisoning as one of the 10 most severe food-borne illnesses in ____________ (name of 

country or territory)? ___ Yes ___No ___ I’m not sure

If yes, would it rank in the top ___ 1 to 5 or ___ 6 to 10?

23_Tester_301-312_Lang.indd 311 3_Tester_301-312_Lang.indd 311 9/24/09 10:00/24/09 10:00
23_Tester_301-312_Lang.indd 312 3_Tester_301-312_Lang.indd 312 9/24/09 10:00

/24/09 10:00
History of Reef Coral Assemblages 

on the Rhomboid Shoals of Belize

Richard B. Aronson, Ian G. Macintyre, 

Anke M. Moesinger, William F. Precht, 

and Michael R. Dardeau

ABSTRACT. Coral assemblages of the rhomboid shoals of the Belizean barrier reef have 

undergone dramatic, historically unprecedented changes over the past several decades. 

Before the late 1980s, the fl anks of the shoals exhibited a distinct biological zonation, 

with branching Porites spp. dominant in a shallow zone (0– 3 m water depth); the staghorn coral Acropora cervicornis dominant in an intermediate zone (3– 15 m depth); and 

large, plating agariciids and the lettuce coral Agaricia tenuifolia dominant in a deep zone 

(15– 30 m depth). Acropora cervicornis died off catastrophically from white-band disease 

after 1986 and was replaced by Agaricia tenuifolia in the intermediate zone. Push-cores 

extracted from intermediate depths in previous studies showed that Acropora cervicornis

was the dominant space occupant and primary framework builder for millennia before 

the phase shift to Agaricia tenuifolia. Cores extracted from the shallow zone showed 

that Acropora cervicornis dominated until several centuries ago, when the tops of the 

reefs reached approximately 2 m water depth and branching Porites spp. replaced it. 

In contrast, three cores extracted from the deep zone in the present study showed that 

for millennia the subsurface coral assemblage, like the assemblage on the modern deepreef surface, was dominated by large, plating agariciids and Agaricia tenuifolia. Because 

white-band disease only affects acroporid corals, the unprecedented phase shift that followed the outbreak was confi ned to the intermediate zone. High sea temperatures in 

the summer of 1998 caused coral bleaching and mortality, especially of agariciids in the 

intermediate and deep zones, but to date this event has not left a geologic signature in 

the Holocene record.

INTRODUCTION

Coral reef ecosystems are collapsing at an accelerating rate, jeopardizing 

the ecosystem services that they provide (Hughes et al., 2003; Wilkinson, 2006; 

Carpenter et al., 2008). The common presumption that mortality of hard corals 

(Scleractinia and Milleporina) commenced earlier and was more severe in the 

Caribbean and eastern Pacifi c than in other tropical and subtropical regions 

may not be correct (Bruno and Selig, 2007). Nevertheless, the causes and consequences are best understood for the Caribbean and eastern Pacifi c.

Coral mortality has been elevated in the Caribbean since the late 1970s 

(Gardner et al., 2003). The impacts of global change, including increasing sea 

temperatures, increasing cyclone intensity, and declining aragonite saturation 

Richard B. Aronson, Department of Biological 

Sciences, Florida Institute of Technology, 150 

West University Boulevard, Melbourne, Florida 

32901, USA. Ian G. Macintyre, Department 

of Paleobiology, National Museum of Natural 

History, Smithsonian Institution, P.O. Box 37012, 

MRC 125, Washington, D.C. 20013-7012, USA. 

Anke M. Moesinger and Michael R. Dardeau, 

Dauphin Island Sea Lab, 101 Bienville Boulevard, 

Dauphin Island, Alabama 36528, USA. William 

F. Precht, Florida Keys National Marine Sanctuary, National Oceanic and Atmospheric Administration, 95230 Overseas Highway, Key Largo, 

Florida 33037, USA. Corresponding author: R. 

Aronson (raronson@fi t.edu). Manuscript received 

25 July 2008; accepted 20 April 2009.

24_Aronson_313-322_Lang.indd 313 4_Aronson_313-322_Lang.indd 313 9/24/09 10:23/24/09 10:23
314 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

state (Kleypas et al., 1999; Buddemeier et al., 2004; HoeghGuldberg et al., 2007), are sources of grave concern, but 

coral assemblages throughout the Caribbean have already 

been severely affected by outbreaks of infectious marine 

diseases (Aronson and Precht, 2001b; Sutherland et al., 

2004; Weil et al., 2006). In particular, white-band disease 

(WBD), a bacterial infection that is specifi c to acroporid 

corals, decimated Acropora palmata (elkhorn coral) and 

Acropora cervicornis (staghorn coral) on reefs throughout 

the western Atlantic from the late 1970s through the early 

1990s (Aronson and Precht, 2001a, 2001b). Acroporid 

populations have been reduced so drastically that the two 

species are now listed as threatened under the U.S. Endangered Species Act (Hogarth, 2006) and are classifi ed as 

critically endangered according to the Red List criteria of 

IUCN, the International Union for Conservation of Nature 

(Carpenter et al., 2008). Hurricanes, temperature-induced 

bleaching, declining herbivory, nutrient loading, and predation by corallivores have had additional, interacting impacts 

on coral mortality and the scope for population recovery 

(Aronson and Precht, 2006). Emergent diseases, for example, could be related to or exacerbated by global warming 

and nutrient loading (Harvell et al., 2002; Rosenberg and 

Ben-Haim, 2002; Bruno et al., 2003, 2007; Sutherland et 

al., 2004; Kline et al., 2006). Recent changes on Caribbean reefs were novel events in at least the last 3,000 to 

4,000 years (Aronson et al., 2002a, 2004, 2005a; Wapnick et al., 2004; Hubbard et al., 2005; Greer et al., 2009), 

and Pandolfi et al. (2006) drew a similar conclusion about 

Holocene reef dynamics in Papua New Guinea.

Aronson and Precht (2001a, 2001b, 2006; Precht 

and Aronson, 2006) argued that because WBD was the 

primary cause of recent mortality of Acropora palmata

and Acropora cervicornis in the Caribbean, and because 

the two species were the dominant space occupants at 

depth ranges of 0– 5 and 5– 25 m, WBD was clearly one 

of the most important causes of recent coral mortality 

in the region. Mass mortality of the acroporids was followed by two types of phase shifts. Where coral mortality 

exceeded the capacity of herbivores to respond to algal 

growth on the space that had been opened, macroalgae 

rose to dominance (Ostrander et al., 2000; Aronson and 

Precht, 2001a, 2006; Williams et al., 2001; Rogers and 

Miller, 2006). Where herbivory was suffi cient to control 

the algae, brooding, self-fertilizing corals, primarily of the 

families Agariciidae and Poritidae, replaced the acroporids (Aronson and Precht, 1997; Greenstein et al., 1998; 

Bythell et al., 2000; Knowlton, 2001; Green et al., 2008). 

The shift to macroalgal dominance has not been as widespread as previously supposed (Bruno et al., 2009).

An important exception to the overall Caribbean 

trend is the Flower Garden Banks (FGB) in the northwestern Gulf of Mexico, where coral cover has held steady at 

40%– 60% at depths of 17– 26 m from the 1970s to the 

present. Aronson et al. (2005c) explained the persistently 

high coverage of living corals based on the historical absence of the cold-sensitive acroporids. Coral mortality has 

been far lower at the FGB than elsewhere in the Western 

Atlantic region because no acroporids were present to die 

of WBD. The appearance of Acropora palmata at the FGB 

in the past few years could be related to global warming 

(Precht and Aronson, 2004).

An ecosystem-level version of this biogeographic argument is that reef zones historically not dominated by 

acroporids should not have undergone phase shifts at the 

same time as the adjacent Acropora-dominated zones. In 

this study we examined the millennial-scale history of the 

coral assemblage near the bases of the rhomboid shoals 

in the central shelf lagoon of the Belizean barrier reef. We 

cored the deep-reef framework of two of the shoals, reconstructed the history of the coral assemblage during the late 

Holocene, and completed a model of reef development 

over the last several thousand years from present sea level 

down to the bases of the shoals. Although Acropora cervicornis dominated at intermediate depths for millennia until the late 1980s, acroporids apparently did not dominate 

the deep zone for at least the past 1,500 to 2,000 years, 

providing an opportunity to test our hypothesis of the occurrence and timing of phase shifts.

ZONATION AND PALEOECOLOGY 

OF THE RHOMBOID SHOALS

The rhomboid shoals are uncemented, atoll-like reefs 

lying within the central shelf lagoon of the Belizean barrier reef. The sloping outer fl anks of the rhomboid shoals 

displayed a clear pattern of coral zonation from at least as 

far back as the early 1970s, when the fi rst rigorous ecological observations were made, until 1986 (Westphall, 1986; 

Aronson and Precht, 1997; Aronson et al., 1998). A shallow zone (0– 3 m water depth) was dominated by branching 

Porites spp., primarily Porites furcata and Porites divaricata, 

mixed with the hydrocoral Millepora alcicornis. Acropora 

cervicornis dominated an intermediate-depth zone (3– 15 m 

depth), with the blade-forming lettuce coral Agaricia tenuifolia as the subdominant. (Agaricia tenuifolia recently has 

been revised to Undaria tenuifolia; however, we will retain 

Agaricia as the generic designation in this paper.) A deep 

zone, extending from 15 m to the lagoon fl oor at 22– 30 m 

24_Aronson_313-322_Lang.indd 314 4_Aronson_313-322_Lang.indd 314 9/24/09 10:23/24/09 10:23
NUMBER 38 • 315

depth, was dominated by large colonies of plating agariciids (Agaricia lamarcki, Agaricia grahamae, Agaricia undata, and Leptoseris cucullata) and Agaricia tenuifolia, 

with scattered massive corals. The total hard-coral fauna 

consisted of approximately 25 species, most of which were 

rare (Aronson and Precht, 1997).

In the decade following 1986, the dominant coral at 

intermediate depths, Acropora cervicornis, succumbed 

to WBD and was replaced by Agaricia tenuifolia. This 

phase shift was mediated by an abundant, herbivorous 

sea urchin, Echinometra viridis, which limited macroalgal 

growth and promoted the recruitment and opportunistic 

growth of agariciids on the dead skeletons of Acropora 

cervicornis (Aronson and Precht, 1997). Agaricia tenuifolia was the fastest growing of the agariciids that recruited 

and, therefore, it became the new dominant.

To determine whether the transition was historically 

unique, Aronson et al. (2002a) extracted push-cores at 

5– 10 m water depth from stations distributed over a 375 

km2 area of the lagoon (Figure 1). Analysis and radiocarbon dating of the cores revealed continuous dominance 

of Acropora cervicornis and upward growth of the reef 

for at least 3,000 years before the late 1980s. Spines of 

Echinometra viridis were present throughout the cores, 

indicating continuously high herbivory. During the past 

three millennia Agaricia tenuifolia grew in small patches 

(of the order of square meters), which appeared as subsurface layers of skeletal plates that were isolated in time and 

space (Aronson et al., 2002a). The recent, area-wide phase 

shift, in contrast, was preserved at the tops of the cores as 

a layer of Agaricia tenuifolia plates overlying a thin layer 

of taphonomically degraded Acropora cervicornis. This 

signature persisted in the Holocene record despite subsequent hurricanes and bleaching events (Aronson et al., 

2000, 2002b, 2005b). Coring in a lagoonal habitat at Discovery Bay, Jamaica, showed that a more common phase 

shift, in which Acropora cervicornis was killed by WBD 

and replaced by macroalgae as the result of limited herbivory, was similarly unprecedented on a millennial time 

scale (Wapnick et al., 2004).

Cores extracted from the rims and ridges of the shoals 

near the present sea level revealed that Acropora cervicornis dominated the shallowest portions of these reefs for at 

least several millennia until approximately 500 years ago 

(Westphall, 1986; Aronson et al., 1998, 2005a; Macintyre 

et al., 2000). At that time the reef tops grew to within 

2 m of sea level, and branching Porites spp. replaced 

Acropora cervicornis as the dominant coral taxon. 

Since then, the Porites-dominated assemblage has kept 

up with the slowly rising sea level, forming the shallow 

zone. The shallowing-upward, successional sequence in 

the shallow zone contrasts with the post-1986, diseaseinduced replacement of Acropora cervicornis by Agaricia 

tenuifolia at intermediate depths.

As part of the worldwide reef-bleaching event of 

1997– 1998 (Wilkinson, 2000), which was related to the 

El Niño– Southern Oscillation and probably augmented by 

global warming, a high-temperature anomaly in the summer of 1998 bleached almost all corals in the intermediate and deep zones of the rhomboid shoals (Aronson et 

al., 2000, 2002b). Agaricia tenuifolia is particularly prone 

to temperature-induced bleaching (Robbart et al., 2004), 

and populations of this coral at intermediate and deeper 

depths experienced nearly complete mortality. Mortality 

rates were lower, but still very high, for plating agariciids. 

The dead coral skeletons were colonized primarily by thin 

algal turfs and the sponge Chondrilla aff. nucula (Aronson et al., 2002b), which Rützler et al. (2007) have now 

described as Chondrilla caribensis. Agariciid populations 

had not recovered as of December 2008 (W. F. Precht, personal observation). Branching Porites corals in the shallow zone were less affected by the 1998 thermal anomaly. 

These corals did not bleach to the extent the agariciids did, 

and as a result they did not experience large-scale mortality 

(W. F. Precht and R. B. Aronson, personal observation).

MATERIALS AND METHODS

In April 2008, we extracted six push-cores in water 

depths of 14.0– 19.5 m from the reefs at Channel and Elbow Cays, in the center of our 375 km2 study area (see 

Figure 1). Push-coring requires less equipment than mechanical techniques such as rotary drilling and percussion vibracoring. By eliminating the need for tripods and 

other heavy equipment, push-coring offers easier logistics, 

greater mobility, and a much lower cost per core. Penetration and recovery of cores dominated by branching and 

foliose corals have been excellent in the shallow and intermediate-depth zones of the rhomboid shoals, as well 

as on uncemented lagoonal reefs in Panama and Jamaica 

(Dardeau et al., 2000; Aronson et al., 2004; Wapnick et 

al., 2004). Rotary drilling is not an option because branching and foliose corals generally are broken up and fl ushed 

out of the core barrel. As a result, recoveries are poor in 

lagoonal and fore-reef environments dominated by fragile 

corals (Glynn and Macintyre, 1977; Halley et al., 1977; 

Macintyre et al., 1981; Shinn et al., 1982).

Dardeau et al. (2000) described the push-coring 

method in detail. Briefl y, aluminum tubes, 5 m long and 

24_Aronson_313-322_Lang.indd 315 4_Aronson_313-322_Lang.indd 315 9/24/09 10:23/24/09 10:23
316 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 1. Map of the central shelf lagoon of the Belizean barrier reef, showing the rhomboid shoals and the locations of 

the two coring stations. Three of the six cores extracted were analyzed for this study, as noted on the map. (Modifi ed from 

Aronson et al., 2002a.)

24_Aronson_313-322_Lang.indd 316 4_Aronson_313-322_Lang.indd 316 9/24/09 10:23/24/09 10:23
NUMBER 38 • 317

7.6 cm (3 in.) in diameter with teeth cut into their leading 

ends, were driven by hand into the uncemented reef framework. The tubes were rotated in using adjustable core slips 

with handles and tapped with a sliding hammer-weight, 

sleeved over the top, to aid in penetration. The tubes cut 

through, penetrated, and captured the loose framework 

of branching and foliose coral skeletons, and they cored 

through most massive coral heads as well. Although head 

corals are rare in the subsurface at shallow and intermediate depths, they are more common in the deep zone. The 

cores were sealed with plastic caps and electrical tape, 

extracted from the reef, and transported to the laboratory 

for analysis.

Estimates of recovery were obtained at intervals during the coring process by dropping a weighted fi berglass 

measuring tape down the open core barrel. In previous 

studies these measurements, along with simultaneous 

measurements of penetration, confi rmed that material 

entered the tubes continuously as they were forced into 

the reef. In some cases in the present study the tube cored 

through a massive coral and was plugged by it, preventing 

further recovery as the tube was forced deeper into the 

uncemented framework. We used the penetration depth 

at the point at which the tube was plugged to calculate 

percent recovery. Comparison of fi nal recoveries measured 

before extraction with recoveries measured after extrusion 

in the laboratory showed that little or no material was 

lost from the bottoms of the tubes during extraction. Of 

course no material was lost from cores that were plugged 

at their bases by massive corals.

There were no indications of signifi cant voids in the 

reef framework. In no case did the tube suddenly drop 

vertically while we were driving it into the reef. We also 

saw no reversals in the in situ estimates of recovery, which 

would have indicated episodic compaction during coring.

Three of the extruded cores were analyzed at intervals of 5 cm. The constituents of each interval retained 

on a 5 mm sieve were cleaned of matrix, sorted to species, dried to a constant mass, and weighed to the nearest 

milligram. In earlier studies, we showed from regression 

analysis that, for the coral constituents, log(mass) was a 

strong predictor of log(volume), as measured by water 

displacement.

In the manner described previously by Wapnick et al. 

(2004), we assessed the degree of taphonomic degradation 

of the Acropora cervicornis material— encrustation, surfi cial erosion, and internal boring— using a modifi ed version of the rank scales of Greenstein and Moffat (1996). 

The average taphonomic condition of each coral fragment 

was rated as good, intermediate, or poor. The good rating 

was applied to fresh-looking pieces that had little or no 

encrustation, retained essentially all their surface sculpture, and showed little to no evidence of internal boring. 

Poor fragments were those with extensive encrustation, 

surfi cial erosion, and/or boring; degradation was extensive 

enough that the structure of the corallites was completely 

obscured. Fragments were rated as intermediate if their 

condition, averaged over the three categories, fell between 

good and poor. A coral taxon, or a taxon in a particular 

taphonomic condition, was considered dominant in a 5 

cm interval if its mass exceeded the mass of each of the 

other taxa/conditions in that interval.

A coral sample from the bottom of each core was radiocarbon dated by Beta Analytic, Inc. (Miami, Florida), 

using standard techniques. Measured dates were corrected 

for isotopic fractionation to generate conventional dates, 

which are expressed as radiocarbon years before 1950 

(14C year). Conventional dates were calibrated to calendar 

years before 1950 (CalBP).

RESULTS

The cores captured the framework of loose coral skeletons surrounded by a light gray watery matrix of sandy 

mud. The matrix was almost entirely carbonate, with only 

a trace of noncarbonate material. It was less compact 

than the matrix in cores collected from the shallow and 

intermediate zones (Aronson et al., 1998; Macintyre et al., 

2000; Aronson et al., 2002a). X-ray diffraction analysis 

of sediment samples revealed a notable lack of high magnesium calcite in the sand and silt fractions. The majority 

of high magnesium calcite was found in the clay fraction, 

corroborating our earlier conclusion of active precipitation of micritic high magnesium calcite without signifi cant 

cementation (Macintyre and Aronson, 2006). Spines of 

Echinometra viridis in the matrix indicated that those herbivores were present during the time interval represented 

by the cores.

Three of the six cores we collected provided penetrations, recoveries, and bottom dates suffi cient to analyze 

temporal trends in the coral assemblage of the deep zone 

(Table 1). Cores BZ08-3 and BZ08-5 from Channel Cay 

were both plugged by heads of Porites astreoides at penetration depths of 2– 3 m. Core BZ08-6 from Elbow Cays 

penetrated nearly 3.5 m. Bottom samples consisting of 

Porites astreoides from the bases of cores BZ08-3 and 

BZ08-5, and plating Agaricia from the base of BZ08-6, 

were radiocarbon dated. The remaining three cores yielded 

recoveries of 65 cm or less and were not analyzed.

24_Aronson_313-322_Lang.indd 317 4_Aronson_313-322_Lang.indd 317 9/24/09 10:23/24/09 10:23
318 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

The mean recovery for the three cores analyzed was 

33.0% of penetration depth (1.53 SD). This fi gure is 

slightly lower than the mean of 35.9% obtained for cores 

from intermediate depths on the rhomboid shoals and considerably lower than the mean of 62.3% for cores from 

intermediate depths in Bahía Almirante, a coastal lagoon 

in Panama (Dardeau et al., 2000). The low recoveries in 

the present study probably refl ect the open reef framework 

of the rhomboid shoals (compared to Bahía Almirante), 

combined with the low sediment content of the matrix in 

the deep zone (compared to intermediate depths on the 

rhomboid shoals).

All three cores were dominated by agariciid corals (Figure 2). These corals were primarily large, plating 

forms, which characterized the living community until 

1998 and that now characterize the modern, postbleaching death assemblage in the deep zone. Agaricia tenuifolia was more common near the tops of cores BZ08-5 and 

BZ08-6 than lower in those cores. The agariciids were in 

mixed taphonomic condition, with most intervals containing both intermediate and poor material. The skeletons 

from the top 20 cm of the cores were in neither better nor 

worse condition than those further down.

Slope angles in the vicinity of the coring sites, measured with an inclinometer (Aronson et al., 2002a), were 

36°– 39°. Those slopes were less steep than the critical angle of 45°, above which Agaricia tenuifolia skeletons are 

transported downslope (Aronson et al., 2002a). The critical angle of 45° probably applies to the dead, fragmented 

skeletons of plating agariciids as well.

Core BZ08-3 contained a layer of Acropora cervicornis branch fragments in poor taphonomic condition. This 

layer could have been the result of downward transport 

from intermediate depths. On the other hand, Acropora 

cervicornis is less sensitive to slope angle than Agaricia 

tenuifolia (Aronson et al., 2002b), so an autochthonous 

layer cannot be ruled out. Other coral taxa, including 

branching Porites spp. and Porites astreoides, Montastraea annularis species complex, Colpophyllia natans, 

Madracis auretenra (formerly Madracis mirabilis; Locke 

TABLE 1. Summary statistics for the three cores.

Basal radiocarbon dates a

 Water Percent Conventional date Calibrated date

Core depth (m) Site Penetration (cm) Recovery (cm) recovery (14C year SE) b (CalBP) c

BZ08-3 14.5 Channel 256 81 31.6% 2,730 50 2,420 (1,860–1,560)

BZ08-5 16.2 Channel 216 78 36.1% 2,130 60 1,710 (2,650–2,320)

BZ08-6 15.3 Elbow 347 109 31.4% 1,290 60 840 (940–700)

a Radiocarbon dates are of coral samples from the bases of the cores.

b Conventional dates are measured dates corrected for isotopic fractionation, expressed as radiocarbon years before 1950 (14C year) and accompanied by standard errors (SE). c Calibrated dates (CalBP) are expressed as calendar years before 1950, with 95% confi dence intervals in parentheses.

FIGURE 2. Schematic diagrams of the three extruded cores. The 

lengths of the cores depart slightly from recoveries estimated in the 

fi eld (Table 1). Gray shading indicates a matrix of watery, sandy 

mud; Ag.  Agaricia; Ac.  Acropora; P.  Porites.

24_Aronson_313-322_Lang.indd 318 4_Aronson_313-322_Lang.indd 318 9/24/09 10:23/24/09 10:23
NUMBER 38 • 319

et al., 2007), and Stephanocoenia intersepta, were rare in 

the cores. None of the cores recorded millennial-scale intervals of actively accreting Acropora cervicornis framework, which were represented in the intermediate-zone 

cores by thick accumulations of Acropora cervicornis in 

good taphonomic condition.

DISCUSSION

Shinn et al. (1979; see also Westphall, 1986) extracted 

cores from the fl anks of the Channel Cay shoal, including 

one from the base of the reef near our coring station (see 

Figure 1). Their general statement, that the cores were 

dominated by Acropora cervicornis with agariciids as the 

subdominants, did not draw distinctions between cores 

extracted from the different zones. We found that agariciids were the dominant framework constituents in the 

deep zone.

Core BZ08-3, which contained a layer of taphonomically degraded Acropora cervicornis underlying a thick 

upper most layer of agariciids, could represent a deepeningupward sequence. This scenario seems unlikely, however, 

considering that sea level has risen only approximately 

2 m during the past 3,000 years (Toscano and Macintyre, 2003). Furthermore, the other two cores showed 

no such Acropora cervicornis-dominated layer. Regardless, none of the three cores suggests a recent transition 

from millennia of fast-growing and rapidly accumulating Acropora cervicornis framework to dominance by 

agariciid corals, as was observed in the cores from intermediate depths. The layer of Acropora cervicornis in 

BZ08-3 is more likely derived from material that was 

transported downslope, forming debris fans at the bases 

of the shoals.

Aronson et al. (2005a) compared late Holocene reef 

development between the rhomboid shoals and the uncemented reefs of Bahía Almirante in Panama. The shallow and intermediate zones had been cored extensively in 

both locations, providing an accurate picture of stasis and 

change in the dominant coral taxa. In both cases, however, 

the deep zones were poorly characterized. The dearth of 

push-cores from the bases of the reefs has been primarily 

a consequence of the greater densities of core-occluding 

massive corals in the subsurface, compared to the subsurface of the shallow and intermediate zones.

The cores analyzed in this study allow us to present 

a more comprehensive model of the history of the coral 

assemblages of the rhomboid shoals (Figure 3). In the 

shallow zone, catch-up dynamics gave way to keep-up 

dynamics: the Acropora cervicornis that had dominated 

for millennia during the catch-up phase was replaced centuries ago by branching Porites spp. during the keep-up 

phase. Acropora cervicornis was also dominant for millennia at intermediate depths, but in the late 1980s it 

was nearly extirpated by white-band disease and then replaced by Agaricia tenuifolia. The deep zone, in contrast, 

appears to have been dominated by agariciids for at least 

1,500 to 2,000 years. No recent transitions were evident 

in the deep zone, a result consistent with the hypothesis 

that such shifts were predicated on the prior dominance 

and subsequent mortality of acroporids.

Thus, only the intermediate zone was affected when 

Acropora cervicornis died off regionally in the late 1980s 

to the early 1990s. The subsequent bleaching event in 

1998 killed most of the agariciids on the rhomboid shoals. 

Cores extracted from the intermediate zone in 2004 did 

not display a taphonomic signature of that mass mortality 

event, which would have appeared as a discrete, uppermost layer of taphonomically degraded agariciid skeletons 

(Aronson et al., 2005b). Similarly, because of the mixed 

taphonomic character of the subfossil agariciid material 

in the deep zone, the expected signature of the 1998 event 

had not been observed in the Holocene record of that zone 

as of April 2008.

FIGURE 3. Model of reef development on the rhomboid shoals of 

Belize over the last several thousand years. Gray shading indicates 

that the coral assemblages at intermediate water depths experienced 

a recent transition. Black fi ll represents earlier Holocene and antecedent Pleistocene reef framework at depths not penetrated by the 

cores. Horizontally oriented, subsurface ellipses indicate spatially 

isolated layers of Agaricia tenuifolia and taphonomically degraded 

Acropora cervicornis. (Modifi ed from Aronson et al., 2005a.)

24_Aronson_313-322_Lang.indd 319 4_Aronson_313-322_Lang.indd 319 9/24/09 10:23/24/09 10:23
320 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

ACKNOWLEDGMENTS

We thank M. E. Parrish for assistance with the fi eldwork and R. M. Moody and T. J. T. Murdoch for drafting the illustrations. Fieldwork was supported by a grant 

from the Smithsonian Institution’s Caribbean Coral Reef 

Ecosystems (CCRE) program, and laboratory analysis 

was funded by the Dauphin Island Sea Lab (DISL). K. 

Rützler and M. Carpenter of the CCRE facilitated our 

fi eldwork, which was based at the Smithsonian’s Carrie Bow Cay research station and carried out under a 

research permit from the Belize Department of Fisheries. This is contribution number 833 of the Caribbean 

Coral Reef Ecosystems Program (CCRE), Smithsonian 

Institution, supported in part by the Hunterdon Oceanographic Research Fund; DISL contribution number 393; 

and contribution number 8 from the Institute for Adaptation to Global Climate Change at the Florida Institute 

of Technology.

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/24/09 10:23
Climate and Hydrological Factors 

Affecting Variation in Chlorophyll 

Concentration and Water Clarity 

in the Bahia Almirante, Panama

Rachel Collin, Luis D’Croz, Plinio Gondola, 

and Juan B. Del Rosario

ABSTRACT. Water clarity and productivity are fundamentally important for the distribution of tropical marine organisms. In the Caribbean, changes in nutrient loading 

that result from rapid development are thought to have caused increased planktonic productivity, reduced water clarity, and reduced reef and seagrass health. Here we analyze 

chlorophyll a concentration and water clarity from eight years of environmental monitoring in Bocas del Toro, Panama. Chlorophyll a concentrations did not vary signifi cantly 

among the six sampled sites and showed no signifi cant temporal changes, despite the 

recent rapid development in the region, accompanied by scant wastewater treatment. In 

contrast, water clarity increased signifi cantly during the study period. Because chlorophyll a does not vary closely with water clarity, Secchi depths are likely to refl ect changes 

in suspended particulate matter rather than in phytoplankton biomass. Secchi depths 

decreased with rainfall and wind speed but increased with solar radiation, supporting the 

idea that clarity was not tightly linked to phytoplankton biomass. The decrease in annual 

rainfall, but not wind speed, over the past eight years suggests that the long-term trend in 

Secchi readings is the result of changes in rainfall patterns.

INTRODUCTION

Water clarity and productivity are fundamentally important to the distribution of tropical marine organisms, especially corals. Ocean primary productivity 

is also important for global geochemistry and carbon sequestration (Falkowski et 

al., 1998). Global warming and increase in atmospheric CO2 are expected to infl uence the distribution of the biota, as well as its abundance, and the photosynthetic 

activity of phytoplankton (Falkowski et al., 1998). SeaWiFS satellite imagery 

shows that worldwide oceanic chlorophyll a concentrations are about 0.2 mg/m3

(Yoder et al., 1993) and can reach 5 mg/m3 in coastal upwelling zones (Falkowski 

et al., 1991; Walsh et al., 1978). It is diffi cult to use this method to obtain information on chlorophyll a concentrations for many onshore tropical areas because 

accurate remote sensing is diffi cult in coastal areas with large sediment input and 

because many tropical regions have high frequencies of cloud cover. In such areas 

fi eld measurements of water clarity and chlorophyll a concentrations are vital for 

assessing short-term variation and ground-truthing remote measurements.

Rachel Collin, Luis D’Croz, Plinio Gondola, and 

Juan B. Del Rosario, Smithsonian Tropical Research Institute, MRC 0580-08, Unit 9100, Box 

0948, DPO AA 34002, USA. Corresponding 

author: R. Collin (collinr@si.edu). Manuscript received 29 August 2008; accepted 20 April 2009.

25_Collin_323-334_Lang.indd 323 5_Collin_323-334_Lang.indd 323 9/24/09 9:59/24/09 9:59
324 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Coral reef environments are particularly sensitive to 

changes in water quality, especially changes in nutrients, 

sediment load, and productivity. The paradigm of coral 

reef biology is that reef development and coral health are 

greatest in areas with low sedimentation, low primary productivity, low abundances of zooplankton, and high water 

clarity. These habitats are most conspicuous in the IndoPacifi c and the offshore islands in the Caribbean. In many 

locations these habitats are suffering from reduction of water quality associated with coastal development (Bell, 1992; 

Lapointe, 1992). In the Caribbean, most studies of reefs and 

their waters are conducted in the Bahamas, Puerto Rico, 

Nether lands Antilles, and other offshore islands (Gilbes et 

al., 1996; Otero and Carbery, 2005; van Duyl et al., 2002; 

Webber et al., 2003). In addition there have been some studies of the unusual upwelling sites along the coast of Venezuela and Colombia (Franco-Herrera et al., 2006) and the 

strongly freshwater-infl uenced regions around the Yucatan 

(Herrera-Silveira et al., 2002). However, few studies have 

examined heavily terrestrially infl uenced systems without 

these unusual features in the Caribbean. Here we report the 

results of eight years of physical climatic and water quality 

monitoring in Bahia Almirante, an enclosed Caribbean archipelago that is highly terrestrially infl uenced.

STUDY LOCATION: 

BOCAS DEL TORO, PANAMA

Three bodies of water surround the Bocas del Toro 

Archipelago on the Caribbean coast of Panama: the Bahia 

Almirante and the Laguna de Chiriquí on the landward 

side, and the Caribbean Sea on the exposed coastal side 

(Figure 1). The mainland surrounding the region is largely 

forested, although the completion of a road linking Costa 

Rica to Bocas del Toro and the rest of Panama in the year 

FIGURE 1. Map of the Bahia Almirante region with sampling sites indicated. BTRS Bocas del Toro Research Station; CSS CARICOMP seagrass site; MT instrument platform; STRI Smithsonian Tropical 

Research Institute.

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NUMBER 38 • 325

2000 has resulted in increased lowland deforestation, as 

well as land development for small farms and tourism. 

The landward sides of the islands are fringed with largely 

intact red mangrove forests, although these are also being 

cleared from the landward side. The Laguna de Chiriquí, 

which receives twice the freshwater runoff of Bahia Almirante, has higher nutrient loads and limited coral reef 

development (D’Croz et al., 2005) and is not discussed 

further here.

The Bahia Almirante has signifi cantly more oceanic 

infl uence than the Laguna de Chiriqui and supports welldeveloped coral reefs. It receives runoff from only two rivers of any note. High rainfall (about 3 m/year) and runoff from the San San Pond Sac peat swamp forest often 

result in pronounced haloclines with low-salinity waters 

(which are often cold) overlying full-salinity bottom waters 

(Kaufmann and Thompson, 2005). Surface salinities are 

generally 30– 34 PSS (practical salinity scale) but can drop 

as low as 20 PSS after heavy rains (Kaufmann and Thompson, 2005). Other conditions are relatively aseasonal, with 

mean sea surface temperatures varying from 27.5°C 

(January– February) to 29.7°C (September– October). Average wind speed is about 7 km/h but occasionally exceeds 

20 km/h (Kaufmann and Thompson, 2005). Despite the 

high levels of runoff, N:P was always recorded to be below 

Redfi eld ratios in a previous survey of the area (D’Croz 

et al., 2005). This observation suggests that primary productivity could be nutrient limited and that inputs from 

freshwater runoff or wind mixing could fertilize primary 

productivity in the Bahia Almirante.

The Smithsonian Tropical Research Institute’s Bocas 

del Toro Research Station is on the Bahia Almirante side 

of Isla Colon. As part of the development of the scientifi c 

knowledge base of the station, and as part of the CARICOMP program, various physical and biological features 

of the surrounding environment have been monitored 

since 1999. Here we examine these data (1) to develop a 

baseline to which future studies can be compared, (2) to 

determine if the recent rapid development of the region 

has had an effect on water clarity and phytoplankton biomass, and (3) to explore the physical data to understand 

what factors infl uence the variation in these parameters.

MATERIALS AND METHODS

MONITORING HISTORY

Isla Colon is the site of the Smithsonian Tropical 

Research Institute’s Bocas del Toro Research Station. At 

its inception in 1998 a long-term physical and biological 

monitoring program was initiated. Physical records of air 

and water temperature, rainfall, salinity, solar radiation, 

and wind speed have been kept since 1999 (reviewed in 

Kaufmann and Thompson, 2005). Monitoring of Secchi 

depths and chlorophyll a concentrations was conducted 

approximately biweekly at fi ve sites (see Figure 1) from 

1999 until 2001. The sampling intervals were not equal 

(ranging from 7 to 28 days), so these data were not appropriate for time-series analyses.

The Secchi depths and chlorophyll a monitoring was 

reinitiated at three of these sites and at an additional site 

in 2006 and continues to be measured weekly. At one of 

these, the CARICOMP reef monitoring site (described 

in Guzmán et al., 2005), the Secchi depths have been recorded weekly since 2000. At the CARICOMP seagrass 

site, horizontal Secchi readings have been taken weekly 

since 1999. During the entire period, measurements were 

made by the same three-person team.

SAMPLING LOCALITIES

Sampling sites (Figure 1; Table 1) were chosen in 1999 

to include a range of environments. In 2006 sites were 

chosen to include an onshore– offshore gradient, in which 

we expected more oceanic conditions on one end and terrestrially infl uenced conditions on the other end.

• Colon, 6.3 km northeast of Bocas del Toro Town, is 

the most exposed site. The bottom at 20.5 m is muddy. 

Rough conditions occasionally made it impossible to 

take measurements in this location.

• Cristobal, in the middle of the Almirante Bay, is a site 

7 km from the mainland and surrounded by patch reefs. 

The bottom at 25 m is muddy.

• Pastores is a semienclosed bay, 500 m from the mainland. It is more heavily infl uenced by continental runoff 

and creek discharge than the other sites. Depth at the 

sampling site is 26 m but a nearby coral reef slopes from 

5 to 16 m. Jellyfi shes are abundant at this site.

• Smithsonian Tropical Research Institute (STRI) is the site 

closest to the Bocas del Toro Research Station, 500 m 

from the shore. This site serves as the water monitoring site for the CARICOMP reef site, which is onshore 

of this location, over a reef that slopes from 5 to 20 m. 

The bottom is muddy and sandy with isolated patches 

of coral.

• Bottomwood, between Solarte and San Cristobal Islands, 

is protected from oceanic infl uence. The sampling site is 

near mangrove islets, sand cays, and a shallow coral reef. 

The reef slopes to a fi ne sand bottom at 16 m.

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326 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

• Zapatillas has the highest diversity and abundance of 

coral and octocoral species of any of our sampling sites. 

The bottom at about 15 m is mostly covered by patch 

reefs and fi ne sand.

• The CARICOMP seagrass site is several hundred meters 

along the shore to the northwest of the Bocas del Toro 

Research Station. This shallow (2 m depth) location has 

extensive Thalassia cover, and the small bay is fringed 

by red mangroves.

HYDROLOGICAL MEASURES

Water temperature and salinity were recorded with 

an YSI 85 multiparameter probe (Yellow Springs Instruments, Yellow Springs, Ohio, USA) at the same time and 

depth as the seawater was sampled. Measurements were 

taken at approximately 50 cm. Dissolved oxygen was 

also measured in 2006– 2008. Salinity is expressed in the 

practical salinity scale (PSS) and dissolved oxygen in milligrams per liter.

CLIMATE RECORDS

Rainfall, solar radiation, and wind speed are monitored continuously at the Bocas del Toro Research Station, as described by Kaufmann and Thompson (2005). 

These measurements are taken close to the STRI site (see 

Figure 1). For the purposes of this study average rainfall, solar radiation, and wind speed were calculated for 

3 days and 6 days before each sampling day. We chose 

these periods because Beman et al. (2005) showed that 

phytoplankton blooms can peak 3 to 5 days after nutrient 

input from terrestrial runoff.

Annual rainfall was obtained in two ways. First, an 

hourly tipping bucket measured rainfall from 2002. Because data are incomplete for three of the years (including 

2008), we calculated the average daily rainfall to standardize across the years. The second estimates were from 

the Bocas del Toro airport. These records extend to 1999 

and were also converted to annual daily averages.

SECCHI DEPTHS

Water clarity was measured by lowering a 30 cm diameter Secchi disk into the water until it was no longer 

seen and then raised until it reappeared. The Secchi depth 

was measured according to the length of the submerged 

rope. This operation was repeated three times at each site 

during each measurement. At the seagrass site the Secchi 

was measured horizontally, underwater at 0.5 m depth, 

and was read with a dive mask.

CHLOROPHYLL A

Three replicate water samples were collected by hand 

at 50 cm below the surface in polyethylene bottles and 

placed in a cooler for the return to the laboratory. Two 

liters of each replicate were vacuum fi ltered on Whatman 

GF/F (0.7 m pore size). Filters were wrapped in aluminum 

foil and stored frozen (20°C). A Tefl on pestle was used 

TABLE 1. Study site locations and the data available for each site.

Site Location Secchi depths Chlorophyll a

Colon 9°2237N 1999– 2001 1999– 2001

 82°1237W 2006– 2008 2006– 2008

Cristobal 9°1815N 2006– 2008 2006– 2008

 82°1755W –– 

Pastores 9°1236N 1999– 2001 1999– 2001

 82°1937W 2006– 2008 2006– 2008

STRI a 9°2040N 2000– 2008 1999– 2001

 82°1639W –2006– 2008

Bottomwood 9°1747N 1999– 2001 1999– 2001

 82°1325W –– 

Zapatilla 9°1527N 1999– 2001 1999– 2001

 82°0619W –– 

CARICOMP seagrass 9°2106N 1999– 2008 – 

 82°1529W Horizontal

a STRI, Smithsonian Tropical Research Institute.

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NUMBER 38 • 327

to grind the fi lters in 5 mL 90% aqueous acetone solution. 

The slurry was transferred to 15 mL polypropylene screwcap centrifuge tubes and fi lled to 10 mL with acetone. The 

tubes were kept in the dark at 20°C for 24 h. Extracts 

were centrifuged at 3,000 rpm, and the supernatant was 

analyzed for chlorophyll a following the nonacidifi cation 

fl uorometric method (Welschmeyer, 1994).

STATISTICAL ANALYSIS

Correlation analyses and multiple regression analyses 

were used to describe the relationships between the variables of interest (Secchi depth and chlorophyll a concentration) and the hydrological data and the climate data. 

Student’s t test, analysis of variance (ANOVA), and analysis 

of covariance (ANCOVA) were used to test for differences 

between sites and sampling periods. Because it is likely that 

there is a lag in the response of phytoplankton to the input 

of nutrients from river runoff or turbulence, we looked for 

correlations between Secchi depths or chlorophyll a concentrations and the average of rainfall, solar radiation, and 

wind speed over the previous 3 and 6 days. Because the 3 

day and 6 day results did not differ substantively, only the 

results using the 3 day average are reported here. Because 

rainfall and cloud cover are patchy on a local scale, we only 

examined climatic variables for the STRI and CARICOMP 

seagrass sites. Time-series autocorrelation analyses were applied to Secchi depth and chlorophyll a data. The few weeks 

of missing data were fi lled with the averages values for the 

time series under analysis.

RESULTS

A number of complex relationships were demonstrated 

between the hydrological parameters, Secchi depths, and 

chlorophyll a concentrations at the different sites. Several 

of these relationships vary among the sites, and there are 

a number of interactions between factors; however, the 

following generalizations can be made. (1) Secchi depths 

increased with temperature, salinity, and solar radiation, 

and decreased with rainfall, wind speed, and chlorophyll a

concentration. (2) Correlations between any hydrological characteristic and Secchi depths or chlorophyll a were 

low (r 2 rarely exceeding 0.10) but were higher for all the 

climatic variables (rain and solar radiation had r 2 up to 

0.22). (3) Chlorophyll a concentrations showed no consistent temporal or spatial patterns. (4) Secchi depths were 

not tightly correlated with chlorophyll a concentrations. 

(5) Secchi depths increased and rainfall decreased throughout the study.

HYDROLOGICAL CONDITIONS AT EACH SITE

Hydrological parameters varied somewhat among the 

six sites (Table 2, Figure 2). Salinity was signifi cantly different at all sites (ANOVA with post hoc t test; Table 2), with 

the lowest average salinity in Pastores, the most inland site, 

and the highest average salinity in Colon, the most oceanic 

site. For 1999– 2001 the average temperature at Pastores 

was signifi cantly higher than the other sites and the temperature at Colon was signifi cantly lower. The temperature 

TABLE 2. Summary of physical and biological data from 1999– 2001 and 2006– 2008.

 Dissolved Signifi cant changes

 Temperature, Salinity,a

 oxygen, Secchi depth, Chlorophyll a, between periods

Site Years °C (SD) PSS (SD) mg/L (SD) m (SD) mg/m3 (SD) (t test)

Colon 1999– 2001 28.1 (1.26) 33.0 (1.70) – 9.1 (3.6) 0.44 (0.19) Temperature increased

 2006– 2008 28.6 (0.89) 33.5 (1.31) 5.80 (0.43) 10.0 (3.6) 0.47 (0.23)

Cristobal 2006– 2008 28.8 (0.95) 32.9 (1.46) 5.83 (0.49) 12.4 (3.2) 0.46 (0.25) NA

Pastores 1999– 2001 28.6 (1.29) 31.9 (2.15) – 11.0 (3.3) 0.46 (0.24) Temperature and Secchi

 2006– 2008 29.2 (0.98) 32.4 (1.76) 5.81 (0.51) 13.2 (3.0) 0.49 (0.28) depth increased

STRI 1999– 2001 28.3 (1.16) 32.9 (1.33) – 10.9 (3.9) 0.37 (0.24) Temperature and Secchi

 2006– 2008 28.7 (0.91) 33.0 (1.34) 5.78 (0.49) 13.2 (3.6) 0.43 (0.23) depth increased

Bottomwood 1999– 2001 28.3 (1.24) 32.7 (1.43) – 11.9 (3.7) 0.36 (0.19) NA

Zapatillas 1999– 2001 28.3 (1.28) 33.0 (2.78) – 11.3 (2.6) 0.46 (0.22) NA

a PSS practical salinity scale.

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328 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

at Pastores was also signifi cantly higher than at the other 

sites in 2006– 2008, but there were no signifi cant differences between the remaining sites. Dissolved oxygen did 

not differ between sites.

Temperature increased signifi cantly between the two 

time periods at the three sites for which data were available over both periods (t test, P  0.002 for each site), 

despite an overall temperature decrease during the 2006– 

2008 period. Salinity did not show a signifi cant temporal 

trend during either time period nor did it differ between 

the two periods. Dissolved oxygen was only measured for 

the 2006– 2008 period, where it showed no temporal trend. 

Eight years of data from climatic monitoring at the Bocas 

Research Station instrument platform shows a downward 

trend in rainfall, but little change in average solar radiation or average wind speed (Figure 3).

FACTORS AFFECTING SECCHI DEPTHS

Secchi depths ranged from 2 to 22 m, and the depths 

varied substantially from week to week (Figure 4). SecFIGURE 2. Averages of temperature (A), salinity (B), Secchi depths (C), and chlorophyll concentration (D) from the two sampling periods (1999 

data excluded). Student’s t tests showed signifi cant increases in temperature between periods at Colon, Pastores, and STRI and increases in Secchi 

depth at Pastores and STRI. Single-factor analysis of variance (ANOVA) detected signifi cant (P  0.01) site effects. Signifi cant differences between 

groups of sites within either sampling period are indicated with letters, so that bars both labeled with “A” are not signifi cantly different from each 

other but are different from those otherwise labeled with post hoc tests. Specifi c letters were assigned arbitrarily, but A– C refer to 2000– 2002 data 

and W– Z refer to 2006– 2008 data. Bars one standard deviation (1 SD) of the mean. (Salinity is expressed in the practical salinity scale, PSS.)

chi depths showed signifi cant effects of site, and signifi -

cant associations with temperature, salinity and chlorophyll a concentrations during both the 1999– 2001 and 

2006– 2008 periods (ANCOVA; Table 3). The correlation of any one variable with water clarity was low, with 

FIGURE 3. Long-term trends in climatic variables. Yearly averages for rainfall, solar radiation, and wind speed during the past 

8 years show the decline in average daily rainfall. Daily averages 

are used because missing data prevent the use of cumulative data. 

(Rainfall is mm/d.)

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NUMBER 38 • 329

the highest r 2 value for temperature at 0.13– 0.17. Secchi depths increased with temperature (Ordinary Least 

Squares regression [OLS]: 1999– 2001, r 2 0.13, P 

0.001; and 2006– 2008, r 2 0.17, P  0.001), and 

salinity (OLS: 1999– 2001, r 2 0.10, P  0.001; and 

2006– 2008, r 2 0.06, P  0.001) and decreased with 

chlorophyll a concentration (OLS: 1999– 2001, r 2 0.09, 

P  0.0001; and 2006– 2008, r 20.06, P  0.001). The 

average Secchi depth was signifi cantly lower for the exposed Colon site than for the other sites in both time 

periods (see Table 2, Figure 2). Analysis of the data from 

the two different periods showed different combinations 

of interaction effects (see Table 3).

Climatic variables were more tightly correlated with 

Secchi depth than were the seawater variables. Using the 

six years of complete climate data from the STRI site, we 

found that Secchi depths at the STRI site show signifi cant 

effect of year (P  0.0001), a marginal effect of rainfall 

(P 0.056), and signifi cant effects of solar radiation (P

0.002) and wind speed (P  0.001), but no signifi cant 

interactions between these factors. For the CARICOMP 

seagrass site there was no effect of year, but rainfall and 

wind speed over the prior 3 days were signifi cant (P 

0.01), as well as the interaction between rainfall and solar radiation (P  0.0008). Secchi depth decreased with 

the amount of rainfall (r 2 0.22 and 0.23, respectively, 

with P  0.001) and wind speed (r 2 0.21; P  0.001) 

at both sites and increased with solar radiation (r 2 

0.21 and 0.15, respectively, with P  0.0001) at the STRI 

site but was only signifi cant by its interaction with rainfall in the seagrass site. The interaction at the seagrass 

site showed that Secchi distances decreased more quickly 

with rainfall at high levels of solar radiation than at low 

solar radiation.

Secchi depths increased over the long term: they increased from 1999– 2001 to 2006– 2008 at Pastores and 

STRI (t test, P  0.0001 for both) but not at Colon. Least 

squares regression showed a signifi cant increase in Secchi 

depths (r 2 0.02; n 381; P  0.0002; slope 0.3) 

with date over the 8 years of weekly sampling at STRI. 

The horizontal Secchi data from the nearby CARICOMP 

FIGURE 4. Variation in Secchi depths (top graph) and chlorophyll a

(bottom graph) concentrations over time for the 2006– 2008 dataset. 

Straight line is the trend line of depth or concentration on that date. 

Superimposed lines show individual variation.

TABLE 3. Analysis of covariance (ANCOVA) effects of physical variables on chlorophyll a concentration and Secchi depth 

in 1999– 2001 and 2006– 2008 data after stepwise removal of 

nonsignifi cant variables.

Sum of 

Source df a squares F ratio P

Secchi depth, 1999– 2001

 Site 4 235.03 6.78 0.0001

 Temperature 1 100.97 11.65 0.0008

 Salinity 1 290.63 33.53 0.0001

 Chlorophyll a concentration 1 150.82 17.40 0.0001

 Site*salinity b 4 104.02 3.00 0.02

 Salinity*temperature b 1 67.31 7.76 0.006

Secchi depth, 2006– 2008

 Site 3 556.41 21.77 0.0001

 Temperature 1 454.35 53.33 0.0001

 Salinity 1 216.91 25.46 0.0001

 Oxygen 1 2.86 0.33 0.56

 Chlorophyll a concentration 1 47.15 5.53 0.02

 Site*temperature b 3 70.34 2.75 0.04

 Temperature*oxygen b 1 49.58 5.82 0.02

Chlorophyll a, 1999– 2001

 Site 4 0.38 2.30 0.06

 Temperature 1 1.24 30.11 0.0001

 Salinity 1 0.06 1.43 0.23

 Site*salinity b 4 0.55 3.34 0.01

 Salinity*temperature b 1 0.31 7.58 0.006

Chlorophyll a, 2006– 2008

 Temperature 1 0.26 4.90 0.03

 Salinity 1 2.41 45.35 0.0001

 Oxygen 1 0.25 4.67 0.03

a df Degrees of freedom.

b * Run with only two-way interactions.

25_Collin_323-334_Lang.indd 329 5_Collin_323-334_Lang.indd 329 9/24/09 9:59/24/09 9:59
330 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

seagrass site show no long-term trend. When these values 

are binned by month, there is a marginal effect of month 

on the Secchi depths in the seagrass site (P 0.07) and a 

signifi cant effect of month at the reef site (P 0.0007). 

Greater Secchi depths were recorded from drier months 

and sunnier months (Figure 5), a result also found by 

Kaufmann and Thompson (2005).

FACTORS AFFECTING CHLOROPHYLL A CONCENTRATIONS

Chlorophyll a concentration varied between 0.04 

and 1.66 mg/m3. Similar to Secchi depths, concentrations 

varied substantially from week to week and with no clear 

seasonal component to the variation (see Figure 4). During the fi rst 14 sampling dates of the 1999– 2001 study 

period, chlorophyll a concentrations were measured with 

a spectrophotometer. An ANOVA testing for effects of 

site and method showed that the results from the spectrophotometer were signifi cantly higher (site: F 3.96; df

4; P  0.005; method: F 26.8; df 1; P  0.0001; 

n 328). Therefore values obtained from the spectrophotometer were excluded from the subsequent analyses 

and this dataset included only data from 2000– 2001 or 

2006– 2008.

Although the average chlorophyll a concentrations 

did not differ between the two periods (t test, P  0.05), 

there were different patterns for the two sampling periods. The only common results were that chlorophyll a

concentration decreased with temperature, and that the 

variables examined explained no more than 10% of the 

variance in chlorophyll a concentrations. Data from 

2000– 2001 showed a signifi cant effect of temperature 

and a marginal effect of site, but no effect of salinity

(ANCOVA; see Table 3). There were signifi cant interactions between site and salinity and between site and temperature (Table 3). Overall, chlorophyll a concentrations 

decreased with temperature (OLS: n 328; r 2 0.06, 

P  0.0001). Results from 2006– 2008 were different: 

there were signifi cant effects of temperature and salinity, 

but not of site or oxygen concentration, nor were there 

signifi cant interactions (Table 3). Chlorophyll a concentrations decreased with temperature (OLS: n 402; r 2 

0.03, P 0.002) and salinity (r 2 0.11, P  0.0001) but 

these factors explained very little of the variation.

Climate data were poorly linked to chlorophyll a

concentrations. Average wind speed for the 3 days before 

sampling was positively correlated with chlorophyll concentration (r 2 0.19, P  0.005) but this appeared to be 

caused by a few periods with extremely high winds. ChloFIGURE 5. Bar graph with monthly averages of Secchi depths, rainfall, solar radiation, and wind speed for the 8-year dataset showing 

that months with higher average Secchi depths also had lower average rainfall. Bars 1 SD of the mean.

25_Collin_323-334_Lang.indd 330 5_Collin_323-334_Lang.indd 330 9/24/09 9:59/24/09 9:59
NUMBER 38 • 331

rophyll a concentration was independent of both rainfall 

over 3 days prior and average solar radiation over the 3 

days before the measurements.

TIME SERIES

Both the Secchi depths and chlorophyll a concentrations 

varied considerably from week to week (see Figure 4). To 

determine if this variation has a temporal autocorrelation, 

we conducted a time-series analysis. For 1999– 2008 Secchi depth is temporally auto-correlated at both the CARICOMP seagrass and the STRI sites (seagrass: Fisher’s 

kappa 9.9, P  0.01; for coral: Fisher’s kappa 12.2, 

P  0.001). Over the shorter period, 2006– 2008, Secchi 

depth was temporally auto-correlated at Colon (Fisher’s 

kappa 8.59, P  0.01), Cristobal (Fisher’s kappa 7.39, 

P  0.02), and STRI (Fisher’s kappa 6.91, P  0.04) 

but not Pastores (P  0.05). Chlorophyll a concentrations, 

on the other hand, showed an autocorrelation only for Colon (P  0.005). Examination of the autocorrelation function shows that, over the short term (lag of up to several 

months), the autocorrelation function appears stationary 

(Figure 6). However, a peak around the 52 week lag (Figure 6) is evidence of seasonal externally driven periodicity 

and suggests an annual cycle that is not obvious from plots 

of the raw data (see Figure 4).

DISCUSSION

The overall values for the data presented here are 

similar to those reported for the Bahia Almirante by 

D’Croz et al. (2005), Kaufmann and Thompson (2005), 

and Carruthers et al. (2005). We report some longterm trends that were not detected by Kaufmann and 

Thompson, who closely examined the patterns of daily 

FIGURE 6. Autocorrelation function for 8 years of Secchi data for STRI and CARICOMP seagrass sites and chlorophyll a concentrations for 2 

years for Colon (signifi cant autocorrelation) and STRI (no signifi cant autocorrelation) sites.

25_Collin_323-334_Lang.indd 331 5_Collin_323-334_Lang.indd 331 9/24/09 9:59/24/09 9:59
332 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

and monthly variation in physical parameters. Comparing the YSI 85 probe measures of temperature and salinity between the 2000– 2002 sampling period and the 

2006– 2008 period, we found signifi cant increases in water temperature and salinity. This fi nding appears to be 

associated with the recent trend toward lower rainfall in 

the region.

Annual rainfall is typically high, in excess of 3,000 

mm, in the Bahia Almirante, and the mean freshwater runoff is approximately 1,600 mm per year (IGNTG, 1988). 

However, average daily rainfall per year dropped from 

12.48 mm in 2002 to 7.91 mm in 2007 (see Figure 3). 

Reduced rainfall likely affected the hydrological conditions in Bahia Almirante, which result from the interaction 

between river discharge and ocean intrusion (D’Croz et 

al., 2005). During the 1999– 2001 sampling period, rainfall was high and salinity showed the typical increasing 

trend from Pastores, the site nearest the mainland, to the 

ocean-exposed sites at Colon and Zapatilla. This pattern 

in surface salinity is consistent with the expected high dilution at nearshore sites resulting from river discharge into 

the bay. The inshore-to-offshore salinity gradient was not 

apparent during the 2006– 2008 sampling period, presumably because of the reduction of river discharge and consequent greater infl uence of salinity from open ocean waters 

(see Figure 2).

LONG-TERM TREND IN SECCHI DEPTHS

The most striking long-term trend we detected was 

the surprising increase in Secchi disk depths. During the 8 

years of monitoring, visibility has increased by 2 m (a rate 

of 0.25 m/year) for several of the sites. Long-term trends 

of decreased Secchi depths have been reported for monitoring in other areas. For example, in a dataset from the 

Baltic Sea spanning 77 years, Secchi depths have decreased 

0.05 m/year (Sandén and Håkansson, 1996), and a decrease of 0.03 m/year was reported in the Menai Strait in 

Wales (Kratzer et al., 2003). The few reports of increased 

Secchi depths were associated with bioremediation or efforts to reduce untreated sewage outfall. For example, Secchi depths increased at 0.05 m/year in Narragansett Bay, 

Rhode Island, coincident with reductions in anthropogenic 

total suspended solids (Borkman and Smayda, 1998), as 

at one of several sampled sites in the Southern California Bight (Convers and McGowan, 1994). Our measures 

show a much more rapid change in Secchi depths than 

these previous studies.

The observed changes in Secchi depths were not in the 

expected direction. A number of complicated, interacting 

factors can infl uence water clarity, as measured by Secchi 

disk, but many of them would indicate a decrease in Secchi depth. The ongoing rapid development of tourism in 

Bocas del Toro, particularly on Isla Colon, is accompanied 

by an increase in wastewater input to the Bahia Almirante. 

Changes in Secchi readings can refl ect changes in particulate matter (from runoff or wind-induced turbidity) but 

can also be caused by changes in phytoplankton biomass 

or yellow pigments (mostly humic and fulvic acids) in the 

water. Deforestation and coastal development can affect 

all three of these factors. Inputs from untreated wastewater as well as runoff from deforested areas can increase 

the nutrients, particulate matter, and yellow pigments in 

the water. In addition, increased nutrients often lead to 

increased primary productivity, which can result in higher 

standing phytoplankton biomass. These anthropogenic effects have been increasingly affecting coral reef habitats 

throughout the Caribbean, where wastewater disposal is 

the leading cause for eutrophication and decreased water 

clarity (Szmant, 2002). We had expected to see a long-term 

reduction in water clarity as a result of similar changes in 

Bocas del Toro.

Secchi depth is often strongly correlated with chlorophyll a concentration and has been used as a proxy for productivity in highly seasonal upwelling zones or temperate 

lakes. This method is often favored because it is cheaper, 

faster, and easier to obtain than a quantifi cation of chlorophyll a concentration. Sandén and Håkansson (1996) reviewed four studies as well as their own data that showed 

a relationship between Secchi depths and chlorophyll a

concentrations. The relationships are reported as power 

functions and show chlorophyll a to scale with Secchi 

depth to the 1.47– 2.6 power. Megard and Berman (1989) 

showed that the proportion of light attenuation caused 

by chlorophyll concentration differed between neritic and 

pelagic seawater, but there were clear relationships nonetheless. Here we found that chlorophyll a concentration 

explained only 6%– 9% of the variance in Secchi depths. 

In addition, mean chlorophyll a concentrations were relatively low in the Almirante Bay, near 0.5 mg m3, which is 

the suggested threshold value for oligotrophic conditions 

required for coral reef development (Bell, 1992). Therefore, these measures are not consistent with the presence 

of phytoplankton blooms resulting from anthropogenic 

nutrient enrichment. They do, however, suggest that even 

small increases in nutrients or chlorophyll a concentrations 

in this region could result in a shift from coral-dominated 

to algal-dominated benthic communities.

It seems unlikely to us that there has been a drop in the 

load of anthropogenic suspended solids and/or nutrients 

25_Collin_323-334_Lang.indd 332 5_Collin_323-334_Lang.indd 332 9/24/09 9:59/24/09 9:59
NUMBER 38 • 333

during the past eight years, despite the probable decrease 

in the volume of runoff. In fact, it appears that, if anything, these inputs have increased. So, what is the cause 

of the long-term trend in Secchi depth? The correlation 

analysis and the monthly trends (see Figure 5) both suggest that rainfall and solar radiation are the most closely 

associated with Secchi depth. However, rainfall is the only 

variable showing a strong annual trend consistent with the 

increased Secchi depths, and rainfall over the three days 

before the measurements was the variable most highly correlated with Secchi depths of any hydrological or climate 

variable examined. Solar radiation, although it is positively 

correlated with Secchi depths on the reef, does not show 

the pronounced long-term trend that rainfall does. The effect of wind on Secchi depth similarly does not explain the 

long-term trend. It could, however, explain the fact that 

Colon, the most exposed site, with the highest winds had 

consistently lower Secchi depths than the other sites. Windinduced turbidity, which resuspends bottom sediment, is 

the likely cause of the limited water clarity at this site.

CONCLUSION

The baseline data reported here will be useful for future studies of anthropogenic effects in the unique Bocas 

del Toro archipelago. Rapid local development is progressing in the face of little information on the impact of 

such development and the factors affecting such impacts 

(e.g., water residence time or currents in the Bahia Almirante). It is likely that anthropogenic inputs of nutrients 

and suspended particulate matter will contribute to eutrophication of some areas. This study suggests that despite 

the impact of development, patterns of water clarity and 

chlorophyll a concentrations in the region are currently 

driven mainly by large-scale climate patterns. There is little evidence of a tight relationship between these measures 

and features of the local water mass, nor is there evidence 

of eutrophication at the sites we sampled. Future sampling 

closer to highly developed areas is necessary to document 

and monitor the impact of development on water quality.

ACKNOWLEDGMENTS

We thank Arcadio Castillo for help in the fi eld, James 

Roper for comments on the manuscript, the Hunterdon 

and Johnson Oceanographic Research Endowments for 

fi nancial support, and Empresa de Transmisión Eléctrica 

Panamá for supplying the rainfall data from the Bocas del 

Toro airport.

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Cause of Coral Reef Decline? Estuaries, 25:743– 766.

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R. P. M. Bak. 2002. Factors Infl uencing the Short-Term Variation 

in Phytoplankton Composition and Biomass in Coral Reef Waters. 

Coral Reefs, 21:293– 306.

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25_Collin_323-334_Lang.indd 334 5_Collin_323-334_Lang.indd 334 9/24/09 9:59/24/09 9:59
Nutrient and Chlorophyll Dynamics 

in Pacifi c Central America (Panama)

Luis D’Croz and Aaron O’Dea

ABSTRACT. Strong wind jets from the Caribbean and the Gulf of Mexico cross Central America through topographic depressions in the cordillera during the boreal winter, 

pushing Pacifi c coastal waters offshore, lowering sea levels at the coast, and causing 

coastal upwelling. Where high mountains impede the winds, this phenomenon does not 

occur. The Panamanian Pacifi c shelf is an excellent example of this variability. The coast 

is divided into two large areas, the Gulf of Panama and the Gulf of Chiriquí. To investigate hydrological conditions between the two gulfs, we sampled the water column during 

upwelling and non-upwelling seasons in each region. In both gulfs during non-upwelling 

conditions, surface-level nutrients are poor, and the chlorophyll maximum occurs around 

30 m where the thermocline intersects the euphotic zone. Oxygen-poor waters (2 ppm) 

commonly occurred below the thermocline. During the dry season, wind strength increased and strong upwelling was observed in the Gulf of Panama. The thermocline rose 

and surface waters became nutrient enriched and chlorophyll a levels increased. Welloxygenated waters were compressed to shallow depths. In the Gulf of Chiriquí, wind 

strength was weaker, surface waters did not become enriched with nutrients, and surface 

chlorophyll a remained low. We did observe a shallowing of the thermocline in the Gulf 

of Chiriquí, but in contrast to the Gulf of Panama, wind mixing was not strong enough 

to result in sea-surface cooling and nutrient enrichment. We postulate that the convergence of a shallow thermocline and internal waves in the Gulf of Chiriquí is the likely 

mechanism that causes pockets of deep water to occasionally migrate into surface waters, 

leading to restricted and ephemeral upwelling-like conditions. Although its effects upon 

shallow-water communities remain to be studied, we propose that the process may be 

more likely to occur during the boreal winter when the thermocline is shallower.

INTRODUCTION

One of the most pervasive hydrological events to infl uence the shelf waters of Pacifi c Central America is upwelling. Intermittent or seasonal upwelling develops in the gulfs of Tehuantepec (Mexico), Papagayo (Costa Rica), and 

Panama (Legeckis, 1988; McCreary et al., 1989; Xie et al., 2005), driving extensive planktonic productivity and shaping the secondary production of biological 

communities (Jackson and D’Croz, 1997; O’Dea and Jackson, 2002).

The shelf waters along the Pacifi c coast of Panama are among the most dynamic in the region. Here, the coastal shelf is naturally divided into two large gulfs 

by the Azuero Peninsula: the Gulf of Panama (shelf area, 27,175 km2) and the Gulf 

Luis D’Croz and Aaron O’Dea, Smithsonian 

Tropical Research Institute, Box 0843-03092, 

Panama, Republic of Panama. Corresponding 

author: L. D’Croz (dcrozl@si.edu). Manuscript 

received 13 May 2008; accepted 20 April 2009. 

26_D'Croz_335-344_Lang.indd 335 6_D'Croz_335-344_Lang.indd 335 9/24/09 10:21/24/09 10:21
336 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of Chiriquí (shelf area, 13,119 km2) (Figure 1). The Gulf 

of Panama experiences strong seasonal upwelling while the 

Gulf of Chiriquí exemplifi es a non-upwelling environment 

(Dana, 1975; Kwiecinski and Chial, 1983). This distinction is customarily explained using geographic differences 

between the two gulfs. Seasonal upwelling in the Gulf of 

Panama develops during Panama’s dry season, corresponding to the boreal winter, when northeast trade winds cross 

to the Pacifi c over low areas in the isthmian mountain range, 

pushing warm and nutrient-poor coastal surface water offshore, lowering the nearshore sea level, and causing the upward movement of colder and nutrient-richer deep water 

(Smayda, 1966; Forsbergh, 1969; Kwiecinski et al., 1975; 

D’Croz et al., 1991; D’Croz and Robertson, 1997). The established model proposes that because western Panama has 

higher mountain ranges that block the winds, surface waters 

in the Gulf of Chiriquí are not displaced out to the Pacifi c, 

and no upwelling as such occurs there.

The structure of shallow biological communities between the two regions supports this inference. Coral reefs, 

which respond poorly to upwelling conditions, are more 

extensive in size in the Gulf of Chiriquí than in the Gulf of 

Panama (Glynn, 1977; Glynn and Maté, 1997), whereas 

small pelagic fi sh species from the Gulf of Panama represent a large proportion of the total estimated fi shery resource in the country (NORAD, 1988). Satellite imagery 

shows both wind speeds and chlorophyll content of surface 

waters to be lower in the Gulf of Chiriquí than the Gulf of 

Panama during the dry seasons (Pennington et al., 2006).

However, the statement that upwelling does not occur 

in the Gulf of Chiriquí is supported by sea-surface data 

derived from satellite imagery analysis or from the measurement of properties in the shallow section of the water 

column. Hydrological profi les of the water column have 

documented the shoaling of the thermocline in the Gulf 

of Chiriquí, yet there appears to be no clear association 

between the physical forcing of this event with the windinduced upwelling in the Gulf of Panama. Nevertheless, 

the movement of pockets of cool water that bring nutrients into the upper layer may be a more common occurrence in the Gulf of Chiriquí than previously suspected 

(D’Croz and O’Dea, 2007).

It is therefore essential that we obtain detailed and 

comparable hydrological data from both gulfs if we wish 

to explain variability in biological communities along the 

Pacifi c coast of the Isthmus of Panama today and through 

geologic time (O’Dea et al., 2007). In this paper we expand the information presented in our previous study 

(D’Croz and O’Dea, 2007), adding new hydrological and 

biological data from the Gulf of Chiriquí and the Gulf of 

Panama, and we further discuss the issue of whether upwelling takes place in the Gulf of Chiriquí.

FIGURE 1. Map of the Republic of Panama showing sampling sites. Red dots represent the location of the 

rainy season samplings in the Gulf of Panama (a  18 December 2004) and in the Gulf of Chiriquí (a  13 

July 2003; b  17 December 2004). Blue dots represent the location of the dry season samplings in the Gulf 

of Panama (a  29 February 2000) and in the Gulf of Chiriquí (a  1 March 2000; b  13 April 2007). 

Yellow squares indicate the location of the meteorological stations.

26_D'Croz_335-344_Lang.indd 336 6_D'Croz_335-344_Lang.indd 336 9/24/09 10:21/24/09 10:21
NUMBER 38 • 337

MATERIALS AND METHODS

STUDY AREA

Panama’s Pacifi c shelf is located from 07°30 to 

09°01N and 78°10 to 82°52W. The shelf is predominantly occupied by low-salinity surface water, similar to 

the water mass found over the center of the tropical Pacifi c 

Ocean at about 10°N (Wyrtki, 1967; Fiedler and Talley, 

2006). The climatology is governed by the Inter-Tropical 

Convergence Zone (ITCZ), the position of which defi nes 

the seasonal pattern of rainfall and winds. The rainy season 

develops between May and December when the ITCZ is 

located over or slightly to the north of Panama and winds 

are light and variable in direction. The dry season develops between January and March when the ITCZ moves 

south of Panama, a time period characterized by predominating intense northeast trade winds. The mean annual rainfall recorded at meteorological stations near the 

coast (1999– 2004) was 2,760 mm in the Gulf of Chiriquí 

(David) and 1,880 mm in the Gulf of Panama (Tocumen). 

Approximately 94% of the annual rainfall in both areas 

corresponded to the rainy season, the months of September and October being the rainiest in both regions. The 

estimated sizes of the drainage basins are 11,846 km2 in 

the Gulf of Chiriquí and 33,828 km2 in the Gulf of Panama. River discharges into both gulfs typically follow the 

seasonal trend described for rainfall. Detailed discussions 

on wind-stress, rainfall, and river discharge patterns are 

presented in D’Croz and O’Dea (2007). The tidal regime 

is semidiurnal, and the sea-level difference during spring 

tides is 6 m (Glynn, 1972).

SAMPLING PROCEDURES

Sampling research cruises were conducted in the gulfs 

of Panama and Chiriquí using the Smithsonian Tropical 

Research Institute’s R/V Urracá (see Figure 1). Samplings 

were scheduled to correspond with different times of the 

year, representing contrasting hydrological conditions (upwelling and non-upwelling). Surface-to-bottom profi les for 

salinity, temperature, dissolved oxygen, and chlorophyll a

were recorded with a CTD (conductivity, temperature, 

depth) multiparameter profi ler (Ocean Seven 316, Idronaut Srl, Milano, Italy). Hydrological casts with the CTD 

corresponding to the dry season were carried out in both 

gulfs on 29 February 2000 and 1 March 2000 and in the 

Gulf of Chiriquí on 13 April 2007. Rainy season CTD 

casts were carried out in the Gulf of Chiriquí on 13 July 

2003 and in both gulfs during 17 and 18 December 2004. 

The water column was sampled at discrete levels to study 

nutrient and chlorophyll a concentrations. Water samples 

were collected using Niskin bottles during the dry season 

of the year 2000 (29 February to 1 March) and during 

the rainy season of the year 2004 (17 and 18 December). 

Three replicate water samples per selected depth were collected at each site. Two liters of each individual replicate 

water sample were immediately sieved through Nitex 

(350 m) to exclude zooplankton and vacuum fi ltered on 

Whatman GF/F fi lter (0.7 m pore size) for chlorophyll a 

analysis. An aliquot from each fi ltrate was set apart for the 

determination of dissolved inorganic nutrients. Filters and 

water samples were stored frozen (20°C) until analysis. 

Salinity is expressed using the Practical Salinity Scale (pss) 

indicated by UNESCO (1981). Results from the chlorophyll a analyses were used to check the calibration of the 

CTD’s fl uorometer. The depth of the euphotic zone (1% 

incident radiation) was estimated from Secchi disk readings (Parsons et al., 1984). The light attenuation coeffi -

cient was calculated as Kd  f/zs where zs is the Secchi 

depth and f  1.4.

ANALYSIS OF SAMPLES

Not later than two weeks after sampling, fi lters holding the phytoplankton were analyzed for chlorophyll a

using the non-acidifi cation fl uorometric method (Welschmeyer, 1994). Water samples were analyzed for NO3

 

NO2

 (nitrate  nitrite), Si(OH)4 (silicate), and PO43

(phosphate) by colorimetric methods using an Alpkem 

Flow Solution IV automated analyzer. Minimum detection 

limits were 0.02 M for nitrate, 0.01 M for nitrite, 0.12 

M for silicate, and 0.02 M for phosphate.

ANALYSIS AND PRESENTATION OF DATA

Water quality variables, namely temperature, salinity, dissolved oxygen, dissolved inorganic nutrients, and 

chlorophyll a, are presented graphically as profi les of the 

samplings. Overall differences in between the two gulfs 

were assessed with the Mann– Whitney test (U) by taking 

the median of each variable from samples collected in the 

top 30 m of the ocean where the highest hydrological variability occurred (Table 1). Water transparency data were 

compared using the paired t test. We followed the practice 

of taking the position of the 20°C isotherm to represents 

the depth of the center of the permanent thermocline in 

the eastern Pacifi c Ocean (Wyrtki, 1964; Fiedler et al., 

1991; Xie et al., 2005). Pearson correlations with Bonferroni adjustment were used to test statistical relationships 

among variables.

26_D'Croz_335-344_Lang.indd 337 6_D'Croz_335-344_Lang.indd 337 9/24/09 10:22/24/09 10:22
338 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

RESULTS

THERMOHALINE STRUCTURE

Both the Gulf of Panama and the Gulf of Chiriquí 

exhibit the typical tropical coastal ocean water structure of cool deep waters leading upward to a shallow 

thermocline topped by warm surface waters. However, 

signifi cant differences occur between the two gulfs with 

respect to climatic variability. During the rainy season, 

the thermal structure in both gulfs is remarkably similar 

(see Table 1). Sea-surface temperatures (SSTs) are invariably warm (27°– 28°C), and the thermocline sits at approximately 60 m (Figure 2).

During the dry season, thermal conditions become dissimilar between the two regions (Table 1). In our observations, the thermocline in the Gulf of Panama rose sharply 

and nearly broke at the surface, resulting in a signifi cant 

cooling of surface waters to 22°C (Figure 3a). Simultaneously, the thermocline in Gulf of Chiriqui rose to around 

30 m, compressing warm SSTs into shallow waters (Figure 

3b). However, the shoaling of the thermocline in Chiriquí 

was not as intense as that seen in the Gulf of Panama and 

did not result in SST cooling.

In general, salinity profi les in both regions revealed 

a sharp gradient from high-salinity deep water to fresher 

surface waters. Seasonal variability in surface salinities 

in both gulfs was very similar (Table 1). During the rainy 

season, both regions experienced high freshwater dilution in the upper-layer waters, with surface salinities 

below 30 on the pss (see Figure 2). The halocline was 

located at 60 m depth, coinciding with the thermocline. 

During the dry season, lower rainfall led to increased 

salinities in the surface waters of both gulfs (Figure 3). 

However, the effect was more striking in the Gulf of 

Panama as the halocline shoaled and salinity in surface 

waters reached 34.

In April 2007, the thermohaline structure in the 

Gulf of Chiriquí departed drastically from the typical 

condition as the thermocline/halocline shoaled to 20 m. 

Despite this condition, however, SSTs remained warm 

(Figure 3c).

CHLOROPHYLL

Concentrations of surface chlorophyll were always below 0.30 g/L in both gulfs during the rainy season (Table 

1), but a deep chlorophyll maximum developed from 30 m 

to 50 m, lying above the thermocline (Figure 2). The deep 

chlorophyll maximum contained most of the chlorophyll a 

in the water column in both gulfs, concentrations reaching 

1 g/L during the rainy season. The dry season upwelling 

changed this pattern in the Gulf of Panama, as the chlorophyll maximum moved into shallower waters, where concentrations surpassed 4 g/L (Figure 3a). Surface chloroTABLE 1. Average value of hydrological variables in the top water column (30 m) in the gulfs of Panama (GP) and Chiriquí (GC); SE 

standard error of the mean. Statistical tests were either Mann– Whitney U test or paired t test (*P 0.05, **P 0.01, ***P 0.001, 

ns  nonsignifi cant).

 Dry season values Rainy season values

Hydrological GP GC Statistical GP GC Statistical

variables (Mean  SE) (Mean  SE) value a,b (Mean  SE) (Mean  SE) value a,b

Temperature (°C) 17.97  0.92 27.17  0.92 16.0* a 26.75  0.54 28.61  0.05 18.0 ns a

Salinity (pss) c 34.18  0.29 32.98  0.29 12.0* a 31.67  0.64 30.48  0.38 3.0 ns 

Chlorophyll a (g L1) 1.82  0.65 0.83  0.65 4.0* a 0.23  0.13 0.18  0.06 8.5 ns a

Dissolved oxygen (ppm) 3.45  0.27 4.78  0.27 13.0* a 3.98  0.16 4.38  0.01 4.0 ns a

NO3

 (M) 14.37  2.48 3.72  2.48 1.0** a 0.99  0.34 0.36  0.02 2.5 ns a

PO4

3 (M) 1.08  0.21 0.39  0.21 1.0** a 0.43  0.07 0.24  0.03 4.0 ns a

N:P ratio 12.82  1.10 7.77  1.10 1.0** a 2.11  0.36 1.49  0.10 3.0 ns a

Si(OH)4 (M) 8.99  1.03 4.40  1.03 5.0* a 5.40  0.71 4.87  0.47 13.0 ns a

Secchi depth (m) 4.20  0.00 14.80  0.00 1591.0*** b 20.00  0.00 19.00  0.00 2.0 ns b

Euphotic zone (m) 13.8  0.00 48.63  0.00 1394.2*** b 65.71  0.00 62.43  0.00 188.4 ns b

a Mann– Whitney U test. b Paired t test. c pss  practical salinity scale.

26_D'Croz_335-344_Lang.indd 338 6_D'Croz_335-344_Lang.indd 338 9/24/09 10:22/24/09 10:22
NUMBER 38 • 339

phyll a remained at very low values in the Gulf of Chiriquí 

during the dry season, but the deep chlorophyll maximum 

became remarkably intense at 30 m where concentration 

reached 3 g/L (Figure 3b).

DISSOLVED OXYGEN

Dissolved oxygen profi les followed the typical pattern of well-oxygenated surface waters lying on top of 

deeper oxygen-poor waters. During the rainy season, severe hypoxic conditions (2 ppm) were recorded below 

the strong oxycline, at 50 m and nearly coincident with 

the thermocline (see Figure 2). Oxygen concentrations in 

waters above the thermocline were strongly correlated 

with temperature in both the Gulf of Panama (r  0.91; 

P 0.001) and the Gulf of Chiriquí (r  0.89; P 

0.001) during the rainy season. This arrangement, however, had strong seasonal variation in the Gulf of Panama 

during the dry season, as the oxycline rose to 25 m and 

compressed the oxygenated waters into shallow depths 

(Figure 3). Dissolved oxygen below this depth rapidly declined to less than 1 ppm (Figure 3a), whereas waters in 

the Gulf of Chiriquí only became hypoxic below the 50 m 

oxycline (Figure 3b). No correlations were confi rmed between dissolved oxygen and temperature in any of these 

regions during the dry season.

DISSOLVED NUTRIENTS

Both gulfs exhibit a strong vertical gradient of upwardly 

decreasing nutrient concentrations. Nitrate in surface waters 

was depleted in both gulfs during the rainy season, with values below 0.5 M (Figure 4). During the dry season, nitrate 

concentrations at the surface were observed to increase 10 

fold in the Gulf of Panama when the nutricline shoaled to 

around 10 m (Figure 5a). No similar surface enrichment 

was detected in the Gulf of Chiriquí, where a strong nutricline was developed at 60 m (Figure 5b).

FIGURE 2. Profi les of dissolved oxygen, chlorophyll a, salinity, and temperature in the Gulf of Panama and 

the Gulf of Chiriquí during the rainy season. a  Gulf of Panama, 18 December 2004; b  Gulf of Chiriquí, 

13 July 2003; c  Gulf of Chiriquí, 17 December 2004.

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340 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Overall, the patterns of phosphate resembled those of 

nitrate, but concentrations were lower by an order of magnitude. Concentrations of phosphate in excess of 1 M were 

usually found below 30 m depth. Phosphate concentrations 

in surface waters remained relatively low (0.3 M) in the 

Gulf of Chiriquí during both climatic seasons (Figures 4b, 

5b). However, phosphate enrichment of surface waters 

clearly occurred in the Gulf of Panama during the dry season when the nutricline shoaled and phosphate concentrations in the top of the water column reached about 1.0 M 

(Figure 5a).

Silicate profi les followed similar trends to that of the 

nitrate and phosphate (Figures 4, 5). Although silicate 

concentrations were similar in surface waters in both gulfs 

during the rainy season, they doubled in the Gulf of Panama during the dry season (Table 1).

Dissolved nutrients in the upper 50 m had a high degree of relationship with temperature and salinity. During 

the rainy season, nitrate concentrations were inversely correlated to temperature in both the Gulf of Chiriquí (r 

– 0.78; P 0.001) and the Gulf of Panama (r  – 0.97; P 

0.002). In the dry season, nitrate in the Gulf of Panama was 

negatively correlated to temperature (r  – 0.98; P 0.044) 

and directly related to salinity (r  0.98; P 0.049). Nitrate was negatively correlated to temperature in the Gulf of 

Chiriquí during the dry season (r  – 0.89; P 0.016), but 

not to salinity (r  0.67; P  0.159). Phosphate was negatively correlated to temperature during the dry season in the 

Gulf of Panama (r  – 0.98; P 0.038) and in the Gulf of 

Chiriquí (r  – 0.97; P 0.036). Dry season phosphate was 

also correlated to salinity in the Gulf of Chiriquí (r  0.98; 

P 0.05).

The extremely low nitrate to phosphate ratios (N:P) 

suggest that phytoplankton growth in both regions was 

under severe nitrogen limitation during the rainy season 

(Figure 6). The N:P ratio was below 2:1 in surface water 

and increased with depth, surpassing the value of 10:1 

below the depth of 50 m. During the dry season, N:P raFIGURE 3. Profi les of dissolved oxygen, chlorophyll a, salinity, and temperature in the Gulf of Panama and 

the Gulf of Chiriquí during the dry season. a  Gulf of Panama, 29 February 2000; b  Gulf of Chiriquí, 1 

March 2000; c  Gulf of Chiriquí, 13 April 2007.

26_D'Croz_335-344_Lang.indd 340 6_D'Croz_335-344_Lang.indd 340 9/24/09 10:22/24/09 10:22
NUMBER 38 • 341

tios within the euphotic zone largely increased in both regions, becoming closer to the N:P ratio of 16:1 suggested 

as favorable for phytoplankton growth (Redfi eld, 1958).

WATER TRANSPARENCY

Water transparency was seasonably stable in the Gulf 

of Chiriquí but varied considerably in the Gulf of Panama 

(see Table 1). Water transparency in both gulfs was higher 

during the rainy season when the euphotic zone was approximately 60 m deep, in contrast to the limited transparency and shallow euphotic zone (14 m) observed in the 

Gulf of Panama during the dry season upwelling.

DISCUSSION

Our data on bottom-to-surface profi les reveal the dynamics of hydrological conditions along the Pacifi c coast of 

Panama during times of both upwelling and non-upwelling. 

During the non-upwelling rainy season, both gulfs exhibit 

extremely similar hydrological structures dominated by the 

FIGURE 4. Mean profi les of silicate (Si), phosphate (P), and nitrate (N) in the Gulf of Panama and the Gulf 

of Chiriquí during the rainy season. a  Gulf of Panama, 18 December 2004; b  Gulf of Chiriquí, 17 December 2004.

26_D'Croz_335-344_Lang.indd 341 6_D'Croz_335-344_Lang.indd 341 9/24/09 10:22/24/09 10:22
342 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

development of an intense thermocline at approximately 

60 m. Surface waters tend to have low salinities and are 

warm and nutrient depleted. Low N:P ratios in surface 

waters during the rainy season suggest that phytoplankton growth is strongly nitrogen limited. Consequently, the 

standing stock of chlorophyll a is maintained at relatively 

low levels in surface waters. Phytoplankton does however 

peak at subsurface levels as the nutrient-rich thermocline 

waters intersect the euphotic zone, increasing N:P ratios 

and favoring algal growth. The strong inverse correlation 

between nutrients and sea temperature is consistent with 

the coincidence of a shallow thermocline and strong nutricline typical of the eastern tropical Pacifi c Ocean (Enfi eld, 

2001). As such, the seasonal movement of the thermocline 

represents a key source of nutrients for phytoplankton. 

Our sampling sites were far offshore and therefore silicate 

concentrations were not as high as previously reported for 

the inner shelf (D’Croz and O’Dea, 2007) even though the 

concentration of silicate in the Gulf of Panama is reported 

to be the highest in the eastern Pacifi c as a consequence of 

the intense runoff in the area (Pennington et al., 2006).

During the dry season, the hydrological patterns of the 

two gulfs become dissimilar. In the Gulf of Panama strong 

upwelling of cold deep waters into coastal and surface waFIGURE 5. Mean profi les of silicate (Si), phosphate (P), and nitrate (N) in the Gulf of Panama and the Gulf 

of Chiriquí during the dry season. a  Gulf of Panama, 29 February 2000; b  Gulf of Chiriquí, 1 March 

2000.

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NUMBER 38 • 343

ters drives signifi cant changes in the hydrological properties 

of the water column. The thermocline migrates vertically 

upward, leading to cooling, increased salinity, and nutrient 

enrichment on surface waters. Surface N:P ratios become 

closer to the Redfi eld value and, as a result, phytoplankton 

growth intensifi es, leading to a reduction in water clarity. 

A shallow oxycline also develops and oxygen concentration below the oxycline is reduced, often leading to severe 

hypoxic conditions. In contrast, the oxycline in the Gulf of 

Chiriquí is deeper and deep water remains hypoxic. Low 

oxygen minima are nonetheless typical in the eastern tropical Pacifi c as a combination of high algal growth at the 

surface, a strong pycnocline that impedes the ventilation of 

waters below, and the sluggish circulation of deep waters 

(Fiedler and Talley, 2006). The report of large fi lamentous 

Thioploca -like sulfur bacteria on shallow sediments in both 

regions strongly suggests that the inner shelf is exposed to 

episodes of reduced oxygen (Gallardo and Espinoza, 2007).

A signifi cant relationship between wind-stress index 

(calculated from the sum of northerly winds) and sea level 

provides an explanatory mechanism for upwelling in the 

Gulf of Panama (Schaefer et al., 1958; Legeckis, 1988; 

Xie et al., 2005). Surface waters are displaced into open 

ocean by strong northerly winds during the dry season, 

and deep waters move vertically upward to replace them 

(Fleming, 1940; Smayda, 1966; Forsbergh, 1969). Consequently, wind stress is inversely related to SST in the Gulf 

of Panama during the dry season but not during the rainy 

season (D’Croz and O’Dea, 2007).

Data from the Gulf of Chiriquí are scant but did suggest that upwelling does not occur, because wind stress 

during the dry season is normally one-third of that of 

the Gulf of Panama (Kwiecinski and Chial, 1983) and it 

does not displace surface waters offshore. High mountain 

ranges running along western Panama impede the fl ow of 

northerly winds across to the Gulf of Chiriquí (see Figure 1), whereas mountain ranges in central Panama are 

low, allowing strong wind jets to form toward the Gulf 

of Panama. Despite this clear distinction, our data show 

that similar hydrological changes to those that occur in the 

Gulf of Panama do take place in the Gulf of Chiriquí. During the dry season, and concurrent with strong upwelling 

in the Gulf of Panama, we observed deeper waters rise toward shallower depths in the Gulf of Chiriquí. This movement led to a substantial compression of the mixed layer 

and the corresponding rise of available nutrients within 

the euphotic zone, shifting the chlorophyll maximum 

above the shallow thermocline. Although direct evidence 

of prolonged surface water cooling was not observed, we 

postulate that cooling and nutrient-enrichment episodes 

in the Gulf of Chiriquí may occur and that their intensity is dependent upon the depth to which the thermocline 

reaches in the eastern Pacifi c during the boreal winter. 

Nonetheless, the process is clearly much less intense than 

that in the Gulf of Panama. Despite substantial shifts in 

deeper water conditions in the Gulf of Chiriquí, surface 

waters remain warm and nutrient poor, presumably because wind stress is not strong enough to cause the advection of deep, cool, and nutrient-rich waters to the surface 

(D’Croz and O’Dea, 2007). However, ocean forces such as 

internal waves might change the oceanographic structure 

in the Gulf of Chiriquí, causing brief periods of advection 

of deep cold water to the surface layer (Dana, 1975). Longterm records from data loggers deployed in coral reefs give 

evidence of such brief SST drops in the Gulf of Chiriquí 

that are possibly related to internal waves (D’Croz and 

O’Dea, 2007). This effect might be more evident as the 

internal waves approach the shallow coasts around the islands in the Gulf of Chiriquí and may be more likely to 

occur during times of thermocline shallowing.

In conclusion, although the Gulf of Chiriquí does not 

experience the intense seasonal upwelling characteristic 

of the Gulf of Panama, deeper waters do migrate upward 

in synchrony with Gulf of Panama upwelling. This movement is probably caused by an overall shallowing of the 

thermocline across Central America. The difference in intensity of upward movement of the thermocline between 

FIGURE 6. Profi les of average nitrate to phosphate ratios (N:P) in 

rainy (triangles) and dry (circles) seasons: a  Gulf of Panama; b 

Gulf of Chiriquí.

26_D'Croz_335-344_Lang.indd 343 6_D'Croz_335-344_Lang.indd 343 9/24/09 10:22/24/09 10:22
344 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

the two gulfs strongly infl uences the phytoplankton community, with seasonal blooms occurring in the Gulf of 

Panama but not in the Gulf of Chiriquí. Deeper waters do 

nonetheless experience similar patterns of seasonal hydrographic change, and shallow waters of the Gulf of Chiriquí 

can be exposed to brief pulses of cold and nutrient-rich 

waters by advection. However, the effects of thermocline 

migration and advection on the shallow-water communities of the Gulf of Chiriquí remain to be studied in detail.

ACKNOWLEDGMENTS

Juan B. Del Rosario, Plinio Góndola, and Dayanara 

Macías assisted in the collection and processing of the 

samples. Sebastien Tilmans and Juan L. Maté reviewed the 

manuscript. Rainfall data were kindly provided by Empresa 

de Transmisión Eléctrica S.A., Panama. We acknowledge the 

participants, skipper, and crew of the R/V Urracá for their 

assistance during the cruises. The Government of the Republic of Panama granted the permits for the collections.

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26_D'Croz_335-344_Lang.indd 344 6_D'Croz_335-344_Lang.indd 344 9/24/09 10:22/24/09 10:22
Growth and Nutrient Conservation 

in Rhizophora mangle in Response 

to Fertilization along Latitudinal 

and Tidal Gradients

Ilka C. Feller, Catherine E. Lovelock, 

and Cyril Piou

ABSTRACT. Mangroves form heterogeneous marine ecosystems with spatial differences 

in structural complexity, biodiversity, biogeochemistry, and hydrology that vary at local 

and regional scales. Although mangroves provide critical ecosystem goods and services, 

they are threatened globally by human activities, including nutrient over-enrichment. 

Our goal was to determine if enrichment with nitrogen (N) or phosphorus (P) interacts 

with forest structure and latitude to alter growth and nutrient dynamics. We established 

a series fertilization experiments across more than 2,000 km and 18° of latitude from the 

Indian River Lagoon (IRL), Florida, to Twin Cays, Belize, to Bocas del Toro, Panamá. At 

each site, we fertilized individual trees with one of three treatment levels (control, N, 

P) in two intertidal zones (fringe, scrub) and measured their responses for four years. 

We tested the effects of nutrient over-enrichment on growth, resorption effi ciency, and 

resorption profi ciency of the red mangrove Rhizophora mangle. All sites were nutrient 

limited, but patterns of nutrient limitation varied by zone and latitude. At IRL, growth 

was N limited; at Twin Cays, the fringe was N limited, but the scrub forest was P limited; at Bocas del Toro, the fringe was N limited, but the scrub forest was both N- and P 

limited. Nutrient enrichment had dramatic and complex effects on nutrient conservation. 

Adding nutrients to mangrove ecosystems affected growth and the nutrient recycling, but 

the pattern depended on location, site characteristics, and the nature of nutrient limitation. Predicting how forests will respond to nutrient over-enrichment requires an assessment of spatial heterogeneity at multiple scales of response.

INTRODUCTION

Mangrove ecosystems are coastal wetlands dominated by woody plants that 

span gradients in latitude (30°N to 37°S), tidal height (1 m to 4 m), geomorphology (oceanic islands to riverine systems), sedimentary environment (peat to alluvial), climate (warm temperate to both arid and wet tropics), and nutrient loading 

(oligotrophic to eutrophic). Throughout their distribution, mangroves are critical 

not only for sustaining biodiversity in these intertidal forests but also for their direct and indirect benefi t to human activities. As a detritus-based ecosystem, the leaf 

litter from these trees provides the basis for adjacent aquatic and terrestrial food 

webs (Odum and Heald, 1975). Mangroves function as nurseries for many of the 

sport and commercial fi shes found in deeper waters and provide feeding grounds 

Ilka C. Feller, Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, Maryland 21037, USA. Catherine E. 

Lovelock, Centre for Marine Studies/School of 

Integrative Biology, University of Queensland, St. 

Lucia, Queensland 4072, Australia. Cyril Piou, 

Institute of Forest Growth and Computer Science, 

Technical University Dresden, Germany; currently 

at Institut Nacional de la Recherche Agronomique, 

Unité Mixte de Recherche–ECOBIOP, F-64310 

Saint-Pée sur Nivelle, France. Corresponding 

author: I. Feller (felleri@si.edu). Manuscript received 21 July 2008; accepted 20 April 2009. 

27_Feller_345-358_Lang.indd 345 7_Feller_345-358_Lang.indd 345 9/24/09 10:23/24/09 10:23
346 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

for large reef fi shes (Nagelkerken et al., 2000; Mumby et 

al., 2004). As a result, mangrove-assimilated energy and 

nutrients are exported to surrounding coral reefs (Dittmar 

and Lara, 2001). Besides supporting and renewing coastal 

fi shing stock, mangroves also benefi t human economic development by stabilizing shorelines. This stabilization is a 

critical function in tropical coastal areas that may be battered periodically by tropical storms, hurricanes, and tsunamis (Danielson et al., 2005; Barbier, 2006).

Despite repeated demonstration of their ecological and 

economic importance, mangroves are one of the world’s 

most threatened ecosystems (Valiela et al., 2001; Alongi, 

2002; Barbier and Cox, 2003; Rivera-Monroy et al., 2004; 

Duke et al., 2007). In addition to direct destruction, increasing input of human-caused nutrient pollution is widely recognized as one of the major threats to mangroves and other 

marine environments worldwide (NRC, 1995, 2000, 2001; 

Duce et al., 2008). However, system-specifi c attributes may 

lead to large differences among coastal and estuarine systems in their sensitivity and susceptibility to these increasing nutrient levels (Cloern, 2001). The complex suite of 

direct and indirect responses in coastal systems to nutrient 

over-enrichment include changes in water chemistry, distribution and biomass of plants, sediment biogeochemistry, 

decomposition processes, nutrient cycling, nutrient ratios, 

phytoplankton communities, habitat quality for metazoans, and ecosystem functions.

Relatively little is known about how the structure and 

function of mangrove ecosystems are altered by nutrient 

enrichment. In temperate salt marshes and mangroves, ecological processes have been shown to be nitrogen- (N) limited (Valiela and Teal, 1979; Feller et al., 2003b). The few 

tropical and subtropical mangrove wetlands that have been 

studied were shown to be both phosphorus- (P) and N limited (Boto and Wellington, 1984; Feller, 1995; Feller et al., 

1999, 2003a, 2003b; Lovelock and Feller, 2003; Lovelock 

et al., 2004). Because mangroves are responsive to processes 

operating at multiple spatial scales, comparisons along a 

broad latitudinal gradient in climate and across narrow 

tidal gradients will improve our understanding of the relative impacts of global versus local factors on the structure 

and function of these ecosystems. In this study, we focused 

on the mangrove Rhizophora mangle (red mangrove), an 

evergreen tree that has a large geographic range throughout 

the Atlantic-East Pacifi c region (Duke, 1992). Along the Atlantic coasts of North and South America, its distribution is 

continuous and spans almost 60° of latitude from its northern limit along the coast of Florida at 29°42.94N (Zomlefer et al., 2006) to its southern limit along the coast of Brazil at 27°53S (Shaeffer-Novelli et al., 1990). In this study, 

our goals were to determine how nutrient availability varies 

among R. mangle forests spanning a temperate to tropical 

gradient and how nutrient over-enrichment affects plant 

growth and nutrient conservation. We manipulated nutrient availability and measured responses of trees fertilized 

with nitrogen (N) or phosphorus (P) growing along intertidal gradients in similar habitats at three locations along 

this latitudinal gradient to test the following hypotheses.

1. Nutrient availability varies along a latitudinal gradient 

with a decreasing supply of P relative to N toward the 

tropics (Vitousek, 1984; Vitousek and Sanford, 1986; 

Crews et al., 1995). This hypothesis predicts increasing P limitation in mangrove forests at lower latitudes 

and N limitation at higher latitudes (Güsewell, 2004; 

McGroddy et al., 2004; Reich and Oleksyn, 2004; 

Kerkhoff et al., 2005).

2. Delivery, uptake, or assimilation of P is more strongly 

affected by tidal fl ushing and concomitant factors that 

vary spatially than is that of N (Smith, 1984; McKee 

et al., 2002). This hypothesis predicts differences in N 

versus P limitation within mangrove forests at different 

intertidal elevations (Ross et al., 2006). Specifi cally, N 

limitation is predicted for the low intertidal where tidal 

fl ushing is greater (residence time is shorter) than in the 

high intertidal where P limitation is predicted.

3. Because of difference in growth rates along climatic 

gradients, the mechanisms used by plants to recycle and 

conserve nutrients will be more effi cient at higher latitudes (Oleksyn et al., 2003). This hypothesis predicts 

increased nutrient conservation by mangroves growing 

near their temperate limit (Lovelock et al., 2007).

4. As nutrient availability increases, nutrient conservation 

mechanisms become less effi cient (Shaver and Melillo, 

1984; Vitousek, 1984; Schlesinger et al., 1989; Escudero et al., 1992). This hypothesis predicts that the effects of nutrient loading on mangrove forests will differ 

depending on whether a system is N- or P limited, with 

the expectation that the limiting nutrient will be more 

effi ciently and tightly conserved (Feller et al., 1999).

MATERIALS AND METHODS

SITE DESCRIPTIONS

We compared the effects of nutrient over-enrichment 

on plant growth and nutrient dynamics in Rhizophora mangle L. at three locations along the Atlantic and Caribbean 

coasts from Florida to Panamá spanning a climatic gradient of more than 2,000 km and 18° of latitude (Figure 1): 

27_Feller_345-358_Lang.indd 346 7_Feller_345-358_Lang.indd 346 9/24/09 10:23/24/09 10:23
NUMBER 38 • 347

(1) Indian River Lagoon (referred to hereafter as IRL), 

Florida; (2) Twin Cays, Belize (referred to hereafter as Twin 

Cays); and (3) Bocas del Toro, Republic of Panamá (referred 

to hereafter as Bocas) (Table 1). Table 2 provides a summary of the characteristics for the three locations (Koltes et 

al., 1998; McKee et al., 2002; Feller et al., 2003a; Feller and 

Chamberlain, 2007; Lovelock et al., 2005). Forest structure 

at the three locations was heterogeneous and characterized 

by complex gradients in tree height that included a narrow 

seaward fringe of uniformly tall (4 m) trees dominated 

by R. mangle, varying in width from 5 to 20 m (Figure 2). 

Tree height decreased rapidly to landward with interior 

areas dominated by old-growth stands of low stature, or 

“scrub,” trees (1.5 m) (Table 3). The black mangrove 

(Avicennia germinans L.) and the white mangrove (Laguncularia racemosa (L.) Gaertn. f.) were also present in each 

of these locations, typically near the landward ecotone. The 

hydrogeomorphic settings were variable among the three 

locations. IRL and Bocas were continental in contrast with 

Twin Cays, which is a low oceanic island. However, Twin 

Cays and Bocas were more similar in mineralogy (Phillips et 

al., 1997; Macintyre et al., 2004; Coates et al., 2005), with 

mangrove forests atop a carbonate platform and deep peat 

deposits. All sites were microtidal with mixed semi diurnal 

tides (Kjerfve et al., 1982; Kaufmann and Thompson, 

2005). The fringe zones at the three locations were similarly 

well fl ushed, but the hydrological conditions of the scrub 

zones varied. At Twin Cays, these interior portions of the 

forest were completely inundated and waterlogged (McKee 

et al., 2007). In contrast, the Bocas scrub zone drained completely at low tide (Lovelock et al., 2005). At IRL, the scrub 

zone drained completely at low tide during the summer but 

remained inundated for days during the winter (Feller et al., 

2003b).

In the IRL, our experimental sites were situated on the 

lagoonal side of two barrier islands. The fringe site was in 

Avalon State Park on North Hutchinson Island, St. Lucie 

County; the scrub site was in the Hobe Sound National 

Wildlife Refuge on Jupiter Island, Martin County. In 

this area, soil was composed primarily of marine sand 

with mangrove forests adjacent to coastal strand vegetation and maritime hammocks. Descriptions of forest 

FIGURE 1. The three study sites used in this study span more than 

18° of latitude and extend from the Indian River Lagoon (IRL), 

Florida, in the north, to Twin Cays, Belize, and to Bocas del Toro, 

Panama, in the south.

TABLE 1. Hydrogeomorphic characteristics of the study sites along a latitudinal gradient from the Indian River Lagoon (IRL), Florida, to Twin Cays, Belize, to Bocas del Toro (Bocas), Panama.

Characteristic IRL Twin Cays Bocas

Latitude 27°33N, 80°13W 16°50N, 88°06W 9°09N, 82°15W

Freshwater infl ow Medium Low High

Type of landscape Continental Oceanic Continental

Topographic relief Medium Low High

Nutrient fl ux High Low Medium

Mineralogy Siliclastic/carbonate Peat/limestone Peat/limestone

Annual rainfall 1.3 m 2.8 m 3.5 m

Mean temperature range a 12.4°– 23.6°C (w) 18.3°– 29.9°C (w) 20.1°– 31.1°C (w)

 22.6°– 31.9°C (s) 22.2°– 31.3°C (s) 21.9°– 31.8°C (s)

Mean tidal range 37 cm 34 cm 19 cm

Major disturbances Anthropogenic, hurricanes Anthropogenic, hurricanes Anthropogenic, fl ooding

a w  winter; s  summer.

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348 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

structure, hydro-edaphic conditions, growth, nutrient dynamics, and photosynthesis at the Avalon State Park site 

were previously reported (Feller et al., 2003a; Lovelock 

and Feller, 2003).

At Twin Cays, our fringe and scrub sites were located 

on the two largest islands of this 92-ha mangrove archipelago, 10 km offshore. Descriptions of forest structure, 

biogeochemistry, ecophysiology, growth, and nutrient dynamics were previously reported (Rützler and Feller, 1996; 

McKee et al., 2002; Feller et al., 2003b, 2007; Lovelock 

et al., 2006a, 2006b, 2006c, 2006d). These oceanic mangroves islands are underlain by deep deposits of mangrove 

peat 8 to 12 m thick (Macintyre et al., 2004; McKee et 

al., 2007).

At Bocas, fringe and scrub sites were located on three 

islands (San Cristobal, Solarte, Isla Popa) in Almirante Bay 

and the Chiriqui Lagoon in a vast network of mangrove 

islands and mainland peninsulas covering approximately 

2,885 km2 (De Croz, 1993; Guzman and Guevara, 1998; 

Guzman et al., 2005; Lovelock et al., 2004, 2005). Here, 

mangroves occurred adjacent to tropical rainforests and 

grew on peat approximately 5 m deep atop ancient coral 

reef limestone (Phillips and Bustin, 1996; Phillips et al., 

1997). This location was outside the hurricane belt, but 

fl ooding was common. Earthquakes are episodic (Phillips 

et al., 1994, 1997; Phillips and Bustin, 1996) and are likely 

to be the major nonanthropogenic disturbance regime infl uencing these forests.

EXPERIMENTAL DESIGN

Fertilization experiments were set up at IRL in January 1997, at Twin Cays in January 1995, and at Bocas in 

January 1999. To compare responses, we used a three-way 

factorial analysis of variance (ANOVA) design (i.e., 3 nutrient enrichment treatment levels [Control, N, P]  2 

zones [fringe, scrub]  3 locations [IRL, Twin Cays, Bocas]  3 sites per location  3 replicate trees per site, for 

a total of 162 trees). Nutrient treatment was randomly asTABLE 2. Characteristics of the mangrove forest structure in the fringe and scrub zones at the Indian River Lagoon (IRL), Florida, to 

Twin Cays, Belize, to Bocas del Toro (Bocas), Republic of Panama. Data are from Koltes et al. (1998), McKee et al. (2002), Feller et al. 

(2003a), Lovelock et al. (2005), and Feller and Chamberlain (2007).

 Salinity (‰) Tree height (m) DBH (cm) Stem density Basal area

Location Zone (mean SE) Species (mean 1 SE) (mean 1 SE) (stems0.1 ha1) (m20.1 ha1)

IRL Fringe 32.7  0.7 Rhizophora mangle 3.9  0.1 4.5 3,953 6.4

 Laguncularia racemosa 3.2  0.3 6.1 1,343 3.9

 Avicennia germinans 3.8  0.3 4.8 671 1.2

 Scrub 32.4  0.5 Rhizophora mangle 1.7  0.1 2.5  0.2 2,386 1.5

 Laguncularia racemosa 4.5  0.4 4.6  0.7 477 1.0

 Avicennia germinans 1.6  0.0 1.2  0.0 73 0.01

Twin Cays Fringe 36.9  1.2 Rhizophora mangle 3.2  0.2 7.3  0.4 401 2.1

 Laguncularia racemosa 2.2 a 2.9 a 3 a0.2 a

 Avicennia germinans 2.2 a 4.0 a 3 a0.01 a

 Scrub 39.4  1.2 Rhizophora mangle 0.8  0.1 2.4  0.2 897 0.4

Bocas Fringe 34.4  0.6 Rhizophora mangle 3.9  0.1 5.3  0.6 850 1.6

 Scrub 33.3  1.9 Rhizophora mangle 0.7  0.1 1.5  0.1 3,357 0.7

a Based on occurrence of a single tree in each zone.

FIGURE 2. Mangrove forests at each of our study sites are characterized by a distinctive tree-height gradient with tall trees fringing the 

shoreline and scrub trees in the interior.

27_Feller_345-358_Lang.indd 348 7_Feller_345-358_Lang.indd 348 9/24/09 10:23/24/09 10:23
NUMBER 38 • 349

signed within each zone and site. Trees were amended with 

150 g N as NH4 (45:0:0), or P fertilizer as P2O5 (0:45:0), 

per centimeter diameter breast height, as described in 

Feller (1995). Doses (150 g) of fertilizer were sealed in 

dialysis tubing and placed in each of two holes 30 cm 

deep, cored into the substrate on opposing sides of a tree 

beneath the outermost margin of its canopy, and sealed. 

Experiments at IRL and Twin Cays were fertilized twice 

per year. Because of limited access, the Bocas experiment 

was fertilized once per year. Thus, growth responses were 

normalized to the annual rate of fertilizer application. For 

controls, holes were cored and sealed but no fertilizer was 

added. Direct fertilizer application to the root zone of our 

target trees was used because all sites were fl ooded at high 

tides and fertilizer broadcasted on the surface would have 

washed away.

TREE GROWTH

To quantify growth, we measured the length of fi ve 

initially unbranched shoots in sunlit positions in the outer 

part of the canopy of each tree at the three locations. To 

compare growth responses among the three locations, 

we calculated the annual shoot elongation based on the 

amount fertilizer added per location (cm 	 year
1 kg
1).

LEAF NUTRIENT DYNAMICS

To determine the relative effects of nutrient overenrichment on the ability of R. mangle to conserve nutrients invested in foliage, we measured N, P, and potassium (K) concentrations in green and senescent leaves. 

For green leaves, we sampled the youngest, fully mature 

green leaves from penapical stem positions in sunlit portions of the canopy. Fully senescent yellow leaves with 

well-developed abscission layers were taken directly 

from the trees. Leaf area was determined with a LiCor 3000 Leaf Area Meter (Lincoln, Neb., USA). Leaf 

samples were dried at 70°C in a convection oven and 

ground in a Wiley Mill to pass through a 40 mesh (0.38 

mm) screen. Concentrations of carbon (C) and N were 

determined with a Model 440 CHN Elemental Analyzer 

(Exeter Analytical, North Chelmsford, Mass., USA) at 

the Smithsonian Environmental Research Center, Edgewater, Md. Concentrations of P and K were determined 

using an inductively coupled plasma spectrophotometer 

by Analytical Services, Pennsylvania State University, Pa. 

Nutrient concentrations expressed on a leaf area basis 

(mg 	 cm_

2) were used to calculate N, P, and K resorption 

effi ciencies (NRE, PRE, KRE), as below (Chapin and Van 

Cleve, 1989):

TABLE 3. Three-way factorial analysis of variance (ANOVA) results on the seven response variables: shoot elongation (Growth), N-, P-, 

and K-resorption effi ciencies (NRE, PRE, KRE), and N-, P-, and K-resorption profi ciencies (NRP, PRP, KRP). The kind of transformation conducted on response variables for normalization and homogeneity of variances is given in the second line of column headings. 

Results are in the form of F statistical values for each effect and the corresponding level of signifi cance: ***P  0.001; **P  0.01; 

*P  0.05; and for P  0.1.

 Growth NRE PRE KRE NRP PRP KRP

 Log(x) Exp(x) Exp(4x) Exp(x) Log(x) Log(1000x) Log(x)

Factor df F P F P F P F P F P F P F P

Location (L) 2 24.2 *** 28.6 *** 126 *** 16.5 *** 86.1 *** 373 *** 18.9 ***

Zone (Z) 1 0.11 65.2 *** 4.57 * 0.96 75.4 *** 0.29 5.18 *

Treatment (T) 2 23.4 *** 10.4 *** 75.4 *** 14.6 *** 40.3 *** 108 *** 36.8 ***

L  Z 2 12.0 *** 3.21 * 1.21 0.78 2.88 ~ 7.15 ** 1.98 

L  T 4 12.9 *** 4.37 ** 12.5 *** 5.60 *** 2.16 ~ 23.6 *** 8.13 ***

Z  T 2 17.8 *** 3.27 * 4.36 * 8.97 *** 4.77 ** 13.4 *** 25.0 ***

L  T  Z 4 4.9 ** 4.35 ** 1.30 4.27 ** 7.95 *** 4.21 ** 8.61 ***

 Residuals 140

resorption efficiency N, P, or K (mg cm =

− 	 2

)green leaf − −

−

N, P, or K (mg cm

N, P, or K (mg cm

	

	

2

2

)

)

senescent leaf

green leaf

×100

27_Feller_345-358_Lang.indd 349 7_Feller_345-358_Lang.indd 349 9/24/09 10:23/24/09 10:23
350 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

The absolute levels to which N, P, and K were reduced (% 

dry mass) in senesced leaves (indicated as %Nsenesced leaf, 

%Psenesced leaf, and %Ksenesced leaf, respectively) were used directly as indices of N, P, and K resorption profi ciencies 

(NRP, PRP, KRP), as below (Killingbeck, 1996):

resorption profi ciency  the level to which N, P, or K 

has been reduced in senescent leaves (% dry mass).

Note that low levels for %Nsenesced leaf, %Psenesced leaf, and 

%Ksenesced leaf are indicative of high resorption profi ciency 

whereas high levels indicate low resorption profi ciency. 

Concentrations less than 0.7% are considered complete 

resorption for N and concentrations less than 0.04% are 

considered complete resorption for P (Killingbeck, 1996). 

Higher values indicate incomplete resorption. In this study, 

we considered values less than 0.3% N and less than 0.01% 

P as the ultimate resorption potential for R. mangle, as 

proposed by Killingbeck (1996). Comparable values for K 

resorption potential have not been determined.

STATISTICS

Our data were grouped by nutrient treatment (Control, N, P)  zone (fringe, scrub)  location (IRL, 

Twin Cays, Bocas), to compare seven response variables 

of R. mangle, including growth responses, N-, P-, and 

K-resorption effi ciencies, and N-, P-, and K-resorption 

profi ciencies. Three-way factorial analyses of variance 

(ANOVA) were applied for each response variable. When 

an ANOVA found signifi cant effects, Tukey’s honestly signifi cant difference (HSD) tests were applied to examine 

pairwise differences within and among the treatment levels. To respect the assumptions of heterogeneity of variances and normality, the response variables were transformed using logarithms and exponentials. To investigate 

relationships between nutrient content of green and senescent leaves as well as among nutrient resorption profi ciencies, we used the Spearman rho () correlation test on the 

ranked row values. These analyses were conducted using 

the R software 2.7.0 (R Development Core Team, 2008).

RESULTS

TREE GROWTH

There was a signifi cant three-way interaction of nutrient enrichment  location  zone on growth rates of R. 

mangle trees (see Table 3; Figure 3). For control trees in the 

fringe zone, the rate of shoot elongation at IRL was signifi -

FIGURE 3. Rhizophora mangle growth (cm 	 year
1 	 kg
1) measured as elongation of individual shoots per year (normalized to fertilizer application at each site) at Indian River Lagoon (IRL), Twin Cays, and Bocas del Toro, in two zones (fringe, scrub), and in response to nutrient 

enrichment with nitrogen (N) or phosphorus (P). (IRL and Twin Cays data from Feller et al., 2003a, 2003b).

27_Feller_345-358_Lang.indd 350 7_Feller_345-358_Lang.indd 350 9/24/09 10:23/24/09 10:23
NUMBER 38 • 351

cantly lower than at Bocas (HSD adjusted P  0.001) but 

similar to those at Twin Cays (HSD adjusted P  0.070), 

which had similar values. There were no signifi cant differences in shoot elongation rates for control trees in the 

scrub zone among all the locations. N caused signifi cant 

increases in shoot elongation rates for fringe and scrub 

trees at IRL, but only for fringe trees at Twin Cays and Bocas. However, shoot elongation for N fringe trees in the 

IRL was lower than observed at Bocas (HSD adjusted P 

0.089). N caused similar increases in shoot elongation 

in the fringe at Bocas and Twin Cays. In the scrub zone, 

P increased growth at Twin Cays (HSD adjusted P 

0.001) and Bocas (HSD adjusted P  0.095), although 

the rates were much higher for Twin Cays (HSD adjusted 

P  0.047). P had no effect on growth in either fringe 

or scrub zones at IRL. The N treatment had no effect on 

growth rates in the scrub zones at Twin Cays and Bocas.

NUTRIENT CONSERVATION

The impact of fertilization on N-, P-, and K-resorption 

effi ciencies varied by location and zone (Figure 4a– c). For 

N-resorption effi ciency (NRE), there was a signifi cant 

three-way interaction among location, zone, and nutrient 

enrichment (see Table 3; Figure 4a). Values ranged from 

26% to 68%. In control trees at all locations, NRE was 

consistently highest for the fringe. At IRL, N caused a 

slight decline in values for fringe but not scrub trees. At 

Twin Cays, N had no effect on NRE in the fringe where 

growth was N limited. However, P caused an approximately 40% increase in NRE for the P-limited scrub trees 

(HSD adjusted P  0.001). Although N had no effect 

on the growth of scrub trees at Twin Cays, it did result in 

a slight increase in NRE. Overall, values for NRE were 

lowest at Bocas.

There were signifi cant two-way interactions among 

nutrient enrichment  location and nutrient enrichment 

 zone on P-resorption effi ciencies. However, the threeway interaction among nutrient enrichment  location 

zone was not signifi cant (see Table 3, PRE; Figure 4b). 

PRE values ranged from 36% to 80%. Overall, IRL had 

the lowest PRE. Here, values for control fringe and scrub 

trees were approximately half those at Twin Cays and Bocas where values were similar. N caused a slight increase 

in PRE for IRL fringe and scrub trees. At Twin Cays and 

Bocas, N had no effect in either zone, but P caused an 

approximately 50% decrease in PRE for scrub trees and 

an approximately 25% decrease for fringe trees.

For K-resorption effi ciency (KRE), we found a signifi -

cant three-way interaction of nutrient enrichment  location  zone (see Table 3; Figure 4c). In the IRL, values 

were uniformly low but positive in both zones, and nutrient enrichment had no effect. For control fringe trees at all 

locations, KRE was consistently positive. Overall, the lowest KRE values occurred at Twin Cays. The negative values for senescent foliage from control scrub trees at Twin 

Cays and Bocas indicated that K accumulated in leaves 

rather than being resorbed by the plant during senescence. 

At Twin Cays and Bocas, P caused a signifi cant increase 

in KRE by scrub trees, but had little effect on fringe trees. 

However, N had no signifi cant effect on KRE in either 

zone.

Fertilization also had striking and complex effects on 

resorption profi ciencies, measured as the %Nsenesced leaf, 

%Psenesced leaf, and %Ksenesced leaf, that varied by location and 

zone (Table 3; Figure 5a– c). Concentrations of N, P, and 

K in senesced leaves were positively associated with their 

concentrations in green leaves (Spearman values for N, P, 

and K  0.52, 0.87, and 0.65, respectively, all signifi cantly 

different than 0 with P  0.0001). There was no relationship between %Nsenesced leaf and %Psenesced leaf (Spearman 

 0.03, P  0.66), but %Ksenesced leaf was signifi cantly 

correlated with %Nsenesced leaf (Spearman  0.19, P 

0.02) and with %Psenesced leaf (Spearman  
0.43, P 

0.0001). For NRP, there was a signifi cant three-way interaction among location, zone, and nutrient enrichment 

(see Table 3; Figure 5a). The %Nsenesced leaf ranged from a 

low of 0.28% for P scrub trees at Twin Cays to a high 

of 0.91% in N fringe trees at Bocas. For control trees 

from the fringe and scrub zones, values were similar at 

IRL and Bocas but were signifi cantly lower at Twin Cays, 

which indicated increased NRP. N caused an increase of 

20% in %Nsenesced leaf from the fringe at IRL but had little 

effect on fringe trees at the other locations. In the scrub 

zone, N had no effect on %Nsenesced leaf at IRL and Twin 

Cays, but signifi cantly higher values at Bocas resulted in 

a decrease in NRP. P had little effect on either fringe or 

scrub zones at IRL and Bocas, but it caused a dramatic 

decrease in %Nsenesced leaf and a corresponding increase in 

NRP in scrub trees at Twin Cays.

We found the highest levels of %Psenesced leaf (0.06%) 

in the control trees in both zones at IRL, which indicated 

low PRP compared to Twin Cays and Bocas. Fertilization 

with N or P had no detectable effect on these levels at 

IRL (Figure 4b; all HSD adjusted P  0.5). Very low levels (0.01%) of %Psenesced leaf in both zones at Twin Cays 

and Bocas indicated high PRP in the range of maximal P 

resorption (Figure 6). N had no effect on values in either 

zone at Twin Cays or Bocas. P caused the most dramatic 

increase in %Psenesced leaf, with a concomitant decrease in 

27_Feller_345-358_Lang.indd 351 7_Feller_345-358_Lang.indd 351 9/24/09 10:23/24/09 10:23
352 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 4. Resorption effi ciencies for (a) nitrogen (N), (b) phosphorus (P), and (c) potassium (K) at Indian River Lagoon (IRL), Twin Cays, and 

Bocas del Toro (Bocas) in two zones (fringe  open bars, scrub  hatched bars), and in response to nutrient enrichment with nitrogen (N) or 

phosphorus (P). (IRL and Twin Cays data from Feller et al., 2003a, 2003b).

27_Feller_345-358_Lang.indd 352 7_Feller_345-358_Lang.indd 352 9/24/09 10:24/24/09 10:24
NUMBER 38 • 353

FIGURE 5. Resorption profi ciencies for (a) nitrogen, (b) phosphorus, and (c) potassium at Indian River Lagoon (IRL), Twin Cays, and Bocas 

del Toro (Bocas) in two zones (fringe, scrub), and in response to nutrient enrichment with nitrogen (N) or phosphorus (P).

27_Feller_345-358_Lang.indd 353 7_Feller_345-358_Lang.indd 353 9/24/09 10:24/24/09 10:24
354 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

PRP, for both the fringe and scrub zones at Twin Cays 

(both HSD adjusted P  0.001). At Bocas, there was a 

similar increase in %Psenesced leaf with P in the scrub zone 

(HSD adjusted P  0.001), whereas the response in the 

fringe zone was comparatively smaller and not signifi cant 

(HSD adjusted P  0.694).

There was also a signifi cant three-way interaction 

among location, zone, and nutrient enrichment on KRP 

(see Table 3; Figure 5c). Values for control trees in both 

zones at IRL and Bocas were similar with no differences 

between zones. Neither N nor P had any effect at IRL, 

but P caused a signifi cant decrease in %Ksenesced leaf in 

both zones at Bocas. The %Ksenesced leaf ranged from a low 

of 0.26% for P scrub trees at Bocas to a high of 1.56% 

in control scrub trees at Twin Cays, which was more than 

double the K concentrations in senescent foliage of fringe 

trees. In the Twin Cays scrub zone, P caused a fourfold 

decrease in %Ksenesced leaf, resulting in an associated increase 

in KRP.

DISCUSSION

Long-term fertilization experiments at IRL, Twin 

Cays, and Bocas del Toro demonstrated that these three 

locations, which were arrayed along a latitudinal gradient, 

were nutrient limited. However, system-specifi c attributes 

resulted in signifi cant differences in patterns of nutrient 

limitation and responses to fertilization. Although the 

mangrove ecosystems at these locations exhibited similar 

tree-height gradients dominated by Rhizophora mangle, 

they differed in several hydrogeomorphic and structural 

FIGURE 6. N-resorption profi ciency (%Nsenesced leaf) versus P-resorption profi ciency (%Psenesced leaf) for Rhizophora mangle by location (Indian River Lagoon [IRL], Twin Cays, Bocas del Toro), nutrient enrichment 

treatment level (control [], N [▫], P []), and intertidal zone (fringe [closed symbols] or scrub [open 

symbols]).

27_Feller_345-358_Lang.indd 354 7_Feller_345-358_Lang.indd 354 9/24/09 10:24/24/09 10:24
NUMBER 38 • 355

features (see Tables 1, 2). The locations also differed in 

substrate types; that is, the soil at IRL was composed of 

Pleistocene marine sands while the soils at Twin Cays and 

Bocas site were deep deposits (6– 12 m) of mangrove peat 

formed during the Holocene (Phillips and Bustin, 1996; 

Lovejoy, 1998; Macintyre et al., 2004). Our experimental 

site in the IRL was in a young forest, less than 40 years 

old, in an abandoned mosquito impoundment (Rey et 

al., 1986). In contrast, the experiments at Twin Cays and 

Bocas were in old-growth forests. Although no data are 

available for a direct comparison, it is likely that the forests at Bocas are older than at Twin Cays because of differences in their exposures to hurricanes (Stoddart, 1963; 

Carruthers et al., 2005). Overall, stem density was lowest 

at Twin Cays. Stem density in the IRL fringe was approximately 10 times greater than at Twin Cays and 4 times 

greater than at Bocas. On the other hand, the density of 

trees in the scrub forest was highest at Bocas.

Growth of R. mangle stems, which we used as a bioassay of nutrient limitation in our fertilization experiments, 

varied among IRL, Twin Cays, and Bocas. However, the 

responses did not support Hypothesis 1 of increasing P 

limitation toward the tropics (Vitousek, 1984; Vitousek 

and Sanford, 1986; Crews et al., 1995). This hypothesis 

predicted that P limitation would be greatest at Bocas, 

which was located at the lowest of the three latitudes compared in this study. Instead, shoot elongation indicated an 

order that ranged from N limitation in both fringe and 

scrub zones at IRL, to N limitation in fringe and scrub as 

well as P limitation in scrub at Bocas, and to N limitation 

in fringe and P limitation in scrub at Twin Cays. The magnitude of the growth responses to fertilization with the 

limiting nutrient at each location was also consistent with 

this order, that is, IRL  Bocas  Twin Cays, with the 

most severe P limitation and the greatest growth response 

to P fertilization in the scrub zone at Twin Cays.

The differences in growth responses that we observed 

at the three locations suggest that nutrient limitation 

within and among mangrove ecosystems is likely determined by several features of their geomorphology, including sediment/nutrient fl ux, tidal range, and substrate type. 

These fi ndings contrast with other studies that attribute P 

limitation in the tropics mainly to differences in the age 

of soils between tropical and temperate regions, with the 

most P-limited forests on the oldest soils (Vitousek, 1984; 

Vitousek and Sanford, 1986; Crews et al., 1995; Güsewell, 

2004; McGroddy et al., 2004; Reich and Oleksyn, 2004; 

Kerkhoff et al., 2005).

Based on fi ndings from Twin Cays (Feller, 1995; Feller 

et al., 2003a, 2007), McKee et al. (2002) hypothesized 

that the shift from N limitation in fringe zone around the 

periphery of the island to severe P limitation in scrub zone 

in the interior was the result of differences in factors associated with tidal fl ushing. Our results from the other 

two locations compared in this study partially support 

this hypothesis. Although all locations were N limited in 

the fringe, growth in the scrub zone at Bocas was limited 

by both N and P. This fi nding again differs from the IRL 

where growth was N limited in both zones (Feller et al., 

2003b). These patterns along tidal gradients indicate that 

differences in nutrient limitation among the three locations are the result of variations in tidal fl ushing, external 

nutrient supply, substrate, and endogenous biological processes. The scrub forests in the interior areas have a low 

tidal exchange and a low supply of exogenous nutrients, 

whereas the fringe zones are well fl ushed with a higher net 

exchange of nutrients. Mangroves at the IRL and Bocas 

locations are in continental settings with medium to high 

relief, freshwater infl ow, and nutrient fl ux. However, their 

tidal regimes and underlying soils differ dramatically. In 

contrast with IRL where mangroves are growing on sandy 

soils, mangroves at Twin Cays and Bocas are growing on 

peat. Although both of these locations are associated with 

low-nutrient coral reef ecosystems, Twin Cays receives 

negligible terrigenous inputs of freshwater or sediments 

whereas Bocas mangroves experiences a high fl ux of nutrients from several rivers draining into the archipelago. In 

addition, patterns of nutrient limitation in these systems 

may be affected by local patterns of N2 fi xation (Joye and 

Lee, 2004; Borgatti, 2008).

Resorption of phloem-mobile nutrients from leaves 

during senescence is an important nutrient conservation 

strategy for plants that infl uences many ecological processes, including primary production, nutrient uptake, 

competition, and nutrient cycling (Chapin, 1980). To 

resolve the relative degree to which latitude and nutrient enrichment affect the ability of R. mangle to conserve 

nutrients invested in foliage, we examined resorption of 

N, P, and K. Across location, zone, and nutrient treatment levels, our results indicate that a major control of 

the nutrient concentrations in senesced leaves was nutrient 

concentration in green leaves, which is consistent with a 

global dataset compiled by Kobe et al. (2005). Specifi cally, 

concentrations of N, P, and K in senesced leaves were positively associated with their concentrations in green leaves. 

In contrast to Oleksyn et al. (2003), who predicted that 

nutrient resorption effi ciencies should increase with latitude, we found the lowest effi ciencies at IRL, our northernmost location, consistent with Lovelock et al. (2007). 

We also found the most effi cient nutrient conservation for 

27_Feller_345-358_Lang.indd 355 7_Feller_345-358_Lang.indd 355 9/24/09 10:24/24/09 10:24
356 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

N and P at Twin Cays, the location positioned at the intermediate latitude. Although the levels to which nutrients 

were conserved varied by nutrient, location, and zone, the 

patterns did not fall clearly along a latitudinal gradient. 

All experimental trees at the three locations, except for the 

N trees in the scrub zone at Bocas, had less than 0.7% 

N concentrations in their senescent leaves, which is within 

the range of complete resorption in the model proposed by 

Killingbeck (1996) (see Figure 6). In the Twin Cays fringe 

and the P-fertilized scrub trees, the N concentration in 

senesced leaves was less than 0.3%, which was found to 

be the maximal level to which N can be reduced in senescent leaves of evergreen species and is regarded by Killingbeck (1996) as the ultimate potential resorption for N. In 

Killingbeck’s model, less than 0.04% Psenesced leaf represents 

complete resorption of P for evergreens. All experimental 

trees at Twin Cays and Bocas had values below this threshold and thus exhibited complete P resorption. Moreover, 

control and N trees in the scrub and fringe zones at Twin 

Cays and Bocas had 0.01% Psenesced leaf or less, which is the 

maximal level to which P can be reduced in senescent leaves 

in evergreens representing the ultimate potential resorption 

of P. Comparable levels of %Psenesced leaf have been reported 

for mangroves elsewhere (Alongi et al., 2005). In contrast, 

all the trees at IRL had values for Psenesced leaf greater than 

0.04%, which represents incomplete resorption. In contrast 

to suggestions by Aerts and Chapin (2000), the results presented here indicate there are nutritional controls on nutrient 

resorption in R. mangle. Nutrient enrichment clearly altered 

resorption of N and P at Twin Cays and Bocas but had no 

effect at IRL. Enrichment with P resulted in increases in N 

and K resorption effi ciency and profi ciency at Twin Cays and 

Bocas but had the opposite effect on P resorption. Similarly, 

N decreased N resorption, but only in the N-fertilized 

trees in the scrub zone at Bocas. These fi ndings suggest that 

P enrichment may have either increased the requirements for 

N and K in R. mangle or it may have increased its physiological capacity to conserve these nutrients during leaf senescence. Increased resorption of N and K in response to 

P may also indicate that under P-limiting conditions these 

nutrients become limiting when P is added to the system. 

Although we found no relationships between growth and N 

or P concentrations in green leaves, we did observe a weak 

but signifi cant relationship between %Kgreen leaf and growth 

rates (r  0.230, F  8.723, P  0.01). These results indicate that K availability may be important to the structure 

and function of some mangrove forests (Kathiresan et al., 

1994), which warrants further study.

In conclusion, our results indicate that nutrient overenrichment of the coastal zone will alter forest structure and 

nutrient dynamics in mangrove ecosystems. We showed that 

fertilization altered growth and nutrient conservation in R. 

mangle, but the patterns did not correspond with a latitudinal gradient. Growth was consistently N limited for trees 

in fringing forests, which have higher water exchange rates 

compared to scrub forests, supporting the hypothesis of 

Smith (1984) and McKee et al. (2002) that open systems are 

more likely to be N limited than P limited. In the IRL, scrub 

trees in the interior of the forest were also N limited. Patterns of nutrient limitation became more complex at lower 

latitudes. Phosphorus limitations characterized the scrub 

zone at Twin Cays whereas both N and P limitations were 

widespread in the scrub zone at Bocas. Our results clearly indicated that the phenotypic potential of R. mangle to resorb 

N, P, and K from senescing leaves varied as a function of 

nutrient availability, which was driven by differences in hydrology and substrate along latitudinal and tidal gradients.

ACKNOWLEDGMENTS

We thank the Governments of Belize and Panamá for 

permission to use study sites at Twin Cays and at Bocas 

del Toro; Klaus Rützler, Valerie Paul, and Rachel Collin 

for support and permission to work at the Smithsonian 

marine laboratories at Carrie Bow Cay, Fort Pierce, and 

Bocas del Toro; Michael Carpenter, Woody Lee, and Gabriel Jacome for logistical arrangements; Anne Chamberlain for assistance in the laboratory and in the fi eld. Financial support was provided by the Caribbean Coral Reef 

Ecosystems Program (CCRE), Smithsonian Institution; the 

Smithsonian Marine Station at Fort Pierce (SMSFP); and 

the National Science Foundation DEB-9981535. This is 

contribution number 842 of the CCRE, supported in part 

by the Hunterdon Oceanographic Research Fund, and 

SMSFP contribution no. 757.

LITERATURE CITED

Aerts, R., and F. S. Chapin III. 2000. The Mineral Nutrition of Wild 

Plants Revisited: A Re-Evaluation of Processes and Patterns. Advances in Ecological Research, 30:1– 67.

Alongi, D. M. 2002. Present State and Future of the World’s Mangrove 

Forests. Environmental Conservation, 29:331– 349.

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Underwater Spectral Energy Distribution 

and Seagrass Depth Limits along an Optical 

Water Quality Gradient

Charles L. Gallegos, W. Judson Kenworthy, 

Patrick D. Biber, and Bret S. Wolfe

ABSTRACT. We measured in situ inherent optical properties and seagrass maximum 

depth distribution in widely differing optical water types, including turbid green waters 

of the Indian River Lagoon (IRL, Florida, USA), a mix of turbid and clear waters in Panama, and very clear waters in Belize. We used Hydrolight to model in situ spectral energy 

distributions and measured leaf absorbance spectra (Thalassia testudinum) to distinguish 

between photosynthetically available radiation (PAR) and photosynthetically usable radiation (PUR). Attenuation coeffi cients for PAR and PUR were nearly indistinguishable 

in Belize and Panama and differed only slightly in the IRL. Grass grew to depths of penetration of 33% of PAR in the IRL, 14% in Panama, and approximately 5% in Belize, 

although we expect the value for Belize is an underestimate because conditions more 

turbid than are typical were prevailing at the time of the measurements. Corresponding 

percentages for PUR were 27%, 12%, and 5% for IRL, Panama, and Belize, respectively. 

These regional differences in light requirements were striking, and less than half of the 

difference could be attributed to latitudinal variations in incident light. We conclude that 

factors other than spectral energy distribution that covary with water clarity control 

site-specifi c light requirements of seagrasses. Possibilities include epiphytes and sediment 

quality.

INTRODUCTION

Seagrasses are important primary producers that play a role in the stability, 

nursery function, biogeochemical cycling, and trophodynamics of many coastal 

and estuarine ecosystems and as such are important for sustaining a broad spectrum of organisms (Hemminga and Duarte, 2000). Seagrasses are potentially 

sensitive indicators of declining water quality because of their high light requirements (11%– 37% surface irradiance) compared to those of other aquatic 

primary producers with much lower light requirements (1%) (Dennison et 

al., 1993; Zimmerman, 2003). Seagrass communities have declined in coastal 

regions worldwide (Orth et al., 2006), which is usually attributed to reductions 

in water clarity brought about, at least initially, by accelerated eutrophication in 

the coastal zone (Krause-Jensen et al., 2008).

Management efforts aimed at preserving and restoring seagrass systems generally focus on improving water clarity (Batiuk et al., 2000; Kenworthy and 

Haunert, 1991; Steward and Green, 2007), based on the high light requirements 

Charles L. Gallegos, Smithsonian Environmental 

Research Center, 647 Contees Wharf Road, Edgewater, Maryland 21037, USA. W. Judson Kenworthy, Center for Coastal Fisheries and Habitat 

Research, NCCOS, National Oceanic and Atmospheric Administration, 101 Pivers Island Road, 

Beaufort, North Carolina 28516, USA. Patrick 

D. Biber, Department of Coastal Sciences, The 

University of Southern Mississippi, Gulf Coast Research Laboratory, 703 East Beach Drive, Ocean 

Springs, Mississippi 39564, USA. Bret S. Wolfe, 

Department of Environmental Science, University of Virginia, Clark Hall, 291 McCormick 

Rd., Charlottesville, Virginia 22904, USA. Corresponding author: C. Gallegos (gallegosc@si.edu). 

Manuscript received 23 July 2008; accepted 20 

April 2009.

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360 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of seagrasses and the reduction in light penetration associated with eutrophication (Ralph et al., 2007). Deciding 

on the extent of water quality improvements (or limit of 

allowable deterioration) requires more detailed knowledge of the wavelength-specifi c light requirements of seagrasses. Based on a survey of available literature, Carter 

et al. (2000) determined that mesohaline and polyhaline 

submerged grass communities in Chesapeake Bay require 

a long-term average of 22% of surface irradiance at the 

deep edge of the grass meadow for survival. Gallegos and 

Kenworthy (1996) determined a similar requirement for 

mixed beds of Thalassia testudinum, Halodule wrightii, 

and Syringodium fi liforme in the Indian River Lagoon 

(IRL) near Ft. Pierce, Florida. In contrast, Steward et al. 

(2005) found 20% to be near the minimum for the IRL, 

while the average light requirement was 33% of annual 

incident irradiance, similar to the wide range (24%– 37%) 

reported for the southern Indian River Lagoon (Kenworthy 

and Fonseca, 1996). More recently, Duarte et al. (2007) 

analyzed 424 reports of seagrass colonization depths and 

light attenuation and found generally higher light requirements for plant communities growing in shallow, turbid 

waters than in clear, deep waters. The authors suggested 

that large differences in light requirements between shallow- and deep-growing seagrasses may be partially attributed to differences in the quality of light. Seagrasses may 

grow deeper in clear water because there is more highenergy blue light available for photosynthesis, whereas 

in shallow turbid water the shorter blue wavelengths are 

rapidly attenuated.

The wavelength specifi city of light absorption by 

seagrasses has implications for setting water quality requirements needed to protect or restore these plants in 

eutrophic waters that are dominated by ineffi cient green 

wavelengths. The absorption of light by the complement of 

pigments (chlorophyll a and chlorophyll b) in seagrasses is 

highly wavelength selective, with absorption peaks in the 

blue (centered around 450 nm) and red (centered around 

670 nm) regions of the visible spectrum, and a broad absorption minimum in the green between 500 and 600 nm 

(Drake et al., 2003; Zimmerman, 2003). Wavelengths of 

light that are poorly absorbed by the plant are relatively 

ineffi cient at driving photosynthesis (Drake et al., 2003; 

Falkowski and Raven, 2007).

Light requirements of seagrasses that have been determined to date (Batiuk et al., 2000; Kenworthy and 

Fonseca, 1996) have been based on photosynthetically 

available radiation (PAR, 400– 700 nm) because of the 

widespread availability of underwater quantum sensors. 

PAR measurements weight quanta of all visible wavelengths equally. By contrast, measurements of photosynthetically usable radiation (i.e., PUR; see Morel, 1978) 

weight quanta in proportion to the effi ciency with which 

they are absorbed. There are no sensors for direct measurement of PUR; it must be calculated from the underwater spectrum (measured or modeled) weighted by the 

relative absorption spectrum of the plant of interest.

Using a bio-optical model of light penetration in the 

mesohaline Chesapeake Bay, Gallegos (1994) determined 

that the 22% surface PAR requirement for seagrasses occurred at the same depth as the penetration of 16% of surface PUR. The distinction is potentially important because 

the penetration of PUR is more sensitive to the concentration of phytoplankton chlorophyll (i.e., eutrophication) 

than is the penetration of PAR, for the reason that phytoplankton chlorophyll absorption selectively removes those 

same wavelengths most effi ciently used in photosynthesis 

by seagrass. Thus, by basing light requirements on PUR 

rather than on PAR, we would predict greater restoration 

benefi t from chlorophyll reduction, and greater seagrass 

losses from chlorophyll increases, than by light requirements based on PAR (Gallegos, 1994).

The objective of this work was to determine whether 

the distinction between PAR and PUR requirements 

could be determined from in situ depth distributions of 

seagrass communities. The distinction cannot be drawn 

from depth distributions at a single site such as Chesapeake Bay or the IRL, because within these systems the 

underwater spectrum is peaked in the green, and thus 

there is insuffi cient spectral variability in available light 

to differentiate between depth limits based on PAR compared with PUR. The gradient of optical water quality 

types across locations of the Smithsonian Marine Science 

Network, however, offers a potentially ideal scenario 

for making this determination. All three of the dominant seagrass species found in the IRL also occur in the 

tropical waters of Carrie Bow Cay, Belize, and Bocas del 

Toro, Panama. In optically clear waters, the underwater 

spectrum peaks in the blue, near an absorption peak of 

chlorophyll a or b. In blue water, therefore, PUR penetrates deeper than PAR, and plants should grow to relatively deeper depths in blue tropical waters if PUR rather 

than PAR is the determining factor. To investigate this 

distinction, we surveyed seagrass distributions and measured inherent optical properties (IOPs), from which we 

calculated underwater light spectra at the deep edges of 

grass beds, to test the hypothesis that across the optical 

water quality gradient seagrass would grow to a consistent depth of penetration of PUR but a variable percentage of PAR.

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NUMBER 38 • 361

METHODS

STUDY SITES

Station locations are shown in Figure 1. We occupied 

stations in the clear tropical waters off Carrie Bow Cay, 

Belize (station Blue Ground Range, BGR), and in Bahia 

Almirante, Panama (station STRI [Smithsonian Tropical 

Research Institute]), a station receiving colored-water discharge from a nearby creek in Panama (station SN03), and 

the more eutrophic waters of the Indian River Lagoon, 

Florida (ICW194; see Figure 1). Detailed characteristics 

of these sites are given by Lang (2009) in the Introduction 

to this volume.

OPTICAL PROPERTIES

We measured in situ profi les of IOPs, the spectral absorption and beam attenuation coeffi cients, at nine wavelengths (412, 440, 488, 510, 532, 555, 650, and 715 nm) 

using a WETLabs ac-9 instrument with a 0.1 m pathlength, equipped with a pressure sensor to measure depth. 

A Seabird SBE-5T pump provided water fl ow to the ac-9 

and a WETLabs MPAK unit that controlled pump and instruments and logged data.

Measured absorption and beam attenuation coeffi cients were corrected for temperature according to the 

manufacturer’s protocols. We corrected absorption coeffi -

cients for scattering errors (Kirk, 1992) by the Zaneveld et 

al. (1994) algorithm that subtracts a fraction of measured 

scattering coeffi cient from absorption (Equation 1):

aaca tw m tw m − − ( ) ( ) ( ( ) ( )) λλ λλ =− −  (1)

where at– w() is the scattering-corrected absorption coeffi cient less pure water absorption at wavelength , am is 

the measured non-water absorption coeffi cient subject to 

scattering error, ct– w is the measured non-water beam attenuation coeffi cient, and  is a coeffi cient that accounts 

FIGURE 1. Locations of stations in the Indian River Lagoon, Florida (upper left), Belize (upper right), and 

Panama (lower right). Lower left panel shows overview of Caribbean. Light gray shading in Belize panel 

indicates coral reef habitat.

28_Gallegos_359-368_Lang.indd 361 8_Gallegos_359-368_Lang.indd 361 9/24/09 10:00/24/09 10:00
362 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

for overall errors with the refl ective tube absorption meter 

of the ac-9 that result from a failure to collect all scattered 

light (Kirk, 1992). In this work we verifi ed the assumption 

that non-water absorption at the longest ac-9 wavelength 

(715 nm) was not measurable in the laboratory (Tzortziou 

et al., 2006). Thus, we calculated  by Equation 2:

 = − −

a

c a

m

tw m

( )

() ()

715

715 715 (2)

We measured the absorption spectrum of Thalassia 

testudinum leaves in an integrating sphere (LICOR 1800-

12S) interfaced to an Ocean Optics USB2000 spectrometer. A clean segment of leaf was placed on a microscope 

slide over the opening to the sphere and illuminated with 

a fi beroptic microscope light source. Black tape on the 

slide obscured the portion of the opening not covered 

by the leaf. Percent transmittance (%T) of the leaf was 

calculated referenced to the slide and tape without a leaf 

in place. Absorbance was calculated as ln(%T), and 

the spectrum was normalized to the value at the absorption peak at 675 nm. Measurements on eight leaves collected from the deep edge at the site in Belize were averaged. Similar measurements made in Panama had similar 

results.

RADIATIVE TRANSFER MODELING

To calculate spectral diffuse attenuation coeffi cients 

and underwater light spectra, we used the commercially 

available radiative transfer model, Hydrolight 4.2, which 

is extensively documented by Mobley (1994). User input consists of specifi cations for IOPs, boundary conditions, and assumptions on inelastic scattering processes. 

We used the pure-water absorption coeffi cients of Pope 

and Fry (1997) and pure-water scattering coeffi cients for 

freshwater from Buiteveld et al. (1994). We used in situ 

estimates of absorption, attenuation, and scattering coeffi cients binned at 0.5 m intervals. Following Tzortziou et 

al. (2006), we used the Fournier– Forand scattering-phase 

function, the shape of which was shown by Mobley et al. 

(2002) to be well specifi ed by the backscattering ratio. We 

omitted inelastic scattering processes because our interest 

is in downwelling irradiance, and these processes primarily affect only calculations of upwelling radiance. For incident irradiance and the distribution of total irradiance 

between direct and sky irradiance we used the built-in 

RADTRAN routine for the time, location, and estimate of 

approximate cloud cover.

From the simulations of spectral downwelling irradiance we calculated PAR according to its defi nition 

(Equation 3):

PAR z Q z d E z

h d d () (, ) (,) = = ∫ ∫ l l lh

l

400

700

400

700

 (3)

where Q is the quantum fl ux, Ed is the spectral downwelling irradiance in energy units, h is Planck’s constant, l

is the wavelength and h  2c/ l is the frequency of light, 

and c is the speed of light in vacuum. PUR was calculated 

in an analogous manner, weighted by the plant absorption 

spectrum, measured at the deep edge of the Belize site:

PUR z Q z a d Th () (, ) () = ∫ l ll 

400

700

(4)

where ãTh (l) is the absorption spectrum of T. testudinum 

normalized to its peak at 675 nm and to unit sum. For 

comparison of attenuation rates, PAR and PUR were both 

normalized to their values at the surface. 

SEAGRASS SURVEYS

At each sampling site a pair of scuba divers entered 

the water to visually confi rm the seagrass bed (T. testudinum) deep edge, defi ned as the visible transition between 

vegetated and unvegetated bottom. Once the physical 

boundaries of the meadow edges were identifi ed underwater, the divers laid out two 10 m long transects parallel to the edge of the seagrass bed. At 1.0 m intervals 

along each transect, the divers visually estimated seagrass 

cover in a 0.25 m2 quadrat using the Braun-Blanquet scale 

(1965). The Braun-Blanquet cover abundance scale is a visual assessment technique for estimating the canopy cover. 

Values are 0.1  solitary shoot, with small cover; 0.5 

few shoots, with small cover; 1  numerous, but less than 

5% cover, 2  5%– 25% cover, 3  25%– 50% cover, 4 

50%– 75% cover, and 5  more than 75% cover.

At the same location each diver counted the number 

of seagrass short shoots in either a 0.25 m2 or 0.0625 m2

quadrat, depending on the shoot density. Short shoot 

counts were multiplied by the appropriate scaling factor 

and averaged for the 10 quadrats to obtain an estimate 

of the number of short shoots per square meter. For comparison of deep edge seagrass characteristics, we also surveyed relatively shallow sites at the Blue Ground Range 

station in Belize (2.4 m) and the STRI station in Panama 

(1.8 m). At SN03 in Panama we only surveyed at the deep 

28_Gallegos_359-368_Lang.indd 362 8_Gallegos_359-368_Lang.indd 362 9/24/09 10:00/24/09 10:00
NUMBER 38 • 363

edge. Deep edge data for the IRL are from annual surveys by the South Florida Water Management District 

(http://my.sfwmd.gov/gisapps/sfwmdxwebdc/dataview

.asp?queryunq_id1797).

RESULTS

SEAGRASS DEPTH LIMITS

At the Blue Ground Range station in Belize, the deep 

edge of the Thalassia testudinum meadow was located at 

10– 11 m. The deep edge was a distinct transition from 

a sparse cover of T. testudinum to unvegetated, fi ne carbonate mud. Recently germinated seedlings of the small 

opportunistic species Halophila decipiens were observed 

just outside of the deep edge of the T. testudinum meadow. 

Braun-Blanquet cover values ranged from 0.5 (a few individual short shoots) to 1 (5%). Thalassia testudinum

short shoot densities ranged from 0 to 48 shoots m2, 

averaging 22.4 shoots m2. At the shallow Blue Ground 

Range transect, T. testudinum Braun-Blanquet scores 

ranged from 3 to 4, indicating that cover generally varied 

from 25% to 75%, while densities ranged from 176 to 

416 shoots m2, averaging 310 shoots m2. At the shallow station T. testudinum was 14 times more dense than 

at the deep edge. No other seagrass species were observed 

at this station.

At the STRI station in Panama we located the deep 

edge of the T. testudinum at 8.5 m. The transition edge 

of the T. testudinum meadow was distinct; however, there 

was considerably more H. decipiens just downslope of the 

edge than there was at the Blue Ground Station in Belize. 

Thalassia testudinum short shoot densities ranged from 

0 to 56 shoots m2, averaging 18 shoots m2, similar to 

the deep edge at the Blue Ground Range Station in Belize. Braun-Blanquet values ranged from 0 to 1, indicating 

that cover was generally less than 5%. We also observed 

three quadrats with a relatively sparse cover of Halodule 

wrightii. At the shallow STRI station (1.8 m), T. testudinum densities ranged from 160 to 528 shoots m2 with 

an average of 465, 25 times the density at the deep edge 

and more dense than the shallow station at Blue Ground 

Range in Belize. Braun-Blanquet values ranged from 3 to 

4, similar to the shallow station at Blue Ground Range 

(BGR) in Belize.

At the SN03 site in Panama, the deep edge of the T. 

testudinum bed was located at 2.4 m. Short shoot densities ranged from 0 to 288 m2, with a mean value of 114. 

The deep edge of the T. testudinum meadow was marked 

by a transition from T. testudinum to unvegetated sediment. Braun-Blanquet scores ranged from 0 to 3, indicating cover values less than 50%.

Seagrass depth limits in the IRL at the site where optical measurements were made in 2001 were reported as 

0.92 m for beds described as continuous and dense, with a 

lower limit of 50% to 60% cover.

OPTICAL PROPERTIES

A wide range of optical properties was observed 

among the four sites (Figure 2a). Based on absorption 

spectra, Belize had the clearest water while the most turbid water occurred in the IRL. The two sites in Panama 

were intermediate. The rank order of sites was different 

for scattering coeffi cients (Figure 2b), with scattering coeffi cients at the Panama shallow site (SN03) being the highest and the Panama deep site (STRI) the lowest.

ABSORPTION SPECTRUM

Normalized absorption by T. testudinum was similar to measurements by other investigators (Zimmerman, 

2003), having peaks in the red wavelengths (680 nm), a 

broad maximum at blue wavelengths (400– 490 nm), and 

a trough at green wavelengths (525– 625 nm) (Figure 3, 

solid line). This spectrum was used to calculate PUR from 

simulated downwelling spectral irradiance according to 

Equation 4. However, even at the local minimum at 555 

nm, measured absorption was still 37% of the red peak. 

On considering that T. testudinum has no chlorophyll pigments that absorb green wavelengths (Zimmerman, 2003), 

we also constructed a hypothetical photosynthetic action 

spectrum based on chlorophyll absorption alone, consisting 

of Gaussian curves with peaks at 410, 430, 455, 642, and 

680 nm for an alternate calculation of PUR (see Figure 3, 

dashed line). The hypothetical action spectrum is expected 

to produce the maximal separation between PAR and PUR, 

especially in turbid green water, because the trough in the 

hypothetical chlorophyll absorption spectrum at green 

wavelengths is much more pronounced compared with the 

measured absorption spectrum, which includes an unquantifi ed contribution by photosynthetic carotenoids. This hypothetical chlorophyll-based action spectrum serves as a 

site-independent sensitivity test for the greatest possible 

difference between PAR and PUR for a higher plant. We 

did not measure absorption spectra in the IRL, so they are 

unknown. The hypothetical spectrum allows a comparison 

among sites in the absence of measurements at all sites.

28_Gallegos_359-368_Lang.indd 363 8_Gallegos_359-368_Lang.indd 363 9/24/09 10:00/24/09 10:00
364 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

PAR AND PUR PROFILES

Profi les of normalized downwelling PAR and PUR 

based on the measured absorption spectrum (PURm) and 

PUR based on the hypothetical action spectrum (PURh) 

are shown for the stations having the least and the most 

separation between PAR and PUR in Figure 4. The diffuse attenuation coeffi cients for each of the three quantities are reported for all stations in Table 1. At the Blue 

Ground Range station in Belize, diffuse attenuation coeffi cients for PAR and PURm were indistinguishable, while 

that for PURh was only 7% higher than for PAR (Table 1). 

The largest differences among the three attenuation coeffi cients occurred at the IRL. The relative differences between attenuation coeffi cients for PAR and PURm (13%) 

and between PAR and PURh (31%) were similar for the 

IRL and SN03 site in Panama, although the absolute coeffi cients were smaller at SN03 (Table 1).

The percentages of surface light remaining at the deep 

edges of the seagrass beds varied widely among the locations, from about 5% at the Blue Ground Range site in 

Belize to about 30% at the IRL (see Table 1). The percentages based on PUR were, as expected, lower than those 

based on PAR, but the differences among sites was still 

large (Table 1). Because of the extremely large differences 

among sites in the percentage of light at the seagrass bed 

deep edge, the calculation of PUR did not yield a consistent value across sites. The overall range was, however, 

somewhat smaller for PUR than for PAR (Table 1). Spectra of downwelling irradiance at the deep edges calculated 

by Hydrolight are shown in Figure 5. The overall fraction of surface irradiance remaining at the deep edges at 

the different locations follows the percentages in Table 1. 

Qualitative differences in the spectra of light remaining at 

FIGURE 2. Surface water absorption spectra (a) and surface water 

scattering spectra (b) at sites sampled in Belize, Panama, and Florida.

FIGURE 3. Normalized absorption spectra used for calculating photosynthetically usable radiation, based on absorption spectrum measured on Thalassia testudinum leaves (solid line), and a hypothetical 

action spectrum derived by assuming only light absorbed by chlorophylls a and b drive photosynthesis in Thalassia (dashed line).

28_Gallegos_359-368_Lang.indd 364 8_Gallegos_359-368_Lang.indd 364 9/24/09 10:00/24/09 10:00
NUMBER 38 • 365

the deep edges also occur. Because of absorption by water, 

virtually no light is present at wavelengths greater than 

600 nm at the BGR location in Belize and very little at 

STRI in Panama. Increasing amounts of red wavelengths 

are present at the SN03 and IRL sites as a result of the 

shallower depths of the deep edges. The peaks of the in 

situ spectra shift progressively toward green wavelengths 

along the progression from BGR to IRL, and the greatest 

similarities are at 400 to 410 nm, where the percentage of 

surface irradiance remaining ranges from 2% to 6%.

DISCUSSION

At all three study sites we were able to locate a distinct 

deep edge of the Thalassia testudinum meadows, characterized by a transition from moderate and sparsely vegetated seagrass to either unvegetated substrate or patches 

of the smaller, low light adapted seagrass Halophila decipiens. Where we were able to sample shallower sites in 

Belize and Panama, there were substantially higher densities of T. testudinum. The presence of H. decipiens at the 

Blue Ground Range (BGR) station in Belize and the STRI 

site in Panama further confi rmed that we were sampling 

at light-limiting edges of the T. testudinum distribution. 

Halophila decipiens is a small, ruderal species of seagrass 

commonly found growing in deep or turbid water and has 

lower light requirements than T. testudinum (Kenworthy, 2000; Gallegos and Kenworthy, 1996; Kenworthy 

et al., 1989). The presence of H. decipiens at these two 

stations was a good indication of light-limiting conditions 

for Thalassia. Although we did not record H. decipiens at 

SN03 in Panama, a thorough visual examination by divers 

at deeper depths than the observed T. testudinum distribution confi rmed there were no seagrasses growing beyond 

2.4 m depth.

Attenuation coeffi cients for PAR and PUR were nearly 

indistinguishable in Belize and Panama and differed only 

slightly in the IRL. Based on these one-time profi les, we 

calculated that seagrass grew to depths of penetration of 

FIGURE 4. Vertical profi les of photosynthetically active radiation 

(PAR, solid line), and photosynthetically usable radiation (PUR) 

based on measured absorption spectrum (PURm; dashed line) and 

hypothetical action spectrum (PURh; dotted line) in (a) Belize and 

(b) the Indian River Lagoon (IRL), Florida. Profi les were normalized to the irradiance incident at the surface (100%).

TABLE 1. Depths of seagrass deep edge (Zmax) and attenuation 

coeffi cients for photosynthetically active radiation (KPAR) and 

photosynthetically usable radiation (PUR) weighted by measured 

absorption spectrum of Thalassia testudinum leaves (KPURm) or 

weighted by a hypothetical action spectrum (KPURh; see Figure 2). 

Percentage of surface light penetrating to the seagrass deep edge 

is given in parentheses.

 Zmax KPAR KPURm KPURh

Site a (m) (m1) (m1) (m1)

BGR, Belize 10 0.293 0.293 0.314

 (5.2%) (5.4%) (4.2%)

STRI, Panama 8.5 0.232 0.247 0.304

 (13.6%) (12.0%) (7.4%)

SN03, Panama 2.4 0.836 0.945 1.098

 (14.1%) (11.0%) (7.7%)

IRL, Florida 0.92 1.157 1.301 1.52

 (32.7%) (27.1%) (21.8%)

a BGR, Blue Ground Range; STRI, Smithsonian Tropical Research Institute; SN03, 

Panama creek station; IRL, Indian River Lagoon.

28_Gallegos_359-368_Lang.indd 365 8_Gallegos_359-368_Lang.indd 365 9/24/09 10:01/24/09 10:01
366 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

33% of PAR in the IRL, 14% in Panama, and approximately 5% in Belize. Corresponding percentages for PUR 

were 27%, 12%, and 5% for IRL, Panama, and Belize, 

respectively. The accuracy of these estimates depends on 

the degree to which the profi les were measured under 

conditions that are typical for their respective growing 

seasons. We are fairly certain this was not the case in 

Belize, where strong northerly winds, atypical for the 

season, blew for several days before and on the day of 

sampling. Horizontally sighted Secchi disk visibility at a 

seagrass bed near Twin Cays was 5.5 m during the time 

of our measurements, compared with annual means of 

10.1 m (0.38 m SE) for 2004 and 8.9 m (0.25 m SE) 

for 2005 (see Koltes and Opishinski, 2009: fi g. 6, this 

volume). If the water column were more strongly stirred 

with higher than typical concentrations of particulate 

matter, then our estimates for Belize would be biased low, 

as we suspect they are. The estimated PAR light requirements for the IRL are, however, based on more frequent 

visits and are in agreement with other published estimates 

(Kenworthy and Fonseca, 1996; Steward et al., 2005). The 

limitation of our approach was the inability to determine 

the integral of light requirements for the whole growing 

season from only a few days of measurements. Because of 

this limitation, it is unlikely that the observed depth distribution of the seagrasses is fully captured by PAR and PUR 

percentages calculated, and repeating this study during another season could yield different percentages.

Nonetheless, assuming that the light requirements for 

seagrasses at Belize are similar to those in Panama, the 

regional differences in light requirements between the IRL 

and the two tropical sites remain striking. Qualitatively, 

the differences are consistent with the observations of 

Duarte et al. (2007) that seagrasses growing in shallow, 

turbid waters (e.g., IRL) have higher light requirements 

than those growing in clear, deep water (Panama, Belize). 

Calculation of PUR closed the gap only slightly, leading 

us to conclude that factors other than spectral energy distribution contribute substantially to site-specifi c light requirements of seagrasses, especially at the deep edges. An 

extended growing season in the more tropical locations of 

Belize and Panama could possibly account for some of the 

difference. The tropical sites receive about 7% more incident radiation annually than the IRL site, most of which 

occurs during winter months (November through February) when temperatures are also more favorable in the 

tropics. Other possible differences between sites include 

leaf-shading epiphytes, sediment quality (e.g., grain size 

or organic matter content), and possible periods of low 

oxygen in thermally stratifi ed deeper waters. These latter 

factors have management implications because they are all 

affected by coastal eutrophication. Improved understanding of the factors accounting for site-specifi c differences in 

seagrass light requirements is, therefore, urgently needed.

ACKNOWLEDGMENTS

We gratefully acknowledge the Smithsonian Marine Science Network for Pilot Project funds to conduct these studies. We thank Sam Benson for diving assistance in Belize and 

Amy Lewis for help with optical data reduction and analysis. This is contribution no. 844 of the Caribbean Coral Reef 

Ecosystem Program (CCRE), supported in part by the Hunterdon Oceanographic Research Fund, and Smithsonian Marine Station at Fort Pierce contribution no. 787.

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/24/09 10:01
Interannual Variation in Gelatinous 

Zooplankton and Their Prey 

in the Rhode River, Maryland

Eileen S. Graham, Danielle M. Tuzzolino, 

Rebecca B. Burrell, and Denise L. Breitburg

ABSTRACT. The lobate ctenophore Mnemiopsis leidyi is an important predator of 

zooplankton and ichthyoplankton both within and outside its native range, and it is a 

dominant consumer within the Chesapeake Bay food web. We sampled the Rhode River, 

a subestuary of Chesapeake Bay, during 2004 and 2005 to quantify the abundances of 

M. leidyi, its scyphomedusan predators, and its mesozooplankton prey, and conducted 

ctenophore egg production experiments in 2004. Despite low mesozooplankton densities, 

ctenophores produced up to 9,380 eggs individual1 day1. Temporal patterns, as well as 

peak abundances, of copepods, ctenophores, and sea nettles (Chrysaora quinquecirrha; 

the major predator of M. leidyi) varied considerably between years. This interannual variation may have been caused by direct and indirect effects of physical factors, especially 

low salinities during 2004, on all components of the food web. In 2004, zooplankton 

abundances peaked in June, M. leidyi abundances steadily increased throughout the summer, and C. quinquecirrha was rare. In contrast, during 2005, C. quinquecirrha density 

increased during midsummer. As this medusa increased in abundance, M. leidyi numbers 

declined and copepod abundances increased. Shallow systems with salinities near the 

minimum threshold for C. quinquecirrha ephyra production may exhibit more extreme 

interannual variability than deeper, higher-salinity systems and may serve as models to 

provide insight into factors controlling gelatinous zooplankton dynamics.

INTRODUCTION

The lobate ctenophore Mnemiopsis leidyi is native to Atlantic and Caribbean estuaries and coastal waters from Massachusetts to southern Argentina 

and has been introduced to several Eurasian systems including the Black, Caspian, Baltic, and North Seas (Purcell et al., 2001; Kube et al., 2007). Mnemiopsis leidyi can tolerate a wide range of temperatures, salinities, and dissolved 

oxygen (DO) concentrations. It occurs in waters with salinities ranging from less 

than 5 to more than 36 (Purcell et al., 2001; Purcell and Decker, 2005) and can 

survive exposure to DO concentrations of 0.5 mg L1 for at least 4 d (Decker et 

al., 2004). Optimal temperatures for M. leidyi reproduction are approximately 

18°– 20°C (Costello et al., 2006).

In late spring and early summer, M. leidyi can be abundant in Chesapeake 

Bay and its tributaries, where it is a dominant consumer, potentially capable of 

clearing much of the daily standing stock of zooplankton and ichthyoplankton 

Eileen S. Graham, Danielle M. Tuzzolino, Rebecca B. Burrell, and Denise L. Breitburg, Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, Maryland 21037, 

USA. (Current addresses: E. Graham, Applied 

Science Associates, Inc., 55 Village Square Drive, 

Wakefi eld, Rhode Island 02879, USA. D. Tuzzolino, University of Delaware, College of Marine 

and Earth Studies, 111 Robinson Hall, Newark, 

Delaware 19716, USA.) Corresponding author: 

D. Breitburg (breitburgd@si.edu). Manuscript received 29 August 2008; accepted 20 June 2009.

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370 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

(Cowan et al., 1992; Cowan and Houde, 1993; Purcell et 

al., 1994; Purcell and Decker, 2005). In mesohaline portions of the Chesapeake Bay system, the major predator 

of M. leidyi, the scyphomedusa Chrysaora quinquecirrha, usually becomes abundant in early July and persists 

through the end of summer (Cargo and King, 1990). As 

C. quinquecirrha population densities increase, M. leidyi

abundances typically decline and zooplankton populations rebound (Purcell and Cowan, 1995). However, in 

years when C. quinquecirrha populations are low, M. 

leidyi may exert much greater and prolonged control 

within the food web. Chrysaora quinquecirrha polyps 

are generally found in salinities of 7 to 20 and strobilate when temperatures exceed 17°C (Cargo and Schultz, 

1967; Cargo and King, 1990). Medusae are most abundant at salinities of 10– 16 (using the Practical Salinity 

Scale) and temperatures of 26°– 30°C (Decker et al., 

2007). Thus, interannual variation in salinity and temperature can strongly affect the timing and spatial distribution of C. quinquecirrha and its control of M. leidyi.

The Rhode River is a small, shallow subestuary on 

the western shore of Chesapeake Bay (Figure 1) characterized by summer salinities that vary interannually in 

both absolute maxima and timing of these maxima. Similar to other tributaries in the Chesapeake Bay system, 

this estuary supports a gelatinous zooplankton food web 

throughout late spring and summer months. The most 

abundant gelatinous species are the zooplanktivorous 

M. leidyi and its scyphomedusan predator and competitor C. quinquecirrha. Average spring– summer salinity 

in the Rhode River is near the lower limit required for 

strobilation by C. quinquecirrha. In addition, interannual variation in water temperature has the potential 

to cause variation in the timing of initial and peak occurrences of these gelatinous species and their prey. As a 

result, the Rhode River can have two distinct gelatinous 

food webs: one in which the top predator (C. quinquecirrha) exerts control over the intermediate consumer (M. 

leidyi) and one in which the intermediate consumer is not 

controlled by predation.

The objectives of this study were to examine temporal and spatial patterns in abundances of M. leidyi and 

C. quinquecirrha within and near the Rhode River and 

to examine how those patterns varied in relationship to 

water temperature, salinity, and the abundance of mesozooplankton prey. We also examined temporal and spatial 

variation in egg production by M. leidyi. This study was 

conducted during the summers of 2004 and 2005, years 

with very different temporal patterns of M. leidyi and C. 

quinquecirrha densities.

FIGURE 1. The Rhode River and its location in the Chesapeake Bay. Dots indicate location of sampling sites; 

the SERC dock is located directly inshore (northwest) of site 4B.

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METHODS

We sampled seven sites: six within the Rhode River 

and one just beyond the mouth of the river in the mainstem Chesapeake Bay. Sites were chosen based on prior 

research conducted in the Rhode River and designed to 

cover its entire length. At each site, weather conditions 

were noted and temperature, DO, and salinity were recorded at the surface and subsequent 1 m depth intervals 

with a YSI 600QS meter. Additional temperature, DO, 

and salinity data were available from the monitoring station located at the dock of the Smithsonian Environmental 

Research Center (SERC) in the Rhode River, which was 

equipped with a YSI 6600 meter (C. Gallegos, SERC, unpublished data).

Gelatinous zooplankton samples were collected in duplicate 3 min stepped oblique tows using a 0.5 m diameter, 

202 m mesh hoop plankton net towed at approximately 

2 knots and equipped with a General Oceanics fl owmeter 

(model 2030). Excess water was strained from the sample, 

total volume of gelatinous zooplankton was measured, and 

all individuals were identifi ed to species and enumerated. 

Bell diameters of C. quinquecirrha and the oral to aboral 

lengths of up to 15 M. leidyi were recorded. Remaining 

specimens of M. leidyi were classifi ed as either larger than 

or equal to or less than 3.0 cm.

Mesozooplankton samples were collected using 0.3 m 

diameter, 202 m mesh paired hoop nets. Samples were 

rinsed through a 2 mm sieve to remove gelatinous zooplankton and preserved with 10% buffered formalin; 

meso zooplankton species were subsequently identifi ed 

and enumerated.

Whole water column chlorophyll data were collected 

by another research group (C. Gallegos, SERC) at the 

four central Rhode River sites (1A, 2A, 3A, 4B; see Figure 

1) on different days during each sampling week. Chlorophyll a (chl a) was measured with a Spectronics Genesis 

5 spectrophotometer and converted into micrograms per 

liter (g L1).

Mnemiopsis leidyi egg production assays were conducted in 2004 using established methodology (Kremer, 

1976; Grove and Breitburg, 2005). Undamaged individuals covering the size range from each site (3– 8 cm) were 

randomly assigned to jars containing 3 L fi ltered Rhode 

River water and left overnight at ambient water temperatures. At approximately 0900 the following morning, 

adult ctenophores were removed and lengths and volumes 

recorded. Water from each jar was strained through a 

35 m sieve, preserved with 10% acid Lugol’s solution 

(Sullivan and Gifford, unpublished data; Grove and Breitburg, 2005), and eggs were enumerated. Egg production 

was normalized by ctenophore volume to facilitate comparisons among individuals.

Data were analyzed using analysis of variance (Proc 

GLM: SAS v. 9.1) on rank-transformed data. Student– 

Newman– Keuls tests were used for a posteriori comparisons. Regression models were used to examine the effects 

of ctenophore volume, site, date, and interactions between 

these factors on egg production. Nonsignifi cant interaction terms with P  0.25 were dropped from statistical 

models.

RESULTS

PHYSICAL PARAMETERS

Temperature, salinity, and DO all varied among sites 

and between years (Table 1; Figure 2; two-way analysis 

of variance [ANOVA]). Surface water temperature varied 

among sites (F  38.21, P  0.01), and was cooler adjacent to, and near the mouth of, the Rhode River and at 

the deeper sites. Surface salinity also varied signifi cantly 

among sites (F  3.55, P  0.01), and was generally highest at the Bay site (Site 73) and at sites near the mouth 

of the Rhode River. Minimum DO concentration varied 

among sites (F  7.33, P  0.01) and was signifi cantly 

lower at the Bay site than elsewhere.

Measurements at the SERC dock indicated that surface water temperatures reached 25°C more than 3 weeks 

earlier in 2004 than in 2005 but exceeded 30°C only during 2005. Salinity remained below 8 except for a brief 

period in 2004 but exceeded 8 for most of the summer in 

2005. Daytime low DO concentrations (2 mg L1) were 

occasionally recorded in the bottom waters during cruises; 

all low daytime DO measurements in 2004 and all but 

one in 2005 were recorded at the Bay site. The continuous YSI 6600 monitor at the SERC dock indicated that 

low DO concentrations occurred near the surface within 

the Rhode River in the early morning hours of both years 

(C. Gallegos, SERC, personal communication, 2004). 

Analysis of our weekly sampling data indicated that temperature (F  5.38, P  0.02), salinity (F  135.18, P 

0.01), and DO concentrations (F  6.39, P  0.01) were 

all signifi cantly higher in 2005 than in 2004.

2004 BIOTA

Chlorophyll a concentrations peaked in early June, 

declined, and then rose continually during the period sampled from mid-June through early September 2004 (see 

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372 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Figure 2). Mesozooplankton samples in both years were 

dominated (95% of individuals) by the calanoid copepod Acartia tonsa. During 2004, mesozooplankton densities varied signifi cantly among dates (F  6.28, P  0.01). 

Peak densities of 4– 7 individuals L1 occurred on 21 June 

and 7 July and then declined to approximately 1.0 individuals L1 for the rest of the season (see Figure 2).

Mnemiopsis leidyi volumes also varied signifi cantly 

among dates (one-way ANOVA on ranks; F  6.08, P 

0.01). Numerical densities and volumes were lowest in 

mid-June (0.62  0.25 individuals m3 and 2.3 

0.77 mL m3, respectively), and then gradually increased 

to a maximum of 51  30.2 individuals m3 and 58  

33.5 mL m3 on 19 August (see Figure 2), the date that 

coincided with highest densities of “recruits” (individuals 1 cm in length). Regression analyses indicated a 

signifi cant relationship between the zooplankton density of the prior week and both M. leidyi volume (r 2 

0.13, P  0.01) and the density of recruits (r 2  0.21, 

P  0.01). However, the previous week’s chl a concentration explained a greater percentage of the variation 

in both these measures of M. leidyi abundance for the 

sites at which chl a data were available (1A, 2A, 3A, 4B) 

(volume: r 2  0.33, P  0.01; density of new recruits: 

r 2  0.25, P  0.01). Chrysaora quinquecirrha abundances were low during 2004. A few medusae were seen 

in the fi eld during August and early September but were 

never caught with either the 0.5 m diameter hoop net 

or the larger 1 m2 neuston net, which was deployed in 

an attempt to more accurately sample the low-density C. 

quinquecirrha population.

2005 BIOTA

Temporal patterns and peak abundances of most biota in 2005 differed from those in 2004 (see Figure 2). 

Mid-June chl a concentrations in 2005 were similar to 

those in the corresponding time period in 2004, and as 

in 2004 generally increased during the remainder of the 

season. However, sampling did not detect an early June 

chl a peak in 2005, and maximum chl a concentrations in 

late summer 2005 reached only about two-thirds the concentrations reached in 2004 (Figure 2). Mesozooplankton 

densities varied among dates (one-way ANOVA on ranks, 

F  4.87, P  0.01). The 21 July peak density of 2.3 individuals L1 was both later and lower than peak densities 

in 2004. Early June through early July mesozooplankton 

densities remained below 1 individual L1 and were similar to mid-July– early September densities in 2004.

The timing of the increase in mesozooplankton densities in 2005 corresponded to a decrease in M. leidyi

densities and the appearance of C. quinquecirrha. M. 

leidyi densities varied signifi cantly among dates (one-way 

ANOVA on ranks: F  13.98, P  0.01). Peak M. leidyi

TABLE 1. Mean environmental conditions measured at each site sampled for 2004 and 2005. See Figure 1 for site locations. Chlorophyll 

a concentrations are whole-water integrated values (C. Gallegos, SERC); minimum dissolved oxygen (DO) values are based on nearbottom measurements; temperature and salinity are from surface waters (1 m depth); NA  site not sampled.

 2004 2005

 Chlorophyll a Minimum DO Temperature Chlorophyll a Minimum DO Temperature

Site (g L1) (mg L1) (°C) Salinity (g L1) (mg L1) (°C) Salinity

73 a NA 2.31 25.40 7.76 NA 3.46 26.26 9.79

1A 24.55 5.20 25.95 8.20 21.37 6.61 26.64 9.26

2A 24.76 5.77 26.66 8.04 37.02 6.88 27.58 9.44

CC NA 4.70 29.14 7.35 NA 5.14 28.91 9.10

3A 32.43 4.73 27.54 7.94 28.20 5.21 28.00 8.87

SC NA 4.23 28.09 7.78 NA 5.31 27.97 9.38

4B 44.34 5.22 28.41 7.29 32.29 5.19 28.62 9.08

a Because of sea conditions, site 73 was not sampled during mid- to late summer 2004 as frequently as other sites; thus, averages are not necessarily representative of physical 

conditions at site 73 relative to other sites measured on the same dates.

FIGURE 2. (facing page) Weekly mean temperature (°C) and salinity 

at the SERC dock (C. Gallegos, unpublished data), and river-wide 

mean (SE) chlorophyll a concentration (g L1), mesozooplankton 

abundance (number L1), and Mnemiopsis (M.) leidyi and Chrysaora (C.) quinquecirrha abundance (volume, mL m3; density, number m3) for 2004 (left) and 2005 (right).

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374 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

densities were higher and occurred earlier in 2005 than in 

2004. Volumes peaked on 16 June (279  205 mL m3), 

declined substantially by the 21 July sample date, and then 

remained low throughout the rest of the season (Figure 2). 

Medusae of Chrysaora quinquecirrha were fi rst caught in 

our sample nets on 18 July 2005, and numbers continually increased over the season, reaching a maximum on 

the last sample date, 7 September (Figure 2). Mnemiopsis 

leidyi densities declined as C. quinquecirrha abundances 

increased. Regression analysis was run on C. quinquecirrha density and the prior week zooplankton density and 

chl a concentrations. Partial r 2 values indicated that C. 

quinquecirrha number explained 41% of the variation in 

the number of M. leidyi recruits whereas prior week zooplankton explained only 17% and 13% of the variation in 

number of recruits and M. leidyi volume, respectively.

MNEMIOPSIS LEIDYI EGG PRODUCTION

Egg production assays were performed on three dates 

in July 2004. Mnemiopsis leidyi produced between 0 and 

668 eggs mL1 of ctenophore. There was a signifi cant 

positive correlation between M. leidyi volume and the 

number of eggs produced, both on each date and for the 

three dates combined (Figure 3). Egg production on each 

date in 2004 differed signifi cantly from all others. Egg 

production was highest on 7 July, 355  28.2 eggs mL1

(n  36); lower on 1 July, 274  25.7 eggs mL1 (n 

33); and lowest on 22 July, 50  8.71 eggs mL1 (n  35) 

(see Table 2).

Mesozooplankton prey density during the week 

leading up to the reproduction assays was estimated by 

averaging mesozooplankton densities measured in samples collected on the day of the egg production assay 

and from the previous week to include food immediately 

available as well as prey quantity potentially affecting 

prior growth and reproduction. Two week average zooplankton densities were 4.13  1.03 (n  6), 2.72 

0.56 (n  7), and 1.03  0.34 (n  7) individuals L1

for 7 July, 1 July, and 22 July, respectively (see Table 2). 

These zooplankton densities corresponded directly with 

the ranked egg production rates on these dates. ANOVA 

indicated that the total number of eggs produced per individual increased signifi cantly with ctenophore volume 

(F  201.24, P  0.01) and average zooplankton density (F  34.87, P  0.01), and varied among sites (F 

5.70, P  0.01), dates (F  13.82, P  0.01), and the 

interaction between sites and dates (F  3.39, P  0.01); 

the model r 2 was 0.80 (P  0.01).

DISCUSSION

Temporal patterns of mesozooplankton, M. leidyi, 

and C. quinquecirrha in the Rhode River differed strongly 

between 2004 and 2005. In 2004 mesozooplankton 

abundances peaked in early summer and then declined as 

ctenophores gradually increased throughout the season. 

C. quinquecirrha medusae were rare, and their appearance did not result in a decline in ctenophore density or 

biomass. In contrast, in 2005, late spring through early 

summer mesozooplankton densities were low and ctenophore density and biomass were high. As C. quinquecirrha

abundances increased in late summer, M. leidyi decreased 

and mesozooplankton densities increased. Peak densities 

of M. leidyi measured during this study in the Rhode River 

(approximately 200 individuals m3 and nearly 300 mL 

m3) are higher than those reported in the Pamlico River, 

FIGURE 3. Total number of eggs produced and volume (mL) of 

each M. leidyi in all three reproduction experiments.

TABLE 2. Mean egg production rate (eggs mL1 ctenophore 

SE) and 2-week mean mesozooplankton density (number L1

 SE) for each reproduction study date.

Date Egg production Zooplankton density

1 July 274 ( 25.7) 2.72 ( 0.56)

7 July 355 ( 28.2) 4.13 ( 1.03)

22 July 50 ( 8.7) 1.03 ( 0.34)

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NUMBER 38 • 375

North Carolina (just over 60 mL m3; Miller, 1974) or the 

mid-Chesapeake Bay (Purcell et al. 2001), but similar to 

abundances reported for Narragansett Bay, Rhode Island 

(Deason, 1982; Sullivan et al., 2001). Peak Rhode River 

densities measured in this study were lower, however, than 

those reported for systems such as the Black and Caspian 

Seas to which M. leidyi has been introduced (Kideys and 

Romanova, 2001; Bilio and Niermann, 2004).

Interannual variation in salinity likely contributed to 

observed interannual differences in gelatinous zooplankton densities and food web interactions, but the effect of 

interannual variation in water temperatures is less clear. 

Low salinities in 2004 likely resulted in the low densities 

of C. quinquecirrha in that year. Chrysaora quinquecirrha

polyps are generally not found in salinities less than 7 and 

become more abundant as salinities increase to between 

7 and 10 (Cargo and King, 1990). During 2004, surface 

salinity did not reach 5 until mid-June, or 7 until July, and 

never reached 10. In contrast, surface salinity reached 7 

by mid-June and 10 by early August in 2005. We suggest 

that salinities below 5 in May and early June also delayed 

or reduced early-season M. leidyi reproduction in Rhode 

River in 2004 (Purcell et al., 2001). We were unable to 

fi nd published studies that report M. leidyi reproductive 

rates at salinities below 5. However, if this hypothesis is 

correct, there is a very narrow margin between salinities 

that prevent recruitment of C. quinquecirrha and allow M. 

leidyi populations to grow unchecked by predation and 

salinities that hinder M. leidyi populations by limiting reproduction. The combined effects of salinity on these two 

gelatinous species in Rhode River in 2004 appears to have 

resulted in a persistent M. leidyi population that did not 

become abundant until mid- to late July but then remained 

abundant at least through early September.

Although surface waters warmed earlier in the season 

during 2004 than during 2005, the effect of this warming on gelatinous zooplankton seasonal abundances is 

not clear and may have been overwhelmed by other factors. Spring temperatures were 5°C higher in 2004 than 

in 2005. By early May of both years, however, temperatures exceeded the 9°– 13°C minimum temperature required for M. leidyi reproduction (P. Kremer, University of 

Connecticut, unpublished data), and by mid-May of both 

years, temperatures exceeded the 17°C threshold required 

for strobilation by C. quinquecirrha (Cargo and King, 

1990; Purcell and Decker, 2005). In addition, there are 

no data to suggest that temperatures that occurred during the warmer 2004 spring should have reduced growth 

or reproduction of either gelatinous species. By late July 

2005, surface water temperatures exceeded 30°C, the temperature at which M. leidyi suffers mortality in laboratory 

experiments (D. Breitburg, unpublished data). However, 

M. leidyi could have avoided high midday surface temperatures by moving lower in the water column, and the 

appearance of predatory C. quinquecirrha is a more parsimonious explanation as the major cause of the seasonal 

ctenophore decline during 2005, given the high percentage 

of M. leidyi with damage indicative of encounters with 

medusae (Purcell and Cowan, 1995; Kreps et al., 1997).

With a mean depth of 2 m, the shallow bathymetry of 

the Rhode River may limit the potential for coexistence of 

M. leidyi and C. quinquecirrha. In the Rhode River, densities of M. leidyi averaged less than 2 mL m3 in August and 

September 2005 when C. quinquecirrha densities reached 

an average of 2– 6 mL m3. In contrast, Keister et al. 

(2000) found 26.6 mL M. leidyi m3 in the Patuxent River, 

Maryland, when C. quinquecirrha density averaged 11.8 

mL m3. The deeper water column of the Patuxent, which 

includes a bottom layer with variable and sometimes severely hypoxic DO concentrations (Breitburg et al., 2003), 

may provide greater opportunity for spatial separation of 

M. leidyi and C. quinquecirrha and increase survival of M. 

leidyi at moderate C. quinquecirrha densities.

Prey availability could limit M. leidyi abundance and 

production, but our data do not suggest that low mesozooplankton densities were likely to have caused the large 

interannual variation in ctenophore abundances. Mesozooplankton densities were higher in 2004 than in 2005, 

and the temporal pattern of mesozooplankton and ctenophore abundances was more suggestive of ctenophore 

control of mesozooplankton than the reverse. An inverse 

relationship between copepod densities and ctenophore 

abundance has been noted previously in both Chesapeake 

Bay (Feigenbaum and Kelly, 1984; Purcell and Cowan, 

1995) and Narragansett Bay (Sullivan et al., 2001). In both 

years of our sampling, high densities of M. leidyi recruits 

were found in the Rhode River during periods of lowest 

mesozooplankton densities. We did not sample microzooplankton, however, and cannot rule out their potential infl uence on ctenophore abundance.

The maximum egg production we measured in the 

Rhode River (9,000 eggs individual1 M. leidyi day1) 

was lower than the maximum reported value of 14,000 

eggs individual1 day1 (Kremer, 1976; Reeve et al., 

1989) but well within the range of values reported elsewhere. Mnemiopsis leidyi egg production in the Rhode 

River was similar to that of fi eld-collected ctenophores 

from elsewhere in Chesapeake Bay (Purcell et al., 

2001), including the Patuxent River (D. Breitburg and 

R. Burrell, unpublished data). Mnemiopsis leidyi from 

29_GrahamBreitburg_369-378_Lang.375 375 9_GrahamBreitburg_369-378_Lang.375 375 9/24/09 10:20/24/09 10:20
376 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

the Patuxent produced a maximum of 610 eggs mL1 of 

ctenophores at mesozooplankton abundance of 1 individual L1, which is very close to the rate found in this 

study of 668 eggs mL1 at 2.2 mesozooplankton individuals L1. Variation among dates in the relationship between zooplankton density and egg production suggests 

an interesting pattern of trade-offs in energy allocation 

to somatic growth versus reproduction, or nutritional 

constraints.

Predicted changes in sea-surface temperatures and 

rainfall throughout the world may lead to changes in 

the geographic ranges of many aquatic organisms. The 

Rhode River provides an interesting model that may aid 

predictions of climate change-related shifts in ranges and 

predator – prey dynamics because it is often near the threshold of salinity tolerances and the dynamics of the system can 

fl uctuate markedly from year to year. These characteristics 

of the Rhode River allowed us to examine the gelatinous 

zooplankton food web within the river during two distinct 

years: one with, and one without, strong infl uence by a top 

predator. Differences in species abundances and food web 

interactions observed here may help to predict dynamics in 

other systems as environmental conditions, and the range 

of C. quinquecirrha, change. Although generally considered a nuisance species by swimmers and fi shermen, C. 

quinquecirrha may benefi t fi sheries and habitat by controlling densities of M. leidyi, which is an important predator 

of oyster larvae— a prey not utilized by C. quinquecirrha

(Purcell et al., 1991; Breitburg and Fulford, 2006).

ACKNOWLEDGMENTS

We thank Charles Gallegos and Sam Benson (SERC) 

for the chlorophyll, temperature, and salinity data from 

their cruises and monitoring station. We also thank the 

Smithsonian Environmental Research Center NSF-REU 

program, the Smithsonian Institution Women’s Committee, and the Smithsonian Institution Marine Science Network for funding.

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Patterns of Water Quality and Movement 

in the Vicinity of Carrie Bow Cay, Belize

Karen H. Koltes and Thomas B. Opishinski

ABSTRACT. Meteorological and oceanographic conditions have been monitored at 

the Smithsonian Field Station at Carrie Bow Cay, Belize, since 1993 through the Caribbean Coastal Marine Productivity (CARICOMP) program, and since 1997 through an 

automated monitoring system operated by the Caribbean Coral Reef Ecosystems Program (CCRE). Collectively, the two datasets represent a unique resource that provides 

a mechanism to improve our understanding of changing environmental conditions on 

the Mesoamerican Barrier Reef and, particularly, the conditions governing water quality and movement around Carrie Bow Cay. Especially evident is the broad infl uence on 

water quality of seasonal climate patterns as well as short-term events such as cold fronts 

and major storms. Among several variables examined, wind direction appears to be a 

good indicator of water quality conditions. From March to June, prevailing northeasterly airfl ow and limited rainfall result in higher water quality along this portion of the 

Belize Barrier Reef. Under decreased trade or increasing westerly winds, especially during 

periods of higher rainfall from October to January, turbid coastal water moves (drifts or 

is pushed) out onto the reef from the lagoon. The most signifi cant fi nding, however, has 

been a dramatic loss of water quality along this portion of the Belize Barrier Reef since 

monitoring began at Carrie Bow Cay in 1993.

INTRODUCTION

Carrie Bow Cay, Belize, has been the site of extensive biological, geological, 

and ecological study as part of the Smithsonian Institution’s Caribbean Coral 

Reef Ecosystem (CCRE) program (Rützler and Macintyre, 1982). Despite more 

than three decades of multidisciplinary research, however, relatively little is 

known about the complex interaction of physical factors that infl uence the reef 

environment, including winds, tides, temperature, and rainfall. These physical 

parameters provide the context for understanding and predicting relationships 

between reef organisms and their environment, but such parameters require accurate and consistent measurement over long time periods to establish a reliable 

description of baselines and trends. This is particularly true of water quality and 

movement, as the constant mixing and motion of water masses, bathymetry, and 

proximity to sediment inputs lead to signifi cant spatial and temporal variability.

Establishing baselines and trends for environmental conditions has also become 

increasingly important as Belize, as well as neighboring countries, experience rapid 

Karen H. Koltes, U.S. Department of the Interior, 

Washington, D.C. USA; Thomas B. Opishinski, 

Interactive Oceanographics; East Greenwich, 

Rhode Island. Corresponding author: K. Koltes 

(Karen_Koltes@ios.doi.gov). Manuscript received 

29 August 2008; accepted 20 April 2009

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380 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

urban and economic growth from the recent expansion 

of agriculture, aquaculture, and tourism. As the coastline 

and mangrove cays of Belize have experienced accelerated 

development over the past few decades, the barrier reef 

environment has been subjected increasingly to chronic 

and acute disturbances from terrigenous inputs. Poorly 

managed exploitation of coastal and offshore natural resources, extensive land modifi cations from dredging, land 

reclamation, deforestation, and conversion, and effl uents 

from sewage and agriculture/aquaculture are delivering 

increased loads of sediments, nutrients, pesticides, herbicides, and other man-made chemicals to the central lagoon 

(Gibson and Carter, 2003). Eroded sediments and the residues of fertilizers and pesticides are also entering Belize’s 

coastal waters from the more than 300,000 hectares of 

banana, oil palm, sugar cane, citrus, and pineapple crops 

cultivated across the wider Mesoamerican region (Burke 

and Sugg, 2006).

Early qualitative observations suggested that a period 

of heavy rainfall in the central portion of Belize was followed within 1 to 2 days by the appearance of a plume of 

low-salinity, turbid water over the fore-reef at Carrie Bow 

Cay (CBC). For major storms, the lens could be signifi cant 

in duration and thickness. Rainfall from Hurricane Mitch, 

a Category 5 storm, approached 2 m over Central America between 29 October and 1 November 1998, causing 

severe fl ooding, landslides, and mudfl ows. Much of the 

storm discharge entered the Gulf of Honduras, where it 

fl owed north as a highly turbid, plankton-enriched water 

mass, reaching the Belize shelf on 3 November 1998 (Andréfouët et al., 2002; Sheng et al., 2007). On 15 November 

1998, K. Koltes observed this surface lens to be about 15– 

20 m in thickness in the waters adjacent to CBC. Further in 

situ characterization of the lens was not possible because of 

the closure of the fi eld station, but recent numerical modeling of satellite images of terrestrial runoff plumes in the 

Gulf of Honduras confi rms that infl uxes of sediments and 

nutrients are reaching the central reefs from local and more 

distant origins (Andréfouët et al., 2002; Tang et al., 2006; 

Chérubin et al., 2008; Paris and Chérubin, 2008).

Consistent monitoring of environmental variables began at Carrie Bow Cay in 1993 as part of the Caribbean 

Coastal Marine Productivity Program (CARICOMP). 

CARICOMP is a regional scientifi c effort to study land– sea 

interaction processes, to monitor for change on a local and 

regional scale, and to provide appropriate scientifi c information for management (Kjerfve et al., 1999; http://www

.ccdc.org.jm/frontpage.html). In 1997, an automated environmental monitoring system (EMS) was installed at Carrie Bow Cay that provides an independent set of weather 

and water quality measurements. It was one of the earliest 

monitoring systems to process and transfer real-time data 

from a remote geographic location to a website for public 

access (http://nmnhmp.riocean.com). To our knowledge it 

is still the only automated system continuously monitoring oceanographic and meteorological conditions on the 

outer Mesoamerican Barrier Reef. In December 1997, a 

catastrophic fi re destroyed the fi eld station, suspending 

all monitoring except the automated water temperature 

measurements under the CARICOMP program. The full 

complement of CARICOMP measurements resumed after the station reopened in late 1999, and the automated 

measurements resumed after a new EMS was installed in 

September 2000.

Together, the CARICOMP and EMS datasets have 

provided a nearly continuous record of climatic and 

oceanographic conditions along the central portion of the 

Belize Barrier Reef. The 15 years of water temperature 

and Secchi disk measurements likely now constitute the 

longest continuous records for the Belize Barrier Reef and 

are among the longest for the entire Mesoamerican region. 

The data serve as an important resource for researchers to 

examine long-term trends, episodic events, and short-term 

and seasonal cycles (McField and Kramer, 2004). The data 

also allow comparative studies with other reef ecosystems 

to assess biodiversity and correlate environmental factors 

with biological phenomena. Data have been used to characterize prevailing conditions (Koltes et al., 1998) as well 

as the anomalous conditions that occur during extreme 

climatic events such as the El Niño– Southern Oscillation 

(ENSO) of 1997– 1998 (Aronson et al., 2002) and powerful storms such as the Category 5 hurricanes Mitch, Keith, 

Iris, Dean, and Wilma.

These long-term datasets are beginning to yield reliable descriptions of meteorological and oceanographic 

conditions around Carrie Bow Cay. We report here on 

preliminary analyses of the patterns, trends, and relationships that are emerging from these long-term records, with 

special reference to factors that control water quality and 

movement around Carrie Bow Cay.

METHODS

Carrie Bow Cay is a small island (0.7 acres) located 

in the central province of the Belize Barrier Reef (Burke, 

1982) about 18 km from the mainland (16°48N and 

88°05W; Figure 1). Carrie Bow Cay lies on the barrier 

reef proper between two tidal passes, a relatively rare occurrence along the otherwise nearly continuous barrier 

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NUMBER 38 • 381

reef. It is in close proximity to deep ocean water (300 m) 

to the east. A line of cays to the west that includes Twin 

Cays is part of a fault-block ridge that separates the shallower back-reef lagoon from the deeper Lagoon Channel 

that parallels Belize’s shoreline. Although shoal formations 

are the outcome of a variety of factors such as currents and 

sea level changes, the present-day patterns of parallel shoals, 

reefs, and mangrove islands in this area resulted principally 

from faulting along a NNE trend during the Pliocene era 

(Dillon and Vedder, 1973; Macintyre and Aronson, 1997).

CARICOMP MEASUREMENTS

Scientifi c monitoring of meteorological and oceanographic conditions under the CARICOMP program has 

included daily measurement of precipitation (mm) and air 

temperature (°C) at Carrie Bow Cay (“C” in Figure 1) and 

weekly measurement of surface water temperature (°C) and 

salinity (‰) at a permanent monitoring station in the seagrass 

beds adjacent to Twin Cays (“lagoon”; “A” in Figure 1; water depth 1.2 m) and in the ocean seaward of the drop-off 

(“drop-off”; “E” in Figure 1; water depth 300 m). Bottom water temperatures have been recorded continuously 

at intervals of 15– 48 min at the permanent CARICOMP 

monitoring sites in the lagoon (“A” in Figure 1), in the seagrass beds adjacent to Carrie Bow Cay (“B” in Figure 1; 

water depth 2m), and on the inner fore-reef (“D” in Figure 

1; water depth 13.5m) using Onset Corporation’s model 

HOBO, StowAway, and TidbiT data loggers (0.2°C).

Water quality characteristics that are associated with 

water transparency have been measured by Secchi disk as 

horizontal distance (m) taken 0.5 m below the surface in 

the lagoon (“A” in Figure 1) and vertical distance (m) at the 

drop-off (“E” in Figure 1). From 1993 to 1997, water transparency was measured once a week between 1000 and 1200 

using a 30 cm diameter disk with black and white quadrants. In 1999, the CARICOMP protocol was modifi ed to 

take advantage of the 20 cm diameter black and white disk 

that is more available commercially. The difference in the 

diameters of the two Secchi disks has little effect on the measurements, particularly compared to other sources of error 

such as sun angle, cloud cover, sea state, wind, currents, and 

observer difference (Steel and Neuhausser, 2002; Hou et al., 

2007). In 2002, the Secchi disk measurements were increased 

to two times per week to more accurately characterize water 

quality trends. No water transparency measurements were 

made during adverse weather conditions, particularly over 

the drop-off, during closure of the station in the fall of 1993 

and 1994, and for approximately two years following destruction of the fi eld station from the fi re in 1997.

To better characterize water quality, especially during storm events, light intensity loggers were mounted on 

a cinder block (water depth 13.5 m) at the permanent 

CARICOMP monitoring site on the inner fore-reef (note 

“D” in Figure 1). Onset Corp.’s model StowAway LI was 

used from 2002 until 2005 when Onset ceased manufacturing this model; Onset’s model HOBO UA-002-64 Pendant Temp/Light has been used since 2005. Light intensity 

(lumens/ft2) was recorded at intervals from 5 s to 15 min 

over periods ranging from days to weeks from 2002 to 

2008. While deployed, the light logger was kept free of 

sediment and epibionts by periodically wiping the surface 

of the housing. The StowAway LI was designed to measure relative light levels (e.g., sun versus shade) and was 

calibrated for incandescent sources (spectral response, 

200– 1,100 nm; range, 0.001– 1,000 lumens/ft2). The 

FIGURE 1. Map of the central province of Belize showing the location of the Smithsonian Institution’s Field Station (16°48N and 

88°05W) at Carrie Bow Cay. Note the Lagoon Channel that separates the outer lagoon platform from the mainland. Inset upper 

right: Location of the CARICOMP permanent monitoring sites in 

the seagrass beds near Twin Cays (A  “lagoon”) and Carrie Bow 

Cay (B), on the inner fore-reef slope (D) and seaward of the barrier reef (E  “drop-off”), and (C) the Environmental Monitoring 

System on Carrie Bow Cay. Inset lower left: The Belize National 

Meteorological Service stations at Melinda Forest (MF), Maya King 

(MK), Savannah Forest (SF), and Punta Gorda (PG).

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382 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

HOBO UA-002-64 Pendant Temp/Light was designed to 

measure relative light levels indoors or outdoors (spectral 

response, 200– 1,200 nm; range, 0– 30,000 lumens/ft2). 

Our objective was to establish patterns in relative light levels, and hence water transparency, by comparing in situ 

irradiance on the inner fore-reef (“reef irradiance”) to that 

at the surface (“incident irradiance”). No attempt was 

made to relate these measurements to biologically active 

wavelengths.

ENVIRONMENTAL MONITORING SYSTEM

The EMS continuously records meteorological and 

oceanographic conditions at Carrie Bow Cay. A marinegrade wind monitor (RM Young model 05106), LI-COR 

model LI-200 pyranometer, temperature/relative humidity sensor (Vaisala model HMP50), and barometric pressure sensors monitor meteorological conditions. The 

weather sensors, mounted on an aluminum tower above 

the main laboratory, are approximately 13 m above 

ground level (“C” in Figure 1). Rain is measured with 

a Texas Electronics solid-state tipping bucket rain gauge 

(model 525USW). The pyranometer features a silicon 

photovoltaic detector designed to measure solar radiation 

under conditions of unobstructed natural daylight. Measurements of wind speed (mph) and direction (0°– 360°), 

solar radiation (W/m2), rain accumulation (mm) and rate 

(cm/h), barometric pressure (mbar), air temperature (°C), 

and relative humidity (%) are recorded every 10 min.

Oceanographic conditions are monitored via a YSI 

model 6600EDS multiparameter water quality sonde, 

mounted inside a stilling tube. The sonde is mounted on 

the dock on the west side of Carrie Bow Cay about 0.6 m 

below the surface of the water (“C” in Figure 1). Every 

10 min, measurements are taken of water level (m), water 

temperature (°C), salinity (‰), dissolved oxygen (% saturation), pH, and turbidity (NTU).

Data acquisition of both oceanographic and meteorological systems is managed automatically by a datalogger and control system and transmitted by radio to 

a server on the mainland. A regular program of maintenance, including calibration of sensors to manufacturer’s standards (Eaton et al., 2005) and minimization of 

fouling, is followed to maintain the best possible data 

quality. Data are subjected to a quality assurance/quality 

control (QA/QC) process to remove outliers and invalid 

and suspect data before they are included in the historical archives. The QA/QC process also incorporates established criteria and procedures to correct for sensor 

and fouling drift (Wagner et al., 2006).

The data have contributed to new and existing research studies, publications, and management programs 

for both Smithsonian researchers and an increasing number of organizations from the region (e.g., Renken and 

Mumby, 2009).

ANALYSIS

The annual means and standard deviation of Secchi 

disk measurements from 1993 to 2008 for the lagoon (n 

787) and drop-off (n  727) were calculated, and the 15-

year trend in water quality was determined by least-squares 

regression analysis. To evaluate seasonal patterns in water 

quality, monthly means were calculated for the Secchi measurements from the lagoon because horizontal measurements 

are generally more reliable than vertical measurements (Steel 

and Neuhausser, 2002) and were more often taken during 

adverse weather conditions.

To examine annual variation in wind patterns, monthly 

wind rose plots were generated for Carrie Bow Cay using 

approximately 350,000 wind measurements collected between 2003 and 2008. A wind rose plot is a combination 

of a polar plot and a histogram that depicts the distribution of wind speed and the frequency of occurrences that 

wind blows from 1 of 16 cardinal directions (N, NNE, 

NE, etc.). Seasonal and geographic patterns of rainfall 

were derived by calculating monthly mean precipitation 

for Carrie Bow Cay and four coastal stations (Melinda 

Forest, Mayaking, Savannah Forest, and Punta Gorda; see 

Figure 1, lower inset) maintained by the Belize National 

Meteorological Service (2003– 2008).

Previous oceanographic studies at Carrie Bow Cay 

suggested that tides play a major role in controlling water 

movement, and hence water quality, around Carrie Bow 

Cay (Greer and Kjerfve, 1982; Kjerfve et al., 1982). To 

examine the role of tides, reef irradiance was compared to 

meteorological and oceanographic variables using a harmonic regression analysis model based on linear regression algorithms to compute constituents. Specifi cally, we 

compared reef irradiance to incident irradiance and then 

wind direction and intensity, tidal stage, and precipitation 

from all stations. The objective of the analyses was to extract harmonic constituents to judge the relative strength 

of the tidal forcing on the light patterns. The analyses were 

inconclusive because tidal components were small relative 

to the strong solar forcing inherent to the measurements of 

light and from the lack of a strong diurnal or semidiurnal 

signal in the “microtides” of Belize (Kjerfve et al., 1982).

To establish annual changes in light, monthly means 

were computed for reef and incident irradiance from 2003 

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NUMBER 38 • 383

to 2008. The analyses included more than a half million 

reef irradiance samples and approximately 350,000 measurements of incident irradiance. The monthly means were 

normalized with respect to the maximum monthly mean 

observed in each set of light measurements; this established 

a common datum reference and allowed comparisons of 

monthly and seasonal variations and patterns. Additional 

qualitative analyses of the various time series suggested 

that a consistent correlation existed between patterns of 

reef irradiance and both seasonal and short-term changes 

in wind direction. A comparative analysis of conditions 

during periods of normal weather conditions and specifi c 

weather “events” was undertaken to further defi ne the localized infl uence of wind direction and other parameters 

on water quality over the fore-reef and to identify external 

(regional) events that are observed in the Carrie Bow Cay 

measurements.

To establish annual changes in light, monthly means 

were computed for reef (n 500,000) and incident irradiance (n 350,000) from 2003 to 2008. The monthly 

means were normalized with respect to the maximum 

monthly mean computed for each set of light measurements; this established the maximum mean for each set 

as a common reference point and allowed comparisons of 

monthly and seasonal variations and patterns. Additional 

qualitative analyses of the various time series suggested 

that a consistent correlation existed between patterns of 

reef irradiance and both seasonal and short-term changes 

in wind direction. A comparative analysis of conditions 

during periods of normal weather conditions and specifi c 

weather “events” was undertaken to further defi ne the localized infl uence of wind direction and other parameters 

on water quality over the fore-reef and to identify external (regional) events that are observed in the Carrie Bow 

measurements.

RESULTS

Signifi cant temporal and spatial variability exists in 

the records of the meteorological and oceanographic variables. Particularly evident are longer-term seasonal patterns as well as signatures of short-term events such as 

cold fronts and major storms. The most signifi cant fi nding, however, has been a dramatic decline in water clarity 

along this portion of the Belize Barrier Reef since monitoring began at Carrie Bow Cay in 1993 (Figure 2). Mean 

annual Secchi distance (horizontal) declined from 12.8 m 

in the lagoon in 1993 to 8.7 m by 2008, a loss of almost 

0.3 m/year. During the same period, mean annual Secchi 

distance (vertical) declined from 23.8 m to 15.6 m over the 

drop-off or by about 0.5 m/year.

Comparisons of monthly means of water transparency, wind direction, and precipitation show that seasonal 

weather patterns strongly infl uence water quality (Figure 3). 

From February through May, the prevailing northeasterly 

airfl ow (Figure 3, left) is associated with a uniformly dry 

pattern across all stations (Figure 3, right). Monthly rainfall 

amounts average less than 75 mm. By June, a divergence can 

be seen among the stations, with those to the south receiving 

increasingly greater amounts of rain relative to the stations 

to the north, including Carrie Bow Cay. The sharp onset of 

the rainy season in the south is partly the result of the intrusion of the Inter-Tropical Convergence Zone as it migrates 

northward (http://hydromet.gov.bz/Climate_Summary.htm).

FIGURE 2. Annual mean and standard deviation of Secchi disk 

distance (horizontal, m) in the lagoon (top) and over the drop-off 

seaward of Carrie Bow Cay (vertical, m; bottom) from 1993 to 

2008. There has been a dramatic and signifi cant (P  0.001) loss 

of transparency in the waters around Carrie Bow Cay during the 

past 15 years.

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Rainfall maxima also diverge in terms of timing. 

Mean monthly rainfall peaks in June– July in southern 

Belize, with approximately 900 mm at Punta Gorda; the 

maximum at Carrie Bow Cay (about 290 mm) occurs in 

October. The marked shift in rainfall patterns beginning 

in June is accompanied by consistent northeasterly winds 

and tropical waves moving westward from June to November (http://hydromet.gov.bz/Climate_Summary.htm). 

Cold fronts, or “northers,” occur frequently from December to February and are associated with the southerly 

extension of the North American high-pressure system. 

During the peak season of December and January, cold 

fronts pass through Belize approximately every 10 days, 

the signatures of which appear in the temperature profi les 

on the fore-reef (Figure 4).

Monthly Secchi disk measurements in the lagoon (see 

Figure 3, right) correlate with the seasonal shift in climate 

patterns. Water transparency peaks in August (12.6 m), 

while incident irradiance is high (Figure 5) and the winds 

are still predominantly from the NE (see Figure 3, left). This 

peak also corresponds to a break in the rainy season on the 

mainland known as the “Mauga” (http://hydromet.gov.bz/

Climate_Summary.htm). In contrast, the break in the rainy 

season occurs in July at Carrie Bow Cay (see Figure 3, 

right). Water transparency reaches a minimum in January 

(8.4 m) around the winter solstice and the period when 

cold fronts, characterized by strong NW winds, reach a 

peak (Figure 3, left). This period of increased storm activity and resulting high sea states also interrupts routine 

Secchi disk measurements such that the winter means may 

be biased upward.

The seasonal pattern of reef irradiance is similar to 

that observed for water transparency measured by Secchi 

disk (see Figure 5) and is largely governed by changes in 

incident irradiance. Maximum irradiance occurs around 

the solstice, with reef irradiance showing a peak in June 

compared to August for Secchi disk distance (see Figure 2) 

and July for incident irradiance. However, reef irradiance 

attenuates more rapidly toward the winter solstice relative to incident irradiance. By December, reef irradiance 

has fallen to less than 40% of its summer peak whereas 

incident irradiance has fallen only to 60% of its summer 

FIGURE 3. Left (facing page), Monthly means of wind speed and direction at Carrie Bow Cay for 2003– 2008. 

The wind rose depicts the distribution of wind speed and direction: the length of each “spoke” indicates the 

percentage of time that winds blow from 1 of 16 cardinal directions (N, NNE, NE, etc.); the categories within 

the spoke represent the speed. Trade winds are the dominant pattern from March to September. Wind patterns are most variable during the transitional months of October/January/February. Right (above), Monthly 

means of rainfall at Carrie Bow Cay and the four Belize National Meteorological Service stations (left axis), 

and water transparency in the lagoon (horizontal Secchi disk distance [m], right axis) from 2003 to 2008.

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386 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 4. Water temperature on the inner fore-reef at 13.5 m from 29 July 2004 to 11 December 2006. 

Note the signatures of cold fronts in the temperature profi le between October and January and a late season 

cold front that passed 1– 3 April 2005.

FIGURE 5. Monthly mean of reef irradiance (inner fore-reef, 13.5 m) and incident (surface) irradiance 

(2003– 2008), normalized to allow comparisons among the light recording instruments. Reef irradiance attenuates at an accelerated rate relative to incident irradiance approaching the winter solstice.

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NUMBER 38 • 387

peak. Decreased light levels around the winter solstice 

may be caused by lower sun angle, increased turbidity 

and/or higher sea states associated with the winter climate 

pattern.

Flow of turbid water into the area can also be seen 

in fi ner-scale comparisons of reef and incident irradiance 

(Figure 6) that suggest turbidity is transported from more 

distant locations. Following two days of light winds that 

had shifted from NNE fi rst to the south and eventually to 

the NW, turbid water fl owed on to the fore-reef, driving 

light levels down by about 50% despite nearly full incident 

irradiance. At least some of the fl ow may be related to 

tides (Figure 7), but as previously mentioned, the mixed, 

semidiurnal microtide of this region has made it diffi cult 

to analyze the role of tides.

DISCUSSION

The constant mixing and motion of water masses, localized inputs of sediments, and changing meteorological 

conditions produce strong spatial and temporal variations 

in conditions along the Belize Barrier Reef. These factors 

present a challenging analysis, especially when combined 

with Carrie Bow Cay’s complex geomorphology that includes cuts in the reef to the north and south where disparate bodies of water mix together. Nevertheless, initial 

analyses have shown signifi cant correlations between 

certain weather conditions, both episodic and seasonal, 

and water properties. Particularly evident are longer-term 

seasonal patterns, as well as signatures of discrete events 

such as the passage of cold fronts and other changes from 

FIGURE 6. Progression of a turbidity event: Early in July 2005, light levels on the reef were among the highest recorded for reef irradiance (bottom, right axis). Beginning on 7 July, winds that had been blowing from the northeast at 15 mph began to taper off and remained calm through 

9 July, as shown in the daily wind rose (top; see Figure 3 for description of wind rose). On 10 July, the winds increased at Carrie Bow Cay and 

heavy rainfall occurred on the mainland, particularly to the south (middle; stations as in Figure 3, right). Incident irradiance (lumens[L]/ft2; bottom, left axis) remained high, but light levels on the reef dropped by nearly 50%. The drop in reef irradiance is attributed to a sediment plume, 

possibly from the south, that drifted over the fore-reef under conditions of little or no wind. Winds shifted around again to the northeast by 

11 July, and subsequent mixing of water returned light levels over the reef to near maximum by 13 July.

30_Koltes_379-390_Lang.indd 387 0_Koltes_379-390_Lang.indd 387 9/24/09 10:27/24/09 10:27
388 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

the typical weather patterns. Strong correlations are also 

apparent during less prominent variations in weather and 

particularly changes in wind direction such as those observed in July 2005. We found several other instances in 

which light levels on the reef dropped signifi cantly when 

winds simply tapered off completely during the 24 to 

48 hour “calm” period that often preceded a cold front. 

We also document a substantial decline of water quality 

around Carrie Bow Cay over the past 15 years.

Patterns of water transparency are driven largely by incident solar radiation, refl ecting the strong seasonal cycle of 

solar radiation. However, variations in those patterns are 

useful at tracking short- and long-term changes in water 

transparency. The pattern of decreased light intensity on the 

fore-reef as a function of incident solar radiation in December versus June likely refl ects the higher rainfall, consistent 

northwesterly winds, and frequent “northers” of the winter months and is consistent with recent simulation models 

showing locally higher turbidity during the winter months 

(Paris and Chérubin, 2008) from increased precipitation. 

This seasonal cycle is also apparent in the record of Secchi 

disk measurements. The difference observed between the 

timing of the maximum quality measured by Secchi disk and 

those measured by light logger may refl ect the differences in 

the sampling period (1993– 1998 versus 2002– 2008). The 

disparity may also refl ect the fact that the light logger data 

have not been collected as often during the spring– summer 

months as they have been during fall– winter months.

FIGURE 7. Hourly, weekly, and monthly means of tidal elevation (m) and water temperature (°C) measured at the dock at Carrie Bow Cay. 

Tidal elevation (top) reveals a complex pattern with a seasonal increase in elevation in October, when water temperature (bottom) reaches a 

maximum, that is typical of the Caribbean.

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NUMBER 38 • 389

Although additional modeling and analysis are required, particularly of tidal currents, preliminary results 

suggest a strong link between climate patterns and water 

quality and movement along the barrier reef in the central province of Belize. We propose that, under the typical 

pattern of prevailing trade winds, sediment-laden riverine 

input is pushed shoreward and held along the coast where 

it fl ows south in the Lagoon Channel. A southerly fl ow 

of water immediately adjacent to the shoreline is consistent with circulation models that have been developed for 

the Gulf of Honduras (Ezer et al., 2005). We also suggest 

that the fault-block ridge along the eastern boundary of 

the Lagoon Channel forms a natural “sill” or “dam,” facilitating the segregation of turbid coastal water driven 

shoreward by wind forcing. Under the infl uence of “oceanic” water, turbidity over the fore-reef at Carrie Bow 

Cay is generally lower.

Localized turbidity events are triggered when the northeasterly fl ow of the trade winds changes in either speed or 

direction. Turbid water that is normally contained along 

the coast spills over the submarine ridge of the Lagoon 

Channel and drifts or is pushed out across the outer (backreef) lagoon and onto the fore-reef. Changes in the prevailing weather patterns are also frequently accompanied by 

periods of rain on the mainland that discharge additional 

sediment and freshwater into the lagoon, increasing the 

volume and degree of turbid coastal water and spillover 

onto the reef platform.

The dramatic loss of water quality at Carrie Bow Cay 

over the past 15 years also suggests longer-term effects of 

increasing sediment and nutrient loads to the lagoon from 

the rapid modifi cations of the Belizean coastline and that 

of neighboring countries. Recent hydrological models of 

the Mesoamerican Barrier Reef estimated that runoff and 

associated river discharge have doubled and sediment delivery has increased 20 fold under present-day land use 

changes compared to a hypothetical “natural” (unaltered) 

state (Burke and Sugg, 2006). Although the modeling suggested that Belize contributed only about 10%– 15% of the 

sediment load to the region, the Belize River was identifi ed 

as a signifi cant contributor of sediments and nutrients to 

the Mesoamerican Barrier Reef. In the central and southern portions of Belize, large amounts of fertilizers used to 

cultivate citrus and bananas and the direct discharges of 

domestic sewage produce high nutrient levels in several areas along the coast (Gibson and Carter, 2003). Shrimp and 

other aquaculture operations are also discharging effl uents 

directly to the lagoon. These sediments appear to become 

entrained in the Gulf of Honduras gyre and, over the long 

term, are driving down water quality across the region.

Increasing turbidity also appears to be related to a 

wider regional increase in sedimentation and nutrient enrichment in the Gulf of Honduras (Burke and Sugg, 2006). 

Hydrological models indicate that sediment delivery increases southward along the coastline of Central America 

with Honduras contributing an estimated 80% of the 

sediment and half of the nutrients to the region. Circulation models of the Gulf of Honduras suggest that these 

sediments and nutrients are carried north along the Mesoamerican Barrier Reef by the Caribbean Current (Thattai 

et al., 2003). Recent modeling of satellite images indicate 

that runoff from watersheds in northern Honduras can 

extend as far north as Glovers Reef atoll (Andréfouët, 

2002; Paris and Chérubin, 2008). Based on modeling of 

satellite images and the hydrological models of Burke and 

Sugg (2006), Chérubin et al. (2008) concluded that concentrations of buoyant matter from terrestrial runoff into 

the Gulf of Honduras were high from October to January. 

Plumes were transported by a cyclonic gyre toward the 

Yucatan, creating seasonal variation in the concentration 

of runoff loads along the Mesoamerican Barrier Reef. The 

infl uence of terrestrial runoff was maximal from October 

to January and minimal from March to April.

Long-term in situ measurements of the sort presented 

here are relatively rare. Although the results of our analyses are preliminary, they already demonstrate the value of 

these measurements for advancing our understanding of 

the range and complexity of interactions of natural and 

human-induced variables governing the conditions around 

Carrie Bow Cay and across the region. These in situ data 

are also critical to ground-truthing remotely sensed data 

such as the satellite-generated sea-surface temperature 

(SST) records used to calculate bleaching thresholds during the 1998 ENSO (Aronson et al., 2002). Finally, our 

data are beginning to yield reliable descriptions of water 

quality conditions in the central portion of the Belize Barrier Reef, including those conditions that have accompanied the rapid modifi cations of the Belizean coastal zone 

during the past few decades. Most signifi cantly, the dramatic loss of water quality documented by these long-term 

records has signifi cant biological, management, and economic implications for Belize and the other countries of 

the Mesoamerican Barrier Reef.

ACKNOWLEDGMENTS

This research was funded by grants from the Smithsonian Institution’s Caribbean Coral Reef Ecosystems Program. We thank Dr. Klaus Ruetzler for his support and 

encouragement of the monitoring programs and Mike 

30_Koltes_379-390_Lang.indd 389 0_Koltes_379-390_Lang.indd 389 9/24/09 10:27/24/09 10:27
390 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Carpenter for exceptional support to the fi eld effort. We 

thank the many station managers who have assisted with 

data collection, especially noting the dedicated efforts of 

Dan Miller and Claudette DeCourley over many years. 

Dan has been largely responsible for maintaining the light 

meters on the reef. Dr. Randi Rotjan also generously assisted with the light loggers. We thank John Tschirky who 

has been part of the CARICOMP program since its inception. We thank two reviewers for helpful criticisms that 

improved the manuscript. This is contribution number 

846 of the Caribbean Coral Reef Ecosystems Program 

(CCRE), Smithsonian Institution, supported in part by the 

Hunterdon Oceanographic Research Fund.

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A Numerical Model Study of the Infl uence of the Caribbean Current and Eddies. Ocean Dynamics, 55:458– 475.

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Greer, J. E., and B. Kjerfve. 1982. “Water Currents Adjacent to Carrie 

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Cay, Belize.” In The Atlantic Barrier Reef Ecosystem at Carrie 

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Reefs of Belize.” In Proceedings of the Eighth International Coral 

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pp. 203– 222. Balboa: Smithsonian Tropical Research Institute.

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(accessed 25 May 2009.)

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Meso-American Region. Coral Reefs, 27(4):773– 781 (doi:10.1007/

s00338-008-0396-1).

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Reef Macroalgae Using a Bayesian Belief Network Approach. Ecological Modelling, 220:1305– 1314.

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Washington, D.C.: Smithsonian Institution Press.

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Response of the Mesoamerican Barrier Reef System to Hurricane 

Mitch and Coastal Freshwater Inputs: A Study Using Sea-Viewing 

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and Variability of Water Discharge and Sediment Load in the Inner 

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30_Koltes_379-390_Lang.indd 390 9/29/09 1:59
Global Change and Marsh Elevation 

Dynamics: Experimenting Where Land 

Meets Sea and Biology Meets Geology

J. Adam Langley, Marc V. Sigrist, James Duls, 

Donald R. Cahoon, James C. Lynch, 

and J. Patrick Megonigal

ABSTRACT. Coastal marshes must accumulate soil to keep up with rising sea levels. It is 

unknown how the response of these ecosystems to global change will infl uence their ability to continue to keep up with sea-level rise. Here, we describe an in situ experimental 

chamber approach for manipulating key environmental variables, such as atmospheric 

CO2 and soil N availability, in a brackish marsh. We outfi tted each chamber with surface elevation tables (SETs) to closely monitor soil elevation change, a sensitive indicator 

of marsh vulnerability to sea-level rise. Further, the design facilitates measurements of 

ecosystem exchange of CO2, plant productivity, porewater chemistry, and other environmental parameters.

INTRODUCTION

Projecting the impacts of climate change, eutrophication, and other perturbations on ecosystems requires experimental manipulations. Large experimental 

facilities have been built and operated in all types of ecosystems over the past 

decades to provide such data. There are at least six characteristics that complicate experimental manipulations in tidal wetlands. First, such ecosystems can 

be quickly and irreversibly damaged by heavy foot traffi c, so boardwalks must 

be built to minimize long-term impacts on vegetation and soils. Second, because 

many wetlands have deep, low-density, peaty soils, the permanent infrastructure, such as boardwalks and chambers, must be well anchored for stability. 

Third, tidal wetlands are often inundated by tides and can be under more than 

a meter of water during storm surges, which dictates that all buoyant equipment must be soundly fi xed in place. All electrical service and sensitive equipment 

must be positioned high and be easy to remove during extreme fl ooding events. 

Further, emergency shutoff systems must be in place to cut off the electrical 

supply and gas exchange equipment during fl ood events. Fourth, the water that 

fl oods brackish marshes is saline and corrodes most metals. Fifth, the lack of 

shade means that UV-sensitive materials will degrade. Care must be taken to 

select UV-resistant materials, and even those must be monitored and frequently 

replaced. Sixth, high-latitude marshes may experience cold winters. Ice formation can severely damage even rigid and well-anchored infrastructure. Here we 

J. Adam Langley, Marc V. Sigrist, James Duls, and 

J. Patrick Megonigal, Smithsonian Environmental Research Center, 647 Contees Wharf Road, 

Edgewater, Maryland 21037, USA. Donald R. 

Cahoon and James C. Lynch, U.S. Geological 

Survey, Patuxent Wildlife Research Center, 10300 

Baltimore Avenue, BARC-East Bldg. 308, Beltsville, Maryland 20705, USA. Corresponding author: J. A. Langley (langleya@si.edu). Manuscript 

received 13 May 2008; accepted 20 April 2009.

31_Langley_391-400_Lang.indd 391 1_Langley_391-400_Lang.indd 391 9/24/09 10:24/24/09 10:24
392 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

describe a global change experiment in a brackish marsh 

that was designed to overcome these substantial technical 

challenges.

SITE DESCRIPTION

This study took place at Kirkpatrick Marsh, which is 

located on the Rhode River, a subestuary of Chesapeake 

Bay at the Smithsonian Environmental Research Center 

in Edgewater, Maryland. The site is dominated by the C3

sedge, Schoenoplectus americanus (formerly Scirpus olneyi), and less so by two C4 grasses, Spartina patens and 

Distichlis spicata. The soils at this site are organic (80% 

organic matter) to a depth of approximately 5 m. Mean 

tidal range is 30 cm. The high marsh zone is 40– 60 cm 

above mean low water level and is inundated by 2% of 

high tides. Salinity averages 10 parts per thousand (ppt) 

and ranges from 4 to 15 ppt seasonally. Average daily low 

air temperature is 4°C in January, and the average daily 

high is 31°C in July.

To examine the interactive effects of elevated CO2 and 

nitrogen addition, we identifi ed 20 plots of similar plant 

composition in summer 2005. Each plot consisted of one 

octagon (2 m across) that would be enclosed in an experimental chamber to allow for atmosphere manipulation 

and an adjacent rectangular portion (2  1 m) that served 

as a reference plot to account for spatial variation and to 

gauge potential chamber effects.

CONSTRUCTION

WALKWAYS AND EQUIPMENT HOUSING

A main boardwalk and a series of thinner, lighter “catwalks” were built to access each plot without continually 

walking on the marsh (Figure 1; see also Figures 4, 5). The 

main boardwalk, built perpendicular to shore, roughly bisected the experimental plots. Most of the horizontal surfaces of the boardwalks were fi berglass grating (50% open), 

which allowed light to penetrate through the boardwalks, 

sustaining plant life and providing excellent traction. The 

supports for the main boardwalk were built of 10  10 

cm posts sunk 2 m into the ground. The catwalks departed 

from the main boardwalk, forming a perimeter around each 

experimental chamber (Figure 2). These catwalks were less 

than 30 cm above the ground to avoid shading the plots. 

They were built of fi berglass grating (30 cm wide planks) 

laid fl at on supports built of 2.5 cm polyvinyl chloride 

(PVC) that were anchored more than 1 m into the marsh 

using segments of 2.5 cm PVC pipe. After all walks were in 

place, the marsh surface was rarely stepped upon directly.

Three small pump houses, which housed air sample 

pumps and remote datalogging equipment, were built 

alongside the main boardwalk. An analytical shed was 

constructed on the bank 5 m above sea level to house sensitive analytical equipment.

OPEN-TOP CHAMBERS

The chamber design followed that of a previous opentop chamber study in the same marsh (Drake et al., 1989), 

but with several major innovations to enhance durability 

and plot accessibility (Figures 2– 5). In 2006, the chambers consisted of four major components: base, manifold, 

chamber skeleton, and chamber panels. The octagonal 

shape of the chamber was a compromise between two design goals. It approximated a cylinder, which was ideal 

FIGURE 1. An overhead image of the entire CO2 site. The main 

boardwalk connects to 20 experimental plots by smaller catwalks, 

the paths of which are visible. Gas samples are pumped via the pump 

houses to the analytical shed on the bank.

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NUMBER 38 • 393

for uniform air mixing inside the chamber and minimizing dead spots. The fl at surface of each side allowed us 

to enclose the chamber with eight fl at panels that can be 

removed easily for access to the inside of the chamber.

The base of the chamber was an aluminum octagon 

(0.5 cm thick, with an L-shaped cross section) implanted 

10 cm into the marsh surface. In the portion of the base 

that was implanted into the soil, 2 cm holes were cut to 

allow root growth to further stabilize the base. A hollow 

octagonal manifold (cross section, 30 cm high  6.35 cm 

wide) was attached to the base to distribute infl owing air 

equally around the chamber (see Figure 2). Manifolds were 

built from welded aluminum (grade 6061-T5) covered with 

transparent acrylic panels that allowed light transmittance.

Mounted to the top of the manifold was the “skeleton,” consisting of eight vertical legs supporting an octagonal ring oriented horizontally at the top. The skeleton 

was built from 2.5 cm diameter PVC pipe. The only custom pieces in the skeleton were three-way fi ttings on the 

octagonal ring that join two PVC pipes in the ring with 

one leg. The joint was made by tapping female thread into 

the side of a 45° elbow. The legs of the skeleton sat in 

welded supports on the top of the manifold.

Removable rectangular panels were made from aluminum (grade 6063-T52), covered with infrared (IR)-

transparent fi lm (Aclar 22A, Honeywell) that was taped 

on using transparent UV-resistant tape (3M, 851). The 

fi lm does not absorb IR radiation as do other fi lms and 

therefore heat is not allowed to accumulate. The panels 

were attached to the PVC frame with custom-fi tted PVC 

snaps so that any of the eight panels could be removed 

to access any portion of the plot. Further, panels were removed in the winter to prevent damage while CO2 fumigation was terminated.

Finally, after the 2006 growing season, to conserve CO2

and achieve a more stable CO2 concentration by reducing 

wind incursions, an octagonal frustum, or wind foil, was 

added to the chamber design (see Figure 5). The frustum 

was constructed of 1.9 cm PVC, angled inward at 45°, and 

covered with the same fi lm to reduce wind incursions. The 

fi nal dimensions of the chamber were 1.5 m in height, 2 m 

in diameter, and with 1 m sides; the volume is 6.5 m3.

FIGURE 3. Schematic of the surface elevation table (SET) design. 

The SET arm is periodically connected to the SET rod benchmark, 

which has been anchored into the mineral clay underlying the peat 

profi le. Pins are placed through holes in the SET arm to the soil surface to measure changes in elevation occurring over the entire profi le. Any change in elevation of the shallow benchmarks must occur 

as a result of processes occurring beneath the root zone. Root zone 

changes are calculated by subtracting deep zone elevation change 

from total elevation change.

FIGURE 2. Schematic of an experimental chamber and gas sampling system. The ambient CO2 chambers are the same except there 

is no CO2 delivered into the blower stream. Solid (black) arrows 

represent air fl ow; dotted arrows (appearing light gray) represent 

information fl ow.

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394 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

To move ambient air through the open-top chamber, 

a blower (Dayton, 5C095) was mounted on a stand 1.5 

m above the marsh surface to avoid high tides. The blowers were placed at least 6 m away from each chamber and 

oriented to avoid shading the study area (see Figures 1, 

2, 4). PVC chimneys (two 15 cm pipes per blower) were 

affi xed vertically to the top of the blower intake so that the 

blowers would take in air from 4 m above the ground that 

was not infl uenced by biological activity on the ground 

and thus had relatively stable [CO2]. The chimneys were 

capped to prevent rainwater from entering the blower. A 

20 cm diameter duct fed air from the blower to the chamber manifold. Two hundred fi fty-two 1 cm diameter holes 

(the same total area as the intact pipes) were drilled on the 

inside of the manifold, so that air would fl ow in the chambers equally from each side of the octagon. The blowers 

forced 12.5 m3 per minute through the chambers, resulting 

in an approximate chamber air turnover rate of 2 min– 1.

SURFACE ELEVATION TABLES

To take repeatable measurements of soil elevation, 

each plot was outfi tted with a rod surface elevation table 

(SET; see Figures 3, 4) (Cahoon et al., 2002) modifi ed to 

accommodate plot dimensions. Outside each experimental 

chamber, a posthole was dug roughly 15 cm in diameter 

and 20 cm deep. A 30 cm long PVC pipe (15 cm diameter) 

was placed vertically into the hole. In the center of the 

PVC pipe, a series of attachable stainless steel rods was 

driven with an electric hammer through the entire profi le 

of organic matter (4– 5 m depth) and anchored to the point 

of refusal (6– 7 m) into the subsurface mineral clay underlying the marsh. Concrete was poured into the PVC pipe 

to secure the top of the SET rod.

To isolate the infl uence of root zone processes on elevation, we implanted “shallow benchmarks” to a depth 

of 30 cm. The vertical movement of these benchmarks 

results from processes that occur below the top 30 cm 

of soil. The benchmarks were made of aluminum pipe 

(5 cm diameter by 40 cm long). Several 1 cm diameter 

holes were drilled into the sides of the lower 10 cm of 

the pipe to allow roots to grow through and anchor the 

benchmarks in place. Six benchmarks were implanted to 

a depth of 30 cm under the path of the SET arm in each 

chamber, three inside the chamber and three outside. After FIGURE 4. Photograph of SET measurements being made in summer 2006. Each pin is gently lowered to the soil surface, while applying minimal pressure so that the pin does not depress the soil surface. 

(Photograph by M. V. Sigrist.)

FIGURE 5. Photograph showing a chamber with a frustum that was 

added to all chambers before the 2007 growing season. The tubing 

leading to one set of porewater wells, the gas sampling tube, and the 

catwalk is also visible. (Photograph courtesy J. A. Langley.)

31_Langley_391-400_Lang.indd 394 1_Langley_391-400_Lang.indd 394 9/24/09 10:25/24/09 10:25
NUMBER 38 • 395

placement, solid caps were placed on the top of each pipe. 

All these perturbations, as well as boardwalks to service 

each plot, were completed in the summer of 2005, at least 

9 months before the beginning of the experiment.

At intervals ranging from 1 to 3 months, the modifi ed horizontal aluminum SET arm (4 m long compared 

to less than 0.5 m long for the original rod SET design) 

was attached to the top of the SET rod benchmark, leveled 

precisely, and affi xed to an aluminum post at the other 

end. The arm provided a horizontal reference of known 

elevation across the soil surface; changes in the distance 

from this reference surface to the soil surface were a sensitive measure of changes in soil elevation. Fiberglass pins 

(3 mm in diameter), all exactly 91.0 cm in length, were 

placed through precision-drilled holes in the SET arm at 

1 cm increments. Approximately 40 individual measurements were made in each chamber and 40 in each adjacent, unchambered reference plot. Each pin was carefully 

lowered to the soil surface and gently placed so that no 

litter or live plant obstructed the pin. The height from the 

SET arm to the top of each pin was measured to the nearest millimeter (mm), providing a measurement of total 

elevation. Changes in absolute soil elevation were partitioned into either the root zone (top 30 cm of soil) or the 

deep zone (below 30 cm). To measure elevation changes 

occurring in the deep zone, we lowered 2 to 4 pins to the 

surface of each of the six shallow benchmarks (three inside and three outside each chamber) and measured in the 

same manner. We calculated the change in elevation resulting from processes occurring in the root zone, ER, from 

the two measured variables following the equation ER

 ET ED, where ET represented the change in total 

elevation and ED represented elevation change attributable to change in thickness of the deep zone. Surface accretion was also measured using feldspar marker horizons 

in each plot (Cahoon et al., 1995). To eliminate compaction during coring, the deposition rate was estimated by 

taking cryocores (Cahoon et al., 1996) and measuring the 

amount of soil deposited on top of the marker horizon.

Total soil elevation was strongly related to innate spatial and temporal variability of deep zone dynamics. Specifi cally, changes in the thickness of the deep zone followed 

mean monthly sea level through time, and distance from the 

bank predicted the amplitude of that oscillation. To isolate 

treatment effects on various soil elevation parameters, we 

accounted for variation by referencing SET measurements 

in experimental chambers to those in the adjacent, unchambered reference plots, so that relativized E  experimental 

plot E reference plot E, where E  the elevation parameter of interest. We used a repeated-measures multivariate analysis of variance (MANOVA) to test for changes 

in elevation through time; we used t tests to liberally detect chamber effects on elevation parameters at individual 

dates and a two-way analysis of variance (ANOVA) to test 

for treatment differences in surface accretion.

TREATMENT APPLICATION

CO2 DELIVERY AND SAMPLING SYSTEM

Carbon dioxide was delivered to each of the 10 elevated 

CO2 chambers at a rate of approximately 6 L min1 to 

achieve a target concentration of 720 ppm, which is nearly 

double the current ambient concentration of 380 ppm. Each 

CO2 delivery line was controlled with metered valves and 

fed into the intake chimney on the blower for each respective elevated chamber. Adding the CO2 upstream of 

the blower ensured suffi cient mixing before air entered the 

chamber through the manifold.

Two sample lines continuously pumped air from each 

of 20 chambers to instruments located in a nearby shed: 

one line sampled manifold air and the other sampled the 

chamber atmosphere. To achieve a representative sample 

of the chamber atmosphere, air was sampled with a 2 m 

long pipe oriented horizontally across each chamber. The 

pipe was 1.3 cm diameter PVC with caps on both ends and 

a series of 2 mm diameter holes at geometrically increasing intervals away from the center of the pipe. The geometry allowed air drawn from the center of the pipe to be 

a composite sample representing each point on a transect 

through the chamber equally. The sampling pipe was positioned horizontally and adjusted to roughly half the green 

canopy height to best represent the air that photosynthetic 

tissue experienced.

Air was pulled under negative pressure from each 

chamber a short distance to a Tefl on-coated double diaphragm pump (Thomas Industries, 2107-CA14-TFE), 

from which it was pushed under positive pressure to the 

analytical shed (see Figure 1). To avoid drawing water into 

the pumps, they were plugged into normally closed fl oat 

switches (Dayton 3BY75) that cut the power supply when 

the water level approached the height of the gas sampling 

lines. Each of the 40 lines entered a bank of solenoid 

valves (model 3V1, Sizto Tech Corporation), then fl owed 

into a common line, one for manifold lines and one for 

chamber lines. The two solenoid valves controlling each 

chamber opened simultaneously, one with manifold air 

and the other with chamber air; the other solenoid valves 

remained closed so that the contents of only one chamber at a time passed through the common lines to the gas 

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396 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

analyzers. Each chamber was sampled for 2 min to allow 

ample time for air in the common portion of the system 

to be fl ushed out before measurements were logged, which 

meant that each chamber was sampled at least once every 

40 min.

One infrared gas analyzer (IRGA) measured the difference between a chamber’s manifold air (i.e., incoming 

air) and a dry, zero-CO2 reference gas. A second IRGA 

measured the difference between manifold air and chamber air. This confi guration maximized our ability to precisely measure absolute CO2 concentration and to accurately measure the CO2 concentration difference between 

two locations. A LI-6262 (Licor, Lincoln, NE) had dry, 

zero-CO2 air cycling through the reference cell and the 

manifold air passing through the sample cell. A Li-7000 

(Licor) had the manifold air passing through the reference 

cell and chamber air passing through the sample cell. Cell 

A of the LI-7000 was referenced to an analog signal from 

the LI-6262 as the absolute concentration of CO2 and 

H2O in the manifold air.

We monitored the manifold line to determine how 

much CO2 was being delivered to each manifold. The 

chamber air sampling line allowed us to monitor the actual chamber atmosphere and to fi ne tune the CO2 delivery rate to achieve our target concentration in the chamber atmosphere, accounting for photosynthetic drawdown 

and wind incursions.

NITROGEN FERTILIZATION

A total of 25 g N year1 was applied to each high-N 

plot. Ammonium chloride was dissolved in 5 L brackish 

water from the nearby Rhode River, the subestuary adjacent to the site. At fi ve dates (approximately monthly, 

avoiding high tides) throughout the growing season we 

used backpack sprayers to deliver the fertilizer (equivalent 

to 5 g N) solution to 10 plots. Then, the fertilizer solution 

was rinsed from standing vegetation with another 5 L unamended river water applied with backpack sprayers. Each 

fertilization treatment simulated 5 g N m2 in the equivalent of 0.5 cm river water. The 10 unfertilized chambers 

received 10 L unamended river water applied in the same 

manner. The river water was taken from the tidal fetch 

area adjacent to the marsh. Mean annual [NH 4

] in that 

water ranges from 32 to 82 g L1, with a mean of 52, 

and salinity has ranged from 4.0 to 10.6 ppt, with a mean 

of 6.7, over the past 20 years (growing season means from 

biweekly sampling; Thomas Jordan, unpublished data). 

Assuming the added NH 4Cl integrated into the top 40 cm 

of porewater (as our sampling indicates), and excluding 

losses from the ecosystem or plant uptake, we estimated 

that this fertilization would have increased porewater salinity by a maximum of 0.05 ppt, less than 1% of normal 

salinity.

MEASUREMENTS

The chambered experimental plots consisted of two 

halves, one-half geological and one-half biogeochemical. 

All sampling that involved disturbance of soil was performed on the biogeochemical half. All elevation measurements, which were considered to be more sensitive to soil 

disturbance, were performed on the geological half.

ABOVEGROUND BIOMASS

We estimated peak aboveground biomass with a combination of allometry and harvested subplots (Erickson et 

al., 2007). At the end of July of each year, eight 30  30 

cm quadrats were placed in prescribed locations in each 

plot, six inside the chamber and two in an adjacent unchambered control plot. In the quadrats, each Schoenoplectus americanus stem was counted and nondestructively measured for total height, green height, and width 

at half-height. In the corner of each quadrat, we clipped 

and removed all vegetation and litter in a 5  5 cm area. 

Vegetation was sorted according to species. We measured 

the clipped S. americanus stems for total height and width. 

Clippings were dried for 72 h at 60°C and weighed. We 

measured length and width on a subset of freshly clipped 

stems. We used the calculated relationship between linear 

dimensions and dry mass (r 2  0.9) to estimate the mass 

of each live S. americanus stem. To estimate Spartina patens and Distichlis spicata mass, we scaled up from mass in 

the clipped areas to total chamber area.

ROOT PRODUCTIVITY

Three soil cores (30 cm depth  5 cm diameter) were 

taken from each plot and replaced with cylindrical ingrowth bags (30 cm height  5 cm diameter). The bags 

were constructed from 1 cm mesh and fi lled with milled, 

moistened peat so as to achieve the bulk density of in situ 

peat, 0.12 g cm3. Bags were implanted in winter and removed in November the following year. Contents were 

washed over a 1 mm sieve. Large organic fragments were 

picked out by hand. Root mass was separated into fi ne 

(2 mm diameter) and coarse (2 mm) categories, dried 

for 72 h at 60°C, and weighed.

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NUMBER 38 • 397

POREWATER WELLS

We implanted nine porewater wells (three replicates 

at each of three depths: 20, 40 and 80 cm) in each experimental plot. We built wells from 0.6 cm internal diameter rigid Tefl on tubing (GE Polymershapes) plugged at 

the bottom with silicon caulk and open at the top, which 

extended 10 cm above ground. Sixteen holes (1 mm diameter) were drilled into the bottom 10 cm of the Tefl on 

tube to allow ample conductance of porewater into the 

well. A vinyl hose (6 mm [OD], 3 mm inner diameter [ID]) 

was fastened to the top of each well and draped over the 

chamber for easy access from outside the chamber. Wells 

were fl ushed with 60 mL, equivalent to more than total 

well volume, and sampled monthly for a suite of chemical 

parameters using syringes.

NET ECOSYSTEM EXCHANGE (NEE)

The chambers were also designed to allow for measurement of net ecosystem exchange (NEE) of CO2 between the 

atmosphere and the enclosed ecosystem (Figure 6). Periodically throughout the growing season, octagonal caps were 

placed on a subset of chambers. The purpose of the caps 

was not to render the chamber airtight, but to eliminate 

wind incursions and generate a consistent, predictable 

pattern of air fl ow through the chambers. The caps were 

octagons with a crossbeam built from 1.9 cm PVC pipe 

covered with the same IR-transparent fi lm for the chamber 

panels. The fi lm was perforated with 2 cm diameter holes. 

The gas sampling pipe, described above, was raised to a 

height roughly 30 cm below the cap and aligned with the 

cap perforations. This arrangement allowed us to measure 

the [CO2] of air exiting each chamber after it had been 

infl uenced by soil and vegetation.

To estimate fl ow rate of air through the chamber, we 

cut a slit in the air delivery ducts from each blower and 

measured air velocity using a handheld anemometer (AM 

4822, Mastech; www.p-mastech.com). We initially measured the velocity at a range of distances from the duct 

wall and determined that the mean of two measurements 

(centered at 4 cm and 9 cm from the duct wall) adequately 

estimated the average velocity for the entire cross section. 

Multiplying velocity (cm s1) and cross-sectional area (cm2) 

FIGURE 6. Net ecosystem exchange (NEE) of CO2 over three days in July 2007. Negative values represent 

net uptake by the ecosystem. Generally, values are negative in summer daytimes when photosynthetic rate 

surpasses respiration rate. Each point represents the means of approximately 12 individual measurements 

from each of two replicate chambers binned into 2.4-h intervals. amb  ambient; elev  elevated; ambN 

ambient N; elevN  elevated N.

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398 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

yielded volumetric fl ow rate (cm3 s1). The volumetric fl ow 

rate was converted to mass fl ow using air temperatures 

from the site. We calculated NEE as ([CO2]in [CO2]out) 

 fl ow rate.

Because we did not want to incur chamber effects such 

as warming or rain exclusion, we measured NEE on a rotating subset of chambers balanced by treatment, for variable 

intervals from 3 to 7 days. These data will be used to calculate NEE light-response curves for net CO2 uptake during 

the day and NEE temperature-response curves for net CO2

release during the night. The response curve models will be 

driven with continuous measurements of soil temperature 

and photosynthetically active radiation to extrapolate up to 

integrated NEE for a complete growing season (Rasse et al., 

2003). The gas sampling program was adjusted to increase 

the frequency with which NEE chambers were sampled to 

increase resolution for these low signal-to-noise NEE measurements, compared to the relatively stable absolute atmospheric [CO2] data when all chambers are sampled equally.

ENVIRONMENTAL VARIABLES

Soil temperature was measured at 5 and 15 cm depth 

using type-T thermocouples. Wind speed was monitored 

with an anemometer (O14A-L, Campbell Scientifi c, Logan, 

UT). Water level was recorded using a differential pressure transducer (PS-9805, Northwest Technologies) placed 

at the bottom of a 0.5 m well. All environmental data 

were logged on a combination of a multiplexor (AM32T, 

Campbell Scientifi c) for temperature and a datalogger 

(CR10X, Campbell Scientifi c), which were positioned 

remotely in the marsh to minimize analog signal degradation. Information was then relayed digitally between 

the marsh and main datalogger (CR1000, Campbell Scientifi c) using multidrop interfaces (MD485, Campbell 

Scientifi c).

RESULTS AND DISCUSSION

TREATMENT APPLICATION

Average daily mean CO2  SE was 394  1.2 ppm in 

ambient and 707  6.0 ppm in elevated chamber atmosphere 

in 2007, a treatment difference of 313 ppm. The standard 

deviation among daily means for individual chambers averaged 21.9 and 59.0 ppm for individual ambient and elevated chambers. The variation in means between days was 

driven by differences in wind speed (Figure 7). High winds 

resulted in incursions of ambient air into elevated chambers, thereby diluting the elevated [CO2]. On the other 

hand, stillness allowed respired CO2 to accumulate overnight, which increased background [CO2] in ambient and 

elevated chambers. Because this buildup affects each treatment equally, the difference between ambient and elevated 

chambers persisted. However, wind incursions drove down 

concentrations in elevated chambers only, which decreased 

the difference between ambient and elevated [CO2].

In 2006, before chambers were equipped with frusta, 

ambient and elevated chambers [CO2] were 395 and 669, 

a difference of 274 ppm. Although the mean [CO2] could 

have been elevated in the chamber without adding frusta, 

the fl uctuations with wind would have been extreme, and 

the expense of the additional CO2 was deemed prohibitive.

The [NH 4] in porewater was successfully increased by 

the N addition by a factor of 2.9, from 17 to 64 mol L1

averaged over the growing season in 2006. The factor by 

which N addition increased porewater [NH 4] was much 

higher early in the season and declined as growing plants 

took up N.

MEASUREMENT VALIDATION: CHAMBER EFFECTS

Elevation

To examine the possibility of chamber effects on elevation, we examined the measurements in the ambient CO2, 

FIGURE 7. The CO2 treatment and wind speed from four varying 

days in August 2007. The shaded areas represent hours of darkness when the CO2 delivery was shut down. During those off hours, 

all chambers were at ambient [CO2]. During still nights, ambient 

[CO2] approached concentrations much higher than well-mixed atmospheric [CO2] as respired CO2 accumulated relatively near the 

ground.

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NUMBER 38 • 399

low-N (no added N) treatment (Figure 8). The in-chamber 

measurements were very similar to those in the reference 

plots. Both sets of data revealed signifi cant changes in elevation through time (repeated-measures MANOVA, P 

0.05). Most notably, all plots experienced a dip of roughly 

0.8 cm in total elevation during March 2007, followed 

by a strong recovery. This dip was driven entirely by dynamics in the thickness of the deep zone. Compared to 

absolute changes in elevation (range, 1.2 cm), the differences between in-chamber and reference elevation were 

relatively small (range, 0.2 cm). There was a trend of 

a chamber effect on total elevation driven by deep zone 

dynamics. This effect was signifi cant in summer 2007 but 

has vanished since then. The relativized root zone thickness in ambient CO2, low-N chambers never differed from 

zero (t test, P  0.40 for all dates), which indicated that 

there was not a detectable chamber effect in this stratum 

where we expected treatment effects to be manifested.

Surface Accretion

One criticism of the design was that the chambers, by 

enclosing plots, may have excluded sediments from being 

deposited on the marsh surface. The difference between 

in-chamber and reference accretion measured with cryocores in November 2007 was small (0.058 cm) and did 

not differ signifi cantly from zero (95% confi dence interval: 0.18 to 0.07, n  20). The treatment means also did 

not differ from each other (two-way ANOVA: CO2, P 

0.10; N, P  0.10) or from the reference plots (chamber 

effect: P  0.10; Figure 9).

CONCLUSIONS

The design of our fi eld experiment proved robust to a 

number of challenges unique to tidal salt marsh environments, including saltwater corrosion and deep tides. More 

importantly the chamber design allowed us to consistently 

elevate atmospheric CO2. The frustum was a key feature 

of the chamber because it average-stabilized and raised the 

[CO2] in the elevated treatment, likely resulting in saved 

FIGURE 8. Elevation data from the fi ve ambient CO2, low-nitrogen 

(N) plots. Change in total elevation is partitioned between changes 

in thickness of either the deep zone or root zone. Top panel: elevation and thicknesses from inside the experimental chambers; middle 

panel: from the adjacent reference plots; bottom panel: difference 

between the in-chamber and reference measurements (relativized). 

There was a slight chamber effect on total elevation, driven by contraction of deep zone thickness. Root zone did not differ from zero.

FIGURE 9. Surface accretion measured as the accumulation of matter on top of the marker horizon inside the chamber versus that 

outside the chamber. It was thought the chambers may exclude exogenous sediment, but there was no difference between in-chamber 

(black bars) and outside-chamber (reference plot, white bars) accretion rates. Amb  ambient; Elev  elevation.

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400 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

CO2. N addition yielded higher porewater N concentrations as expected, but further chemical analyses are 

needed for a more precise estimate of the magnitude of 

the N treatment. The SET design allowed for sensitive 

measures of soil elevation change. The chambers, perhaps 

by virtue of their mass, appeared to slightly depress soil 

elevation. However, there was no chamber effect in the 

root zone where the most important treatment effects are 

expected to occur. Further, the size of the chamber effect 

on elevation was small (0.2 cm; Figure 8, bottom panel) 

relative to the natural range of variation in those elevation 

parameters (1.2 cm; Figure 8, middle panel).

ACKNOWLEDGMENTS

We thank J. Keller, G. Peresta, B. Drake, E. Sage, 

A. Martin, D. McKinley, S. Chapman, K. White, and N. 

Mudd from the Smithsonian Environmental Research 

Center for construction and maintenance of the fi eld experiment. The fi eld study was supported by the U.S. Geological Survey Global Change Research Program, U.S. 

Department of Energy (grant DE-FG02-97ER62458), the 

U.S. Department of Energy’s Offi ce of Biological and Environmental Research through the Coastal Center of the 

National Institutes for Climatic Change Research at Tulane University, and the Smithsonian Institution.

LITERATURE CITED

Cahoon, D. R., J. C. Lynch, and R. M. Knaus. 1996. Improved Cryogenic Coring Device for Sampling Wetland Soils. Journal of Sedimentary Research, 66:1025– 1027.

Cahoon, D. R., J. C. Lynch, B. C. Perez, B. Segura, R. D. Holland, C. Stelly, 

G. Stephenson, and P. Hensel. 2002. High-Precision Measurements 

of Wetland Sediment Elevation: II. The Rod Surface Elevation Table. Journal of Sedimentary Research, 72:734– 739.

Cahoon, D. R., D. J. Reed, and J. W. Day. 1995. Estimating Shallow Subsidence in Microtidal Salt Marshes of the Southeastern 

United States— Kaye and Barghoorn Revisited. Marine Geology, 

128:1– 9.

Drake, B. G., P. W. Leadley, W. J. Arp, D. Nassiry, and P. S. Curtis. 1989. 

An Open Top Chamber for Field Studies of Elevated Atmospheric 

CO2 Concentration on Saltmarsh Vegetation. Functional Ecology, 

3:363– 371.

Erickson, J. E., J. P. Megonigal, G. Peresta, and B. G. Drake. 2007. Salinity and Sea Level Mediate Elevated CO2 Effects on C3– C4 Plant Interactions and Tissue Nitrogen in a Chesapeake Bay Tidal Wetland. 

Global Change Biology, 13:202– 215.

Rasse, D. P., J. H. Li, and B. G. Drake. 2003. Carbon Dioxide Assimilation by a Wetland Sedge Canopy Exposed to Ambient and Elevated 

CO2: Measurements and Model Analysis. Functional Ecology, 

17:222– 230.

31_Langley_391-400_Lang.indd 400 1_Langley_391-400_Lang.indd 400 9/24/09 10:25/24/09 10:25
Herbivory, Nutrients, Stochastic Events, 

and Relative Dominances of Benthic 

Indicator Groups on Coral Reefs: 

A Review and Recommendations

Mark M. Littler, Diane S. Littler, 

and Barrett L. Brooks

ABSTRACT. Threshold levels (i.e., tipping points where the probability of community 

phase shifts is increased and the potential for recoverability is reduced) for critical bottomup interactions of productivity (e.g., nutrients) and those for top-down disturbances (e.g., 

herbivory) must be known to manage the competitive interactions determining the health 

of coral-dominated reefs. We further posit that latent trajectories (reduced resiliencies/

recoverability from phase shifts) are often activated or accelerated by large-scale stochastic disturbances such as tropical storms, cold fronts, warming events, diseases, and 

predator outbreaks. In highly diverse and productive reef ecosystems, much of the overall 

diversity at the benthic primary producer level is afforded by the interaction of opposing 

nutrient-limiting/nutrient-enhancing and herbivory controls with the local physical and 

spatial variability, such that a mosaic of environmental conditions typically occur in close 

proximity. Although the relative dominance model (RDM) appears straightforwardly 

simple, because of the nature of direct/indirect and stimulating/limiting factors and their 

interactions it is extremely complex. For example, insuffi cient nutrients may act directly 

to limit fl eshy algal domination (via physiological stress); conversely, abundant nutrients 

enhance fl eshy algal growth, with the opposite effect on reef-building corals (via toxic 

inhibition or increased diseases). Furthermore, the effects of controls can be indirect, 

by infl uencing competition. Even this seemingly indirect control can have further levels 

of complexity because competition between algae and corals can be direct (e.g., overgrowth) or indirect (e.g., preemption of substrate). High herbivory (via physical removal) 

also acts indirectly on fl eshy algae through reduced competitive ability, whereas lowered 

herbivory and elevated nutrients also indirectly inhibit or control corals and coralline algae by enhancing fl eshy algal competition. Other ecologically important bottom-up factors, such as reduced light, abrasion, allelopathy, disease vectoring, and sediment smothering, also result from indirect side effects of fl eshy algal competition. These factors tend 

to selectively eliminate the long-lived organisms in favor of weedy fast-growing species, 

thereby reducing desirable complexity and biodiversity.

INTRODUCTION

There has been an exhaustive debate in the coral reef literature over the relative importance of forces that regulate community structure and resilience (i.e., 

the potential to resist stresses and to recover following disturbances). The expansion of the human population and associated increases in destructive fi shing 

Mark M. Littler, Diane S. Littler, and Barrett L. 

Brooks, Department of Botany, National Museum of Natural History, Smithsonian Institution, 

P.O. Box 37012, MRC 166, Washington, D.C. 

20013-7012, USA. Corresponding author: M. 

Littler (littlerm@si.edu). Manuscript received 13 

May 2008; accepted 20 April 2009.

32_Littler_401-414_Lang.indd 401 2_Littler_401-414_Lang.indd 401 9/24/09 10:33/24/09 10:33
402 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

(Hughes, 1994) and nutrient loading (Lapointe, 1999), compounded with ocean warming (Hoegh-Guldberg, 1999) and 

stochastic environmental effects (Precht et al., 2005), have 

been broadly debated to explain the increasing degradation of coral reefs worldwide. Because human population 

growth is not expected to abate, discriminating among 

various stressors is critical to determine conservation 

strategies and to eventually ameliorate the accelerating 

degradation of coral reefs. What has been lacking is the 

ability to rigorously test and differentiate among the possible acute versus chronic stressors— leading to ongoing 

controversy. In an attempt to address this problem, several workers (Mora, 2008; Burkepile and Hay, 2006) have 

conducted broad correlative and statistical assessments 

of communities over large regional scales. These studies 

have suggested a clear interaction between eutrophication 

in conjunction with declining herbivorous organisms as 

direct causes for maintaining present undesirable phase 

shifts on coral reefs.

Such phase shifts have been devastating to the many 

uniquely specialized benthic photosynthetic symbionts 

dominating tropical reefs, which are responsible for some 

of the most productive natural ecosystems known. Four 

major space-occupying groups of benthic primary producers combine to create high coral-reef primary productivity: 

reef-building corals (containing symbiotic algae), crustose 

coralline algae, algal turfs (fl eshy fi lamentous and lowgrowing prostrate forms, and frondose macroalgae. Of 

these, photosynthetic corals create much of the structural 

heterogeneity and complexity and, with coralline algae, 

are primarily responsible for accretion of CaCO3 into the 

reef matrix— making them the most desirable functional 

groups from a management perspective.

A basic objective in management ecology is to determine the mechanisms by which natural and anthropogenic 

factors maintain or alter structure and interactions in biotic communities. Anthropogenic eutrophication and destructive overfi shing (i.e., herbivore removal by trapping, 

netting, poisoning, blasting) are the most tractable factors correlated with the marked global decline in tropical 

reef communities over the past two decades (see reviews 

in Ginsburg, 1994; Birkeland, 1997; papers in Szmant, 

2001). The theoretical framework involving “top-down” 

regulation by predators and “bottom-up” control by resource availability in terrestrial systems was fi rst proposed 

by Hairston et al. (1960), concepts that were later used 

(Atkinson and Grigg, 1984) to describe mechanisms that 

regulate the structure of coral-reef communities. These 

factors provide a valuable perspective (Figure 1) to assess 

and manage the human activities that affect the interactive mechanisms controlling stable states, tipping points, 

phase shifts, and recovery among the dominant functional 

groups of primary producers on tropical reefs.

In healthy coral-dominated reefs, nutrient concentrations are extremely low and attachment space is occupied 

by a broad diversity of three-dimensional overgrowing organisms. Given these conditions, the major tenets of the 

management model proposed by Littler and Littler (2006: 

fi g. 1, relative dominance model [RDM]) are (1) that competition for space and light is crucial in determining the relative abundances of major benthic photosynthetic organisms, 

and (2) that the outcome of competition for these resources 

is most often, but not exclusively, controlled by the complex 

interactions of biological factors (top-down controls such 

as grazing) and environmental factors (bottom-up controls 

such as nutrient levels). As suggested by Grime (1979) 

for terrestrial plants and expanded for marine macroalgae (Littler and Littler, 1984; Steneck and Dethier, 1994), 

primary producer abundance and evolutionary strategies 

are controlled by physical disturbances (i.e., factors that 

remove biomass) coupled with physiological stresses (i.e., 

factors that limit metabolic production). In the conceptual 

relative dominance model (RDM; see Figure 1), grazing 

physically reduces biomass (top-down) and nutrients control production (bottom-up). The complex natural interactions between herbivory and nutrients are most dramatically impacted by large-scale catastrophic disturbances 

such as tropical storms (Done, 1992), warming events 

(Macintyre and Glynn, 1990; Lough, 1994), cold fronts 

(Precht and Miller, 2007), diseases (Santavy and Peters, 

1997), and predator outbreaks (Cameron, 1977). These 

events serve to trigger or accelerate the ultimate long-term 

phase shifts postulated in the RDM. Such stochastic events 

selectively eliminate the longer-lived organisms in favor of 

faster-growing fl eshy macroalgae, which are often competitively superior (Birkeland, 1977). However, nutrients and 

herbivory, in the absence of large-scale disturbances, are 

both suffi cient to maintain phase shifts independently or 

in concert (Smith et al., 2001; Armitage and Fong, 2004; 

Littler et al., 2006a).

On undisturbed oligotrophic coral-reef habitats, the 

effects of well-documented top-down physical controls via 

intense herbivory prevail, where changes in grazing intensity often show acutely rapid effects. Conversely, bottom-up 

stimulatory controls are more chronic, the result of lack of 

nutrient availability, overcompensation by grazers, and a 

slower growth response, compared with acute physical destruction by herbivory. However, under persistent elevated 

nutrient conditions (relative to low [near-undetectable] 

concentrations), consistent coral declines can occur, con32_Littler_401-414_Lang.indd 402 2_Littler_401-414_Lang.indd 402 9/24/09 10:33

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NUMBER 38 • 403

comitant with algal increases that may lead to enduring 

states throughout all combinations of herbivory (Littler 

et al., 2006a). Changes in bottom-up controls and their 

interactions not only alter the dominance patterns of the 

major benthic functional groups on coral reefs but, hypothetically, could have profound long-term consequences 

mediated through structural transformations and chemical modifi cations to reef systems and their herbivorous 

fi sh populations. In other words, excessive nutrient enrichment not only increases the productivity and biomass of 

weedy macroalgae via bottom-up controls that alter patterns of competitive dominance (Littler et al., 1993) but, 

over the long term, may lead to coral habitat degradation 

through (1) reduced spatial heterogeneity by overgrowth 

(Johannes, 1975; Pastorok and Bilyard, 1985; Szmant, 

1997) and (2) nighttime anoxic conditions (tolerated by 

macroalgae, but not by coral competitors and herbivorous 

predators; Lapointe and Matzie, 1996) that could indirectly reduce top-down grazer effects. Furthermore, fl eshy 

macroalgal blooms, irrespective of how they are induced, 

decrease the growth and reproductive capacity of the more 

structurally complex reef-building corals (Tanner, 1995; 

Miller and Hay, 1996; Bellwood et al., 2006; Hughes et 

al., 2007), as well as inhibit coral larval recruitment (Birkeland, 1977; Tomascik, 1991; Ward and Harrison, 1997) 

and survival (Lewis, 1986; Hughes et al., 1987; Hughes, 

1989; Wittenberg and Hunte, 1992). Such complicated 

feedback loops following eutrophication (e.g., anoxia) are 

known to occur in seagrass meadows (Sand-Jensen and 

Borum, 1991; Duarte, 1995) and could also explain decreases in fi sh populations on coral reefs with long-term 

histories of eutrophication.

CORAL-REEF MANAGEMENT

The data relevant for long-term reef management consist of (1) many important short-term caging and feeding 

experiments (in the case of exceedingly well-documented 

top-down herbivory effects), (2) circumstantial evidence 

(Hallock et al., 1993), (3) correlative biogeographic surveys contrasting oligotrophic versus eutrophic systems 

(Littler et al., 1991; Verheij, 1993; Mora, 2008), (4) comparative experiments on systems containing natural nutrient gradients (Lapointe et al., 2004, 2005b; Vroom et al., 

2005), (5) physiological assays (Littler and Littler, 1990; 

Lapointe et al., 1997), and (6) logistically complicated, in 

situ, long-term, experimental/causality studies, in the case 

of bottom-up nutrient controls (Smith et al., 2001; Littler 

et al., 2006a). Top-down control by abundant populations 

FIGURE 1. The competition-based relative dominance model 

(RDM). All the functional indicator groups occur under the conditions of every compartment of the model; however, the RDM predicts which group will most often dominate. Light to dark shading indicates declining desirability of each functional group from 

a management perspective. Crustose coralline algae are posited to 

be competitively inferior and dominate mainly by default, that is, 

where fl eshy algae are removed by herbivores and some corals are 

inhibited by nutrients. The dashed lines approximate tipping points 

where declining herbivory and increasing nutrients reach critical levels that begin to reduce resilience to and recoverability from phase 

shifts. One vector can partially offset the other; for example, high 

herbivory can delay the impact of elevated nutrients, or low nutrients 

may offset the impact of reduced herbivory. As a baseline for healthy 

coral-reef habitats, herbivore population abundances and diversity 

should be high and palatable test plants should show at least greater 

than 50% loss 6 h1 (i.e., 6 h half-life) during a replicated series of 

midday in situ exposures. Hypothetical nutrient tipping points (i.e., 

thresholds that sustain algal growth) are thus far indicated to be quite 

low (i.e., 0.1 M soluble reactive phosphorus [SRP], 1.0 M dissolved inorganic nitrogen [DIN]), as suggested by laboratory growth 

experiments, case studies for macroalgal overgrowth of coral reef 

communities, and in situ experimental nutrient enrichment research 

(Bell, 1992; Bell and Elmetri, 1995; Lapointe et al., 1993, Bell et al., 

2007). We further posit that latent trajectories (reduced resilience/

recoverability from phase shifts) are often triggered or accelerated 

by large-scale stochastic disturbances such as tropical storms, cold 

fronts, warming events, diseases, and predator outbreaks. Although 

these are events from which coral reefs have recovered for millions 

of years in the absence of humans, when tipping points remain surpassed, less-desirable stable states can persist.

32_Littler_401-414_Lang.indd 403 2_Littler_401-414_Lang.indd 403 9/24/09 10:33/24/09 10:33
404 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of large mobile herbivores is particularly well studied for 

coral reefs, beginning nearly fi ve decades ago with the caging study of Stephenson and Searles (1960 As examples, 

Sammarco et al. (1974), Ogden and Lobel (1978), Sammarco (1980), Carpenter (1986), Lewis (1986), Morrisson (1988), and numerous other workers (see review by 

McCook et al., 2001) have demonstrated that lowering 

herbivory in low-nutrient habitats (usually assumed) often 

results in rapid increases in low-growing stages of fl eshy 

macrophytes.

In the study of Lewis (1986) on the same reef fl at studied by Littler et al. (2006a, 2006b), increases in a dominant vegetative algal turf form (Vaughaniella stage) with 

its upright fertile Padina blades, not blooms of mixed 

macroalgae, followed short-term (11 week) reductions of 

herbivorous fi sh grazing under conditions of low nutrient 

levels. Lewis’ (1986) table 4 (although pseudoreplicated) 

shows statistically signifi cant, but relatively small, increases (26%) in the above Vaughaniella-turf stage and its 

reproductive Padina blades; however, in contrast to several literature citations, no signifi cant increases occurred 

in any of the abundant upright macroalgal dominants such 

as Turbinaria turbinata and Halimeda spp. Such low mats 

are unique in containing an abundance of nitrogen-fi xing 

blue-green algae that can enrich other members within 

the low-growing algal community (Adey and Goertmiller, 

1987; Adey, 1998). In presumably higher-nutrient environments, herbivore removals usually result in dramatic 

blooms of larger frondose macroalgae (Bellwood et al., 

2006: fi g. 4; Hughes et al., 2007).

Throughout the past decade, many biologists and 

managers have not recognized the importance of chronic 

nutrient enrichment and associated eutrophication problems facing coral reefs. A recent study (Littler et al., 2006b) 

provided a detailed review and discussion of the misinterpretations, misunderstandings, and suboptimal experimental designs that pervade the literature in regard to nutrient 

enrichment and the health of coral reefs. Overgrown 0.5 L 

porous clay-pot diffusers (“mini-reefs,” following a decade of recruitment, colonization, and competition) were 

utilized (Littler et al., 2006b) to evaluate protocols for 

studies of controlled nutrient enrichment on coral reefs. 

A commonly used nutrient source, Tree Food Stakes containing up to 6% chlorine, resulted in a signifi cant 11-

fold and 20-fold decrease of fl eshy algae and calcareous 

coralline algae, respectively, relative to the control treatments, while blue-green algae (Cyanobacteria) became 

signifi cantly (6 fold) more abundant. Osmocote-fi lled 

mini-reefs showed no signifi cant differences from the 

controls for any of the indicator groups. By avoiding the 

pitfalls of suboptimal study areas, insuffi cient duration of 

colonization/competition studies, inadequate nutrient detection limits, and inappropriate sources of enrichment in 

future research, the potential to provide new insights into 

the nutrient status of coral reefs will be greatly improved. 

Nutrient research is logistically diffi cult and, because the 

growth responses are relatively slow (i.e., chronic), requires more emphasis on multifaceted approaches carried 

out over suffi ciently long time periods. Optimally, studies 

should include in situ enrichment experiments that test the 

long-term competitive interactions of functional indicator 

groups on healthy coral-dominated reefs, in addition to 

precisely monitoring water column nutrient levels, tissue 

C:N:P ratios, and algal physiological response assays.

Although nutrient data are typically lacking in coralreef herbivory studies, natural background levels in conjunction with ample water motion are usually assumed to 

exceed levels that are limiting to macroalgal growth (Fong 

et al., 2003). As pointed out by Lewis (1986), large frondose macroalgae such as Sargassum and Turbinaria do occur in oligotrophic reef areas adjacent to coral colonies (see 

also Littler et al., 1986; McCook et al, 2001; Vroom at 

al., 2005); however, many of these frondose forms occupy 

microhabitats that generate increased current acceleration, 

such as the reef crest and tops of patch reef rocks, implicating higher nutrient fl uxes (Atkinson et al., 2001). Also, 

large biomass/standing stocks of slow-growing perennial 

macroalgae (e.g., rockweeds) can develop over time under 

low inorganic nutrient concentrations; rainforests are good 

illustrations of this as well. Furthermore, Sargassum spp. 

can coexist with corals in oligotrophic waters by utilizing 

particulate organic sources of nutrients (Schaffelke, 1999); 

therefore, in this particular situation, large plant biomasses 

of low diversity do not necessarily indicate detrimentally 

abundant dissolved nutrients. Tissue analyses of mid-shelf 

Sargassum transplants on the great barrier reef (McCook, 

1999) revealed a C:N ratio of 32:1 and a C:P ratio of 

1261:1, exceeding values for pelagic Sargassum in the nutrient-impoverished Sargasso Sea (C:P  877:1; Lapointe, 

1995), which are compelling for substantial N limitation 

and severe P limitation. A further consideration is the nowubiquitous presence of signifi cant anthropogenic nitrogen 

sources (from burning fossil fuels) in rainfall worldwide 

(Vitousek et al., 1997), making the term “pristine” relative, 

at best. The demise of copious coral cover (Pollock, 1928) 

and concomitant rise in frondose algae (Doty, 1971) and 

coralline algae (Littler, 1971) on the reef fl at at Waikiki, 

Hawaii, was the fi rst phase shift from coral to macroalgal 

domination that was postulated (Littler, 1973) as caused 

by increases in eutrophication (bottom-up control).

32_Littler_401-414_Lang.indd 404 2_Littler_401-414_Lang.indd 404 9/24/09 10:33/24/09 10:33
NUMBER 38 • 405

Eutrophication affects coral reefs to different degrees 

and on varying scales. Several studies (Atkinson et al., 

1995; Grigg, 1995; Steven and Broadbent, 1997; McCook, 

1999; Bongiorni et al., 2003) indicated no substantial adverse responses of coral species to elevated nutrients. However, other laboratory and fi eld experiments (Pastorok and 

Bilyard, 1985; Tomascik and Sander, 1987; Muscatine et 

al., 1989; Stambler et al., 1991; Jokiel et al., 1994; Koop 

et al., 2001) have concluded that corals are negatively affected by increased levels of nutrients and that diversity 

suffers. Numerous in situ observations exemplify the types 

of shifts from coral dominance to algal dominance that 

suggest linkages with chronic nutrient loading, including 

case studies in Hawaii (Littler, 1973; Banner, 1974; Smith 

et al., 1981; Maragos et al., 1985; Grigg, 1995), Venezuela (Weiss and Goddard, 1977), the Red Sea (Mergener, 

1981; Walker and Ormond, 1982), Barbados (Tomascik 

and Sander, 1985, 1987), American Samoa (Green et al., 

1997), Reunion Island (Cuet et al., 1988; Naim, 1993), 

Bermuda (Lapointe and O’Connell, 1989), the Great 

Barrier Reef (Bell, 1992), the Florida Keys (Lapointe et 

al., 1994), Martinique (Littler et al., 1993), and Jamaica 

(Goreau et al., 1997; Lapointe et al., 1997).

In a number of cases, herbivory patterns alone (similar to nutrient levels) do not explain the distribution and 

abundance of benthic algae on coral reefs (Adey et al., 

1977; Hay, 1981; Hatcher, 1983; Hatcher and Larkum, 

1983; Carpenter, 1986). Several studies (Hatcher, 1981; 

Schmitt, 1997; Lirman and Biber, 2000) found no signifi cant correlation between grazing intensity and algal 

biomass. A dramatic increase in algal biomass resulting 

from eutrophication, without any simultaneous reduction 

in herbivore populations, was reported (Fishelson, 1973). 

The importance of the very low nutrient levels involved in 

eutrophication (i.e., nutrient threshold hypothesis, NTH), 

either natural or anthropogenic, has only recently come to 

light (Bell, 1992; Lapointe et al., 1997; Small and Adey, 

2001; Bell et al., 2007) regarding the potential for phase 

shifts from corals toward macroalgal dominance. These 

kinds of biotic phase shifts also have been attributed to 

overfi shing of herbivore stocks (see Hughes, 1994 on 

Jamaican reef trends), in concert with cultural eutrophication (Goreau et al., 1997; Lapointe et al., 1997). It is 

now clear (Burkepile and Hay, 2006; Mora, 2008) that 

both herbivory and nutrient levels interact on large scales 

as major factors in maintaining or degrading coral-reef 

health.

We hasten to point out that individuals of all the functional indicator groups can and do occur under the conditions of every compartment of the RDM (see Figure 1); 

however, the model predicts which group most often will 

dominate (as does the very similar fi g. 2a in Bellwood et 

al., 2004). Such apparent presence/absence anomalies, 

on closer inspection, are often scientifi cally logical but 

have led to different perspectives. Following large coral 

bleaching events and die-offs in Belize, we have observed 

dramatic increases in chemically defended sponges (e.g., 

Chondrilla) and Cyanobacteria (blue-green algae) under 

high levels of grazing by sea urchins and fi shes. Other observations that appear counterintuitive include some corals 

growing in high-nutrient habitats, some large fl eshy macroalgae growing under low nutrients, certain turf algae exposed to high herbivory, and the frequent coexistence of 

crustose corallines and the other functional groups. We 

agree with these observations and have addressed such 

anomalies herein.

The general applicability as well as the limitations of 

the RDM can be demonstrated further in relationship to 

a number of recent studies. For example, nutrients and 

herbivory are not independent, and the positive effects of 

nutrients on marine plant productivity and growth can actually make plants more palatable and susceptible to grazers (McGlathery, 1995; Boyer et al., 2004). Furthermore, 

nutrient increases are sometimes associated with coral 

inhibition (Koop et al., 2001) as well as coral diseases 

(Harvell et al., 1999, 2002; Bruno et al., 2003), and algal 

blooms can serve as disease vectors (Nugues et al., 2004). 

The sophisticated enrichment study (ENCORE) on a large 

and carefully controlled scale (Larkum and Koop, 1997; 

Encore Group, 2001) did not produce supportive results 

because (1) ambient nutrient levels within the lagoon at 

One Tree Island are well above tipping-point concentrations that may be inhibitory to some corals, while being 

more than suffi cient to support luxuriant frondose macroalgal growth (Bell, 1992; Larkum and Koop, 1997; Bell 

et al., 2007) and (2) the test organisms were isolated on 

raised grids to measure growth rates, precluding natural 

encroachment, overgrowth, or other competitive interactions crucial to testing the RDM. However, all increases 

in nutrient levels did adversely affect coral reproduction 

(Koop et al., 2001). Additionally, several short-term (4 

months) studies (Thacker et al., 2001; Belliveau and Paul, 

2002; Miller et al., 1999; McClanahan et al., 2002) reported lack of algal stimulation following nutrient enrichment, further documenting the low ambient nutrient concentrations sustaining ample algal growth.

In contrast, two in situ experimental studies conducted over longer time scales in healthy coral-reef settings 

(Smith et al., 2001; Littler et al., 2006a), in conjunction 

with natural successional and competitive interactions, 

32_Littler_401-414_Lang.indd 405 2_Littler_401-414_Lang.indd 405 9/24/09 10:33/24/09 10:33
406 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

provided the most relevant causality data demonstrating 

the importance of both nutrient and herbivory infl uences; 

the present review builds on these fi ndings. The paper by 

Lapointe (1997) was the fi rst to put forth a convincing 

case for the effectiveness of the RDM in addressing harmful algal bloom issues on coral reefs. Additionally, highly 

diverse living model systems of coral-reef communities 

(i.e., mesocosms), operated for decades (Small and Adey, 

2001), clearly have demonstrated that minute increases 

in nitrogen and phosphorus reduce coral growth (sometimes causing substantial die-backs). Such self-contained 

systems require continuous removal of nutrients by algalturf scrubbers or protein skimmers in combination with 

an abundance of fi sh and invertebrate grazers to maintain 

a high coral and algal diversity. The burgeoning awareness of coral-reef degradation worldwide (see Ginsburg, 

1994; chapters in Birkeland, 1997; Gardner et al., 2003), 

particularly from coastal eutrophication (Bell, 1992; Windom, 1992; Nixon, 1995; Lapointe, 1997, 1999) and destructive overfi shing (Hughes, 1994; Jackson et al., 2001), 

makes this management perspective relevant and opportune (see Figure 1).

Although harmful macroalgal blooms on coral reefs 

have long been attributed to nutrient enrichment and 

eutrophication (Littler, 1973; Banner, 1974; Johannes, 

1975; Smith et al., 1981; Lapointe, 1997; Lapointe et al., 

2005a, 2005b), some reef biologists have countered that 

such changes in benthic community structure routinely 

result primarily from natural stochastic events (Precht et 

al., 2005), overfi shing of herbivorous fi sh stocks (Hughes, 

1994; Pandolfi et al., 2003; Lesser, 2004), or loss of keystone grazers, such as the long-spined sea urchin Diadema 

antillarum (Jackson et al., 2001). Although generally supported, these last observations are not typical of the majority of grazer reduction experiments in extreme oligotrophic 

environments (see Lapointe, 1999), most of which have 

reported an expansion of small low-growing algal forms 

rather than macroalgal blooms (as predicted in Figure 1). 

It is encouraging that the critical role of excess nutrients 

on coral reefs has begun to receive attention in recent review papers (Scheffer et al., 2001; Hughes et al. 2003; 

Bellwood et al., 2004; Pandolfi et al., 2005; Burkepile and 

Hay, 2006; Mora, 2008). Some scientists (e.g., Precht et 

al., 2005) downplay declining resilience issues, instead emphasizing fundamental stochastic factors such as upwellings, hurricanes, and cold fronts (see caption, Figure 1). 

These occurrences represent unmanageable events from 

which coral reefs have recovered for millions of years, but 

not in the presence of modern human infl uences such as 

destructive overfi shing and nutrient pollution (see Mora, 

2008). There are strong interactions between catastrophic 

stochastic factors and the roles of herbivores and nutrients 

that strongly impact reefs. For example, coral mortality 

following hurricanes and coral bleaching events opens up 

large amounts of new two-dimensional space readily colonized by fast-growing algae. Such increases in productivity and the area available for grazing hypothetically satiate the herbivore pressure over large areas, assuming that 

natural herbivore populations have an upper limit in the 

amount of reef area that they can graze effectively (Williams et al., 2001; Mumby, 2006). This diluted grazing 

pressure and reduction in suitable shelter could in turn 

lead to further increases in algal cover and a decline in the 

recovery capacity (i.e., resilience) of coral communities. 

Thus, stochastic processes are unquestionably important 

factors in determining the trajectories of reef health and 

interact with the processes discussed herein.

To establish the baseline conditions and detect subsequent changes, a combination of environmental, survey, inventory, and bioassay data are essential to characterize and 

monitor the ambient nutrient and herbivory environments 

and antecedent nutrient history of a given management 

area. Valid and reliable data are the cornerstone needed 

to prioritize among different management strategies and 

motivate the local populace and politicians/lawmakers to 

support and implement the goals necessary for responsible 

management. The RDM provides a clear visual depiction 

that is easily understood and, therefore, can serve as a 

convincing illustrative aid. It is essential that assessment 

and monitoring methods should be both simple and rapid 

to use. Chlorophyll a concentration (determined by fl uorometric or spectrophotometric methods; see Bell and Elmetri, 1995) is an especially useful ancillary indicator of 

water column enrichment because phytoplankton blooms 

can rapidly attenuate critical light energy while buffering inorganic nutrient pulses. Along with nutrient levels, 

chlorophyll a serves as a valuable tipping-point indicator, 

where levels in excess of 0.2– 0.3 g L1 indicate approaching overabundances of nutrients (Bell et al., 2007).

Water column nutrient concentrations represent the 

net sum of internal cycling, algal assimilation, and external 

inputs, relative to macroalgal growth demands (Lapointe, 

1997), and therefore offer the most direct method to assess 

nutrient excesses on any given coral reef. Consequently, a 

nutrient threshold model based on nutrient concentrations 

(rather than on nutrient fl uxes) is not only valid but is 

likely the best index of nutrient status. Low-nutrient tipping points, where increasing nutrients reach hypothetically critical levels that begin to reduce recoverability from 

phase shifts (i.e., 1.0 M dissolved inorganic nitrogen 

32_Littler_401-414_Lang.indd 406 2_Littler_401-414_Lang.indd 406 9/24/09 10:33/24/09 10:33
NUMBER 38 • 407

[DIN]  nitrogen: 0.014 ppm N or 0.040 ppm NO3 and 

0.10 M soluble reactive phosphorus [SRP]  phosphorus: 0.003 ppm P or 0.007 ppm PO4), have been broadly 

corroborated (in developing the nutrient threshold hypothesis [NTH]; Bell, 1992; Lapointe et al., 1993; Bell et al., 

2007) for sustaining macroalgal overgrowth of seagrass 

beds and coral reefs. The physiological/kinetic basis for 

such low-nutrient tipping points is the hyperbolic Monod 

relation (Droop, 1985; Bell et al., 2007), which is also supported by controlled, high-fl ux, continuous-culture laboratory experiments (Caperon et al., 1971 DeBoer et al., 

1978; Lapointe and Tenore, 1981). In our experience, if 

modern analytical instruments can detect measurable nutrient levels, so can growth-limited macroalgae.

Additionally, a wealth of in situ coral-reef studies carried out in areas characterized by nutrient levels only moderately above the putative 0.1 M SRP and 1.0 M DIN 

tipping points (Larkum and Koop, 1997; Miller et al., 

1999; Thacker et al., 2001) have reported minimal algal 

stimulation following experimental nutrient enrichment, 

further documenting the low natural nutrient concentrations required for ample algal growth and their widespread 

applicability. Some corals can tolerate high levels of DIN 

and SRP; however, nutrient tipping points not much above 

the present analytical limits of detection represent levels 

of resource availability at which resilience begins to be reduced (Scheffer et al., 2001), such that stochastic or other 

disturbances and stresses can trigger coral-reef ecosystem 

shifts toward sustained dominance by macroalgal stable 

states. Moreover, the macroalgal overgrowth experimentally stimulated (Smith et al., 2001; Littler et al., 2006b) 

in reduced-grazing/elevated-nutrient treatments demonstrates that ambient nutrient concentrations inhibitory to 

growth under the natural turbulence levels found on coral 

reefs are similar to those reported above for other tropical marine algae. It should be noted that the remote reef 

in the northwestern Hawaiian Islands studied by Smith et 

al. (2001) had nutrient levels at or above the hypothetical 

levels needed to sustain macroalgal growth (i.e., 1.1 M 

DIN and 0.2 M SRP). This system, with its present lack 

of macroalgae and dominance by unbroken thickets of 

three branching and one massive coral species, may be the 

result of overcompensation by intense grazing and, consequently, could be susceptible to a future relative dominance reversal.

Littler et al. (2006a: tbl. 1) give typical baseline herbivorous fi sh assay and population density data contrasting natural Belize Barrier Reef sites of low and high 

herbivory. Based on similar experiments conducted worldwide on coral reefs by a range of workers (Hay, 1984; 

Lewis and Wainwright, 1985; Paul et al., 1987; Sluka 

and Miller, 2001; Littler et al., 2006a), Littler and Littler 

(2006 posited that less than a six hour half-life (50% 

mean loss per 6 h for palatable algae) during a series of 

in situ, midday, assay periods is indicative of a healthy 

level of herbivory for the particular habitat(s) tested. Herbivore abundances also should be enumerated by counting 

numbers of individuals (by species), from midmorning to 

midafternoon throughout a typical day for weather (Littler et al., 2006a, see their table 1), at fi xed distances on 

either side of random replicates of standardized transect 

lines. Video transects are quick; enumeration can be done 

later in the laboratory, and the videos provide a permanent record of the target species (Littler et al., 1986).

FUNCTIONAL INDICATOR GROUPS

The fast growth and turnover rates of fl eshy algae 

compared to other reef organisms suggest their value as 

early-warning indicators of reef degradation. Representatives of ubiquitous algal form/function groups (from 

Littler and Littler, 2006) are increasingly encountered as 

dominants on reefs, particularly those subjected to human 

activities (see Littler and Littler, 2006: fi g. 2).

REEF-BUILDING CORALS (CNIDARIA)

A predominance of diverse corals and calcareous 

coralline algae are universally accepted as the most desirable components of biotic reefs because of (1) their 

three- dimensional architecture, which provides habitats 

for a myriad of other reef organisms (largely responsible 

for much of the heterogeneity/high biodiversity), (2) their 

roles in producing the massive carbonate structure of 

reefs, and (3) their aesthetic qualities. The vertical structure and horizontal canopies of branching forms allow 

abundant populations of shade-dwelling crustose coralline 

algae to co-occur. Reef-building corals, while preyed upon 

by a few omnivorous fi shes and specialist invertebrates 

(e.g., crown-of-thorns sea star), generally achieve dominance under the top-down control of intense herbivory 

(Lewis, 1986; Lirman, 2001) and extremely low nutrient 

concentrations (Bell, 1992; Lapointe et al., 1993). Massive corals are resistant to grazing at the higher levels of 

herbivory (Littler et al., 1989). Hard mound-shaped forms 

show relatively little colony mortality under high grazing 

pressure, even though occasionally rasped by parrotfi shes. 

Contrastingly, some delicately branched corals such as 

Porites porites are quite palatable and readily eaten by 

32_Littler_401-414_Lang.indd 407 2_Littler_401-414_Lang.indd 407 9/24/09 10:33/24/09 10:33
408 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

parrotfi shes (e.g., Sparisoma viride; Littler et al., 1989; 

Miller and Hay, 1998). Nutrient increases are sometimes 

associated with coral diseases (Harvell et al., 1999, 2002; 

Bruno et al., 2003). As mentioned earlier, numerous corals tolerate elevated nutrient levels (Atkinson et al., 1995; 

Steven and Broadbent, 1997; Bongiorni et al., 2003), but 

their diversity suffers. Conversely, others are physiologically inhibited by increases in nitrate (e.g., Montastrea annularis and Porites porites: Marubini and Davies, 1996), 

ammonium (e.g., Pocillopora damicornis: Stambler et al., 

1991; Muller-Parker et al., 1994), and orthophosphate 

(e.g., Porites compressa: Townsley, cited in Doty, 1969; 

P. damicornis and Stylophora pistillata: Høegh-Guldberg 

et al., 1997). Nutrient inhibition of coral larval settlement 

also has been shown for Acropora longicyathis (Ward and 

Harrison, 1997). During the extensive ENCORE program 

on Heron Island, all increases in nutrient levels adversely 

affected coral reproduction (Koop et al., 2001).

MACROALGAE

With an increase in nutrients, the growth of harmful fl eshy algae is favored over that of the slower-growing 

but highly desirable corals (Genin et al., 1995; Miller and 

Hay, 1996; Lapointe et al., 1997), and the latter become 

inhibited by competition for space and light, increased 

diseases, and physiological inhibition. On healthy oligotrophic coral reefs, even very low nutrient increases may 

exceed critical levels that can shift relative dominances by 

stimulating macroalgal production while inhibiting corals. 

As indicated earlier, large biomass, or standing stocks, of 

slow-growing perennial macroalgae (e.g., rockweeds) can 

develop over time under low inorganic nutrient concentrations (McCook, 1999), and Sargassum spp. can coexist 

with corals in oligotrophic waters by utilizing particulate 

organic sources of nutrients (Schaffelke, 1999). Therefore, 

in this particular situation, large plant biomasses do not 

necessarily indicate detrimentally abundant dissolved nutrients. Filamentous and frondose algae can outcompete 

corals (Birkeland, 1977; but see McCook et al., 2001), 

many of which are inhibited under elevated nutrient levels 

(reviewed in Marubini and Davies, 1996). Fast-growing algae are not just opportunists that depend on disturbances 

to release space resources from established longer-lived 

populations but become the superior competitors (Birkeland, 1977) when provided with suffi cient nutrients. As a 

result, frondose macroalgae as a group are now generally 

recognized as harmful to the longevity of coral reefs because of the linkage between excessive blooms and coastal 

eutrophication (ECOHAB, 1997). Potential competitive 

dominance of fast-growing macroalgae is inferred from 

their overshadowing canopy heights, as well as from inverse correlations in abundances between algae and the 

other benthic producer groups (Lewis, 1986), particularly 

at elevated nutrient concentrations (Littler et al., 1993; 

Lapointe et al., 1997). Macroalgae, such as Halimeda

spp., also gain competitive advantage by serving as carriers of coral diseases (Nugues et al., 2004). The fl eshy 

macroalgal form-group has proven to be particularly attractive to herbivores (see Hay, 1981; Littler et al., 1983a, 

1983b) and only becomes abundant where grazing is decreased or swamped by excessive algal growth (chemically 

defended forms, e.g., Cyanobacteria, are exceptions). Such 

overcompensation by herbivory may explain some of the 

reported cases (Crossland et al., 1984; Szmant, 1997; 

Smith et al., 2001) of specifi c corals surviving high-nutrient reef environments.

CRUSTOSE CORALLINE ALGAE

The predominant members of this indicator group, 

the coralline algae, tend to be slow-growing, competitively 

inferior taxa abundant in most reef systems (Littler, 1972). 

However, they span a spectrum of morphotypes from thin 

sheet-like crusts to thick massive pavements to upright 

branched and columnar coral-like heads that contribute 

to both cementation and bulk. This functional group is 

highly resilient and is able to recover or restore the coralreef system relatively more quickly, given that some crustose coralline algae chemically attract and facilitate the 

survival of coral larvae (Harrington et al., 2004) whereas 

the other two algal functional groups inhibit larval settlement. Because crustose corallines continually slough upper surface layers, they play a key role, as do fi lter-feeding 

corals, in physically preventing the settlement and colonization of many undesirable fl eshy fouling organisms on 

coral reefs (Littler and Littler, 1997). Crustose corallines, 

because of their slow growth rates, tolerate low nutrient 

levels and generally are conspicuous, but not dominant, 

under low concentrations of nutrients and high levels of 

herbivory (Littler et al., 1991). Accordingly, they do well 

under both low and elevated nutrients; that is, most are 

not inhibited by nutrient stress and many are maintained 

competitor free by surface cell layer shedding (Johnson 

and Mann, 1986), even at lower levels of grazing (Littler 

and Littler, 1997). Therefore, crustose coralline algae do 

not require elevated nutrients, as might be inferred from 

the RDM (Figure 1); instead, their rise to dominance is 

largely controlled indirectly by the factors infl uencing 

the abundances of the other groups, primarily corals and 

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NUMBER 38 • 409

fl eshy macroalgae. The key point is that crustose corallines 

predominate mainly by default (i.e., under conditions of 

minimal competition), where either corals are inhibited by 

elevated nutrients or fl eshy algae are removed by intense 

herbivory. In independent corroboration of the herbivory 

portion of the RDM, a gradient of frondose- to turf- to 

coralline algal groups was closely correlated with escalating herbivory on coral reefs (Steneck, 1989).

LOW-GROWING AND TURF ALGAE

The turf algae are mostly dense fi lamentous and lowgrowing frondose members of all four algal phyla and tend 

to become dominant under minimal inhibitory top-down 

and stimulatory bottom-up controls. Domination by lowgrowing algae suggests desirably low nutrient levels but an 

inadequate herbivory component. Their relatively small 

size and rapid perennation results in moderate losses to 

herbivory at low grazing pressures. They have opportunistic life history characteristics, including the ability to maintain substantial nutrient uptake and growth rates under 

low-nutrient conditions (Rosenberg and Ramus, 1984), 

and also contain an abundance of nitrogen-fi xing Cyanobacteria (Adey and Goertemiller, 1987; Adey, 1998) that 

can enrich other low-growing members of the dense turf 

community. Algal turfs have been shown to be favored 

under reduced nutrient-loading rates (Fong et al., 1987) 

or infrequent nutrient pulses (Fujita et al., 1988) and can 

form extensive horizontal mats.

DISCUSSION

This paper directly addresses the goals of an imperative research agenda (ECOHAB, 1997) by providing a 

management perspective and assessment strategies for the 

mechanisms that initiate and sustain harmful blooms of 

algae that degrade coral-reef ecosystems. The complex interactions of herbivory and nutrients can change gradually 

with no apparent effects to induce subtle declines in resiliency and recoverability of coral/coralline-dominated reef 

systems (Scheffer et al., 2001). As mentioned, these systems then become vulnerable to catastrophic impacts by 

large-scale stochastic disturbances that typically trigger or 

accelerate such low-resilience reef systems (Scheffer et al., 

2001; Bellwood et al., 2004). Most importantly, recovery 

to coral domination cannot occur unless tipping points are 

returned to healthy levels, and even then alternative stable 

states may persist. For example, when catastrophic events 

selectively eliminate the longer-lived organisms in favor of 

early-successional fl eshy algae (Littler and Littler, 1984), 

the settlement of coral planulae is prevented and the algae 

persist as competitively superior states (Birkeland, 1977; 

Lewis, 1986). For completeness, we also point out the obvious devastating effects of toxic spills, carbonate mining, 

land-fi ll, and sediment inundation, some of which also are 

associated with nutrient pollution and algal blooms.

Because of global-scale degradation of coral-reef ecosystems (Ginsburg, 1994; Wilkinson, 1999), it is important to obtain relevant information on tipping points for 

both top-down herbivory (relatively fast acting, acute) and 

bottom-up nutrient controls (slower acting, chronic), both 

of which are reemphasized. As the fi rst approximation, we 

posit that on a healthy reef system, herbivore abundances 

and diversity should be high, and palatable test plants 

should show at least a 50% mean loss per six hours (i.e., 

6 h half-life) during a series of midday in situ assays. 

Table 1 in Littler and Littler (2006 summarizes baseline 

assay and critical fi sh population data of this sort for two 

natural coral-reef zones of low and high herbivory.

Nutrient threshold points (where increasing water 

column nutrients reach critical resilience levels such that 

they reduce recovery from phase shifts) have been widely 

postulated (as 1.0 M DIN and 0.10 M SRP [NTH]; 

Bell, 1992; Lapointe et al., 1993; Bell and Elmetri, 1995) 

for potential macroalgal overgrowth of coral-reef communities. As mentioned earlier, a further useful tipping-point 

indicator is water column chlorophyll a, where levels in 

excess of 0.2– 0.3 g L1 also indicate detrimental overabundances of nutrients (Bell and Elmetri, 1995).

CONCLUSIONS

Assessment protocols for determining and monitoring 

the status of any given coral reef are suggested: these include (a) herbivore population assessments, (b) herbivory 

assays, (c) water column nutrient levels, and (d) standing 

stocks of functional indicator groups. These measurements can reveal quantitative tipping-point levels beyond 

which resilience to and recovery from undesirable phase 

shifts begin to become critically reduced. Tipping-point 

approximations are reviewed and posited both for inorganic nutrients and for herbivory.

This review specifi cally addresses the relatively acute 

top-down effects of herbivory and the more chronic 

bottom -up effects of nutrient enrichment on critical indicator groups of benthic primary producers: reef-building 

corals, crustose coralline algae, dense turf algae, frondose 

macroalgae, and herbivore associates.

32_Littler_401-414_Lang.indd 409 2_Littler_401-414_Lang.indd 409 9/24/09 10:33/24/09 10:33
410 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

A predominance of massive corals and calcareous coralline algae relative to frondose macroalgae and low-growing 

algae indicates a healthy spatially heterogeneous condition 

refl ecting low nutrients and high herbivory. With a few exceptions, an abundance of frondose macroalgae illustrates 

the least desirable condition of elevated nutrient levels and 

reduced herbivory, possibly refl ecting eutrophication in 

concert with destructive herbivore fi shing practices. A high 

coverage of coralline algae suggests healthy high herbivory 

levels but also suggests problems with elevated nutrients that 

may be inhibitory to some corals. Domination by dense lowgrowing and turf algae indicates desirably low nutrient levels but also suggests an inadequate herbivory component.

From a management perspective, levels of herbivory 

and herbivore populations and of nutrients rank among 

the most useful quantitative indicators of coral-reef resilience and recoverability, whereas the degree of health, 

degradation, and mortality are inferred by the relative 

abundances of functional indicator groups.

The bioassay and indictor group monitoring approaches provide powerful perspectives and essential 

measurement criteria to enable resource managers to protect coral reefs and similar coastal systems from eutrophication, destructive overfi shing, and initiation of harmful algal blooms. Human population growth has always 

been accompanied by changes in land and sea use and 

by increased exploitation of natural resources, attitudes 

that continue to cause broad alterations in the structure 

of coral-reef communities. Unless curbed, anthropogenically induced phase shifts will expand geographically at 

an accelerated pace. However, solutions are available, 

which include the use of Marine Protected Areas, banning 

of destructive fi shing practices (e.g., trapping, poisoning, 

blasting, netting), and regulations protecting keystone herbivorous fi sh species (e.g., parrotfi sh, surgeonfi sh) from 

market exploitation. Fisheries controls must be backed up 

by strategies to regulate the effects of pollution along with 

an international commitment to reduce the emission of 

greenhouse gases and, fi nally, the implementation of longterm strategies to reduce or stabilize the ultimate cause of 

all these stressors, the world’s human population growth.

ACKNOWLEDGMENTS

Support for this work came from a Scholarly Studies 

Grant (Smithsonian Institution, Offi ce of Fellowships and 

Grants), the Caribbean Coral Reef Ecosystems (CCRE) 

Program (administered by Klaus Ruetzler, the Smithsonian Marine Station at Ft. Pierce (Valerie Paul, Head Scientist), and the National Museum of Natural History. This is 

CCRE contribution number 847, supported in part by the 

Hunterdon Oceanographic Research Fund, and SMSFP 

contribution number 763.

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Impacts of Human Disturbance on Soil 

Erosion Potential and Habitat Stability of 

Mangrove-Dominated Islands in the Pelican 

Cays and Twin Cays Ranges, Belize

Karen L. McKee and William C. Vervaeke

ABSTRACT. The Mesoamerican Barrier Reef System (MBRS) is the longest unbroken 

reef in the Western Hemisphere and contains hundreds of mangrove-dominated islands. 

These islands provide critical habitat supporting marine biodiversity and create a selfsustaining system that counterbalances sea-level rise. Undisturbed mangrove islands 

build vertically through accumulation of organic matter (peat), which forms a strong, 

erosion-resistant matrix. Clear-cutting and dredging activities for development of tourist 

resorts, fi shing camps, and “improved land” for resale, however, threaten mangrovedominated islands and adjacent seagrass and coral reef assemblages. Effects of mangrove 

disturbance were examined on four islands in the designated marine preserves of Twin 

Cays and the Pelican Cays, Belize. Mangroves were clear cut (1.0– 6.2 ha), and marine 

sediment was dredged from nearby reef fl ats and seagrass beds to raise land elevations 

to support beach vegetation and buildings. Removal of mangroves and especially addition of dredged fi ll signifi cantly altered soil characteristics and decreased shear strength 

and aggregate stability of soil surfaces. Deep cores collected at both island ranges also 

revealed underlying deposits of peat (1.5– 10.8 m thick), which infl uence local land subsidence. Although infi lling with dredged material temporarily raised elevations, the inexorable subsidence of peat through natural processes of compaction and decomposition 

and sea-level rise will ultimately submerge such areas. Our fi ndings thus show that soil 

erosion potential is increased and that long-term stability of islands may be compromised 

by mangrove clearing and dredging activities. Degradation of key biophysical components and critical habitat will ultimately impact ecotourism activities that depend on a 

healthy, natural environment.

INTRODUCTION

Persistence of oceanic mangrove islands is dependent upon maintenance of 

soil elevations relative to sea level. Mangrove-dominated islands can counterbalance rising seas by accumulating organic matter (mangrove-derived peat), 

which gradually builds land vertically (McKee et al., 2007a). In addition, biodiversity of intertidal and subtidal ecosystems in the Caribbean Region is dependent 

upon the presence of mangroves because a number of marine species are exclusively 

associated with the mangrove habitat (Ellison and Farnsworth, 1992; Goodbody, 

2000; Taylor, 2000; Rocha et al., 2005). Mangroves also serve as nurseries for 

many reef fi sh and other marine organisms (Mumby et al., 2004). Consequently, 

Karen L. McKee and William C. Vervaeke, U.S. 

Geological Survey, National Wetlands Research 

Center, 700 Cajundome Boulevard, Lafayette, 

Louisiana 70506, USA. Corresponding author: 

K. McKee (karen_mckee@usgs.gov). Manuscript 

received 9 June 2008; accepted 20 April 2009.

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416 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

changes in mangrove extent may have a cascading effect 

on habitat stability and capacity to keep pace with sealevel rise, as well as on marine biodiversity, in regions with 

mangrove-dominated islands and adjacent seagrass and 

coral reef assemblages.

The Mesoamerican Barrier Reef System (MBRS) off 

the coast of Belize, Central America, contains hundreds 

of mangrove islands in association with extensive seagrass 

beds and coral reefs (www.mbrs.org.bz; accessed 11 June 

2008). Unfortunately, clear-cutting of insular mangroves 

has greatly accelerated in Belize and other locations in 

recent years for development of tourist resorts, fi shing 

camps, and “improved land” for resale (K. L. McKee, 

personal observation). Even if such areas are ultimately 

abandoned and allowed to recover, recolonization by 

mangroves may be extremely slow, if it occurs at all. For 

example, a site on Twin Cays, an island range that was 

clear cut in 1992, is slowly recovering, but regenerating 

mangroves are still sparse and have taken 15 years to 

reach sapling size (1– 2 m tall) (McKee et al., 2007b). 

In addition to removal of mangroves, bottom sediments 

are dredged from adjacent seagrass beds and reef fl ats and 

pumped onto cleared mangrove areas to raise elevations 

suffi ciently to support beach vegetation and buildings. 

This type of disturbance thus destroys multiple ecosystems, which require many years for recovery. In the interim, there may be additional consequences from the loss 

of habitat stability and increased erosion.

The specifi c objectives of this study were to assess the 

potential for changes in soil erosion and habitat stability 

on mangrove islands subjected to clear-cutting and dredging activities. The work focused on the designated marine preserves of Twin Cays and the Pelican Cays ranges, 

which have been highlighted as critical habitat for marine 

biodiversity in the region (Macintyre and Rützler, 2000; 

Macintyre et al., 2004a).

STUDY SITE

The MBRS is the longest unbroken reef in the Western 

Hemisphere and extends 220 km from the southern part 

of the Yucatan Peninsula to the Bay Islands of Honduras. 

Two main areas where clear-cutting and fi lling of mangrove 

islands has occurred were studied: Twin Cays and the Pelican Cays. Twin Cays, which consists of two larger and two 

smaller islands, is located in the central part of the barrier 

reef system and about 2 km west of the reef crest (Figure 1). 

The Pelican Cays archipelago is located 21 km south of Twin 

Cays and contains multiple mangrove-dominated islands 

(Figure 1). Twin Cays and the Pelican Cays ranges have been 

a major focus of mangrove research by the Smithsonian Institution (Macintyre and Rützler, 2000; Macintyre et al., 

2004a). These mangrove islands are far from the mainland, 

and peat cores contain no terrigenous sediment (Cameron 

and Palmer, 1995; McKee and Faulkner, 2000; Purdy and 

Gischler, 2003; Macintyre et al., 2004b). The only source of 

freshwater is rainfall, and the entire landform is intertidal 

(mean tide range [neap] 0.2 m). The vegetation on undisturbed islands is dominated by Rhizophora mangle L. (red 

mangrove), which is the most common mangrove species 

in the Caribbean Region. The area has been impacted by 

numerous hurricanes and tropical storms.

Twin Cays occurs in the Central Province of the barrier reef (16°50N, 88°06W) (see Figure 1). Mangrove 

communities were established at Twin Cays about 8,000 

years ago on the Pleistocene surface of the Belize Barrier 

Reef Platform when it was fl ooded during the Holocene 

Transgression (Macintyre et al., 2004b; Purdy and Gischler, 2003). Deep deposits of peat (as much as 11 m thick) 

have developed as Twin Cays accreted vertically with 

rising sea level (Macintyre et al., 2004b; McKee et al., 

2007a). Cores collected through these deposits indicate 

that the primary means of vertical land movement is accumulation of mangrove organic matter (mostly root matter) 

(McKee et al., 2007a). At Twin Cays, fi ve areas ranging in 

size from 0.1 to 6.2 ha have been cleared and elevations 

raised by infi lling with dredged material, beginning in the 

early 1990s and continuing until the present; small fi shing camps consisting of one or more buildings have been 

established. Our study targeted the largest site on East Island that was clear cut and fi lled in 1995.

The Pelican Cays occur in the south central lagoon 

of the reef system (16°39.8N, 88°11.5W). Here, mangroves have developed as part of a complex network of 

coral ridges that surround deep circular ponds (Macintyre 

et al., 2000). There are several mangrove cays, including 

Northeast Cay, Fisherman’s Cay, Manatee Cay, Cat Cay, 

Ridge Cay, Avicennia Cay, Co Cat Cay, the Bird Cays, and 

several unnamed smaller cays. Mangroves established at 

the Pelican Cays only within the past 1,000 years (Macintyre et al., 2000; McKee et al., 2007a) but have accumulated deposits of peat as much as 1.5 m thick (McKee and 

Faulkner, 2000). Disturbance at the Pelican Cays began in 

the mid-1990s with mangrove clearing on Northeast Cay. 

Aerial surveys conducted in April 2006 showed disturbed 

areas on Northeast Cay, Co Cat Cay, and Ridge Cay, and 

a follow-up survey in April 2007 showed new areas of 

mangrove clearing and dredging at Manatee Cay and Fisherman’s Cay (I. C. Feller, personal communication).

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NUMBER 38 • 417

FIGURE 1. Map of research area. The Twin Cays and Pelican Cays ranges are circled.

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418 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

MATERIALS AND METHODS

EXPERIMENTAL DESIGN

Sampling of Pelican Cays and Twin Cays was conducted during May 2008. The sampling design was a splitplot in which the main plot was disturbance type (fi xed 

effect) and the subplot was spatial position relative to the 

shoreline (fi xed effect). Two disturbance levels were designated: undisturbed and disturbed. Undisturbed, reference 

areas exhibited no visible signs of human activity. Disturbed 

areas were characterized by removal of mangroves by clearcutting followed by deposition of dredged marine sediment. 

Islands with a disturbed area of this type were identifi ed 

initially by aerial photography. Four islands were selected 

for soil sampling based on disturbance history and accessibility: one in the Twin Cays range (East Island) and three 

in the Pelican Cays range (Manatee, Fisherman’s, and Ridge 

Cays). Extent of natural and disturbed areas at each study 

location was estimated from satellite imagery (Landsat 7, 

May 2008; http://landsat.usgs.gov) and aerial photographs 

(April 2006, 2007; I. C. Feller, unpublished) and confi rmed 

by ground-truthing (May 2008).

At each island, two transects were established perpendicular to the shoreline and traversing the island to a 

distance of 100 m inland. One transect was located in the 

disturbed area and the other in an adjacent undisturbed 

forest. Fourteen to sixteen sampling stations were preselected along each transect in a stratifi ed-random design; 

that is, two to four stations occurred within each of fi ve 

intervals (0– 10, 11– 30, 31– 50, 51– 70, and 71– 100 m 

from the shoreline). In the disturbed areas, some portions 

were not clear cut (but may have been buried by dredged 

fi ll) or were clear cut and remained free of dredged fi ll; 

these zones were sampled as well. The reference transect 

originated along the same shoreline and was oriented in 

the same direction as the disturbed transect, although the 

length was not always the same (as a consequence of variation in island confi guration). Each island was considered 

to be a replicate block.

At each sampling station, percent cover of herbaceous 

vegetation and mangrove canopy was estimated visually. 

The following soil variables were measured: bulk density, 

texture, shear strength, organic matter content, particle 

size distribution, and aggregate stability (as described below). A surface core (30 cm depth) was also collected at 

each disturbed island to determine the thickness of dredged 

material. Also, deeper cores were collected at one island at 

Twin Cays (West Island) and one undisturbed island in the 

Pelican Cays (Cat Cay) to determine the stratigraphy and 

composition of deposits beneath these islands.

ANALYSES

Soil Shear Strength

Soil shear strength was determined with a Torvane device (H-4212 1, Humbolt Manufacturing Company, Durham Geo-Enterprises), which measures the torque required 

to shear or deform the soil (McGinnis, 1997). Soil strength 

was measured at the soil surface, and the only selective 

criterion was fl atness, because the Torvane required a fl at 

or nearly fl at surface for accurate measurements. Five replicate measurements were made at each sampling station 

and averaged.

Soil Aggregate Stability

Duplicate soil cores (2 cm diameter  10 cm long) 

were collected at each station. The cores were carefully 

extruded onto a board, and the upper 1 cm was severed 

with a knife, providing a total soil volume of 3.14 cm3 per 

sample. One core was used for stability testing and the 

other was placed into a Ziplock bag for determination of 

soil bulk density and texture (described below).

Soil aggregate stability was determined based on a 

modifi cation of standard methods (Angers and Mehuys, 

1993; Herrick et al., 2001) to better assess the substrates 

(peat, marine sediment) and the types of erosive forces 

(waves, currents) typical of the mangrove habitat. In the 

fi eld, cores were placed in collection boxes, which protected them from disturbance until processing. Because 

the soils in this study were naturally moist to saturated, 

samples were not dried before measurement. Each core 

was transferred to a sieve (#20 mesh, 850 μm) and gently lowered into a container of water, then scored as to 

initial structural integrity. The core was then gently agitated by repeated dipping (fi ve times) in water and again 

assessed. Initial stability (based on slaking or disintegration of the core) was scored as 0 (soil too unstable to 

sample), 1 (50% of structural integrity lost upon immersion or less than 10% of soil remained on sieve after 

fi ve dips), 2 (10%– 25% of soil remained), 3 (25%– 75% 

of soil remained), or 4 (75%– 100% of soil remained). 

After initial assessment, 200 mL water was poured over 

the sample; the material remaining on the sieve and that 

washed through the sieve (including the portion from 

the initial assessment) was transferred to separate bags 

for drying and weighing. Samples were oven dried at 

60°C for 24 h and weighed. The percent by weight of 

material retained on the sieve was calculated. These two 

measures were designated as Stability Index 1 and 2, 

respectively.

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NUMBER 38 • 419

Soil Water Content, Bulk Density, and Texture

At the laboratory, the soil was weighed wet, dried at 

60°C to constant mass, and reweighed to determine moisture content (percent water in soil sample). Dry bulk density was calculated by dividing the dry mass by the volume (g cm3). The dried soil was ashed at 550°C for 6 h 

to determine mineral mass after organic loss on ignition. 

Percent organic matter content was calculated as 100 minus the percent ash. Particle size distribution (PSD) was 

determined (only for mineral sediments) based on a micropipette method (Burt et al., 1993). Subsamples (three 

or four) collected within each zone along a transect were 

combined to provide suffi cient mass for PSD.

Peat Coring

Deep cores were collected to the point of refusal with 

a Russian peat corer, which extracts uncompressed cores 

in sections 0.5 m long (McKee et al., 2007a). At Twin 

Cays, seven cores were collected across a transect traversing West Island (west to east) to depths to 10.8 m. At Cat 

Cay, nine cores were similarly collected, but the maximum 

depth was 1.5 m because the peat layer was thinner. A 

deep core was also collected at Manatee Cay (disturbed 

area). Each core was extracted and transferred to a halfsection of polyvinyl chloride (PVC) pipe, wrapped with 

plastic wrap, and refrigerated until processing. At the fi eld 

station, each core section was logged, photographed, and 

thicknesses of major strata measured. Subsamples were 

taken at intervals of approximately 10 cm and washed 

on a 1 mm mesh sieve; plant fragments were identifi ed to 

species using a key as described previously (McKee and 

Faulkner, 2000). At all disturbed sites, shallow cores (5 cm 

diameter  30 cm deep) were collected with a piston corer 

to determine the thickness of the dredged fi ll.

RESULTS

GENERAL OBSERVATIONS

Large areas of Twin Cays, Fisherman’s Cay, Manatee 

Cay, and Ridge Cay were clear cut (Table 1), and marine 

sediment had been dredged from a nearby reef fl at and 

pumped to the island interior. Scars on the seafl oor were 

visible from the air (Figure 2), showing that large areas 

(0.6 to 1.0 ha) of reef fl at had been disturbed. The mangrove areas disturbed at these four study sites varied from 

1.0 to 6.2 ha, accounting for up to 34% of the mangrove 

area per island (Table 1). In most cases, the woody debris from clear-cutting had been burned and only stumps 

remained to mark the past presence of mangrove trees. 

All four disturbed sites had received varying amounts of 

dredged marine sediment that had created a relatively fl at, 

homogeneous landscape of dry, highly refl ective, inorganic 

substrate (Figure 3). The dredged material varied in depth 

from 12 to 25 cm and contained coral, shells, and sand 

that indicated the marine origin of the materials. All the 

sites examined at the Pelican Cays were fi lled with material 

dredged from nearby reef fl ats, as evidenced by the presence of carbonate sand (Halimeda spp.), shells, and coral 

fragments. At Twin Cays, the dredged fi ll was composed of 

TABLE 1. Summary of natural and disturbed mangrove areas at two island ranges: Twin Cays (East 

and West) and Pelican Cays (Manatee Cay, Fisherman’s Cay, and Ridge Cay). A dash (– ) indicates data 

were not obtained.

 Twin Cays Pelican Cays

Measurement East Island West Island Manatee Cay Fisherman’s Cay Ridge Cay

Total island area (ha) 41.4 17.6 12.6 24.3 3.4

Undisturbed area (ha)

 Natural ponds 9.8 2.0 4.3 6.2 0.1

 Mangrove 28.7 13.0 6.3 11.9 2.3

Disturbed area (ha)

 Clear-cut only 1.2 1.4 – –– 

 Clear-cut  fi lled 1.7 1.2 2.0 6.2 1.0

Percent disturbed area

 Island 7% 14% 16% 26% 29%

 Mangrove only 9% 17% 24% 34% 30%

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420 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

quartz sand, indicating a mainland origin. With the exception of a narrow fringe of uncut trees and occasionally a 

lone tree, no mangrove canopy remained in these disturbed 

areas. In some cases, dredged material had buried the aerial roots of intact trees along some shorelines, and these 

trees had subsequently died (Figure 4). At all disturbed 

sites, mangrove associates (Conocarpus erectus) and common coastal beach species were present, but total cover 

was low (10%). The most common herbaceous species 

included Batis maritima L., Sesuvium portulacastrum (L.) 

L., Distichlis spicata (L.) Greene, Paspalum distichum L., 

Salicornia virginica L., Spartina spartinae (Trin.) Merr. ex 

A. S. Hitchc., Rhabdadenia bifl ora (Jacq.) Muell.-Arg., 

Cyperus spp., Ipomoea pescaprae ssp. Brasiliensis (L.) van 

Ooststr., Ageratum littorale Gray, and Typha sp. In unvegetated areas, a biological crust of unidentifi ed composition 

had sometimes formed a thin surface layer on top of the 

dredged fi ll.

In contrast, the reference sites contained intact mangrove canopy (dominant species R. mangle with subdominants Avicennia germinans (L.) L. and Laguncularia racemosa (L.) Gaertn. f.), low herbaceous cover 

(5%; most commonly B. maritima), and undisturbed 

substrate that was dark in color, saturated with water, and 

composed of live and dead mangrove roots and other organic matter. Abundant aerial roots of intact mangrove 

vegetation (prop roots and pneumatophores) formed an 

interlacing network that contributed to the overall structural integrity of the reference areas and also served as substrate for a variety of epiphytes and epibionts. The forest 

fl oor was usually covered by algal-microbial mats (Rhodophyta, Chlorophyta, Cyanophycota, Bacillariophyta), 

typical of mangrove forests in this region (K. L. McKee, 

unpublished data).

SURFACE SOIL CHARACTERISTICS AND EROSION POTENTIAL

Major differences in surface soil characteristics and 

potential for erosion occurred between reference and 

disturbed areas (Table 2). The surface soil of reference 

forests was peat composed of a matrix of live and dead 

mangrove roots, fi lamentous algal-microbial mats, and 

FIGURE 2. Aerial photograph of Fisherman’s Cay and Manatee Cay in April 2007 showing mangrove areas 

that were clear cut and fi lled with marine sediment dredged from an adjacent reef fl at (indicated by red circle 

and arrow pointing to white fi lled area on the cay). (Photograph by I. C. Feller.)

33_McKee_415-428_Lang.indd 420 3_McKee_415-428_Lang.indd 420 9/24/09 10:30/24/09 10:30
NUMBER 38 • 421

trapped organic matter that retained its structural integrity even when disturbed by sampling. Bulk density was 

low (0.17 g cm3), and water (68%) and organic contents 

(60%) were high. Despite its organic nature, the reference 

soil (peat) had high shear strength (overall mean, 0.084 

kg cm2), which varied little spatially (Figure 5). Core samples retained their shape and showed little or no slaking 

upon immersion in water (Stability Index 1 3.98) and 

little loss of material upon repeated agitation (Stability 

Index 2 87%). When stability indices were plotted as 

x– y coordinates, the reference sites grouped together, indicating little difference among islands (Figure 6).

In contrast, the surface soil in disturbed areas was 

composed of inorganic carbonate particles derived primarily from calcareous algae (Halimeda spp.), coral fragments, and shells (PSD showed that 90% of the mass 

was sand or larger particles). This material had a high bulk 

density (0.72 g cm3) and low water content (30%) and 

organic content (9%). Soil shear strength (0.044 kg cm2) 

in disturbed areas was lower overall compared to reference areas and varied spatially (see Figure 5). Aggregate 

stability was lower overall (Stability Index 1 2.14, Stability Index 2 47%), and differed among island locations (see Figure 6). Many cores were friable and readily 

disintegrated when disturbed mechanically. Where vegetation or biological crusts had developed on the dredged 

material, the shear strength was higher, but aggregate stability remained low; that is, cores typically did not retain 

their integrity and exhibited a high degree of slaking in 

water. The mass retained on the sieve was composed of 

particles greater than 1 mm in diameter (Halimeda chips, 

coral fragments, shells). Shear strength increased overall 

with increasing distance along some disturbed transects 

because of the absence of dredged fi ll at interior stations 

where the old peat surface remained exposed (e.g., Twin 

Cays). In such cases, the exposed peat substrate retained 

high shear strength and high aggregate stability despite the 

removal of the mangroves.

PEAT STRATIGRAPHY

Mangrove islands in the Twin Cays and Pelican Cays 

ranges were underlain by deposits of peat, varying in 

maximum thickness from 1.5 m (Cat Cay and Manatee 

FIGURE 3. Views of disturbed (upper panels, A and B) and reference (lower panels, C and D) areas showing 

detail of soil surfaces. A circular quadrat in panel D (0.1 m2) provides scale.

33_McKee_415-428_Lang.indd 421 3_McKee_415-428_Lang.indd 421 9/24/09 10:30/24/09 10:30
422 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 4. Red mangrove trees along the shoreline of disturbed areas: some trees died as a result of burial 

with dredged fi ll (right).

TABLE 2. Summary of analysis of variance (ANOVA) results for soil characteristics. The main plot factor (disturbance) was tested with 

within-subject error (island); subplot factor (spatial position) and interactions were tested with residual error. Values are the F ratio; 

signifi cance: *P 0.05, **P 0.01, ***P 0.001,  P 0.0001, ns not signifi cant.

 Aggregate stability Vegetative cover 

Source Shear Bulk Organic Water 

of error strength Index 1 Index 2 density matter content Herbaceous Mangrove

Disturbance 50.24** ** 180.0  86.4** ** 184.0  353.2** ** 350.0**** 6.78* 191.3****

Island (block) 6.23*** 7.01  1.93 ns 21.2** ** 5.52** 2.42 ns 7.80  7.95** **

Position 1.36 ns 4.85** 3.53** 1.23 ns 0.68 ns 3.02* 1.87 ns 1.99 ns

Disturbance  position 5.70*** 3.95** 1.29 ns 6.58**** 2.82* 8.67**** 1.70 ns 1.59 ns

Cay) to more than 10 m (Twin Cays) (Figure 7). At Cat 

Cay, a series of cores traversing the island showed that peat 

thickness was greatest on the southern, leeward side and 

decreased toward the northern, windward shore. Botanical 

matter in the peat consisted predominately of mangrove 

roots with fragments of leaves and wood. Beneath the peat 

layer was sand and/or coral. Deeper peat layers were dominated by R. mangle, whereas upper layers (0– 50 cm) in 

the island interior contained remains of A. germinans. At 

Twin Cays, cores across an east– west transect were 7.5 to 

10.8 m thick, with two of the cores reaching the limestone 

platform underlying this range. These cores also consisted 

33_McKee_415-428_Lang.indd 422 3_McKee_415-428_Lang.indd 422 9/24/09 10:31/24/09 10:31
NUMBER 38 • 423

of mangrove peat, predominately R. mangle. In the island interior, surface layers of A. germinans peat varied 

in thickness from 50 to 100 cm, similar to the pattern observed at Cat Cay.

DISCUSSION

The MBRS is a unique and valuable resource to the 

Central American countries of Belize, Honduras, and 

Guatemala (www.mbrs.org.bz; accessed 11 June 2008). 

Destruction of mangrove islands has rapidly accelerated 

in this system as a result of attempts to transform these 

sensitive and fragile habitats into environments more attractive to tourists. Because there are few sand-based 

islands underlain by shallow limestone platforms and 

suitable for development, mangrove-dominated islands 

have been targeted for conversion. In addition to the two 

ranges included in this study (Pelican Cays, Twin Cays), 

other mangrove ranges in the vicinity also have undergone 

similar mangrove clearing and fi lling (e.g., Blue Ground 

Range, Tobacco Range, Coco Plum) (K. L. McKee, personal observation). Survey lines found during this study 

indicate plans for further development at many of these 

island ranges.

EFFECTS OF MANGROVE REMOVAL 

AND DREDGED FILL ON EROSION

Although the direct and indirect effects of mangrove 

clear-cutting and marine dredging are many and varied, our 

study focused on the specifi c consequences for erosion and 

FIGURE 5. Spatial variation in soil shear strength (A), organic matter (B), bulk density (C), and water content 

(D) in reference (squares) and disturbed (circles) mangrove areas. Values are the mean 	 SE (note some SE 

bars are smaller than the symbols).

33_McKee_415-428_Lang.indd 423 3_McKee_415-428_Lang.indd 423 9/24/09 10:32/24/09 10:32
424 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

long-term loss of elevation. Removal of mangroves and 

alteration of the soil surface by dredged fi ll signifi cantly 

altered the potential for erosion and substrate stability at 

Twin Cays and the Pelican Cays. The natural substrate in 

undisturbed mangroves comprised a strong matrix composed of living and dead fi brous roots as well as fi lamentous algae, which formed mats on the soil surface. This 

material was extremely resistant to shearing and retained 

its integrity even when repeatedly agitated by submersion 

in water (see Figure 6). Although some interior areas contained natural deposits of fl occulent material (e.g., microbial mats) that were soft and friable, they were underlain by 

solid peat. Work in other locations, such as the Bay Islands 

of Honduras, found similarly high resistance of mangrove 

peat soils to shearing (McKee and McGinnis, 2002; Cahoon 

et al., 2003). These results demonstrate the high resistance 

to soil erosion afforded by intact mangrove peat.

Removal of mangroves by clear-cutting did not by itself 

appear to have an immediate effect on soil shear strength 

or aggregate stability in the areas sampled. In a few cases, 

clear-cut areas that were not covered by dredged material 

were encountered during surveys (e.g., at Twin Cays), and 

here shear strength was equal to that in reference areas; 

these were all areas that had been previously occupied by 

R. mangle and had only been altered by removal of trees. 

Similarly, some mangrove areas in the Bay Islands of Honduras killed by Hurricane Mitch retained shear strength 

up to two years following mortality because of the strong 

matrix of R. mangle roots forming the peat substrate (Cahoon et al., 2003). However, those areas that had been 

dominated by Avicennia germinans lost soil integrity and 

collapsed following mortality of the trees. Eventually, 

however, the lack of live roots and algal mats may lead 

to loss of shear strength wherever mangroves have been 

removed.

A review of sediment burial effects on mangroves suggests that some species are more sensitive and may suffer 

mortality when subjected to excessive rates of sedimentation (Ellison, 1998). We also found that live trees (R. 

mangle) exposed to dredged fi ll often died— presumably 

the result of smothering of aerial roots. This outcome was 

particularly evident where a narrow (10 m wide) fringe 

of trees was left intact along the shoreline and the dredged 

material overfl owed into this zone (see Figure 4). In cases 

where the shoreline tree zone was wider (20– 30 m), there 

was a higher survival. Without a protective mangrove buffer along the shoreline, these islands may rapidly erode. 

Observations at older sites (Twin Cays) showed rapid 

shoreline retreat (up to 0.3 m per year) where mangroves 

had been removed in 1992 (McKee et al., 2007b).

LONG-TERM CONSEQUENCES FOR ISLAND STABILITY

Oceanic islands are generally vulnerable to disturbance because of their low-lying position and potential for 

submergence as well as exposure to tropical storms, hurricanes, and tsunamis that generate strong erosive forces. 

Mangrove islands in the MBRS have developed and built 

vertically over thousands of years through deposition of 

peat derived from mangrove organic matter (McKee and 

Faulkner, 2000; McKee et al., 2007a). This process occurs 

in the intertidal zone where abundant mangrove roots are 

produced and accumulate biomass because of their slow 

decomposition in the anaerobic environment (Middleton and McKee, 2001). Other biogenic processes include 

formation of algal and microbial mats on the soil surface (intertidal and subtidal) and carbonate sand formed 

from calcareous algae (subtidal) in mangrove ecosystems 

(McKee et al., 2007a; McKee, unpublished data). Growth 

of mangrove root-algal mats and other biofi lms not only 

contributes to vertical accretion but also stabilizes islands 

FIGURE 6. Aggregate stability of soils from reference sites (closed 

symbols) and disturbed mangrove areas (open symbols) at Twin 

Cays (diamond), Fisherman’s Cay (square), Manatee Cay (triangle), 

and Ridge Cay (circle). Stability indices (mean 	 SE) are based on 

maintenance of soil structure upon immersion in water (Index 1) and 

percent of soil retained on a 850 m sieve (Index 2). Probability ellipses (90% confi dence curves) are drawn for each group.

33_McKee_415-428_Lang.indd 424 3_McKee_415-428_Lang.indd 424 9/24/09 10:32/24/09 10:32
NUMBER 38 • 425

FIGURE 7. Peat stratigraphy across Twin Cays (top) and Cat Cay (Pelican Cays) (bottom) and reconstruction of vegetation history. Radiocarbon dates (calendar years before present [Cal YBP]) are based 

on previous work (McKee et al., 2007a).

33_McKee_415-428_Lang.indd 425 3_McKee_415-428_Lang.indd 425 9/24/09 10:32/24/09 10:32
426 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

by trapping and consolidating organic and inorganic sediment that is deposited.

To persist, such oceanic islands must accrete vertically to counterbalance both sea-level rise and local rates 

of subsidence, which vary depending on geomorphology, 

isostacy, and tectonic movements. Mangrove-dominated 

islands have the capacity to self-adjust to subsidence and 

sea-level rise through peat formation. Previous work has 

shown that mangrove islands in Belize and other Caribbean 

areas have kept up with changing sea level for thousands 

of years through the slow accumulation of mangrove roots 

and other organic material and that vertical building rates 

are determined by the health and productivity of the mangrove community (McKee and Faulkner, 2000; Middleton 

and McKee, 2001; McKee et al., 2007a). Peat subsidence 

rates determined at Twin Cays in vegetated areas averaged 

7 mm year1 (McKee et al., 2007a). Similar rates of subsidence were found in the Bay Islands, Honduras (Cahoon 

et al., 2003). Island subsidence combined with eustatic rise 

in sea level (3.5 mm year1; Rahmstorf, 2007) means that 

the relative rise in sea level in this area is at least 10.5 mm 

year1 (assuming negligible deep subsidence). On undisturbed cays with intact mangroves, vertical building from 

peat accumulation should maintain surface elevations 

within the intertidal zone, unless sea-level rise accelerates 

beyond the capacity of the system to compensate.

Removal of mangroves by clear-cutting eliminates the 

main mechanism of peat formation and also may alter the 

environmental conditions necessary for the survival of algal and microbial mats that contribute to sediment trapping and resistance to erosion. Cays disturbed by mangrove clearing and dredged fi ll deposition will continue to 

subside, but peat formation will cease. Even if these areas 

become revegetated with coastal beach vegetation, peat 

cannot form because of oxidizing conditions (caused by the 

higher elevations) and lack of the primary peat builder— R. 

mangle. Although disturbed island surfaces have been temporarily raised by dredged fi ll, the inexorable subsidence of 

underlying peat and rising seas will lead to submergence. 

At current rates of peat subsidence and sea-level rise, the elevation gain from dredging will be offset within 20 years.

IMPLICATIONS FOR SUSTAINABLE ECOTOURISM

The Caribbean Region, and in particular the MBRS, is 

a major destination for “eco-tourists,” who are attracted 

to the tropical climate, clear waters, and abundant marine 

life (Uyarra et al., 2005; Diedrich, 2007). A prerequisite 

for sustainable ecotourism is maintenance of a pristine 

natural environment and protection of all biophysical 

components necessary for healthy ecosystems and habitat 

stability (Casagrandi and Rinaldi, 2002). Unregulated ecotourism enterprises threaten the very features that underpin this industry and, in addition, lead to the degradation 

of natural resources essential to the livelihood of citizens 

(e.g., sport and commercial fi sheries) (Burger, 2000; Hall, 

2001). Although “charismatic” ecosystems such as coral 

reefs receive much attention by conservationists and tourism regulators (Diedrich, 2007), less emphasis is placed 

on mangroves. The mangrove destruction occurring in 

the Belize reef system likely refl ects a general misperception that the land beneath mangrove-dominated islands is 

stable, as well as a failure to recognize mangroves as essential components contributing to habitat stability and 

marine biodiversity— which is what attracts eco-tourists 

in the fi rst place (Uyarra et al., 2005).

Our work suggests that the alterations occurring on 

mangrove islands in the MBRS are inconsistent with sustainable ecotourism. In their natural state, mangroves 

build a peat substrate that is resistant to erosion and 

counterbalances subsidence and sea-level rise. In fact, this 

dynamic peat-building process has allowed mangrove islands such as Twin Cays to persist for the past 8,000 years 

(Macintyre et al., 2004a, 2004b; McKee et al., 2007a). 

Attempts to convert mangrove islands to sand islands, 

with white beaches and coconut palms, will ultimately 

fail because the underlying peat subsidence and rising seas 

will eventually prevail. Filling with marine sediment temporarily raises elevations, but without repeated dredging, 

eventually these cleared areas will become submerged, 

ultimately reducing the total land area of islands in the 

MBRS.

Aerial roots of mangroves additionally provide one of 

the few natural hard substrates for growth of many marine 

organisms in the MBRS (Ellison et al., 1996; Goodbody, 

2000; Macintyre et al., 2000) and also create a permeable 

barrier that dampens wave energy, decreasing shoreline 

erosion (Alongi, 2008). Loss of mangrove fringes directly 

decreases the abundance of marine organisms dependent 

on mangrove roots for substrate as well as that of reef 

species dependent on the mangroves as nurseries (Mumby 

et al., 2004). Although the direct and indirect effects of 

dredging on reef fl ats and seagrass beds were not examined in this study, these effects are likely to be substantial, 

given the sensitivity of such systems to disturbance and 

sedimentation (Nugues and Roberts, 2003; Erftemeijer 

and Lewis, 2006).

Future work should examine the long-term consequences of human activities on the resilience of mangrove 

islands to global change and the contribution of mangroves to terrestrial and marine biodiversity and fi shery 

productivity. In addition, cost– benefi t analyses of man33_McKee_415-428_Lang.indd 426 3_McKee_415-428_Lang.indd 426 9/24/09 10:33

/24/09 10:33
NUMBER 38 • 427

grove clearing and dredging and the consequences for 

sustainable ecotourism should be conducted to provide 

economic rationales for conservation and management of 

mangroves and associated habitats.

ACKNOWLEDGMENTS

We thank the government of Belize for permission to 

work at our study sites, Klaus Ruetzler (Smithsonian Institution (SI)) for support and permission to work at the 

Smithsonian Institution Marine Field Station at Carrie Bow 

Cay (CBC) fi eld station, and Mike Carpenter (SI) for logistical arrangements at CBC. We also thank Amy Bunch, Ada 

Diz, and Heather Dyer of IAP World Services for assistance 

with sample processing and Carole McIvor (USGS), Candy 

Feller (SI), and two anonymous reviewers for comments on 

the manuscript. Any use of trade, product, or fi rm names is 

for descriptive purposes only and does not imply endorsement by the U.S. government. This is contribution number 848 of the Caribbean Coral Reef Ecosystems Program 

(CCRE), Smithsonian Institution, supported in part by the 

Hunterdon Oceanographic Research Fund.

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/24/09 10:33
An Overview of Symbiont Bleaching 

in the Epiphytic Foraminiferan 

Sorites dominicensis

Susan L. Richardson

ABSTRACT. Populations of Sorites dominicensis, an epiphytic foraminiferan that possesses dinofl agellate endosymbionts (Symbiodinium), were sampled from seagrass meadows located in Florida and Belize and surveyed for evidence of bleaching. Symbiont 

bleaching was fi rst documented in S. dominicensis populations in the Indian River Lagoon, Florida, in August 2003. Subsequent surveys indicated high rates of bleaching in 

August 2004, followed by a near eradication of the epiphytic foraminiferal population as 

a result of the 2004– 2005 hurricane seasons. Two contrasting sites in Belize, seagrass beds 

on the reef fl at at Carrie Bow Cay and in Boston Bay, Twin Cays, were surveyed in 2005 

and 2006. High rates of bleaching characterize the S. dominicensis populations living on 

turtle grass on the reef fl at off Carrie Bow Cay, although freshwater runoff from summer 

storms during the rainy season may trigger localized bleaching events. Moderate rates of 

bleaching were also observed in S. dominicensis populations in Florida Bay in July 2007. 

Symbiont bleaching in S. dominicensis appears to be triggered by multiple environmental 

factors: increased water temperatures, high levels of irradiance, and infl ux of freshwater 

during storm events. Seasonal summer bleaching events may leave already compromised 

S. dominicensis populations vulnerable to periodic disturbance by hurricanes.

INTRODUCTION

Sorites dominicensis Ehrenberg, 1839, is one of several living foraminiferal 

species that are host to algal endosymbionts (Hallock, 1999; Lee et al., 1979). 

Benthic foraminiferans with algal symbionts occur in several different clades 

(Soritacea, Alveolinacea, Nummulitacea, Calcarinidae, and Amphisteginidae) 

and are widely distributed in shallow-water, tropical to subtropical reef-associated 

marine ecosystems (Langer and Hottinger, 2000). As a group, foraminiferans 

host a diverse array of endosymbionts, most of which are microbial eukaryotic taxa, including stramenopiles (diatoms and chrysophytes), unicellular rhodophytes, unicellular chlorophytes, and alveolates (dinofl agellates) (Lee, 2006; 

Hallock, 1999). Cyanobacterial endosymbionts have also been isolated from 

two different soritid taxa collected from the Red Sea and the Great Barrier Reef 

(Lee, 2006). Foraminiferans with photosymbionts possess enhanced calcifi cation rates, as well as endogenous sources of nutrition (algal photosynthates) 

that allow them to allocate more of their energy resources to cell growth and 

Susan L. Richardson, Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort 

Pierce, Florida 34949, USA, and Harriet L. Wilkes Honors College, Florida Atlantic University, 

5353 Parkside Drive, Jupiter, Florida 33458, USA 

(richards@fau.edu). Manuscript received 15 August 2008; accepted 20 April 2009.

34_Richardson_429-436_Lang.indd 429 4_Richardson_429-436_Lang.indd 429 9/24/09 9:58/24/09 9:58
430 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

maintenance (Lee, 2006; Hallock, 1999; Duguay, 1983; 

Kremer et al., 1980; Lee and Bock, 1976). The algal endosymbionts presumably benefi t from the mutualism as well, 

gaining access to nutrients that are scarce in oligotrophic 

environments and to refuge from predation (Lee, 2006; 

Hallock, 1999).

The mutalistic association of Sorites and other taxa in 

the more inclusive foraminiferal clade Soritida, with dinofl agellate endosymbionts in the Symbiodinium clade, is 

of particular interest to the marine biological community 

because this clade comprises the zooxanthellae in stony 

corals, soft corals, gorgonians, anemones, jellyfi sh, bivalve 

mollusks, nudibranchs, sponges, and ciliates (Baker, 2003; 

Douglas, 2003; Glynn, 1996). Originally considered to be 

a single pandemic species that was symbiotic with a broad 

range of marine taxa, Symbiodinium microadriaticum is 

now known to be part of a more inclusive and genetically 

diverse clade composed of eight major subclades, identifi ed 

by the letters A– H (Pochon and Pawlowski, 2006; Coffroth 

and Santos, 2005; Baker, 2003; Rowan, 1998; Rowan and 

Powers, 1991, 1992). Symbiodinium symbionts from foraminiferal hosts are found in clades C, D, F, G, and H, 

with clades F and H being composed almost exclusively of 

Symbiodinium isolated from soritid foraminiferans (GarciaCuetos et al., 2005; Pochon and Pawlowski, 2006; Pawlowski et al., 2001; Pochon et al., 2001, 2004, 2006; Rodriguez-Lanetty, 2003). Although there is relatively high 

specifi city between Symbiodinium clades F, G, and H and 

Foraminifera, there appears to be very little congruence 

between host and symbiont phylogenies, indicating that 

coevolution has not taken place, at least not at the taxonomic levels sampled to date (Garcia-Cuetos et al., 2005; 

Pochon and Pawlowski, 2006; Pawlowski et al., 2001; Pochon et al., 2001, 2004, 2006). Although DNA sequences 

have not yet been obtained from the endosymbionts of either the Belizean or Indian River Lagoon populations of 

Sorites dominicensis, Symbiodinium sequences from Florida Keys specimens fall within either clade F (subclade F4) 

or H (Garcia-Cuetos et al., 2005; Pochon and Pawlowski, 

2006; Pochon et al., 2006). In all phylogenies published 

to date, clade H, the dominant phylotype isolated from 

the Florida Keys, branches as the sister group to clade C, 

a clade that is widely distributed in the Indo-Pacifi c, and 

exhibits more sensitivity to bleaching than the other Symbiodinium clades (Garcia-Cuetos et al., 2005; Pochon and 

Pawlowski, 2006; Pawlowski et al. 2001; Pochon et al., 

2001, 2004, 2006; Rowan, 1998, 2004).

The morphological characteristics of Symbiodinium

symbionts isolated in culture from specimens of Sorites 

dominicensis collected from the Florida Keys have been 

described by Lee et al. (1979, 1997). Symbionts are distributed throughout the foraminiferal cytoplasm, with the 

highest densities occurring in the intermediate chambers 

and the lowest densities occurring in the outer chambers 

where the digestive vacuoles are concentrated (Richardson, 2006; Müller-Merz and Lee, 1976). Similar to other 

species of foraminiferans, S. dominicensis is multinucleate and possesses two different types of nuclei: generative 

nuclei that participate in reproduction only, and vegetative nuclei that are transcriptionally active and coordinate 

the day-to-day activities of the cell (Müller-Merz and Lee, 

1976). In S. dominicensis, the generative nuclei are localized in the central initial chambers of the test (external 

shell), which are the chambers with the lowest densities of 

dinofl agellates, whereas the transcriptionally active foraminiferal nuclei are distributed throughout the cytoplasm 

in regions with the high symbiont densities (Müller-Merz 

and Lee, 1976).

Estimates of symbiont population size per cell vary 

depending on the methodology employed (Richardson, 

2006; Doyle and Doyle, 1940). Doyle and Doyle (1940) 

estimated the population of dinofl agellates in a 2-mm 

sized individual of S. dominicensis to be approximately 

1.6 104 using light microscopy. In contrast, confocal 

microscopy of a 2-mm sized individual of S. dominicensis

collected from Jupiter Sound yielded an estimated 4 

103 dinofl agellates, equivalent to a density of 1.27 105

endosymbionts cm2 of cytoplasm (Richardson, 2006) 

(Figure 1). Hemacytometer estimates of endosymbiont 

densities in live individuals of S. dominicensis collected 

from Jupiter Sound indicate that symbiont densities range 

from 6.1 102 to 4.8 105 dinofl agellates cm2, with an 

average of 6.5 104 dinofl agellates cm2 (n  85,  7.9 

104, 2  6.2 109) (Ross and Richardson, unpublished data). Endosymbiont populations linearly increase 

with test size: the average number of symbionts per foraminiferal cell is estimated to be 1,469 (n  85, s  2,919, 

s 2  8,523,907) for an individual with a test diameter of 

1.42 mm (n  85, s  0.62, s 2  0.39) (Ross and Richardson, unpublished data).

Live individuals possess a dark yellowish-brown coloration to their cytoplasm as a result of the dense populations of Symbiodinium in each cell (Figure 2). In healthy 

individuals, the coloration is evenly distributed throughout the test, except for the outer chambers, which appear 

colorless because of the low density or absence of endosymbionts from the zone of cytoplasm where digestion 

takes place (Figure 2). The distinctive coloration of the foraminiferal cytoplasm makes it easy to recognize bleached 

or mottled individuals, as described below.

34_Richardson_429-436_Lang.indd 430 4_Richardson_429-436_Lang.indd 430 9/24/09 9:58/24/09 9:58
NUMBER 38 • 431

FIELD OBSERVATIONS OF BLEACHING 

IN SORITES DOMINICENSIS

Symbiont bleaching has been observed in fi eld surveys 

of epiphytic foraminiferal populations from Florida (Indian River Lagoon and Long Key, Florida Keys) and Belize (Carrie Bow Cay and Twin Cays). Bleaching in Sorites 

dominicensis was fi rst documented in epiphytic populations attached to Thalassia testudinum (turtle grass) growing in Jupiter Sound in August 2003 and August 2004, 

followed by fi eld surveys of populations in Belize in July 

2005 and July 2006. Bleaching was also observed in epiphytic populations of S. dominicensis surveyed from the 

Florida Keys in July 2007 (Richardson, unpublished data). 

Although each of the collecting sites studied hosts seagrass 

meadows dominated by T. testudinum, each locality is 

subject to different physical factors (salinity, temperature, 

water clarity, and subaerial exposure), as well as differing 

levels of anthropogenic impact. Detailed descriptions of 

the fi eld sites in Florida and Belize are given by Richardson 

(2006). Although experimental studies of bleaching in S. 

dominicensis have yet to be carried out, fi eld observations 

indicate that symbiont bleaching may occur in response to 

a number of environmental stressors, including increased 

water temperature, freshwater infl ux, subaerial exposure 

during extreme low tides, and periodic disturbance by 

hurricanes.

FIELD METHODS

Only epiphytic specimens of the foraminiferan Sorites 

dominicensis that were attached to blades of the seagrass 

Thalassia testudinum were examined in the studies described 

below. Blades of T. testudinum were harvested by wading or 

snorkeling. Seagrass leaves were removed at the base of the 

blade, submerged in seawater in a Ziploc bag, and stored in a 

cooler until return from the fi eld. Both sides of each seagrass 

blade were examined for the presence of epiphytic foraminiferans using a binocular dissecting microscope (Leica M5). 

All specimens of the species S. dominicensis were removed 

from the blade using a fi ne paintbrush or dental pick, measured, and stored on cardboard microslides for additional 

study and reference material. The cytoplasmic condition 

(healthy, pale, mottled, totally bleached) and reproductive 

state (nonreproductive, presence of brood chambers, presence of embryos in brood chambers, or postreproductive) 

FIGURE 1. Confocal image of live individual of Sorites dominicensis from Jupiter Sound, Florida. The foraminiferal test is subdivided into hexagonal chamberlets. The dinofl agellate endosymbionts are most densely packed into the intermediate chambers. 

Scale bar  200 m.

FIGURE 2. Live specimens of Sorites dominicensis from Belize, Central America. The two individuals in the upper part of the image 

show patches of bleached cytoplasm. Note that all specimens, except 

for the individual in the lower left, possess few, if any, endosymbionts in the outer two or three chambers. The specimen in the lower 

left is a reproductive individual preparing to undergo multiple fi ssion. The specimen on the upper right is approximately 2 mm in 

diameter.

34_Richardson_429-436_Lang.indd 431 4_Richardson_429-436_Lang.indd 431 9/24/09 9:58/24/09 9:58
432 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of each specimen were noted. Specimens were measured 

using an optical micrometer calibrated to a stage micrometer. Micrographs of representative individuals (healthy, 

mottled, and bleached) were taken using a Nikon Coolpix 

camera with an MCool (Martin Optics) phototube.

Live individuals were recognized by their distinctive 

cytoplasmic coloration as described below, and/or by the 

presence of pseudopodial arrays emanating from around the 

periphery of the protist’s test. Bundles of bifurcating pseudopodia in live individuals are usually covered with a light 

dusting of fi ne-grained sediment, giving the specimens a starshaped appearance. Individuals were recorded as having 

healthy cytoplasm if the cytoplasm possessed an evenly distributed, yellowish-brown coloration (see Figure 2). Individuals were recorded as having a mottled cytoplasm if the cytoplasm contained white-colored patches, interspersed with 

yellowish-brown sections of cytoplasm (Figure 2). Mottled 

individuals contained patches of white cytoplasm that were 

visible on both sides of the disk-shaped test. Specimens were 

recorded as being totally bleached if the test was completely 

white. The tests of postreproductive individuals, that is, individuals that had undergone reproduction by multiple fi ssion, were not included in the tallies of bleached specimens. 

Postreproductive tests are easily distinguished from bleached 

tests by the presence of fragmented brood chambers, undisseminated embryos, and clusters of dispersed juveniles in 

close proximity to the parental test. It is assumed that few, if 

any, of the totally bleached tests had undergone gametogenesis, as microspheric tests (tests formed by syngamy) have 

never been observed in any of the populations of this species 

surveyed by the author.

WATER TEMPERATURE AND BLEACHING

Studies conducted at both the Jupiter Sound and Belize 

sites indicate that elevated water temperature, or a combination of elevated water temperature and subaerial exposure, 

can induce symbiont bleaching in S. dominicensis. Bleaching was fi rst observed in the Jupiter Sound populations in 

2003 during August (Table 1), when water temperatures 

are typically at their maximum, often reaching extremes as 

high as 31°C (RiverKeeper Data, Loxahatchee River District). A relatively low abundance of bleached individuals 

was recorded in late July 2004; however, a resampling of 

the site a few weeks later in August indicated that the incidence of bleaching had risen 14 fold (Table 2). In July 

2004, water temperatures recorded at the Jupiter Sound site 

ranged from 30° to 31°C between 1:00 PM and 3:30 PM during an extremely low spring tide that resulted in the subaerial exposure of major portions of the seagrass bed. No water 

temperature data are available for Jupiter Sound in August 

2004, although the water was uncomfortably hot to the 

touch at the time of collection (Richardson, unpublished). 

Bleaching was undetectable in surveys of the S. dominicensis

populations conducted at other times of the year in both 

2003 and 2004 (Richardson, unpublished data).

In Belize, water temperatures were recorded using 

HOBO Tidbit (Onset) submersible temperature loggers 

deployed for three days in July 2005. One logger was deployed on the reef fl at at Carrie Bow Cay and the other in 

Boston Bay, Twin Cays. The range of water temperatures 

recorded for both sites are listed in Table 3 and Figure 3. 

Although the overall mean temperatures were identical for 

both sites (s  32°C), the reef fl at off Carrie Bow Cay 

experienced a wider range of temperatures (29°– 40°C), 

with higher maximum temperatures recorded during the 

late afternoon and lower minimum temperatures recorded 

at night (Figure 3; Table 3). Correspondingly, the rate of 

bleaching recorded from the reef fl at at Carrie Bow Cay 

was almost fi ve times higher than that observed in BosTABLE 1. Relative abundance of bleached individuals of Sorites 

dominicensis from Jupiter Sound, Florida, during August 2003 

(n  total number of tests examined).

 Percent of tests

 2 Aug 2003 12 Aug 2003

Test condition (n  580) (n  147)

Mottled cytoplasm 1.0% 1.0%

White cytoplasm 15% 12%

Total bleached 16% 13%

TABLE 2. Relative abundance of bleached individuals of Sorites 

dominicensis from Jupiter Sound, Florida during July and August 2004 (n  total number of tests examined).

 Percent of tests

 29 Jul 2004 19 Aug 2004

Test condition (n  446) (n  14)

Mottled cytoplasm 2.0% 29%

White cytoplasm 0% 0%

Total bleached 2.0% 29%

34_Richardson_429-436_Lang.indd 432 4_Richardson_429-436_Lang.indd 432 9/24/09 9:59/24/09 9:59
NUMBER 38 • 433

ton Bay, Twin Cays (Table 4). Although the water temperatures recorded in Boston Bay, Twin Cays, were not 

as extreme as those recorded off Carrie Bow Cay, they 

still were higher than the HotSpot (28.9°C) and bleaching 

(HotSpot  1°C) thresholds derived by NOAA/NESDIS 

for Glovers Reef (Opishinski, 2006). The same sites were 

resurveyed in July 2006, and the incidence of bleaching 

on the reef fl at at Carrie Bow Cay was observed to be 11 

times higher than the incidence of bleaching recorded in 

Boston Bay, Twin Cays, which exhibited almost negligible 

levels of bleaching (Table 5).

FRESHWATER INFLUX AND BLEACHING

In July and August 2006, continued sampling of the 

Carrie Bow Cay and Twin Cays fi eld sites in Belize yielded 

results that indicate that symbiont bleaching in S. dominicensis can also be triggered by an infl ux of freshwater 

during storm events. In July 2006, fi eld collections were 

suspended during a three-day period of intense rain then 

restarted after the storms subsided. After the rainstorms, 

the incidence of bleaching recorded at both sites rose in 

all three categories (pale cytoplasm, mottled cytoplasm, 

TABLE 3. Characteristics of two collecting sites in Belize.

Characteristic Carrie Bow Cay Twin Cays

Water depth 0.5 m 1.0 m

Exposure Exposed during low tides Subtidal

Water clarity Very clear High tannins and mangrove detritus

Water movement Swift current Sheltered with slower current

Temperature range (1– 4 July 2005) 30°– 35°C 29°– 40°C

FIGURE 3. Water temperature variations on the reef fl at at Carrie Bow Cay and in Boston Bay, Twin Cays, 

Belize, as measured at noon and every 2.5 hours thereafter during 1– 4 July 2005.

34_Richardson_429-436_Lang.indd 433 4_Richardson_429-436_Lang.indd 433 9/24/09 9:59/24/09 9:59
434 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

and white cytoplasm) (Table 6). Although bleaching on 

the reef fl at at Carrie Bow Cay was slightly higher than 

the prestorm levels (11% vs. 8.1%), the total poststorm 

incidence of bleaching in Boston Bay was observed to be 

more than 65 times higher than that observed just a few 

days earlier (Table 6). Although the waters in Boston Bay 

are normally of open ocean marine salinities, during heavy 

rains and slack tides cold, brackish water drains off Hidden Lake in the Twin Cays and empties into Boston Bay 

through Hidden Creek (Rützler et al., 2004). Interestingly, 

juveniles were disproportionately impacted by the bleaching event: 34 of 60 of the tests with white cytoplasm appeared to be individuals from the same brood (Table 6).

IMPACT OF HURRICANES AND RECOVERY

Seasonal bleaching events cause increased mortality in 

S. dominicensis, resulting in compromised populations that 

are more sensitive to periodic disturbance by hurricanes. 

Monthly surveys in 2001, 2003, and 2004 indicate that 

S. dominicensis populations normally plummet in the late 

summer, stay low throughout the winter, and eventually 

recover and bloom the following spring in late April and 

May (Richardson, unpublished data). In September 2004, 

the Jupiter Sound site was traversed by two hurricanes, 

Jeanne and Frances (Beven, 2005; Lawrence and Cobb, 

2005). The Jupiter site was situated in the south eyewall 

for both storms, and experienced high winds and storm 

surges and extensive freshwater inundation. Dark, cloudy, 

turbid water continued to characterize the site for several 

months following the hurricanes. Other impacts included 

loss of shading because of downed trees and overgrowth 

of the seagrass by cyanobacterial blooms. The entire epiphytic foraminiferal community at the Jupiter Sound site 

was impacted by the 2004 hurricane season (Richardson, 

unpublished data). Initially, a dramatic reduction in species 

diversity and abundance was observed, with two species 

comprising 92% of the community in April and May 2005. 

By August 2005 the community had rebounded to 2001 

levels of species diversity and density, with the exception 

of the apparent local eradication of S. dominicensis (Richardson, unpublished data). Sorites dominicensis is the only 

species at this site to possess photosynthetic endosymbionts and thus is sensitive to the reduced transmission of 

light in the water column that resulted from the months of 

increased turbidity following the 2004 hurricanes.

In October 2005, Jupiter Sound was impacted by 

Hurricane Wilma (Pasch et al., 2006), although this time 

the region experienced the high winds of the north eyeTABLE 4. Relative abundance of bleached individuals of Sorites 

dominicensis from two localities in Belize during July 2005 (n 

total number of tests examined).

 Percent of tests

 Carrie Bow Cay Boston Bay, Twin Cays

Test condition (n  797) (n  685)

Mottled cytoplasm 4.3% 2.5%

White cytoplasm 14% 1.5%

Total bleached 19% 3.9%

TABLE 5. Relative abundance of bleached individuals of Sorites 

dominicensis from two localities in Belize during July 2006 (n 

total number of tests examined). All specimens were collected 

before a three-day period of intense rain.

 Percent of tests

 Carrie Bow Cay, Boston Bay, Twin Cays,

 21 Jul 2006 23 Jul 2006

Test condition (n  62) (n  349)

Pale cytoplasm 0% 0%

Mottled cytoplasm 3.2% 0.29%

White cytoplasm 4.8% 0%

Total bleached 8.1% 0.29%

TABLE 6. Relative abundance of bleached individuals of Sorites 

dominicensis from two localities in Belize during July and August 2006 (n  total number of tests examined). All specimens 

were collected after a three-day period of intense rain.

 Percent of tests

 Carrie Bow Cay, Boston Bay, Twin Cays,

 1 Aug 2006 27 Jul 2006

Test condition (n  132) (n  369)

Pale cytoplasm 1.5% 0.27%

Mottled cytoplasm 0.76% 2.4%

White cytoplasm 8.3% 16% a

Total bleached 11% 19%

a Of 60 individuals, 34 were juveniles from the same brood.

34_Richardson_429-436_Lang.indd 434 4_Richardson_429-436_Lang.indd 434 9/24/09 9:59/24/09 9:59
NUMBER 38 • 435

wall of the storm. Individuals of S. dominicensis were not 

recovered from the Jupiter Sound site until the summer of 

2007 and did not reach their pre-hurricane densities until 

April 2008 (Richardson, unpublished). A survey of 446 

individuals of S. dominicensis, collected in April 2008, 

yielded a high incidence of bleached individuals (24% total), an unusual event for the spring (Table 7). The trigger 

for this event is unknown; the rainfall during this period 

was below average as the region was experiencing an extended seasonal drought. It is also not known whether the 

population recovered through the reproduction of relict 

populations of S. dominicensis that survived the hurricanes of 2004 and 2005 or whether the site was repopulated through immigrants transported by the Gulf Stream 

from the Florida Keys and/or the Caribbean.

DISCUSSION

The results from the fi eld studies described above document the occurrence of bleaching in Sorites dominicensis, 

a dinofl agellate-bearing foraminiferan, and delineate some 

of the environmental stressors that trigger bleaching. As 

has been observed in corals, bleaching in epiphytic specimens of S. dominicensis may be triggered by multiple environmental factors, such as increased irradiance during 

subaerial exposure at low tide, increased water temperatures, infl ux of freshwater runoff during storm events, and 

catastrophic disturbance during hurricanes. The symptoms of bleaching in S. dominicensis include decrease in 

intensity of coloration (pale appearance), the patchy loss 

of cytoplasmic coloration (mottled appearance), and the 

total loss of cytoplasmic coloration (white tests). Symbiont bleaching in S. dominicensis can be distinguished from 

the loss of cytoplasmic coloration that occurs during the 

process of reproduction through multiple fi ssion as the 

symbiont-rich cytoplasm moves from the central region of 

the test to the periphery where the brood chambers and 

embryos will form. Studies are currently underway to link 

qualitative observations of bleaching in S. dominicensis to 

quantitative studies of symbiont density in bleached specimens using staining techniques that differentiate necrotic 

or apoptotic algal cells.

The relatively high water temperatures recorded on the 

reef fl at at Carrie Bow Cay in July 2005 are not unusual 

for tropical seagrasses, which may experience annual fl uctuations in seawater temperatures ranging from 19.8° to 

41°C (Campbell et al., 2006). Unusually high water daily 

temperatures (40°– 43°C) have been recorded in seagrass 

beds growing in shallow water off Papua New Guinea 

(Fred Short, University of New Hampshire, personal communication, January 2006). In addition to high temperatures, tropical seagrasses growing in shallow- water pools 

in the intertidal zone are subject to desiccation, extremely 

high levels of photosynthetically active radiation, and high 

levels of ultraviolet radiation (Campbell et al., 2006; Durako and Kunzelman, 2002).

Although the underlying mechanisms of bleaching in 

S. dominicensis are unknown, it is hypothesized that several of the proposed mechanisms for bleaching in corals 

may function in foraminiferans as well, such as reduced 

effi ciency of photosystem II resulting from increased irradiance (Venn et al., 2008; Smith et al., 2005), and the 

production of damaging reactive oxygen species via several 

different pathways (Lesser, 2006; Smith et al., 2005).

Soritid foraminiferans have the potential to serve as a 

model system for bleaching, the need of which was recently 

emphasized by Weis et al. (2008). Not only do S. dominicensis and other soritids possess Symbiodinium endosymbionts that are closely related to the zooxanthellae in corals 

and other metazoans, but the small size of S. dominicensis

facilitates investigation of symbiont bleaching in hospite, 

using methods such as in situ hybridization, immunofl uorescence, and other imaging techniques. Future research 

will focus on developing culture methods for S. dominicensis and on exploring cytological methods that will facilitate the visualization of the cell processes underlying the 

bleaching response in foraminiferans.

ACKNOWLEDGMENTS

The fi eld research for this study was funded through 

grants from the Caribbean Coral Reef Ecosystems (CCRE) 

Program, National Museum of Natural History (NMNH), 

Washington, D.C., and the Smithsonian Marine Station at 

Fort Pierce (SMSFP), Florida. I am grateful to Jon, Kathleen, and Scott Moore (Florida Atlantic University, New 

College of Florida, and Indian River Charter High School, 

TABLE 7. Relative abundance of bleached individuals of Sorites 

dominicensis from Jupiter Sound, Florida, 4 April 2008, as determined from examination of 446 tests.

Test condition Percent of tests (n  446)

Pale cytoplasm 5.9%

Mottled cytoplasm 7.8%

White cytoplasm 9.8%

Total bleached 24%

34_Richardson_429-436_Lang.indd 435 4_Richardson_429-436_Lang.indd 435 9/24/09 9:59/24/09 9:59
436 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

respectively) for their invaluable assistance in the fi eld at 

the Jupiter Island site in Florida since 2001. Mike Carpenter (NMNH) provided assistance in the fi eld in Belize 

in 2005. This is contribution number 839 of CCRE, supported in part by the Hunterdon Oceanographic Research 

Fund, and SMSFP contribution number 758.

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New Perspectives on Ecological Mechanisms 

Affecting Coral Recruitment on Reefs

Raphael Ritson-Williams, Suzanne N. Arnold, 

Nicole D. Fogarty, Robert S. Steneck, 

Mark J. A. Vermeij, and Valerie J. Paul

ABSTRACT. Coral mortality has increased in recent decades, making coral recruitment 

more important than ever in sustaining coral reef ecosystems and contributing to their 

resilience. This review summarizes existing information on ecological factors affecting 

scleractinian coral recruitment. Successful recruitment requires the survival of coral offspring through sequential life history stages. Larval availability, successful settlement, 

and post-settlement survival and growth are all necessary for the addition of new coral 

individuals to a reef and ultimately maintenance or recovery of coral reef ecosystems. As 

environmental conditions continue to become more hostile to corals on a global scale, 

further research on fertilization ecology, connectivity, larval condition, positive and negative cues infl uencing substrate selection, and post-settlement ecology will be critical to 

our ability to manage these diverse ecosystems for recovery. A better understanding of 

the ecological factors infl uencing coral recruitment is fundamental to coral reef ecology 

and management.

INTRODUCTION

Coral reefs are facing unprecedented human impacts and continuing acute 

and chronic threats that can impact community structure (Nyström et al., 

2000). Their ability to resist such changes or to recover from them defi nes their 

“resilience” (sensu Holling, 1973). Unfortunately, coral reef ecosystems can be 

resilient in either the more desirable coral-dominated phase or in the less desirable algal-dominated phase (Hughes et al., 2005). Although we know much 

about what causes undesirable “phase shifts” (Done, 1992; Hughes, 1994; 

Pandolfi et al., 2005), we know relatively little about what drives coral community recovery (Connell, 1997).

Scleractinian corals are uniquely important to coral reef ecosystems as 

ecosystem engineers that structure the habitat (Jones et al., 1994, 1997). The 

abundance of live coral drives key ecological processes in the wider coral reef 

community, such as providing recruitment habitat for reef fi sh, lobsters, and 

sea urchins (Lee, 2006; Mumby and Steneck, 2008). In the past 30 years, the 

percent cover of live coral has decreased on a global scale (Gardner et al., 2003; 

Bruno and Selig, 2007), raising the question: How can we increase the number 

of corals in these ecosystems for recovery?

Raphael Ritson-Williams and Valerie J. Paul, 

Smithsonian Marine Station at Fort Pierce, 701 

Seaway Drive, Fort Pierce, Florida 34949, USA. 

Suzanne N. Arnold and Robert S. Steneck, University of Maine, School of Marine Sciences, 

Darling Marine Center, Walpole, Maine 04573, 

USA. Nicole D. Fogarty, Department of Biological Science, Florida State University, Tallahassee, 

Florida 32306-4295, USA. Mark J. A. Vermeij, 

CARMABI, Piscaderabaai z/n, Curacao, Netherlands Antilles. Corresponding author: R. RitsonWilliams (williams@si.edu). Manuscript received 

9 June 2008; accepted 20 April 2009.

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438 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Larval settlement (when they fi rst attach to the benthos) and subsequent survival (recruitment) are processes 

that can control marine population dynamics (Gaines and 

Roughgarden, 1985; Doherty and Fowler, 1994; Palma et 

al., 1999). Although corals can reproduce clonally (Fautin, 2003; Baums et al., 2006), recruitment resulting from 

sexual reproduction is the primary means of recolonization for most species (Connell et al., 1997) and adds genetic variation to coral populations, which may increase 

survival of a species. Coral settlement followed by subsequent recruit survival and growth maintains coral populations and is necessary for coral reef recovery. For this cycle 

to occur on any given reef, larval survival and recruitment 

are dependent on a sequence of three phases: (1) larval 

availability, which integrates gamete production, fertilization success, and connectivity; (2) settlement ecology, 

which relates to larval condition and substrate selection 

behavior; and (3) post-settlement ecology, including substrate-specifi c survival and growth (Figure 1).

This review summarizes existing information on ecological factors affecting scleractinian corals during these 

fi rst three phases of their life, covering the period from 

gamete release to juvenile coral colonies (typically described as 40 mm). We discuss factors that are critical for 

coral recruitment success, and where insuffi cient data exist, 

we draw parallels to concepts that have been developed for 

other marine larvae or adult corals and briefl y discuss their 

relevance for the early life history stages of corals.

LARVAL AVAILABILITY

Larval supply to a reef depends on sequential processes of gamete production, fertilization success, and larval transport (i.e., larval dispersal and connectivity). Basic 

life history traits of corals can greatly infl uence the range of 

strategies that are used to ensure larval availability. Scleractinians have two main reproductive modes: brooding, 

where sperm are released into the water column and taken 

in by conspecifi cs for internal fertilization, and broadcast 

spawning, wherein both egg and sperm are released into 

the environment so that fertilization occurs externally, that 

is, in the water column (Figure 2; Fadlallah, 1983; Szmant, 

1986; Richmond and Hunter, 1990; Richmond, 1997). 

FIGURE 1. Three sequential phases necessary for successful coral recruitment starting with larval availability, 

progressing to settlement ecology, and ending with post-settlement ecology. (Drawn by Mark Vermeij.)

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FIGURE 2. Different modes of reproduction infl uence larval supply in coral species. a, Female 

Stephanocoenia intersepta, a gonochoric spawner, releases eggs. b, A male S. intersepta releases 

sperm. c, The hermaphrodite Montastraea faveolata releases eggs and sperm as bundles that 

fl oat to the surface, where they break apart for fertilization. d, For Acropora palmata (and other 

spawners), fertilization of coral eggs occurs in the water column. e, A larva of Acropora palmata completes development in the water column. f, In contrast, a larva of Porites astreoides

(a brooder) is fully developed when it is released from its parent and contains zooxanthellae. 

(Photographs a, b, by Mark Vermeij; c, e, f, by Raphael Ritson-Williams; d, by Nicole Fogarty.)

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440 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

A minority of reef-building coral species worldwide are 

brooders, but brooding is the dominant reproductive mode 

found in the Caribbean Sea (Szmant, 1986; Richmond and 

Hunter, 1990; Smith, 1992). Broadcast spawning is a more 

common reproductive mode in coral species, and in Australia more than 100 coral species may spawn on a single 

night (Harrison et al., 1984; Willis et al., 1985; Babcock 

and Heyward, 1986). Species representing these modes 

differ in colony size, gametic cycles, larval competency, 

dispersal distance, and zooxanthellae transmission (Richmond and Hunter, 1990). Brooders are typically smaller 

than spawning corals and have multiple planulating cycles 

per year, as opposed to one or two cycles in broadcast 

spawners (Szmant, 1986).

FECUNDITY

Reproductive mode determines the frequency of larval release; however, both abiotic and biotic factors can 

infl uence the amount of gametes produced in corals. The 

production of gametes is only possible when a coral has 

reached an age, and perhaps more importantly a size, capable of reproduction (Hughes, 1984; Szmant, 1986). It is 

diffi cult to measure the impact of stressors on gamete production because it is naturally variable both temporally 

and between individuals within a species (Chorneskey and 

Peters, 1987). As coral cover declines in both the Caribbean 

Sea and the Pacifi c Ocean (Gardner et al., 2003; Bruno 

and Selig, 2007) there are fewer and often smaller adult 

colonies. This change could reduce coral fecundity because small body size reduces gamete production (Szmant, 

1986) and low population densities reduce fertilization 

success (see Fertilization section, below). Even with relatively high adult coral densities the fecundity of individual 

colonies can be decreased by many stressors before and 

during gametogenesis.

Coral bleaching has been observed to stop gametogenesis (Szmant and Gassman, 1990), reduce the number 

of gametes produced (Fine et al., 2001), and decrease fertilization rates in Acropora corals (Omori et al., 2001). 

Nutrients added to the water column decreased the number of successfully developed embryos that were formed in 

the corals Acropora longicyathus and A. aspera (Koop et 

al., 2001). Changes in salinity and sedimentation can also 

reduce gamete production and fertilization success in corals (Richmond, 1993a, 1993b). Guzman et al. (1994) suggested that the increase in injury levels and slower growth 

in corals exposed to an oil spill further reduced gamete 

size, viability, and fecundity. The presence of macroalgae 

adjacent to coral colonies can decrease fecundity (including the number and size of eggs) in the corals Montastraea 

annularis and Montipora digitata (Hughes et al., 2007; 

Foster et al., 2008). Impacts on fecundity are perhaps best 

summarized by Rinkevich and Loya (1987), who suggested that because reproductive activity involves such 

high energy expenditure, any stress that diminishes energy 

reserves will have an effect on adult fecundity.

FERTILIZATION ECOLOGY

Because broadcast spawners only have one or two 

planulating cycles a year, it is imperative that fertilization be successful. In any broadcast species, fertilization 

success is highly variable and largely depends on the 

synchronization of gamete release, gamete compatibility 

(Palumbi, 1994; Levitan et al., 2004), gamete age (Oliver 

and Babcock, 1992; Levitan et al., 2004), and abundance 

of spawning adults (Levitan et al., 1992, 2004). However, 

the health of the spawning colony and environmental conditions during the spawning event also affect fertilization 

success (Richmond, 1997; Humphrey et al., 2008).

During multispecies spawning events, synchronized 

gamete release and species-specifi c gamete recognition 

are critical for fertilization success and reducing the probability of interspecifi c fertilization (hybridization), which 

may result in reduced offspring fi tness (Mayr, 1963); 

however, Willis et al. (2006) suggest a role for hybridization in range expansion and adaptation to a changing 

environment. Species with overlapping spawning times 

typically display low interspecifi c fertilization success in 

laboratory crosses (Willis et al., 1997; Hatta et al., 1999; 

Levitan et al., 2004). Interspecifi c fertilization success is 

usually higher among morphologically similar species, 

suggesting they are more closely related or possibly the 

same species (Willis et al., 1997; Hatta et al., 1999; Wolstenholme, 2004), but interspecifi c fertilization can also 

occur between Acropora species that have very different 

branching morphologies (Hatta et al., 1999). Fertilization success during a mass spawning event could be the 

result of sperm attractant molecules produced by coral 

eggs (Coll et al., 1994; Babcock, 1995) but could also be 

regulated by gamete recognition proteins, such as those 

that ensure species-specifi c fertilization in spawning sea 

urchins (Zigler et al., 2005).

If coral colonies spawn asynchronously or encountered gametes are not compatible, eggs may go unfertilized 

for extended periods of time or sperm may lose its viability. The effect of age on gamete viability and fertilization 

success differs among coral species; Platygyra sinensis

showed reduced fertilization after three hours (Oliver and 

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NUMBER 38 • 441

Babcock, 1992), but in Acropora spp. reduced fertilization success occurred after seven to eight hours (Willis et 

al., 1997; Omori et al., 2001). With increasing gamete 

age, fertilization success is reduced in conspecifi c crosses, 

but aging effects on gamete viability differ between sperm 

and eggs. Montastraea spp. sperm lose viability after two 

hours but eggs stay viable for more than three hours (Levitan et al., 2004). Another consequence of gamete aging is 

an increase in the likelihood of interspecifi c fertilization. 

Hybridization rates between Montastraea faveolata eggs 

and M. annularis and M. franksi sperm increased when 

eggs had aged at least 75 minutes (Levitan et al., 2004). 

Increased interspecifi c fertilization may be caused by a 

breakdown in gamete recognition proteins, but the specifi c 

mechanisms remain to be determined.

The density of spawning individuals plays a critical 

role in fertilization success. If reproductive individual 

densities are too low, fertilization success will be limited 

(also referred to as the allee effect) (Levitan and McGovern, 2005). Coma and Lasker (1997) found that fertilization success in gorgonians was infl uenced by the density 

of gametes, which was determined by nearest neighbor 

distances (approximately 10 m), synchronous gamete release, or hydrodynamic processes. These factors probably 

infl uence scleractinian fertilization success; however, it is 

diffi cult to directly measure species-specifi c sperm concentrations in situ because a number of coral species spawn 

synchronously. Field studies examining sperm concentrations have used either of two methods: (1) measuring the 

percent of fertilized eggs collected at different times and 

locations on the reef or (2) determining the fertilization 

potential of collected surface water samples by adding 

them to unfertilized eggs and recording the proportion of 

eggs fertilized (Oliver and Babcock, 1992; Levitan et al., 

2004). When lower production or dilution resulted in 

locally lower than normal sperm concentrations, fertilization success was reduced (Oliver and Babcock, 1992; 

Willis et al., 1997; Omori et al., 2001; Levitan et al., 

2004). These studies showed peak fertilization potential 

during or shortly after coral species spawn (Oliver and 

Babcock, 1992; Levitan et al., 2004). Hence, synchronized 

gamete release is a mechanism for the high gamete density 

needed to ensure fertilization success.

High gamete concentration brings with it a potential 

risk as well; as sperm densities increase so does the probability of polyspermy, whereby eggs become fertilized by 

more than one sperm cell, which results in lowered fertilization rates and developmental failure (Styan, 1998; Tomaiuolo et al., 2007). Reduced fertilization success at high 

sperm concentrations has been described for several coral 

species (Oliver and Babcock, 1992; Willis et al., 1997; 

Levitan et al., 2004), suggesting polyspermic fertilization 

can occur in scleractinian corals. These fi ndings suggest a 

trade-off between spawning synchronously (i.e., high gamete density) with other conspecifi cs to increase fertilization 

and the potential risk of polyspermy. Polyspermy may 

therefore act as a negative density-dependent mechanism. 

Despite the evidence for polyspermy in coral laboratory 

crosses, fi eld fertilization rates never reached 100% during mass spawning events (97% maximum; Levitan et al., 

2004), suggesting that polyspermic conditions are unlikely 

to occur in nature. In light of recent decreases in adult 

coral populations, reduced adult density and gamete aging 

are perhaps the greatest threats to larval production.

LARVAL TRANSPORT: DISPERSAL AND CONNECTIVITY

After gamete fertilization, developing planula larvae 

transport typically away from reproductive populations 

(called “dispersal”) and to reefs where they recruit (called 

“connectivity”) (Levin, 2006). The density of planulae arriving to a reef determines recruitment strength. Larval 

survival during dispersal varies by means of a combination of hydrodynamic processes, larval energetics, predation pressure (Fabricius and Metzner, 2004), and water 

quality (Richmond et al., 2007).

Reproductive modes can provide insight into dispersal 

potential, even though the planktonic duration of coral 

species can be highly variable and remains undocumented 

for the majority of scleractinian species. For example, 

brooders generally settle within hours after release (Carlon 

and Olson, 1993), whereas broadcast spawners such as 

Acropora spp., Goniastrea spp., Platygyra spp., and Montastraea spp. have planktonic period of 4 to 7 days before 

they are competent to settle and metamorphose (Babcock 

and Heyward, 1986; Szmant, 1986). Larvae of the broadcast spawners Acropora muricata and A. valida settled 

within 9 to 10 days (Nozawa and Harrison, 2008), but 

larvae of the spawning corals Platygyra daedalea and Goniastrea favulus can settle between 2 and 3 days after fertilization, which is sooner than some brooding corals, suggesting that dispersal of these species might be of shorter 

duration than has been assumed from survival estimates 

(Miller and Mundy, 2003). In the absence of settlement 

substrate, a small percentage of Acropora latistella, Favia 

pallida, Pectinia paeonia, Goniastrea aspera, and Montastraea magnistellata larvae survived for 195 to 244 days in 

the water column (Graham et al., 2008). Planulae larvae 

can probably survive drifting in the plankton for long durations until they encounter suitable settlement substrate; 

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442 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

however, the length of the planktonic period will partially 

depend on whether the larvae have acquired zooxanthellae, which give them additional energy reserves, from the 

parent colony (Richmond, 1987).

The frequency of recruitment as a function of distance from a reproductive source population is called a 

“dispersal kernel” (Steneck, 2006). For most planktonic 

larvae it was assumed that relatively long larval survival 

potential in combination with oceanographic transport 

would generally prevent settlement close to a reproductive 

source (Cowen et al., 2006). Recent reviews suggest that 

even though many marine invertebrate larvae have the potential (energy reserves) for long-distance dispersal, they 

often settle locally because of a combination of oceanographic conditions, larval behavior, and increasing mortality associated with planktonic conditions (Cowen et al., 

2000; Strathmann et al., 2002; Levin, 2006). The shape 

of most dispersal kernels is now thought to be skewed toward the reproductive source, that is, increased rates of local recruitment (Figure 3; Steneck, 2006). Most dispersal 

and connectivity research to date has focused on fi shes; 

however, one study measured ecological connectivity of 

coral larvae via a fi eld experiment conducted around the 

isolated Helix Reef in Australia (Sammarco and Andrews, 

1988). They reported that 70% of coral recruitment occurred within 300 m of the larval source and that rates 

of recruitment declined with distance downstream from 

the reef (Sammarco and Andrews, 1988). Further, as expected, broadcasters dispersed farther than did species of 

brooding corals, but the estimated ecologically relevant 

dispersal kernel for both species was remarkably local. A 

recent review discusses the limited dispersal kernel of coral 

planulae (Steneck, 2006); however, there is little experimental evidence for the mechanisms that determine coral 

ecological connectivity.

Recruitment rates must equal or exceed rates of adult 

mortality to sustain a local population. Most dispersal kernels show high rates of recruitment near the reproductive 

source, with recruitment decreasing as distance increases 

(Figure 3). Although that tail is important for gene fl ow, 

that low density of settlement is not suffi cient to sustain 

populations. That is, the ecologically relevant portion of 

a dispersal kernel refl ects the sustained rate of recruitment 

necessary to compensate for rates of mortality. The critical 

level of settlement to sustain populations (i.e., horizontal 

line above each shaded half of Figure 3) is not known; however, colonization rates of the introduced orange cup coral 

Tubastraea coccina can provide some real-world insights 

into the scale of ecological and evolutionary connectivity. 

This brooding species was fi rst introduced to the Netherlands Antilles in 1943 and then spread from island to island through the Caribbean, taking 50 years to reach the 

Bahamas and 60 years to reach Florida (Fenner and Banks, 

2004). Once in a region, local populations grew rapidly. 

This fi nding is consistent with the concept that the biogeographic spread results from the evolutionarily important 

“long tail” of the dispersal kernel, whereas the ecologically 

and demographically signifi cant portion of the dispersal 

kernel controlling local colonization is much smaller and 

more local (Figure 3A). Observations of the spread of T. 

coccina are conservative because some of the spread of 

this species probably resulted from colonized ships moving 

among the regions (Fenner and Banks, 2004).

Ecological connectivity necessary to sustain populations against chronic mortality is much more diffi cult to 

measure than is evolutionary connectivity. Evolutionary 

or genetic connectivity can be directly measured using a 

variety of molecular genetic techniques (reviewed in Hellberg, 2007). In Japan, gene fl ow between islands 30 to 

150 km apart was determined to be consistently higher 

for the spawner Acropora tenuis than for the brooding 

FIGURE 3. Dispersal kernels determine potential connectivity distance between reproductive populations and offspring. A, Distinction between ecologically important recruitment necessary to balance 

against local mortality and evolutionarily important recruitment to 

balance against local extinction. B, Shrinking dispersal kernels resulting from adult coral mortality. (After Steneck, 2006.)

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NUMBER 38 • 443

species Stylophora pistillata, but both coral species had 

unique genotypes across islands separated by 500 km (Nishikawa et al., 2003). In the Caribbean, a genetic break 

was detected for Acropora palmata, roughly dividing populations from the Greater Antilles and western Caribbean 

from populations in the Lesser Antilles and the southern 

and eastern Caribbean (Baums et al., 2005). On the relatively contiguous Great Barrier Reef (GBR), high rates of 

genetic connectivity were observed for both brooders and 

spawners. For example, gene fl ow was detected in all the 

spawners and three of the fi ve brooders despite being separated by 500 to 1,200 km (Ayre and Hughes, 2000). However, the same species of corals were genetically distinct 

on Lord Howe Island, which is separated from the GBR 

by 700 km (Ayre and Hughes, 2004). This observation 

suggests that coral larvae can use islands within the evolutionarily important tail of the dispersal kernel as “stepping 

stones” to maintain genetic connectivity between distant 

reefs separated by long distances (Steneck, 2006).

Although dispersal kernels are useful for visualizing how larval availability declines with distance from a 

source, their ecological effect can be variable. For example, 

without changing the shape of the kernel but reducing the 

number of recruits as a consequence of reduced reproductive output following an adult mortality event (Figure 3B), 

the range of both the ecological and evolutionary parts of 

the kernel can shrink. If this happens, connectivity among 

distant reefs could sever, making recovery following an 

acute disturbance diffi cult or impossible.

SETTLEMENT ECOLOGY

As local and global threats continue to decrease coral 

cover, it is likely that fewer coral larvae will be supplied 

to reefs that may or may not have appropriate settlement 

habitat. For corals, the transitional stage from planktonic 

planula larvae to sessile benthic juveniles involves a twostep process of settlement and metamorphosis. Settlement 

is the behavioral response of a larva when it stops dispersal and selects substrate for recruitment. Metamorphosis 

includes the subsequent morphological and physiological 

changes that pelagic larvae undergo to become benthic 

juveniles. Settlement of coral larvae can be infl uenced by 

habitat qualities that facilitate or inhibit settlement and 

metamorphosis of larvae supplied to a reef (Figure 4). 

Larval settlement behavior can be determined by the conditions the larvae experienced in the plankton or by the 

presence of positive or negative cues on the benthos or in 

the water overlying the reef.

LARVAL CONDITION UPON ARRIVAL

As coral larvae disperse in the plankton they are exposed to water quality conditions that may affect larval 

health, behavior, survival, and settlement success (Vermeij 

et al., 2006). Experiences during early life stages (i.e., depleted energy reserves, nutritional stress, environmental 

stressors, and pollutant exposure) have latent effects on 

later life stages in numerous marine larvae across different phyla (reviewed in Pechenik, 2006). Even short-term 

exposure to stressors or a slight delay in metamorphosis 

can reduce fi tness in juveniles and adults (i.e., decrease 

growth rate, lower competitive ability, reduce survival, 

and decrease fecundity) (Pechenik, 2006). Although the 

mechanisms through which latent effects are mediated are 

not known, it is suspected that transcriptional or translational processes or direct DNA or key enzyme damage are responsible (Pechenik et al., 1998; Heintz et al., 

2000; Pechenik, 2006). As very few studies have tested 

latent effects in coral larvae, we describe some of the patterns found in other marine organisms to highlight how 

pre-settlement stress might impact post-settlement coral 

growth and survival.

Marine invertebrate larvae often rely on external cues 

to trigger metamorphosis. Without these cues, the larval 

period can be prolonged (reviewed in Pechenik, 1990), 

and post-settlement fi tness may be reduced (Pechenik, 

2006). For some invertebrates, including abalones, tunicates, and bryozoans, delayed metamorphosis slowed 

post -metamorphic development (Wendt, 1998; Roberts 

and Lapworth, 2001; Marshall et al., 2003). Depleted 

energy resources during the larval stage may also be an 

important contributor to post-settlement growth and survival. Bennett and Marshall (2005) found that depleted 

energy reserves caused by increased activity in larvae of 

the ascidian Diplosoma listerianum were more costly energetically than extending the larval period or completing 

metamorphosis. Food limitation during the larval period 

can reduce size, total organic content, energy reserves of 

metamorphosed animals, juvenile growth rates, and survival (Miller, 1993; Pechenik, 2002; Thiyagarajan et al., 

2003; Chiu et al., 2007, 2008).

Water quality conditions can directly reduce coral 

larval survival and settlement but also may cause latent 

effects for new recruits. Salinity reductions during presettlement periods can reduce post-metamorphic growth 

rates and survival for various marine invertebrates (Pechenik et al., 2001; Thiyagarajan et al., 2008). Vermeij et 

al. (2006) tested salinity stress on Montastraea faveolata

larvae and how that infl uenced subsequent post-settlement 

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444 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 4. Coral larval substrate selection is critical to post-settlement survival. a, Favia fragum

larvae explore the benthos for a suitable settlement site; some larvae have already attached and 

are beginning to metamorphose. b, Acropora cervicornis settlers are attached to Titanoderma 

prototypum and have metamorphosed. c, A new recruit of Montastraea faveolata has settled on 

coralline algae, which has started to slough its outer layer of tissue, knocking the coral recruit 

off the substrate. d, Montastraea faveolata recruits are being overgrown by a coralline alga. e, 

Montipora capitata larvae have settled on Ulva sp., an ephemeral substrate. f, A Siderastrea 

radians recruit has settled in a high-sedimentation environment. (Photographs a, b, by Raphael 

Ritson-Williams; c, d, by Nicole Fogarty; e, f, by Mark Vermeij.)

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NUMBER 38 • 445

performance. Lower than normal seawater salinity caused 

increased pre- and post-settlement mortality and increased 

the mobility of coral planulae. It was suggested that the 

increased activity of the larvae in the lower salinities was 

an attempt to escape the unfavorable conditions. With 

increased activity, energy reserves were depleted, which 

was suggested to be the cause of pre-settlement mortality, smaller post-settlement size, and lower post-settlement 

survival. Planulae in the lower-salinity treatments settled 

on a greater range of substrate types. This study emphasized the importance of planktonic conditions on the performance of settling coral larvae, which could then infl uence post-settlement ecology.

LARVAL BEHAVIOR IN OVERLYING WATER

Coral larvae possess a wide array of behaviors that 

allow them to enhance the likelihood of successful settlement, including, but not limited to, sensitivity to light 

(Lewis, 1974; Mundy and Babcock, 1998), depth (Carlon, 2001, 2002; Baird et al., 2003; Suzuki et al., 2008), 

and chemical cues (Morse et al., 1994). One fi eld study 

showed that multiple behavioral choices determined the 

larval settlement site of the Caribbean brooder Agaricia 

humilis (Raimondi and Morse, 2000). The larvae swam 

down when restricted to 3 and 8 m but swam toward the 

surface when restricted to 25 m. In further fi eld experiments, larvae settled in response to the coralline alga Hydrolithon boergesenii but would only settle directly on the 

coralline alga when it was on the underside of a settlement 

tile. This study showed that coral larvae are capable of 

complex behaviors, which are determined to some extent 

by their ability to detect and discriminate between positive 

and negative settlement cues in their habitat.

POSITIVE SETTLEMENT CUES

Many marine invertebrate larvae use chemical cues to 

determine the appropriate habitat for settlement (Pawlik, 

1992; Hadfi eld and Paul, 2001). Chemical cues are implicated for both settlement and metamorphosis of corals and 

may be released by conspecifi cs and other organisms that 

indicate appropriate habitat for survival and growth. Research in the Caribbean showed that a membrane-bound 

carbohydrate complex from the coralline red alga Hydrolithon boergesenii induced settlement and metamorphosis in 

the brooded larvae of Agaricia humilis (Morse and Morse, 

1991; Morse et al., 1994). It was suggested that many corals 

require an algal cue for the induction of settlement, indicating a common chemosensory mechanism for settlement and 

metamorphosis among coral larvae (Morse et al., 1996).

Both the larvae of Acropora millepora, a common 

Indo-Pacifi c coral species, and coral larvae collected from 

natural slicks after mass spawning events used coralline 

algae for settlement and metamorphosis (Heyward and 

Negri, 1999). Four species of crustose coralline algae, 

one non-coralline crustose alga, two branching coralline 

algae, and the skeleton of the massive coral Goniastrea

retiformis induced metamorphosis. Chemical extracts 

from both the crustose red alga Peyssonnelia sp. and the 

coral skeleton were highly active, inducing up to 80% 

larval metamorphosis. Coral larvae can also distinguish 

among species of coralline algae. The Australian spawning 

coral Acropora tenuis had different rates of settlement in 

response to different species of coralline algae (Harrington 

et al., 2004). Settlement choice resulted in higher rates of 

post-settlement survival on the preferred coralline algae, 

illustrating the recruitment consequences of larval selectivity. Chemical cues appeared to be involved in this selective 

behavior, because methanol extracts of the coralline red algae Titanoderma prototypum and Hydrolithon reinboldii

both induced metamorphosis of A. tenuis.

Comparative studies have revealed that settlement 

and metamorphosis in response to crustose coralline algae 

is not an obligate trait of all coral species. Two brooding Australian corals were compared for their settlement 

selectivity (Baird and Morse, 2004). Acropora palifera larvae only metamorphosed in the presence of coralline red 

algae, but Stylophora pistillata larvae showed some metamorphosis in unfi ltered seawater and also metamorphosed 

onto glass coverslips. A study in Guam found that larvae 

of the spawning species Goniastrea retiformis preferred 

substrate covered with crustose coralline algae (CCA), but 

the reef-fl at brooding coral Stylaraea punctata preferred 

biofi lmed rubble (Golbuu and Richmond, 2007).

Coralline algae have been identifi ed as a positive settlement cue for some corals, but it is unclear if the biofi lms 

present on these algae or the algae themselves are responsible for the observed settlement behavior (Johnson et al., 

1991; Webster et al., 2004). Biofi lms were isolated from 

the coralline alga Hydrolithon onkodes, and one strain 

of bacteria alone was enough to induce settlement and 

metamorphosis of Acropora millepora larvae (Negri et al., 

2001). When H. onkodes was sterilized in an autoclave 

and treated with antibiotics, it still induced signifi cantly 

more settlement and metamorphosis than seawater or terracotta tiles. Additionally, coral larvae can distinguish between tiles conditioned at different depths, which could be 

related to depth-related differences in bacterial community composition of biofi lms that formed on tiles (Webster 

et al., 2004). Whether the coralline algae or its biofi lm is 

producing the inductive compound(s) may depend on the 

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446 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

coral and the coralline algae species tested. The specifi city 

of bacterial communities to different coralline algal species 

has rarely been investigated (Johnson et al., 1991). With 

the recent development of more refi ned genetic techniques 

it is possible to compare different microbial communities, 

which might enable the identifi cation of the microbe(s) that 

can induce coral larval settlement and metamorphosis.

NEGATIVE SETTLEMENT CUES

Water quality and substrate conditions impact fertilization rates and also may inhibit some coral larvae from normal settlement and metamorphosis. Low coral recruitment 

is commonly documented in the fi eld, yet surprisingly few 

studies have experimentally tested which substrate characteristics might deter coral larval settlement. Coral larval 

survival and settlement can be reduced by many environmental stresses, such as elevated temperatures (Edmunds 

et al., 2001), variation in salinity (Vermeij et al., 2006), 

sedimentation (Hodgson, 1990; Gilmour, 1999), and UVB 

radiation (Kuffner, 2001; Gleason et al., 2006). Survival 

and settlement are reasonable ecological metrics for the effects of stress, but an important gap in our knowledge is 

how sublethal stress infl uences larval behavior and postsettlement health and success (Downs et al., 2005). New 

techniques including cellular biomarkers and differential 

gene expression using microarrays should provide important techniques to measure sublethal stress in coral larvae.

Water quality conditions that are known to impact 

adult corals also have dramatic effects on larval supply 

and settlement. Of the physical conditions that negatively 

infl uence larval settlement, elevated temperature has received the most attention and has the potential to increase 

in frequency and duration as ocean temperatures continue 

to warm. Larvae of the Caribbean brooding coral Porites 

astreoides were killed and had low densities of zooxanthellae when exposed to elevated temperatures for 24 

hours (Edmunds et al., 2001, 2005). High temperatures 

(36°C) killed Acropora muricata larvae within 40 hours 

(Baird et al., 2006), and temperatures of 32°C killed Diploria strigosa larvae and reduced their settlement (Bassim 

and Sammarco, 2003). However, at elevated temperatures 

(29°C) larvae of Stylophora pistillata had the same settlement as at 25°C (Putman et al., 2008), and more larvae 

settled on the CCA in 25°C than in 23°C. Many of these 

studies used different experimental conditions, making it 

diffi cult to compare the effects of temperature on different 

species of coral larvae. Temperature is one stress that is 

relatively well studied, but more research is necessary to 

understand other physical stressors, such as ocean acidifi -

cation (Albright et al., 2008), that will affect coral larvae 

in the future.

Larval interactions with the biological inhabitants 

of reef communities can also reduce larval settlement. 

Algal turfs, macroalgae, and benthic cyanobacteria can 

negatively impact the settlement of coral larvae (Kuffner 

and Paul, 2004; Birrell et al., 2005; Kuffner et al., 2006; 

Birrell et al., 2008a). In the Florida Keys, two brown algae, Dictyota pulchella and Lobophora variegata, reduced 

the total number of Porites astreoides settlers (Kuffner et 

al., 2006). In the Philippines, the algae Sargassum polycystum and Laurencia papillosa decreased larval settlement 

of Pocilloproa damicornis, but water conditioned with 

these algae increased settlement over the seawater controls 

(Maypa and Raymundo, 2004). In Australia, water conditioned with the foliose brown alga Padina sp. reduced 

larval settlement of Acropora millepora; however, water 

conditioned with the brown alga Lobophora variegata

increased settlement (Birrell et al., 2008a). The cyanobacterium Lyngbya majuscula reduced the survivorship of 

Acropora surculosa larvae and settlement and metamorphosis of Pocillopora damicornis in studies conducted on 

Guam (Kuffner and Paul, 2004), and in Florida, the cyanobacterium Lyngbya polychroa caused Porites astreoides

to avoid settling adjacent to it on settlement tiles (Kuffner 

et al., 2006). Some macroalgae and cyanobacteria can act 

as settlement inhibitors for coral larvae, but this was not 

true for all the algae tested. A surprising contrast was observed for Favia fragum larvae, which had high rates of 

settlement and metamorphosis onto live Halimeda opuntia when offered with coral rubble (Nugues and Szmant, 

2006). Coral larvae of Montipora capitata were observed 

to settle onto Ulva sp. (Figure 4e; Vermeij et al., 2009). 

Why these larvae would settle directly onto blades of algae 

is unclear as this substrate is ephemeral, thus probably increasing post-settlement mortality. Little research has been 

done on the mechanisms that algae use to inhibit settlement, but algal qualities such as natural products, shading 

and abrasion, serving as vectors of bacteria, and releasing 

dissolved organic matter may contribute to the negative 

impacts of algae on larval settlement.

Competition from other members of coral reef communities also infl uences larval behavior. Tissue of the scleractinian coral Goniopora tenuidens suspended in seawater 

inhibited metamorphosis of Pocillopora damicornis larvae 

and reduced the growth of new recruits over seven days 

(Fearon and Cameron, 1996). The tissue from Goniopora 

tenuidens also caused increased mortality of larvae from 

P. damicornis, Platygyra daedalea, Fungia fungites, and 

Oxypora lacera. Increased research on the types of benthic 

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NUMBER 38 • 447

organisms and the mechanisms they use for competition 

with coral larvae is an important area for further study. 

An integrated approach to larval stress, physiology, and 

the physical and biological characteristics of settlement 

substrata will reveal the impact of benthic organisms on 

coral larval behavior, settlement, and post-settlement survival. Determining what benthic habitat characteristics are 

necessary for increased settlement will be a critical step for 

managing reef habitats for increased coral recruitment.

POST-SETTLEMENT ECOLOGY

Corals, and most benthic marine organisms, suffer 

high rates of mortality soon after settlement because they 

are small and vulnerable. Post-settlement processes from 

the time corals settle (i.e., attach to the benthos) to recruitment (i.e., survive to some later phase) determines much of 

coral demography (Vermeij and Sandin, 2008). This concept is consistent with the tenet of clonal population biology that states as clonal organisms grow the probability of 

their death declines but the probability of injury increases 

(Hughes and Jackson, 1985). Thus, the two rates of early 

post-settlement mortality and growth can strongly infl uence the local abundance of corals.

POST-SETTLEMENT MORTALITY

Coral recruits can die from a myriad of causes including chronic disturbances such as competition and predation and pulse disturbances such as bleaching and disease. 

However, the chronic disturbances probably drive most 

post-settlement mortality and thus are serious impediments to reef recovery. Caribbean reefs are a case in point, 

with incidences of recovery much lower than Indo-Pacifi c 

reefs as a result of setbacks from chronic disturbances 

(Connell et al., 1997).

Algae, encrusting invertebrates, and sediment have all 

been shown to have deleterious effects on newly settled corals (Figure 5; Rylaarsdam, 1983). Settling corals, with limited stores of energy to invest in competitive interactions, are 

particularly vulnerable when faced with a well-developed 

benthic community structure and limited space (Jackson and 

Buss, 1975; Sebens, 1982; Connell et al., 1997). However, 

the mechanisms, or causes, of reduced growth and mortality 

of newly settled larvae, recruits, and juveniles have, for the 

most part, only recently been investigated.

Encrusting invertebrates (particularly sponges) can be 

especially inhospitable for newly settled corals. In cryptic habitats, newly settled corals are likely to lose out by 

overgrowth of fast-growing heterotrophic groups such as 

sponges, bryozoans, and bivalves (Vermeij, 2005). Aerts 

and van Soest (1997) determined the impact of sponges on 

coral survival to be greatly species specifi c. Physical, chemical, and biological properties of benthic invertebrates 

may inhibit coral growth and survival. Some studies used 

chemical extracts of sponges (Sullivan et al., 1983; Pawlik 

et al., 2007) to show that allelopathy can negatively impact adult corals. Coral recruits are even more susceptible 

to stress, yet surprisingly few studies have examined secondary metabolites for their impact on the early life history 

stages of corals. A fi eld study by Maida et al. (1995) suggested that allelopathy reduced recruitment of corals adjacent to the octocorals Sinularia fl exibilis and Sarcophyton 

glaucum, and both the live octocorals and settlement plates 

with dichloromethane extracts of S. fl exibilis inhibited coral 

settlement and survival. More long-term, small spatial scale 

(millimeters to centimeters) studies are needed to determine 

the effect of benthic invertebrates on post-settlement survival (Edmunds et al., 2004; Vermeij, 2006).

Areas of high algal biomass are known to be poor nursery habitats for settling corals (Birkeland, 1977; Bak and 

Engel, 1979; Harriott, 1983; Birrell et al., 2008b; Vermeij 

and Sandin, 2008; Vermeij et al., 2009). There are several 

mechanisms by which algae may be deleterious to corals. 

Algae may interfere with larval settlement by simply preempting available settlement space (Mumby et al., 2006; 

Box and Mumby, 2007). At least one species of turf algae 

alone (without sediment) has reduced settlement of corals 

in laboratory experiments (Birrell et al., 2005). More direct 

physical interactions including algal shading, abrasion, or 

basal encroachment can result in reduced coral growth or 

increased mortality (Lirman, 2001; McCook et al., 2001). 

Shading by the encrusting brown alga Lobophora variegata

over six months caused a 50% increase in morality of juvenile Agaricia agaricites (less than 20 mm diameter), and 

the mere presence of L. variegata around the coral reduced 

colony growth by 60% (Box and Mumby, 2007). However, 

shading by Dictyota pulchella resulted in no direct mortality 

but caused a 99% decrease in coral growth. Other studies 

have determined that Lobophora variegata (in the absence 

of grazing) is a superior competitor to Caribbean corals, 

including A. agaricites, A. lamarcki, Meandrina meandrites, 

Mycetophyllia aliciae, and Stephanocoenia intersepta, and 

to at least one species of Pacifi c coral, Porites cylindrica (De 

Ruyter van Steveninck et al., 1988; Jompa and McCook, 

2003). Thus, it is likely that community phase shifts to high 

algal biomass decrease recruitment by reducing larval settlement and post-settlement survival (Hughes and Tanner, 

2000; Kuffner et al., 2006).

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448 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Reduced coral recruitment in algal-dominated reefs (Edmunds and Carpenter, 2001; Birrell et al., 2005) is thought to 

be in part the consequence of chemically induced mortality 

or the increased biomass of fl eshy algae actually functioning 

as a reservoir for coral pathogens (Littler and Littler, 1997; 

Nugues et al., 2004). Bak and Borsboom (1984) proposed 

that the reduction in water fl ow adjacent to macroalgae 

could cause increased coral mortality through changes in the 

fl ow regime and increased allelochemical concentrations. 

Most recently, enhanced microbial activity caused by algal 

exudates has been proposed as a mechanism of competition 

(Smith et al., 2006; Vermeij et al., 2009). Kline et al. (2006) 

determined that elevated levels of dissolved organic carbon, 

which can occur in areas of high algal biomass, increased the 

growth rate of microbes living in the mucopolysaccharide 

layer of corals. These studies all suggest that the detrimental 

effect of algae on corals could be mediated by several properties of macrophytes.

On modern reefs, algal-related post-settlement mortality probably decreases the population density of coral 

FIGURE 5. Macroalgae can be a dominant space occupier on degraded reefs and can inhibit coral recruitment at multiple life history stages. a, The macroalgae Dictyota spp. and Halimeda opuntia covered most 

of the benthos on this Belize reef, potentially inhibiting coral settlement. b, Recruits of Acropora palmata

surrounded by Dictyota sp. c, A new recruit of Diploria sp. surrounded by Gelidiella, Jania, Dictyota, and 

the cyanobacterium Dichothrix sp. d, Montastraea annularis overgrown by Halimeda sp. (All photographs 

by Raphael Ritson-Williams.)

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NUMBER 38 • 449

recruits. Vermeij (2006) compared his recruitment study 

in Curacao from 1998 to 2004 to that of Van Moorsel 

(1989) from 1979 to 1981, using the same method in the 

same location. Recruit densities on the topsides of settlement panels in the more recent study were 5.16 times 

lower and recruitment on the undersides was 1.14 times 

lower than the 1979– 1981 study. Macroalgae had replaced CCA as the dominant topside space occupier, creating a less-suitable habitat for coral recruitment compared to the crustose algae that had dominated the same 

site roughly 20 years earlier. In places where Diadema urchin recovery and grazing have reduced algal abundance, 

the population density of juvenile corals has increased 

(Edmunds and Carpenter, 2001; Aronson et al., 2004; 

Macintyre et al., 2005).

While herbivory can improve the recruitment potential by keeping reefs relatively free of algae, it can also be a 

potential cause of mortality for newly settled corals. Grazing rates on exposed outer surfaces of shallow reefs are extremely high, exceeding thousands of bites per square meter per day (Carpenter, 1986; Steneck and Dethier, 1994; 

Steneck and Lang, 2003). Bites, especially from parrotfi sh 

that graze deeply into carbonate substrates, would easily 

kill a newly settled coral. Few studies have documented 

recruit mortality resulting from fi sh grazing (Mumby et 

al., 2006), although it has been suggested as the cause of 

the low number of recruits observed on the top surface 

of settlement plates (Adjeroud et al., 2007). The herbivorous sea urchin Diadema antillarum was shown to be 

a signifi cant agent of mortality for newly settled corals 

(Sammarco and Carleton, 1981). The highest mortality of 

newly settled corals is likely to occur on outer exposed 

surfaces where algal growth rates and herbivore grazing 

rates are greatest and rates of sedimentation are highest. 

In shallow reef habitats where algal growth and herbivory 

rates are greatest, coral recruitment is greater in subcryptic microhabitats (Bak and Engel, 1979). However, which 

microhabitats increase post-settlement survival has rarely 

been tested (but see Babcock and Mundy, 1996).

POST-SETTLEMENT GROWTH RATES

Given the vulnerability of small size classes, the adaptive advantages of rapid growth rates are obvious. Coral 

recruit survival is not merely a function of the attributes 

of the settlement substrate but also of the coral’s ability 

to resist overgrowth by neighboring encrusting invertebrates and algae (Richmond, 1997). As new corals grow, 

their mortality rates decline (Vermeij and Sandin, 2008), 

and they are less likely to be overgrown by competitors 

(Hughes and Jackson, 1985). Often, however, the slow 

growth rates of newly settled corals make this a losing 

battle, and early post-settlement mortality is generally 

high (Figure 6; Bak and Engel, 1979; Edmunds, 2000; Vermeij and Sandin, 2008). Even in a controlled environment, 

laboratory studies showed that a coral that remains less 

than 3 mm in diameter for two or three months has only a 

20% chance of survival (Rylaarsdam, 1983). Field studies 

report a huge amount of variance in early post-settlement 

mortality. Babcock (1985) found post-settlement survivorship over the fi rst three to six months ranged from 16% 

to 71%, whereas more recently Box and Mumby (2007) 

determined a monthly estimated mortality rate for Agaricia agaricites to be 3.5% per month. Annual juvenile coral 

survivorship estimates range from 0% to 77% (Smith, 

1992; Wittenberg and Hunte, 1992; Maida et al., 1994; 

Smith, 1997; Edmunds, 2000).

Different species of corals have distinctly different 

rates of growth and ability to recover following a disturbance (Wakeford et al., 2008). Specifi cally, some of the 

Indo-Pacifi c acroporid corals (e.g., Acropora tenuis) are 

extremely “weedy” and are capable of growing nearly 

6 cm in 1.5 years (Omori et al., 2008); this translates to 

an average growth rate of 3.2 mm/month compared to 

the much slower growth rates reported for Oxypora sp. 

as ranging between 0.2 and 0.5 mm/month (Babcock and 

Mundy, 1996).

Settlement habitat also infl uences growth rates of 

newly settled corals. Subcryptic habitats protect coral recruits from stresses and disturbances common on outer reef 

surfaces, but they will invariably have lower productivity 

potential. Diameters of Platygyra sp. and Oxypora sp. settlers increased one-quarter to one-half as fast in cryptic 

undersides than they did on upper exposed surfaces for the 

two species, respectively (Babcock and Mundy, 1996). Importantly, however, new recruits that selected subcryptic 

microhabitats had higher survivorship despite their slower 

growth rates (Babcock and Mundy, 1996).

VARIABILITY OF POST-SETTLEMENT 

SURVIVAL AND GROWTH: 

THE ROLES OF BIODIVERSITY 

AND LIFE HISTORY STRATEGIES

Before the disease-induced Acropora spp. decline in the 

Caribbean, fundamental differences existed between acroporid-dominated reefs of the Caribbean and Indo-Pacifi c 

regions. Caribbean reefs are largely built by two species of 

Acropora. Both species recruit rarely (Rylaarsdam, 1983; 

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450 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Sammarco, 1985), but their clonal growth created massive 

monocultures of rapidly growing reefs capable of keeping 

up with rising sea level (Adey, 1978). In contrast, there 

are two orders of magnitude more species of Acropora on 

Indo-Pacifi c coral reefs, and the population density of their 

recruits are also orders of magnitude greater on Indo-Pacifi c 

reefs than on Caribbean reefs (Hughes et al., 1999).

Although the high diversity of acroporid corals in 

the Pacifi c spans the spectrum of life history characteristics from weeds (i.e., high reproductive output and rapid 

growth rate; Omori et al., 2008) to trees (i.e., competitively 

dominant, large colonies; Baird and Hughes, 2000), the two 

acroporid species comprising Caribbean reefs require long 

adult lives and considerable clonal propagation. However, 

since the acroporid die-off in the early 1980s, Caribbean 

reefs have fundamentally changed. Because of the resultant algal phase shift (Hughes, 1994), acroporid reefs have 

become hostile to the rare acroporid recruits, and they 

have lost their receptivity for reattachment of encrusting 

fragments (Williams et al., 2008). These changes on many 

FIGURE 6. A time series of the growth of Agaricia sp. settled on a terracotta tile in Bonaire over 3.75 years. 

After March 2007 (e), this recruit is being overgrown by the coralline alga Titanoderma prototypum, a 

known settlement-facilitating species, illustrating just how hazardous the settlement environment can be. 

a, June 2004, recruit diameter is 1.3 mm; b, March 2005, 3.4 mm; c, July 2005, 8.4 mm; d, June 2006, 

15.2 mm; e, March 2007, 16.0 mm; f, March 2008, 12.0 mm. One segment on the scale bar  1 mm. (All 

photographs by Suzanne Arnold.)

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NUMBER 38 • 451

Caribbean reefs may be the primary reason why they appear less capable of recovering from widespread disturbances such as coral disease and bleaching.

The massive, slow-growing coral Montastraea annularis is also a broadcast spawner and framework builder 

in the Caribbean. It also has very low rates of recruitment 

(Hughes and Tanner, 2000) and thus requires long adult 

life to establish its dominance. Although it dominates Caribbean reefs today (Kramer, 2003) and is relatively hardy, 

it too has shown elevated levels of disease in recent years 

(Pantos et al., 2003) and has increased susceptibility to disease after bleaching (Miller et al., 2006). Again, the longterm prognosis for this Caribbean reef builder is poor.

Weedy, brooding species such as Agaricia spp. and 

Porites spp. are the thrust behind the current rates of coral 

recruitment in the Caribbean. The Caribbean brooder 

Agaricia agaricites is often the most abundant recruit on 

Caribbean reefs in recent times (Bak and Engel, 1979). 

This species has well-documented high rates of recruitment and adequate sediment-rejection capabilities yet regenerates poorly from lesions and is often outcompeted by 

other corals (Bak and Engel, 1979). In the past 30 years 

Agaricia tenuifolia has replaced other corals to dominate 

the community on two reefs that had historically different community compositions (Aronson et al., 2004).The 

increasing community dominance observed for Porites astreoides at six sites in the Caribbean is being driven by a 

constant recruitment rate coinciding with reduced percent 

cover of other coral species (Green et al., 2008).

It is possible that these life history-related differences 

are fundamentally changing Caribbean reefs. Are Caribbean reefs today following the paths of forests and other 

marine ecosystems in their shift to weedy, stress-tolerant 

species? (see Knowlton, 2001). A recovery such as seen in 

Palau following the 1998 bleaching event, where sexual 

recruitment and remnant regrowth were equal contributors (Golbuu et al., 2007), has yet to be recorded in the 

Caribbean. Success stories of Caribbean recoveries led by 

broadcast spawning species are scarce (but see Idjadi et 

al., 2006). Thus, the relative importance of sexual versus 

asexual reproduction to recovery in the Caribbean needs 

to be addressed by long-term observations with particular 

focus on recovery following large-scale disturbances such 

as major storms and bleaching events.

Thus, it seems that Caribbean reefs were built by 

corals that have been successful since the Pleistocene 

(Pandolfi and Jackson, 2006) with a strategy of low recruitment, considerable clonal growth, and low postsettlement mortality. However, that strategy may not be 

broadly viable today, given the global climate trajectory 

(Hoegh-Guldberg et al., 2007) and patterns of human 

activities. While Indo-Pacifi c reefs are not immune to declines in rates of coral recruitment in recent years (Wakeford et al., 2008), the higher biodiversity and range of recruitment and post-recruitment strategies (e.g., high rates 

of growth) allow reefs there to be more resilient.

CONCLUSIONS

Coral mortality has increased in recent decades, making coral recruitment more important than ever before in 

sustaining coral reef ecosystems and contributing to their 

resilience. We identifi ed three critical sequential phases to 

the recruitment process of corals: larval availability, larval 

settlement, and post-settlement ecology. All three factors 

are necessary for coral recruitment and, ultimately, for 

maintenance or recovery of coral reef ecosystems.

Most coral planulae available for recruitment are 

probably from relatively local reproduction and relatively 

short-distance connectivity. As adult coral abundance declines, both fertilization success and the effective dispersal distance of corals (see Figure 3B) will likely decline as 

well. Physiological stress on reproducing corals might also 

result in fewer and possibly weaker coral larvae arriving, 

thereby reducing the per capita rate of settlement success.

Once in the vicinity of a coral reef, settling corals respond to a hierarchy of environmental cues both in the 

water and from the reef. Several studies have identifi ed organisms that facilitate or inhibit the settlement and metamorphosis of corals. Crustose coralline algae can facilitate 

coral settlement but, disturbingly, this group of algae is 

becoming rarer on coral reefs as macroalgae become increasingly dominant. Macroalgae are known inhibitors of 

settlement, which may result from their ability to rapidly 

occupy settlement habitat, their suite of secondary metabolites, their microbial communities, or a combination of 

some or all of these mechanisms.

Stressors that impact multiple life history stages of corals 

have the most potential to greatly reduce coral recruitment. 

Poor water quality (such as sedimentation and increased 

temperatures) and the increased abundance of macroalgae 

are known to decrease coral recruitment and negatively 

impact corals at many different life history stages. Human 

impacts on the water quality of marine systems continue to 

grow, and few locations remain untouched (Halpern et al., 

2008). These and other stressors may decrease the reproductive output of corals, physiologically stress the larvae, block 

subcryptic nursery habitats, create negative settlement cues, 

and result in increased post-settlement mortality.

35_Rit-Williams_437-458_Lang.ind451 451 5_Rit-Williams_437-458_Lang.ind451 451 9/24/09 10:21/24/09 10:21
452 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Globally, many Indo-Pacifi c reefs have higher rates of 

settlement, recruitment, and recovery from disturbances, 

which could be the result of higher biodiversity in the region. 

In contrast, Caribbean reefs may have evolved a strategy of 

low recruitment and considerable clonal growth, with low 

post-settlement mortality for its few reef-building acroporid corals. Unfortunately, that strategy may be ineffective 

in the future given the global climate trajectory of higher 

ocean temperatures, acidifi cation, and greater disturbance 

from tropical storms, which will continue to physiologically 

stress corals. Because Indo-Pacifi c reefs have two orders of 

magnitude more acroporid species, weedy and potentially 

resilient strategies could succeed. If current trends continue 

on modern reefs, it is possible that reefs in the future will 

differ from those of the recent past.

ACKNOWLEDGMENTS

Funding for our research on these various topics was 

provided, in part, by the Smithsonian Marine Science 

Network. Special thanks to Klaus Ruetzler and Michael 

Carpenter for facilitating research for RRW, VP, NF, SA, 

and RS at the Carrie Bow Field Station in Belize. SA and 

RS thank the Coral Reef Targeted Research Project (Connectivity), National Fish and Wildlife Fund, Wildlife Conservation Society and the Bonaire Marine National Park 

(STINAPA). VP and RRW thank the Mote “Protect Our 

Reefs” grant program. This is contribution number 849 of 

the Caribbean Coral Reef Ecosystems Program (CCRE), 

Smithsonian Institution, supported in part by the Hunterdon Oceanographic Research Fund, and Smithsonian 

Marine Station at Fort Pierce (SMSFP) contribution number 765.

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/24/09 10:21
Do Indian River Lagoon Wetland 

Impoundments (Eastern Florida) 

Negatively Impact Fiddler Crab 

(Genus Uca) Populations?

Bjorn G. Tunberg

ABSTRACT. Quantitative sampling of fi ddler crabs was performed in June– July between 1992 and 1994 along transects at three St. Lucie County mosquito impoundments, 

Florida, running from the Indian River Lagoon (IRL) shore and across the impoundment 

perimeter dikes, and in one impoundment across the perimeter ditch. A total of 929 specimens representing four species were found: Uca pugilator, Uca rapax, Uca speciosa, and 

Uca thayeri. The quantitative sampling showed that there was no correlation between the 

number of Uca burrow openings on the sediment surface and the actual number of crabs 

in the sediment. Differences were recorded in abundance and distributional patterns between impoundments, but no correlation was recorded between substrate organic content and species distributional patterns. The male/female ratio was close to 1 for all species, except for U. thayeri; the males dominated for this species (ratio, 1.8:1). High water 

temperatures potentially lethal to fi ddler crabs occurred in the impounded marsh in the 

summer. U. pugilator and U. rapax were unlikely to be impacted by the impoundment 

fl ooding as they are highly motile and not very site specifi c. U. speciosa and U. thayeri

were more restricted to the very soft, dark, and wet substrate along perimeter ditch banks 

and may therefore be impacted during periods of fl ooding because they are dependent on 

nonfl ooded areas for feeding and reproduction.

INTRODUCTION

Burrowing crustaceans, such as fi ddler crabs, impact the ecology of associated infaunal communities and, consequently, the ecosystem as a whole (Crane, 

1975; Montague, 1982; Dittman, 1996). According to Montague (1980), fi ddler crabs are the most abundant macrobenthic crustacean inhabitants of North 

American estuaries. Their impacts on bioturbation activity and oxygenation of 

the substrate are considerable (Bertness, 1985). Fiddler crabs may also play an 

important role in recycling nutrients (Macintosh, 1982; Bertness, 1985). They 

feed by scraping up and ingesting surface sediment (Crane, 1975; Kraeuter, 1976; 

Heard, 1982; Macintosh, 1982; Weis and Weis, 2004) and are in that respect 

very important in overturn of substrates. Fiddler crabs are also an important 

food source for birds, fi sh, and mammals (Peterson and Peterson, 1979; Montague, 1980; Grimes et al., 1989; Gilmore et al., 1990). There is a relatively diverse Uca species assemblage within the Indian River Lagoon (IRL) region, with 

seven species reported in the IRL (Salmon, 1967; Kerr, 1976; M. Salmon, Florida 

Bjorn G. Tunberg, Smithsonian Marine Station, 

701 Seaway Drive, Fort Pierce, Florida 34949, 

USA (Tunberg@si.edu). Manuscript received 13 

May 2008; accepted 20 April 2009.

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460 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Atlantic University, personal communication, 1992), four 

tropical species, Uca rapax (Smith), Uca thayeri Rathbun, 

Uca speciosa (Ives), and Uca mordax (Smith), and three 

temperate species, Uca pugnax (Smith), Uca pugilator

(Bosc), and Uca minax (Le Conte). Only four species were 

found during these studies: Uca pugilator, U. rapax, U. 

speciosa, and U. thayeri.

That the impoundment of 90% of the marginal wetlands (primarily for mosquito control) of the IRL has a 

potential negative impact on regional Uca populations has 

been a controversial issue for many years. Each impoundment and the management procedures are described in 

detail in Rey and Kain (1991). Preliminary studies by Gilmore et al. (1991) revealed that no Uca spp. were observed 

from marsh-mangrove habitats in fl ooded (short-term and 

long-term) impoundments, while they were present in large 

numbers at unimpounded sites adjacent to impoundments. 

This difference could be associated with a number of factors, because many aspects of the reproduction of Uca (including courtship, female receptivity, egg maturation, and 

hatching) are closely synchronized with the semidiurnal 

and semilunar tidal cycles (Fingerman, 1957; Barnwell, 

1968; Wheeler, 1978; Zucker, 1978; Montague, 1980; DeCorsey, 1983; Salmon et al., 1986). However, according 

to Fingerman (1957), the tidal rhythm differs between 

species (U. pugilator and U. speciosa). The exclusion of 

natural tidal cycles within several impoundments may 

therefore have serious impacts on populations of Uca

spp. In addition, prolonged periods of inundation that 

usually occur from May to September (management for 

mosquito control) may displace Uca spp., which need 

periods of exposure of the burrow entrances for survival. Periods of heavy precipitation, mainly during the 

summer, may also drastically reduce the salinity within 

these impoundments.

The main objectives of this study were (a) to evaluate 

survival and adaptation of Uca populations to manipulated ecological conditions along the impoundment perimeter ditches (compared with the natural IRL conditions), 

(b) to determine if these potential adaptations differed 

among species, and (c) to elucidate zonation patterns of 

each species (from the IRL shore, across the dike road, 

down to the impoundment ditch).

METHODS

Figure 1 shows the location of the three studied impoundments, which are described in detail in Rey and 

Kain (1991). Blue Hole Point (impoundment [Imp.] #23) 

is a 122 ha breached impoundment. The 20 m breach in 

the western dike allowed natural tidal access between the 

impoundment and the IRL. This breach was a result of a 

severe 1981 winter storm and was left open to the natural 

tidal cycles of the IRL. The main reason for not repairing 

the breach was that this impoundment could be used as a 

reference/control site for numerous impoundment studies 

(James R. David, St. Lucie County Mosquito Control District, personal communication, 1992). Jack Island State 

Preserve (Imp. #16A) is a 161 ha impoundment divided 

into four cells. This impoundment was open via culverts 

to the IRL during the winter months but was artifi cially 

fl ooded during the summer months (early May through 

August). Bear Point (Imp. #1) is a 255 ha impoundment. 

Since August 1993, the culverts here were left open to tidal 

exchange.

Quantitative sampling was performed in these impoundments, Imp. #23 and Imp. #16A in June-July 1992, 

FIGURE 1. The three sampling impoundments (Imp) within St. Lucie County, Florida; SMS Smithsonian Marine Station.

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NUMBER 38 • 461

1993, and 1994 and Imp. #1 in July 1994 along a portion 

of transect lines previously established for burrow counts 

(Gilmore et al., 1991). One transect line had been established in each impoundment. These transects ranged from 

the edge of the IRL (0 m), continued across the artifi cial 

dike, and ended at the impoundment perimeter ditch (Figure 2). Four permanent metal stakes indicated the sampling sites (see below). Because of the very hard substrate 

on top of the actual dike (the road), it was impossible to 

sample these sites (10 m and 15 m) quantitatively (see 

below). The 0 m stake was placed at the waterline (low 

tide) on the IRL side, and the other three stakes (markers) 

were placed at 5 m intervals across the dike, with the 0 m 

stake as the starting point. The 15 m site was between 

the 15 m stake and the upper bank of the perimeter ditch 

(Gilmore et al., 1991; see Figure 2). Additional sites were 

also established for the studies: site A was at the edge of 

the water (low tide) on the dike side of the perimeter ditch 

and site B in the corresponding area of the impoundment 

marsh side of the ditch (Figure 2). It was not possible to 

establish a site B in Imp. #16A, because of the summer 

artifi cial fl ooding, or in Imp. #1, because it was fl ooded 

naturally. The width of the perimeter ditches was about 5 

to 6 m. The ditch shores in all impoundments had a very 

dense (but only about 1.5 to 2 m wide) mangrove vegetation (primarily Rhizophora mangle). Two additional sites 

were established in Imp. #23: site C, about 2 m into the 

impoundment marsh from site B, immediately behind the 

dense mangrove vegetation along the ditch shore (see Figure 2), and site D on the sand fl at within the marsh (25 m 

from the ditch). The distance from site 0 m to site C was 

about 25 m and to site D about 47 m. The sampling sites 

were 2  2 m permanent squares situated at each marker 

(sites 0 m, 15 m, C, and D), within which four replicate samples were randomly collected on each sampling 

date. Sites A and B were sampled the same way (on the 

exposed substrate at low tide) close to the dense mangrove vegetation at each side of the perimeter ditch. The 

Imp. #23 impoundment marsh was never fl ooded during my studies. The random sampling was performed by 

means of a stainless steel cylinder (0.1 m2, 40 cm high) 

with a sharpened bottom edge. Sampling was always performed at low tide and when no, or very few, specimens 

were observed on the sediment surface. Sampling was 

never performed when many crabs were observed out of 

their burrows. Sampling at such times would have resulted in erroneous quantitative results because Uca spp., 

when disturbed on the sediment surface, seek shelter in 

the closest burrow or even migrate out into the water. 

The cylinder was forced down to a sediment depth of 

at least 25 cm. The number of Uca burrows within the 

cylinder area was recorded, and then the sediment was 

removed with a shovel (with a straight edge). The uppermost fraction (0– 10 cm) was sieved (in the fi eld) in 

seawater through a 2 mm stainless steel mesh sieve. In the 

remaining fraction (10– 25 cm) the crabs were removed by 

hand in the fi eld. This procedure was deemed acceptable 

as small crabs only occurred in the uppermost layer of 

the sediment. The specimens were transferred to plastic 

bags and kept in a cooler in the fi eld. In the laboratory, 

the samples were either processed immediately or stored 

in a freezer for later processing. The crabs were sorted by 

hand in a tray fi lled with seawater. They were then placed 

in labeled glass jars in a solution of 5% borax-neutralized formalin, diluted in seawater. After 4 to 5 days the 

formalin was replaced with 70% ethanol. All specimens 

larger than 5 mm carapace width (CW) were later identifi ed and weighed (wet weight) and have been archived 

for possible future studies. All individuals smaller than 5 

mm were regarded as “juveniles.” It was not possible to 

identify these to species level with certainty. The literature sources used for species determination were Tashian 

and Vernberg (1958), Salmon (1967), and Crane (1975). 

A total of 140 quantitative samples were collected during the entire study period: 84 in Imp. #23, 40 in Imp. 

#16A, and 16 in Imp. #1.

Water temperature was measured midafternoon on 26 

July 1993 and 1 August 1994 within the marsh of Imp. #16A 

(which was artifi cially fl ooded), in the middle of the adjacent 

perimeter ditch, and in the IRL (about 5 m from the shore). 

The measurements were taken at 5 cm water depth.

Because many impoundments are closed for natural 

tidal exchange to the estuarine waters of the IRL during 

the artifi cial fl ooding periods (impoundment pumps), salinity may drop rapidly during periods of heavy rainfall. 

FIGURE 2. Cross section of a typical mosquito impoundment in the 

Indian River Lagoon (IRL), showing locations of the fi ddler crab 

sampling sites. The dike road was approximately 1.5 m above low 

tide level in the IRL at three investigated sites (site D is not shown).

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462 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

An experiment was therefore performed to investigate tolerance to rapid salinity changes among the four Uca species. 

The laboratory setup consisted of twenty 2 L round plastic containers equipped with a lid. A separate air supply 

was provided to each container. Four treatments and one 

control (four replicates per treatment) were established: 

100%, 75%, 50%, 25%, and 0% seawater. Laboratorysupplied seawater was diluted with distilled water. The 

salinities of the different treatments were 100% 36– 37 

ppt (parts per thousand), 75% 27– 29 ppt, 50% 19 

ppt, 25% 9– 10 ppt, and 0% 0 ppt, measured with an 

ocular refractometer. The water temperature was very stable during the experimental period, 24.0°– 26.0°C. Each 

experiment lasted for seven days. The crabs were collected 

48 hours before each experiment and acclimated in 100% 

aerated seawater during this period. Seven randomly selected female crabs of each species were placed in each 

experimental container. It was not possible to fi nd enough 

specimens of U. thayeri during the period for these studies. Therefore only 25% and 0% seawater were used as 

treatments, and each replicate contained fi ve crabs. The 

experiments were monitored twice a day, and any dead 

crabs were removed. Water was changed only in the containers where dead crabs were found. These experiments 

were performed between 4 July and 27 July 1994.

Sediment samples for analysis of organic content (loss 

on ignition) were collected in 1994 along the three transects. Three sediment cores (inner diameter, 30 mm) were 

collected to a depth of 5 cm at randomly chosen points at 

each site. As stated above it was not possible to establish 

a site B in Imp. #16A or in Imp. #1. The sediment was 

treated in the laboratory according to the procedures described in Holme and McIntyre (1971).

A one-way analysis of variance (ANOVA) (Holm– Sidak 

method) was performed to compare the respective monitored sites in the three impoundments regarding organic 

content (LOI) in the sediment (Table 1).

RESULTS

ABUNDANCE

Abundance data from the three transects sampled in 

1992, 1993, and 1994 at Imp. #23 and Imp. #16A are presented in Figures 3 and 4, and the one transect sampled in 

1994 at Imp. #1 in Figure 5. High water levels prevented 

sampling 0 m (IRL) at Imp. #16A in 1992 and site A (ditch 

shore) in 1994.

The results from Imp. #23 were similar the three sampling years (Figure 3). U. pugilator and U. rapax were 

relatively evenly distributed across the transect, and a few 

specimens of U. rapax were sometimes observed on the 

dike road (DIKE; see Figure 2). U. speciosa, the dominant 

species, was found only at site 0 m, and in very high densities in the wet, soft, and dark mud on both sides of the 

perimeter ditch (sites A and B). U. thayeri was also found 

on both sides of the perimeter ditch (sites A and B), in addition to a few specimens at site 0 m in 1992.

In contrast, at Imp. #16A (Figure 4), U. pugilator

dominated in abundance at site 5 m whereas U. rapax was 

most abundant at site A (perimeter ditch shore). U. speciosa was almost exclusively found at site A and U. thayeri

at site 0 m.

At Imp. #1 the distributional patterns were similar 

to the other impoundments. However, U. pugilator was 

found in comparatively low densities, whereas U. rapax

was abundant at both sites 0 m and 5 m. U. speciosa was 

found in high densities in the wet muddy areas at site 0 m 

and at site A. U. thayeri was found at the 0 m site and to 

even a greater extent at site A (dike side of the ditch).

No statistical tests were performed to elucidate any 

potential difference between years at each site, but it was of 

higher interest to statistically compare abundance patterns 

between impoundments. Therefore, correlation analyses 

(Pearson product moment correlation) were performed on 

the mean abundance data (1992, 1993, 1994) for sites 0 m 

TABLE 1. One-way analyses of variance (Holm– Sidak method) concerning differences in organic content (LOI) between the different impoundment and sampling sites. Signifi cant differences (P values) are 

in bold italic.

 Site 

Impoundment no. 0 m 5 m 15A C D

23 vs. 16A 0.025 0.068 0.158 0.0002 0.0001 0.001

23 vs. 1 0.148 0.044 0.123 0.124

16A vs. 1 0.004 0.003 0.014 0.00006

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NUMBER 38 • 463

FIGURE 3. Abundance and biomass (wet weight) between 1992 and 1994 of the four fi ddler crab species along the impoundment #23 

transect. Error bars represent  standard error values (N 4). Note the different scaling on the y-axes.

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464 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 4. Abundance and biomass (wet weight) between 1992 and 1994 of the four fi ddler crab species along the transect within 

impoundment #16A. Error bars represent  standard error values (N 4). Note different scaling on y-axes.

36_Tunberg_459-472_Lang.indd 464 6_Tunberg_459-472_Lang.indd 464 9/24/09 10:26/24/09 10:26
NUMBER 38 • 465

FIGURE 5. Abundance and biomass in 1994 of the four fi ddler crab species along the transect within impoundment #1. Error bars represent 

 standard error values (N 4).

to A for each of the four species separately between Imp. 

#23 and Imp. #16A. However, no correlation (P  0.05) 

could be found for any of the species. The same analyses 

were performed for the 1994 data from Imp. #23, Imp. 

#16A, and Imp. #1. The only correlation (positive) found 

was for U. thayeri between Imp. #23 and Imp. #1 (correlation coeffi cient, 0.968; P value, 0.031).

BIOMASS

The biomass (g wet weight) measurements are presented in Figures 3– 5. No signifi cance tests were performed 

concerning the biomass difference among the three years 

for each species.

However, the biomass calculations for the three years 

in Imp. #23 (Figure 3) indicate that changes took place, but 

these changes are based on subjective observations. High 

biomass values were recorded for U. pugilator in 1992 at 

site C and in 1993 and 1994 at site 0 m. High values were 

recorded for U. rapax throughout the entire transect, especially in 1993 and 1994, except at site D. The highest biomass values for U. speciosa were recorded on both sides of 

the perimeter ditch (sites A and B), especially on the marsh 

side of the ditch (site B). High U. thayeri biomass values 

were recorded along the perimeter ditch (sites A and B).

At Imp. #16A the biomass values for U. pugilator

were high at site 5 m all three years (see Figure 4). Relatively high biomass values were recorded for U. rapax at 

sites 5 m and A in 1992. However, data for site A in 1994 

are not available. Low biomass values were recorded for 

U. speciosa at site A in 1992 and 1993. U. thayeri was 

only recorded at low biomass values at site 0 m in 1993 

and 1994 and at site A in 1993 and at site 0 m in 1994.

At Imp. #1 low values were observed for U. pugilator

throughout the transect (see Figure 5), but U. rapax was, 

by far, the most dominant (biomass) species across the entire transect. The only exception was site A, where the values for U. speciosa and U. thayeri were somewhat higher.

REPRODUCTION AND SEX DISTRIBUTION

The percentage of “juveniles” found in 1993 and 

1994 at the different sites within Imp. #23 and Imp. #16A 

is presented in Figure 6. More juveniles were found at 

site 0 m at Imp. #16A compared with Imp. #23. Many 

juveniles were also recorded along these impoundment 

ditch shores (sites A and B in Imp. #23 and site A in Imp. 

#16A). The sex distribution among adults of the four species from the 1992, 1993, and 1994 (combined) collections (June– July) is presented in Figure 7 with the number 

36_Tunberg_459-472_Lang.indd 465 6_Tunberg_459-472_Lang.indd 465 9/24/09 10:26/24/09 10:26
466 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of ovigerous females. As shown, the sex ratio was near 

to 1.0 among all four species except for U. thayeri where 

the male/female ratio was approximately 1.8:1. The highest ovigerous rate was found among U. pugilator (22.0%) 

and the lowest among U. rapax (3.4%). The corresponding fi gures for U. speciosa and U. thayeri were 6.9% and 

10.0%, respectively.

BURROWS

The correlation between the number of burrows and 

the actual number of crabs found within each sample 

in 1992 and 1993 is presented in Figure 8. A Wilcoxon 

signed-rank test showed that there was no correlation 

between these two parameters: P 0.097 (linear regression: R2 0.02, P [analysis of variance] 0.23). This 

fi nding has also been reported by Colby and Fonseca 

(1984). The same lack of correlation was also found by 

the author in a larger and more detailed multiyear study 

at Merritt Island impoundments (close to Cape Canaveral, eastern Florida.).

TEMPERATURE AND SALINITY TOLERANCE

The summer water temperatures within Imp. #16A, the 

perimeter ditch, and in the IRL is presented in Table 2. The 

water temperature was higher within the impoundment 

marsh than in the perimeter ditch and in the IRL.

The laboratory experiment showed that no species 

showed any disturbance or mortality in 100%– 25% seawater. 

However, the reaction toward 0% seawater was severe (Figure 9). U. speciosa and U. thayeri showed very low tolerance 

toward 0% seawater while U. pugilator showed the highest 

tolerance. The reaction from U. rapax was intermediate.

SEDIMENT

The results of the sediment analyses are presented 

in Figure 10. The loss on ignition (organic content) was 

higher in Imp. #16A than in Imp. #23 and Imp. #1 (see 

FIGURE 6. Percentage specimens having a carapace width (CW) less 

than 5 mm (juveniles) of all collected individuals of Uca spp. from 

each site in 1993 and 1994. Note different scaling on y-axes.

FIGURE 7. Sex distribution of all fi ddler crab individuals larger than 

5 mm collected during 1992– 1994 combined within impoundments 

#23, #16A, and #1. The bars show sex distribution for each species 

found throughout the study period; PUG Uca pugilator; RAP 

U. rapax; SPE U. speciosa; THA U. thayeri.

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NUMBER 38 • 467

Table 1). The lowest values on the IRL side (site 0 m) were 

recorded from Imp. #1 and the highest from Imp. #16A. 

At the ditch (site A) the highest organic value was recorded 

at Imp. #16A and the lowest at Imp. #1. Within the marsh 

(site C) (Imp. #23 and Imp. #16A only), the loss on ignition was very high within Imp. #16A and very low within 

Imp. #23. As indicated in Table 1, Imp. #16A deviated 

signifi cantly the most from the other two impoundments, 

with generally the highest organic content (LOI).

FIGURE 8. Relationship between number of burrows and number 

of fi ddler crabs found in each quantitative sample.

TABLE 2. Water temperatures (°C, 5 cm water depth) at impoundment site #16A, measured in midafternoon during July 

1993 and July 1994.

Location a 1993 1994 Mean

Marsh 44.3 42.4 43.4

Ditch 37.1 36.1 36.6

IRL 37.5 35.2 36.4

a Marsh impoundment marsh; ditch impoundment perimeter ditch; IRL 

Indian River Lagoon.

FIGURE 9. Percent survival in fresh (distilled) water of the four fi ddler crab species. Error bars represent standard error values (N 4).

FIGURE 10. Sediment organic content (percent weight loss on ignition) at the sampling sites within the three impoundments in 1994. 

The error bars represent standard error values (N 3). Note different scaling on y-axes.

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468 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Pearson product moment correlation tests were used 

to elucidate any potential correlation between the organic 

content of the sediment (LOI) and the distributional pattern (along the transects) of the four different species. All 

tests were performed on the mean values of each parameter. Only transects where a signifi cant amount of information was available were used for these tests: Imp. #23 

in 1993 and 1994, and Imp. #16A in 1994 (see explanation above). No signifi cant correlation (P  0.05) was 

recorded for any species between abundance and organic 

content, except for U. pugilator at Imp. #23 in 1994, with 

a correlation coeffi cient of 0.797 and a P value of 0.032.

DISCUSSION

Different species of fi ddler crabs prefer different substrates and salinities for reasons of their specifi c physiological tolerances and environmental preferences (Teal, 1958; 

Vernberg et al., 1973). However, the artifi cial environment 

of the impoundments in the IRL, with the perimeter ditch 

and dike, poses a completely new, different type of environment for the Uca populations. The occurrence and distributional patterns of the different species of fi ddler crabs 

in these impoundment dikes and perimeter ditches have 

not been investigated earlier, so this is a fi rst basic study 

on these populations. The results from this study indicate 

that more detailed studies are needed in the future in these 

very extensive artifi cial environments in the IRL.

Uca speciosa and U. thayeri were the most “site- and 

substrate-specifi c” species within these environments, 

whereas U. pugilator, and in some cases also U. rapax, 

were more “generalists.” Uca speciosa and U. thayeri were 

almost exclusively found in the very soft, black, and wet 

substrate close to the water (primarily sites A and B), 

which is clearly demonstrated by the data presented from 

Imp. #23. The highest abundances of U. speciosa were here 

recorded on the perimeter ditch “shores” (sites A and B). 

Given the rich mangrove vegetation, it was expected that 

the very fi ne, wet, and muddy sediment on the ditch perimeter shores (sites A and B) would have a comparatively 

high organic content, but this was not the case (see Figure 

10). Because no correlation between the organic content 

of the substrate and the abundance pattern of the different 

species were found, the grain-size distribution, water content, the chemical content of the sediment, root mat density, physiological tolerances, and interspecifi c inter actions 

may be more important factors in fi ddler crab distributional patterns (Teal, 1958; Ringold, 1979; Bertness and 

Miller, 1984). No root mat areas were investigated in this 

study. The large differences in substrate organic content 

(LOI) between Imp. #23 and Imp. #16A are noteworthy 

(see Table 1).

Large numbers of U. rapax (and to some extent also 

U. pugilator) were quite often observed on the dike roads, 

but U. speciosa and U. thayeri were never seen there. 

Thompson et al. (1989) have also demonstrated that some 

species of desiccated fi ddler crabs, among these U. pugilator, can rehydrate on damp sand.

When the impoundments are being fl ooded, it appears 

that U. rapax, and most likely also U. pugilator, are able 

to migrate under water, across the perimeter ditch (often 

anoxic and with H2S in the sediment), to more suitable 

areas. It is, however, important to note that this has so far 

been confi rmed only for U. rapax. Therefore, the ability 

to relocate to more suitable habitat may be the decisive 

factor in survivorship among Uca species. The banks of 

the perimeter dike (immediately above site A) may therefore act as a temporary “refuge” for some species during periods of impoundment fl ooding. It is also possible 

that further migration takes place toward the IRL shores 

(U. rapax, U. pugilator). However, this question does not 

apply to the rim and road of the dike because of the unsuitable substrate. Furthermore, the distance to the water 

table is also too great (at least 1 m).

The two species U. rapax and U. pugilator are probably 

not adversely affected by impoundment management. Visual 

observations, and also in situ experiments, have revealed 

that these species are highly motile within the impoundment 

areas. According to Thurman (2003) U. rapax is typically 

collected in brackish water. Yoder et al. (2005) have also 

found that the “herding behavior” in U. pugilator is a waterconserving group effect, and this behavior makes them less 

vulnerable to desiccation. Many specimens of U. pugilator

and U. rapax have been observed (by the author) to migrate 

over long distances within and outside the impoundments 

(marked individuals, not reported here). However, further 

studies need to be performed to clarify these patterns.

Although U. pugilator and U. rapax thrive in these 

areas, the fate of the other two species is more uncertain. 

According to the quantitative sampling results and intensive visual in situ studies, U. speciosa and U. thayeri are 

confi ned to substrate-specifi c areas of the impoundments, 

and this may have a negative effect on the populations of 

these species when the impoundments are being managed 

(fl ooded). However, the results from Imp. #16A, which 

was fl ooded frequently for mosquito control, seem to contradict this assumption. In spite of this management, a rich 

community of U. speciosa was recorded on the ditch shore 

(site A), but with low densities of U. thayeri.

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NUMBER 38 • 469

Even though the data on the occurrence of juveniles 

are limited, they indicate that fi ddler crab reproduction 

(species unknown) occurs also in the impoundment perimeter ditch (site A and B). As shown in Figure 6, juveniles 

were, as expected, mainly found close to the water (sites 

0 m, A, and B).

The dilution experiments indicate that none of the 

four species is sensitive to low salinities, a situation that 

rarely occurs within the impoundments. During this experiment U. pugilator was the most tolerant species. 

Thurman, (2003) investigated the osmoregulation of eight 

Uca species and found that U. speciosa and especially U. 

pugilator are able to withstand high “osmotic challenge.” 

Additionally, Thurman (2005) reported that U. rapax is 

best equipped for living in brackish habitats and that U. 

thayeri and U. speciosa are best suited physiologically to 

inhabit low and moderately saline habitats. This observation may explain why the latter two species are able 

to successfully inhabit the impoundment ditch “shores” 

(sites A and B). U. rapax, and most likely also U. pugilator are, as discussed earlier, able to migrate over long 

distances, for example, across the perimeter ditches (when 

the impoundments are being fl ooded) and dikes (studies 

by the author on 1,200 of marked U. rapax individuals). 

However, this is most likely not the case with U. speciosa

and U. thayeri. As U. speciosa is a comparatively small 

species, it may therefore be more vulnerable to desiccation 

than the other three species (Pellegrino, 1984).

High summer temperatures in the shallow impoundment water (see Table 2) pose a threat to the fi ddler crab 

populations. Even though the temperature measurements 

only were performed twice within Imp. #16A (Table 2), 

they show that the temperature in the shallow (fl ooded) 

areas in the impoundment marsh may reach at least 44°C, 

which is signifi cantly higher than in the nearby IRL. Large 

numbers of dead individuals were observed in very shallow water during these high temperature periods (within 

the marsh of Imp. #16A), but never at lower temperatures, 

and it was assumed that death was the result of short-term 

hyperthermia. Replicated laboratory experiments on U. 

pugilator and U. rapax collected inside Imp. #23 showed 

that lethal water temperatures (LD50) on individuals from 

this area are 41°– 42°C. Teal (1958) reported a lethal temperature (LD50) between 39.5° and 40.0°C for U. pugilator, U. minax, and U. pugnax, and Vernberg and Tashian 

(1959) found that U. rapax was more resistant to temperatures of 42°– 44°C than was U. pugnax. Wilkens and 

Fingerman (1965) performed a thorough study on lethal 

temperatures for U. pugilator in both saturated and dry 

air. LD50 in saturated air was reached at 40.7°C, which 

corresponds well to the results from my observations. 

Powers and Cole (1976) have also demonstrated that burrow temperature decreased rapidly with depth, proving 

the major heat refuge for U. panacea on open sand fl ats 

during a study on Mustang Island, Texas. Edney (1961), 

in a study on a number of fi ddler crabs at Inhaca Island, 

Mozambique, found that the temperature within the burrows during the warmer months was considerably cooler 

than the sand on the surface. Preliminary results within 

this study (not presented) also indicate that the temperature drops signifi cantly with sediment depth in the mosquito impoundments.

Genoni (1985), on a study on U. rapax in Florida, 

reported that there were more burrows than fi ddler crabs 

in the sediment. Even if there was no correlation between 

fi ddler crabs (all species) and burrows in the present study, 

the results were often the opposite from the results by 

Genoni (1985). Mouton and Felder (1996) investigated 

the quantitative distribution of U. spinocarpa and U. longisinalis by quantitatively counting the number of Uca

burrows along transects in a Gulf of Mexico salt marsh. 

However, no studies were performed regarding the number of individuals (and species) living in these burrows. 

Excavating the substrate is a very labor-intensive procedure but obviously necessary to be able to evaluate the 

actual fi ddler crab species distribution and abundance 

within specifi c areas (see Methods, above). The studies 

performed by the author in the three St. Lucie County 

impoundments and at Merritt Island (Cape Canaveral) 

impoundments (not reported here) did not produce any 

correlation between burrows and number of Uca specimens. Actually, in several cases when no burrows at all 

were found on the sediment surface within the 0.1 m2

sampling area, large amounts of fi ddler crabs were found 

in deeper areas when excavating the substrate within the 

sampling area according to the description above. Therefore, only counting Uca burrows does not seem to give 

correct data regarding Uca population abundance and 

species distributional pattern. Further detailed studies are 

therefore needed to elucidate this relationship.

In conclusion, these studies in the St. Lucie impoundments do not indicate that the construction and management of IRL mosquito impoundments pose a serious threat 

to fi ddler crab populations. However, the impoundments 

may change the distributional patterns of the different 

species. It is important to note that new, highly suitable 

habitats were created when the impoundments were constructed, such as the perimeter ditch margins (sites A and 

B), especially preferred by U. speciosa and U. thayeri in 

impoundments with tidal access to the IRL. However, the 

36_Tunberg_459-472_Lang.indd 469 6_Tunberg_459-472_Lang.indd 469 9/24/09 10:26/24/09 10:26
470 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

fate of these two species at the marsh side of the perimeter 

ditch (site B) during the prolonged artifi cial summer fl ooding is still unknown.

ACKNOWLEDGMENTS

I wish to thank James R. David (Director, St. Lucie 

County Mosquito Control District) and Frank Evans for 

excellent cooperation and fi nancial support. I am very 

grateful to R. Grant Gilmore for his support during 

these studies. Thanks are due to Tor Carlsson for great 

assistance in the fi eld and laboratory. I am also grateful 

to Professor L. B. Holthuis, Nationaal Natuurhistorish 

Museum, Leiden, the Netherlands, for help identifying some of the specimens. Special thanks are due to 

Johan Tunberg for valuable assistance in the very hot 

and humid impoundment habitats during these summer 

studies. I am also very grateful to Sherry Reed for the 

critical reading and valuable comments on the manuscript. Finally, I am very grateful to the two referees, 

whose comments and criticism signifi cantly improved 

the quality of this manuscript. This study was fi nanced 

by The St. Lucie County Mosquito Control District, 

The Royal Swedish Academy of Sciences, The Harbor 

Branch Oceanographic Institution, and private Swedish 

funds. This is Smithsonian Marine Station at Fort Pierce 

Contribution No. 789.

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8:569– 583.

Bertness, M. D. 1985. Fiddler Crab Regulation of Spartina alternifl ora

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Bertness, M. D., and T. Miller. 1984. The Distribution and Dynamics of 

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Gilmore, R. G., R. E. Brockmeyer Jr., and D. M. Scheidt. 1991. A Preliminary Report: Spatial and Temporal Dynamics of Uca Populations in High Marsh Habitats Vegetated with Algae, Herbaceous 

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Dynamic Hydrology of a Mangrove Island: 

Twin Cays, Belize

Daniel W. Urish, Raymond M. Wright, 

Ilka C. Feller, and Wilfrid Rodriguez

ABSTRACT. The hydrology of an overwashed mangrove island is shown to be both 

complex and dynamic, with a strong interaction between tide-induced fl ow and the resident red mangrove (Rhizophora mangle L.) root system. A topographic map of the tidally fl ooded area of the island was made and related to the tide-induced water levels. The 

fl ooded area approximately doubled during the usual tidal event. The bottom topography is highly irregular with a maximum channel water depth of about 1.5 m, but much 

of the fl ooded area experiences a water depth of less than 0.5 m. Water elevations were 

recorded by automatic water level loggers for periods of time up to 9 months. The usual 

symmetrical parabolic tide signal was transformed into a highly asymmetrical form as it 

moved landward through the tangled root system of the red mangrove forest. A normal 

tide range of 13 cm at the island margin attenuated to 3 cm at a distance of 200 m 

landward, with a lag time of 2 h for highs and 6 h for lows. Maximum fl ow velocities 

of 5 cm/s were measured in the main channels with marked reduction in regions of 

dense mangrove root and shallow water depth. The combined frictional resistance of the 

bottom and associated mangrove roots is characterized by a Manning’s roughness coeffi cient, n, that ranged from 0.084 to 0.445. The changing fl ow pattern within the fl ooded 

mangrove swamp was mapped during a 7 h high-to-low tide period using aerial photography to track the movement of slugs of visible dye placed at three locations. Analysis 

of the sequential time-related photos showed limited lateral dispersion in the tortuous 

main channel but strong tidally controlled fl ow direction changes and dispersion along 

the channel axis. A strong circulatory pattern is observed in a shallow pond at the south 

central terminus of the tidally affected fl ow system. This large shallow pond is sparsely 

populated by dwarf red mangrove and is some 350 m from a primary connection with 

the surrounding lagoon. Poor fl ushing of the pond creates water temperatures ranging 

from 25°C in the winter to 40°C in the summer. High surface water evaporation creates 

a hypersaline condition of 45 ppt salinity in summer. In winter, with the infusion of fresh 

rainwater, salinity of surface water in the pond can be less than 5 ppt. Because of its role 

in the transport of nutrients and detritus, and its fl ushing action, the dynamic hydrological 

system of the mangrove island is a highly important ecological feature of the overwashed 

mangrove island.

INTRODUCTION

Mangrove forests are tropical wetlands with a specialized vegetation adapted 

to waterlogged and saline conditions (Lugo and Snedaker, 1974; Hutchings and 

Saenger, 1987; Ball, 1988). These forests provide energy-absorbing buffers from 

Daniel W. Urish, Raymond M. Wright, and Wilfrid Rodriguez, University of Rhode Island, Engineering Department, Bliss Hall, 1 Lippitt Road, 

Kingston, Rhode Island 02881, USA. Ilka C. 

Feller, Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, Maryland 21037, USA. Corresponding author: D. Urish 

(harbourrose@cox.net). Manuscript received 13 

May 2008; accepted 20 April 2009.

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474 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

hurricane-driven seas, prevent coastal erosion, provide 

a protective habitat for many fi sh juveniles, and are a 

nutrient source for the surrounding waters (Odum and 

Heald, 1972, 1975; Twilley, 1988; Danielson et al., 2005; 

Barbier, 2006, Constanza et al., 2008), as well as a fi ltering mechanism for sediments and pollution (Alongi and 

McKinnon, 2005). Under natural conditions mangroves 

live in a highly dynamic environment and in synergistic 

balance with their natural neighbors. Mangroves have 

evolved features that enable them to cope with an everchanging regime of tidal water ranges, variable salinity and 

temperature, and anoxic soil conditions, but within limits 

(Tomlinson, 1986). The biggest enemy appears to be man, 

who can directly or indirectly destroy, in days, whole mangrove communities that have taken thousands of years to 

develop (Alongi, 2002; Macintyre et al., 2004; Rodriguez 

and Feller, 2004; Taylor et al. 2007; Duke et al., 2007).

It is widely recognized that hydrological patterns determine mangrove structure and function at the ecosystem 

scale (Lugo and Snedaker, 1974; Forman and Godron, 

1986; Twilley, 1995), and general models of mangrove hydrodynamics have been developed (Wolanski et al., 1992). 

In these coastal wetlands, tidal fl ooding and surface drainage infl uence many ecological processes, including habitat 

quality, water movement, fi ltration, and nutrient cycling 

(Forman and Gordon, 1986). Water fl ow also infl uences 

the dispersal and establishment of mangrove propagules 

(Mazda et al., 1999).

The signifi cant role of vegetation and the effect of intertidal root density on tidal movement in mangrove channels has been described by Wolanski et al. (1980) and over 

the broader mangrove swamp environment by Wolanski 

et al. (1992), Furukawa and Wolanski (1996), Mazda et 

al. (1997), and Mazda et al. (2005). Thus, there is a synergistic relationship for the development and growth of a 

mangrove forest that depends on the dynamics and magnitude of tidal inundation into the swamp. Concurrently, 

the frictional resistance of the mangrove roots controls the 

degree of tidal inundation and patterns of movement in 

the mangrove swamp (Wright et al., 1991).

Based on long-term experiments on offshore mangrove islands in Belize, hydrodynamics have been linked 

to distinct patterns of nitrogen (N) and phosphorus (P) 

limitation across the intertidal fl ow system (Feller et al., 

2003). Lovelock (2008) suggested that differences in tidal 

inundation also infl uence soil respiration and belowground carbon sequestion via root production, which is 

the source of the deep peat deposits underlying these islands. McKee et al. (2007) predicted that the ability of 

islands such as Twin Cays to keep pace with rising sea 

levels is dependent on the tight coupling between peat formation and hydrology.

Although these and other studies based at Twin Cays 

have identifi ed tidal fl ooding as an important drive of ecological processes, there is limited knowledge on the specifi c pattern of water movement across these islands. Thus 

the objective of this research was to conduct a detailed 

analysis of tidal characteristics and fl ushing patterns of 

West Island, the smaller of the two main islands in the 

Twin Cays Archipelago.

LOCATION

The Twin Cays Archipelago lies some 22 km off the 

coast of Belize (Figure 1) on the edge of the Belizean Barrier Reef (16°50N, 88°06W). Islands of the Barrier Reef 

and its surrounding waters have been the locations for 

scientifi c ecosystem studies by the Smithsonian Institution since 1972 (Rützler and Macintyre, 1982). Because of 

their pristine condition and relative isolation from anthropogenic effects, the islands and contiguous waters of Twin 

Cays were selected for detailed scientifi c research of oceanic mangroves and associated marine ecosystems (Rützler and Feller, 1996). Field studies of the dynamic hydrology of the Twin Cays mangrove ecosystems were begun in 

1986 and have continued since that time. This particular 

study focuses on the surface hydrology of West Island of 

Twin Cays (Figure 1), a 21.5 ha kidney-shaped landmass 

approximately 900 m long and 400 m wide. According to 

the classifi cation of Lugo and Snedaker (1974), the island 

is an “overwashed mangrove island,” one frequently overwashed by tides and with high organic export.

ISLAND CHARACTERISTICS

The land cover on West Island and effect of man are 

shown in Figure 2, which depicts the natural mangrove 

growth and the man-made clear-cut and dredge-fi ll as 

mapped by I. C. Feller of the Smithsonian Institution 

in 2002. Since then even more mangrove destruction 

has occurred on the east side of the island. The island 

is dominated by the red mangrove, Rhizophora mangle

L., with black mangrove (Avecennia germinans L.) on 

somewhat higher topography in the intertidal zone and 

white mangrove (Laguncularia racemosea L.) above 

the intertidal zone (Rützler and Feller, 1988; Rodriguez 

and Feller, 2004). It is to be noted that the density of 

the mangrove is far from uniform, with sparse dwarf 

red mangrove dominating the interior, and much more 

vigorous red mangrove growth on the island perimeter 

37_Urish_473-490_Lang.indd 474 7_Urish_473-490_Lang.indd 474 9/24/09 10:11/24/09 10:11
NUMBER 38 • 475

and in areas of greater tidal movement. Figure 3 is a 

photograph taken from the island interior showing the 

dwarf red mangrove in the foreground and the distant 

background of taller dense red mangrove growth that 

characterizes the island perimeter. Figure 4 provides a 

botanical rendering of the cross section of the scrub red 

mangrove, showing the relationship between mangrove 

foliage, stem and root structure, average tidal range, and 

hydrogeologic strata. It is to be noted that the typical 

low tide level is near the top of the organic ooze.

The mangroves of Twin Cays have developed on 

an ancient limestone plateau over the past 8,000 years 

(Macintyre et al., 2004). During this time 9– 12 m of 

Holocene mangrove deposits have accumulated on the 

underlying limestone substrate and kept pace with rising sea level (Toscano and Macintyre, 2003; Macintyre 

FIGURE 1. Location map of Twin Cays, Belize, Central America. (Adapted from Rützler and Macintyre, 

1982.)

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476 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 2. Land cover characteristics of West Island, Twin Cays, Belize, based on aerial photographs taken 

in 2002 that show mangrove density and clear-cut areas. (Drawn by Molly K. Ryan of the Smithsonian 

Institution in 2002.)

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NUMBER 38 • 477

et al., 2004; McKee et al., 2007). Macintyre and Toscano 

(2004) found Pleistocene limestone at depths of 8.3 to 

10.8 m below mean sea level in cores at West Island. As 

sea level rose to cover a subaerially eroded limestone 

plateau fringing the coastline, mangrove peat appears in 

the stratigraphic record. The highest topography of the 

island is on the seaward side where deposited sand is no 

more than 1 m above mean sea level. The limestone is 

now found at depths of 9 to 10 m below present sea level 

(Macintyre et al., 2004). The swamp bottom is composed largely of soft silty organic detritus. Exceptions of 

harder bottoms are found in the nearshore swamp channels where stronger tide-induced velocities have scoured 

the channel bottoms.

The climate of Twin Cays is marine tropical with air 

temperatures ranging during the year from 24°C in January to 29°C in June; humidity averages about 78% (Rützler and Ferraris, 1982). Lagoon water temperatures range 

from 23°C in the winter to 31°C in the summer. The microclimate of West Island, particularly that of the interior 

water, has a much greater range. The estimated annual 

precipitation at Twin Cays is about 1,885 mm, based on 4 

years of complete records at the climatological station on 

Carrie Bow Cay, 4 km away. This precipitation is about 

80% of the annual precipitation of the nearest mainland 

climatological station, the Melinda Forest Station, 30 km 

to the northwest. The monthly pattern is much the same 

for both stations. Hurricanes cause seawater to completely 

overwash the low-lying island. However, the natural mangrove ecosystem seems resilient and well suited to survival 

from natural events, viz. hurricanes. No signifi cant adverse 

effects have been observed on Twin Cays; the same cannot be said for the response to man-made features, where 

mangrove clearing results in severe coastal erosion.

Tides in the lagoon area surrounding the island are 

microtidal with an average range of about 15 cm and 

are of the mixed semidiurnal type (Kjerfre et al., 1982). 

The tides exhibit semidiurnal high and lows with a tidal 

cycle periodicity of approximately 12 h and 25 min, but 

display a marked asymmetry with a large tide range following a smaller one. In some cases the larger range is as 

much as 40 cm, followed by a range of only 10 cm. At 

times the smaller range is so small as to appear nonexistent. In other cases certain components of the tide occur simultaneously and create a range as great as 50 cm. 

Once the tidal signal enters the tangled root system of 

the mangrove, the signal changes from a form that is 

approximately parabolic to a highly asymmetrical pattern, in which the rising limb of the fl ood tide is much 

steeper than the falling limb. Concurrently the amplitude 

is attenuated, and the highs and lows of the tidal signal 

lag the open lagoon tide. The spring– neap tidal cycle is 

about 29.5 days and can cause monthly tidal ranges that 

completely “dry up” the interior of the island.

FIGURE 3. Photograph of West Island, Twin Cays, showing dwarf 

red mangrove of island interior with much more vigorous fringe red 

mangrove growth in distance along periphery of the island.

FIGURE 4. Botanical rendering of cross section of dwarf red mangrove showing relationship between mangrove foliage, stem and 

root structure, average tide range, and hydrogeologic strata. (Drawn 

by Molly K. Ryan of the Smithsonian Institution in 1989.)

37_Urish_473-490_Lang.indd 477 7_Urish_473-490_Lang.indd 477 9/24/09 10:11/24/09 10:11
478 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

METHODOLOGY

The information required for a study of the dynamic 

hydrology of West Cay encompassed both spatial and 

temporal data and a wide variety of methods. These methods included fi eld surveying techniques for obtaining the 

island topography and bathymetry, automated water level 

recorders for water levels, automated temperature loggers, 

electromagnetic water current meters, conductivity meters 

for determination of water salinity, and aircraft for photographic recording of dye fl ows, among a host of lesser 

equipment and measuring devices that were employed 

over the study period of 18 years (1988– 2006).

TOPOGRAPHY

Topography was determined for the tidal fl ood region 

extending from open lagoon water at the west side of the 

island along the 350 m long channel and the southern interior pond (Urish et al., 2003; Wright et al., 1991). Some 

36 semipermanent monitor locations were established in 

1988 in the intertidal swamp to obtain water level and water quality measurements. The locations were marked with 

2 cm diameter polyvinyl chloride (PVC) pipes driven into 

the ground in a grid pattern. Horizontal control was established by fi eld measurement with a 35 m long tape and 

conventional level and transit surveying techniques (Wolf 

and Ghilani, 2006), later located with Global Positioning 

System (GPS) technology using a Garmin GPS 76. These 

data were later used for georeferencing of all island features 

(Rodriguez and Feller, 2004). Vertical control for land and 

water measurements was determined from a primary datum reference point on the east side of the island to which 

an arbitrary datum was assigned. The initial elevation assigned to this reference point was 3.05 m with all readings 

later adjusted to an approximate mean lower low water 

(MLLW) after several years of time segments of about 2 

weeks; one long record of 9 months of tidal data was obtained. A datum lower than the typical terrestrial datum of 

“mean sea level” was used to maintain both topography 

and water level values positive to the extent possible.

Two principal surveying transects across the island 

were established: (1) from the lagoon to the bend in the 

channel along an east-to-west run including 6 points (F1 

to A1) and (2) from the bend in the channel to the south 

pond along a north-to-south run of 12 more points (A1 

to A12). In addition, 3 to 5 points were determined perpendicular to each transect point. These secondary points 

were spaced approximately 15 m apart. These established 

points, as located on Figure 5, were the primary location 

references for all subsequent data collection.

Automated pressure transducer water level loggers 

(In-Situ Environmental Data Logger Model SE 1000c 

with pressure transducer probes) were employed at fi ve 

locations for short-term (1– 2 weeks) measurements. 

These units were vented to automatically compensate for 

ambient atmospheric pressure. Later in the study period 

12 of these locations became long-term monitoring stations with automated self-contained water level loggers 

(Remote Data Systems, Navassa, N. C.) that remained in 

place for as long as 12 months to record data at 30 min 

intervals with an accuracy of about 3 mm. Self-contained 

automated temperature loggers (Optic Stowaway by Onset Computer Corporation) were also deployed to record 

temperatures at 30 min intervals for as long as 9 months. 

In addition to the monitor locations, stilling wells consisting of slotted 15 cm diameter PVC pipe for both manual 

and instrumented tide measurements were established at 

both shorelines of the island, and later in the study these 

were correlated with a primary oceanographic/climatological data collection station established at the Smithsonian 

Research Station on Carrie Bow Cay, 4 km southeast. The 

tops of the stilling wells were initially assigned an elevation based on the same arbitrary datum as used at the key 

datum reference points. Elevations were established on 

the tops of all reference station pipes using survey leveling techniques with a Topcon Automatic Level (model 

ATF– 1A). The coordination of tides at West Island and 

Carrie Bow Cay was accomplished by comparison of a 

series of six separate short-term tidal cycle measurements 

taken concurrently at both stations.

HYDROLOGY

Water fl ow direction and velocities during various positions of the tide cycle were determined using conventional 

stream gauging techniques along channel cross-sections, or 

“reaches:” section A– Awas defi ned between survey points 

A1 and D1 and reach B between survey points D1 and E1. 

The measurements were taken at various times during the 

tidal cycle using a Marsh-McBirney electromagnetic current 

velocity meter and standard stream channel cross-sectioning 

methods (Watson and Burnett, 1995). Velocities and water 

depths were measured at 0.6- to 1.5 m intervals perpendicular to the fl ow to provide 25 to 50 individual measurements 

at each cross section. These measurements were then plotted to determine fl ow volumes and fl ow friction factors and 

to examine trends. 

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NUMBER 38 • 479

FIGURE 5. Topographic contour map of interior of West Island showing locations of key monitoring stations and representative channel cross section A– A. Elevation datum  mean lower low water (MLLW). 

Contour interval  6 cm.

37_Urish_473-490_Lang.indd 479 7_Urish_473-490_Lang.indd 479 9/24/09 10:11/24/09 10:11
480 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Water salinity (0.1 ppt), conductivity (0.1 uS), and 

temperature (0.1°C) were measured with a YSI 30 S-C-T 

(Yellow Springs, OH) in the fi eld and in the laboratory. 

Salinity measurements were also made in the fi eld using 

a refractometer (model 366ATC; Vista) with an accuracy 

of 1 ppt.

Flow patterns were also observed and evaluated by 

use of dye studies, both at the surface water level and by 

helium balloon low-level photography in 1990 and 1991, 

and later by high-level aircraft photography during a tidal 

cycle in 1993. Although the balloon photography was only 

of limited value because upper air wind currents caused the 

balloon to drift off the island, aircraft photography was 

highly successful. Large targets, approximately 1  2 m 

in size, were marked and placed at each station for dye 

movement referencing. Continuing runs at 0.5 h intervals 

were made across the island on the same fl ight path at an 

altitude of 150 m. Photographs were taken during each 

run with a SLR camera with AF Zoom 35-70 mm lens 

(Minolta 5000 MAXXUM), thus enabling both the fl ow 

directions and dispersion within the mangrove system to 

be observed. Slugs of Rhodamine fl uorescent dye, a highly 

visible but nontoxic dye, were placed at three stations 

at the start of the observation period. The dye remained 

highly visible during one tidal cycle. Continuing, but diminishing, levels of the fl uorescence were measured in the 

laboratory on water samples taken during three subsequent tidal cycles. The series of photographs taken from 

the aircraft runs were reduced to a time sequence of plots 

and then used by George L. Venable of the Smithsonian 

Institution to produce an animated video of the dye movement for further study.

RESULTS

TOPOGRAPHY

A topographic map of the intertidal fl ood zone region 

of West Island is shown as Figure 5. The highly irregular 

nature of the bottom is evident by inspection of the contour pattern. The region of tidal fl ow and fl ooded area is 

characterized by relatively fl at areas with water depths frequently only about 25 cm over much of the fl ow system, 

but highlighted by sections more than 1 m in depth, such 

as occur between stations A4 and A5. Such deep holes are 

not necessarily coherent with the main fl ow channel. A 

cross-section (A– A) plot (Figure 6) at station A5 depicts 

the extreme changes in channel bottom that exist at this 

location. In contrast, the other signifi cant feature of the 

system is a very large shallow pond of about 2.2 ha at stations A10 to A12 at the south central part of the island. 

This region contains only sparse dwarf red mangrove with 

a fl ooded depth of about 0.25 m. Additionally, examination of the topographic map shows ground level at the east 

shoreline of this pond is about 6 cm lower than the rest 

of the island periphery. At high tides these limited lower 

topographic zones allow lagoon water from outside to enter the internal swamp fl ow system. In particular, high tide 

waters overtop the island perimeter at two other locations 

on the east side into the central region, causing short-term 

hydrological anomalies of temperature and salinity, as well 

as a somewhat irregular tidal signal, in the system.

HYDROLOGY

Figure 7 is a fi ve-day plot showing the typical tidal 

signal as it enters the swamp system at TG2. As the signal 

enters the mangrove system, the frictional resistance of the 

roots cause attenuation in tide amplitude as well as a time 

lag in the highs and lows.

The unique hydrological nature of the fl ow in the 

mangrove ecosystem is characterized by a very shallow 

water depth that averages only about 0.5 m at low tide 

to 0.67 m at high tide, although great variations exist. 

However, because of the very fl at topography, even this 

low tidal fl uctuation causes an extensive and signifi cant 

hydro period of wetting and drying with important implications to the mangrove ecosystem. As depicted on Figure 8, the area typically covered by water during high tide 

is about double that covered by water during low tide. 

Doyle (2003) states that his controlled fi eld experiments 

FIGURE 6. West Island cross section A– Aat station A5 showing 

relative relationship of high and low tides to bottom contours. Green 

 range of fl ooding from the tide; blue  low tide fl ow. Elevation 

datum is arbitrary.

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NUMBER 38 • 481

“suggest that the hydroperiod— the rate and level of tidal 

exchange— plays a much more important role in determining mangrove growth and success than previously documented.” Figure 9 presents a conceptual plot showing 

the wetting– drying cycle during the sequential phases of 

the tide. Perhaps even more important, the tide range is 

suffi cient to cause reversal of fl ow direction and velocity 

throughout the system during each cycle.

Figure 10 shows the changing characteristics of the 

tidal signal at three stations as it moves inland in a tortuous path through the mangrove ecosystem. A tide range 

of 13 cm at the island margin is attenuated to 8 cm at a 

location 50 m landward and to 3 cm at a location 200 m 

landward in the main fl ow channel. Concurrently, there is 

a lag time of 1 h for high tide and 2 h for low tide at 50 m 

landward, and of 2 h for high tide and 6 h for low tide at 

200 m landward. The great difference in lag time between 

highs and lows is caused by the much greater infl uence of 

root density during a receding tide; this is also illustrated 

by the asymmetrical characteristic of the tidal signal as it 

transposes landward.

The seasonal climatic variations had a profound effect 

on the monthly hydrological budget, especially when the 

high evapotranspiration was considered. Figure 11 shows 

the approximate seasonal relationships of precipitation, 

surface water evaporation, and vegetation transpiration 

(evapotranspiration), assuming a total annual rainfall of 

1,885 mm. This value and the estimated monthly values 

are based on limited (about 5 years) available data that 

have been collected at Carrie Bow Cay and correlated 

with the longer-term record at the mainland Melinda 

Forest Station. The potential evapotranspiration values 

for each month were calculated from the Thornthwaite 

equation (Dunne and Leopold, 1978; Thornwaithe and 

Mather, 1987) using a partial record of temperature and 

solar radiation available for Carrie Bow Cay. Examination of the water budget shows a defi cit of precipitation as 

FIGURE 7. Plot of fi ve-day tide sequence showing relative ranges and 

asymmetry of the tide at West Island. Elevation datum  approximate mean sea level. 

FIGURE 8. Plan of West Island showing aerial extent of tidal fl ooding between average daily low and high tides. Stippling on map 

shows relative density of vegetation. (Adapted from drawing by 

Molly K. Ryan of the Smithsonian Institution in 2002.)

37_Urish_473-490_Lang.indd 481 7_Urish_473-490_Lang.indd 481 9/24/09 10:12/24/09 10:12
482 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

compared with evapotranspiration February through June 

during the “dry” season and a surplus during the “wet” 

season months from July through January. This “dry” season water defi cit has an extreme effect on the surface water in the semienclosed interior swamp system, especially 

in the poorly fl ushed shallow pond at the south end of the 

island. Figure 12 is a composite plot of water temperature 

and salinity measured along the main fl ood channel over 

several years during the “dry” and “wet” seasons. Near 

the infl owing/outfl owing location at station F1 the values 

approach those of lagoon water at the periphery of the 

island, but in the shallow pond the value ranges are much 

more extreme, with salinity ranging from 5 to 45 ppt and 

temperatures ranging from 25°C to 40°C. Some temperature and salinities even exceed these values in particularly 

isolated locations.

The elevations of the water surfaces and velocities at 

three stations within the fi rst 150 m inland from the shore, 

as compared with the primary tide signal at shore station 

TG2, are shown in Figure 13. It is to be noted that at all 

stations the maximum velocities occur during the middle 

of the falling tide, with the highest velocities found nearest 

shore. This pattern is comparable with the tidal asymmetry and velocity patterns found by Bryce et al. (2003) in 

mangrove creek systems in Australia. The distribution of 

fl ow and variations of velocity for a typical channel section are illustrated in Figure 14 for a cross section at station A4. The data were acquired during a mid-tide fl ood 

tide at a time of maximum velocity. The upper part of Figure 14 shows depths of water across the section at the specifi c time of the velocity measurements shown in the lower 

part. The velocities shown are an average determined from 

a series of velocities measured at a series of depths over 

the shortest time period possible. As indicated the velocity 

changes dramatically, from 2.0 to 0 cm/s, across the section, although there is a general pattern of greater velocity 

at the deeper parts. However, this is contradictory to the 

observation that the deeper part on the right side does not 

FIGURE 9. Conceptual plot of tidal phases during mixed semidiurnal hydroperiod event. (Adapted from Boulton and Brock, 1999.)

FIGURE 10. Tidal fl uctuation plots at three interior monitoring stations— TG2, A, and B, as shown on photograph at right— during maximum velocity of fl ood tide on 27 May 1988. Yellow dots on the photograph 

are locations of monitor stations. Elevation datum is arbitrary.

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NUMBER 38 • 483

have a high velocity. Inspection of the topographic plan (see 

Figure 5) provides the explanation: The deeper right-hand 

feature is a part of a closed depression, whereas the deeper 

part on the left is continuous with the main channel fl ow.

The average fl ow velocity between points in the swamp 

is refl ective of both the tortuous path of fl ow through the 

mangroves and the frictional resistance of the mangrove 

root system and the channel bottom. This resistance can 

be quantifi ed by inverse calculation of the Manning equation for stream fl ow (Watson and Burnett, 1995). Although the Manning equation was originally developed 

for stream fl ow, it has a logical deterministic relationship 

that has been used successfully by other researchers for 

mangrove fl ow characterization and modeling (Wolanski 

et al., 1980). The Manning equation in MKS unit format 

(Lindsley and Franzini, 1979) is

V RS = 1/n 2/3 1/2,

where V is the average velocity, n is the Manning roughness coeffi cient, R is the hydraulic radius (cross-section 

area divided by wetted perimeter), and S is the slope, or 

hydraulic gradient, of the water surface.

Manning’s roughness coeffi cient, n, was determined at 

various locations in the fl ow system and at various times 

in highly fl uctuating stream depth and current direction. 

The determined values of n for these measurements ranged 

FIGURE 11. Hydrological budget for West Island showing annual pattern of precipitation, evapotranspiration, and temperature. 

Shaded orange area  the “dry season” with net defi cit of water 

from evapotranspiration; blue shaded area  the “wet season” with 

a surplus of precipitation.

FIGURE 12. Plot showing ranges of salinity (black dots) and temperature (circles) during “dry” and “wet” season conditions at the southern shallow pond on West Island. Monitoring stations (see Figure 5) 

with distances from the open water lagoon at the west periphery of 

the island are indicated.

37_Urish_473-490_Lang.indd 483 7_Urish_473-490_Lang.indd 483 9/24/09 10:12/24/09 10:12
484 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

from 0.084 to 0.445, far higher than the typical 0.035 

found even for natural channels with stones and weeds. 

These values however are comparable to those ranges of 

0.2 to 0.7 determined by Wolanski et al. (1992) for fl ow in 

southern Japan mangrove systems. Based on earlier studies, Wolanski et al. (1980) had earlier suggested that n is of 

the order of 0.2– 0.4 in mangrove swamps. Table 1 shows 

the parameters and results for calculation of the Manning 

coeffi cient for section A– A, with depth and velocity characteristics as depicted in Figure 14. It is to be noted in 

Table 1 that the value of n is greatest at shallow water 

depth and lower velocities. Again, this is comparable to 

the fi ndings of Wolanski et al. (1992).

FIGURE 13. Plot of relative elevations (arbitrary datum) and velocities during falling limb of tide at monitor stations C1, E1, and F1 

(see Figure 5). 

FIGURE 14. Water depths and velocities at cross-section A– A, at 

monitoring station A4 (see Figure 5) during a fl ood tide with maximum velocities, on 27 May 1988.

TABLE 1. Summary of hydraulic parameters for cross-section A–Aat Station A4 (see Figure 5).

 Average water Hydraulic slope, Average Manning’s

Observation a depth (cm) S (m/m) velocity (cm/s) Flow (m3/s) coeffi cient, n

 1 11.9 0.000117 0.6 0.034 0.415

 2 13.4 0.000110 0.6 0.037 0.445

 3 14.3 0.000102 1.3 0.085 0.206

 4 14.6 0.000098 1.1 0.069 0.261

 5 16.4 0.000086 1.3 0.097 0.210

 6 20.3 0.000055 1.6 0.145 0.159

a Each observation with the associated calculations is based on 30 measurements across cross-section A–Aas detailed in Figure 14.

37_Urish_473-490_Lang.indd 484 7_Urish_473-490_Lang.indd 484 9/24/09 10:12/24/09 10:12
NUMBER 38 • 485

A dye fl ow study was accomplished during a high tide 

period on 5 June 1993. Single slugs of Rhodamine fl uorescent dye, which produced a distinctive red color, were 

placed at three locations (monitor stations D1, A6, and 

A10; see Figure 5) along the main channel early in the 

morning. Large visual targets were placed at the monitor 

stations in the mangrove swamp to enable referencing the 

dye positions during movement.

The movement of dye was documented by aerial photography from an aircraft fl own in a fi xed fl ight pattern, 

and at a fi xed altitude of 150 m (500 ft.), Runs were made 

at 0.5 h intervals. Figure 15 is a series of drawings made 

from 11 of these runs, depicting the leading edge of the dye 

with time. The 7 h period of measurement relative to the 

position of the tide at the exterior lagoon is depicted on 

the inset tide plot of Figure 15. Figure 16 is a high oblique 

photograph of West Island taken from an altitude of about 

600 m (2,000 feet) showing the position of the dye at 9:10 

AM, shortly after high tide. The aircraft run pattern starts 

over monitor station TG 2 and progresses east, turning 

south to proceed over the large pond at the south end of 

the island. The series of photographs have been converted 

to an animated visual program by George L. Venable of 

the Smithsonian Institution (URL http://www.uri.edu/cve/

dye.mov) that clearly shows the oscillation of the water 

of the mangrove swamp water as the dye at station D1, 

some 70 m from the lagoon, fi rst went to the east, then reversed to fi nally discharge into the lagoon. The dye fl ow at 

station A6 also oscillated, then merged with the out going 

dye from station A10 approximately 120 m south of A6, 

toward the pond. Interestingly, the dye placed at A10, at 

the north margin of the pond, also moved into the pond 

and then fl owed in a circulatory pattern. This pattern may 

be caused by new lagoon water overfl owing the rim of 

the pond to the east because the tide during the period of 

observation was a relatively high spring tide. Finally the 

dye from D1 discharges into the lagoon, and the merged 

A6/A10 dye moves north. Previous water level studies with 

measured levels of fl uorescent dye indicated that this dye 

persists at continuing reduced levels in the central locations 

FIGURE 15. Sequential plots of dye fl ow patterns over a 7 h period from high tide through low tide, during 

dye fl ow test on 5 June 1993. The plot in the lower right-hand corner shows the relative time position of runs 

with tide levels at station TG2.

37_Urish_473-490_Lang.indd 485 7_Urish_473-490_Lang.indd 485 9/24/09 10:12/24/09 10:12
486 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

for several tidal cycles before fi nally being fl ushed and dissipated into the lagoon.

DISCUSSION

An intimate knowledge of the topography of the fl ow 

and fl ood area is essential to an understanding of the ecosystem of a semiclosed mangrove hydrosystem such as 

West Island. The interior water system of West Island is 

primarily tide-induced fl ow, with modifi cations caused by 

precipitation and seasonal climatic change. Hence, it is 

also very important that the climatic factors be considered 

in conjunction with the hydrographic characteristics.

The tidally induced hydrodynamics of the water fl ow 

in tidal channels and ponds of an overwashed mangrove 

island, in conjunction with the topography, greatly affect 

the ecosystem and vitality of the resident mangrove systems. Analysis of the temporal and spatial characteristics 

of a 21.5 ha island hydrological fl ow system shows that 

where fl ooding and current fl ow becomes more vigorous, 

the growth of the red mangrove is enhanced. It was found, 

during the 18-year period of this study, that hydrological 

changes such as increased tidal fl ow, from anthropogenic 

as well as natural causes, enhanced the growth of the red 

mangrove. On the other hand, observations of relict tree 

remains indicate that historically the interior of the island 

experienced a transition in mangrove species from black 

mangrove to dwarf red mangrove, possibly because of 

higher water levels and with poor fl ushing in the island 

interior. This concept is in concurrence with fi ndings of 

Knight et al. (2008) in studies of patterns of tidal fl ooding 

within a mangrove forest in Southeast Queensland, Australia, that “mangrove basin types represent a succession 

in mangrove forest development that corresponds with increasing water depth and tree maturation over time.”

Detailed mapping of the topography of the intertidal 

interior region of the island reveals poorly defi ned fl ow 

FIGURE 16. Aerial photograph of West Island looking to the northwest from an altitude of 600 m during the 

5 June 1993 dye fl ow test, corresponding approximately to the time of run 4 of Figure 15. The dye is evident 

as the red confi guration in the south pond.

37_Urish_473-490_Lang.indd 486 7_Urish_473-490_Lang.indd 486 9/24/09 10:12/24/09 10:12
NUMBER 38 • 487

channels that vary greatly in depth and width. Within this 

system anomalous deep sections exist, further contributing to the complexity of fl ow. The root structure of the 

mangroves and the irregular bottom result in a frictional 

resistance to the fl ow, quantifi ed by Manning’s n as being 

as much as 10 times greater than that of conventional terrestrial stream channels. In studies in mangrove swamps 

on Iriomote Island, Japan, Kobashi and Mazda (2005) 

stress the importance of the hydraulic resistance of mangrove vegetation in determining the fl ow patterns, especially in reducing the velocity component perpendicular 

to the main channel. Accordingly, the interaction of the 

mangrove itself is a determinate factor in stream fl ow and 

the resulting fl ushing action, important to the vitality of 

the mangrove. It appears to be particularly relevant to the 

transport of nutrients and other physicochemical conditions important to the growth of the mangrove. The driving force for the fl ow within the mangrove hydrosystem is 

the ever-changing hydraulic gradient induced by the tide. 

Accordingly, the fl ow moves, at varying velocities, in and 

out of the interior mangrove swamp with the tide. As a 

result the seawater entering the mangroves not only follows a constantly changing path, but is regularly reversed 

in direction, and consequently it takes at least several tidal 

cycles for fl ushing of the island interior. There are indications that the central part of West Island is fl ooding more 

over a span of years, causing commensurate changes in 

the mangrove types capable of surviving in the changed 

regime, a process described by Knight et al. (2008). In 

other areas the geomorphology of the land is changing 

consequent to sediment transport, detrius deposition, and 

subsidence from peat compaction. In this regard Bryce et 

al. (2003), in studies of a small mangrove creek system 

near Townsville, Australia, evaluated the role of hydrodynamics in the sediment transport process. Importantly 

they observed that sediment transport appears to be a 

seasonal phenomenon, with net fl ux going either landward or seaward, but they conclude that the net sediment transport for the overall system may be close to 

long-term equilibrium. They do state that mangrove 

swamp areas (in the tidal overfl ow regions) are most 

likely to be places of sediment accumulation; if so, the 

more shallow areas of West Island, when fl ooded at high 

tide, may experience accumulation from redistribution 

of sediment within the system as well as from direct leaf 

drop and in situ detritus accumulation.

The data showed that the annual pattern of precipitation and temperature greatly affects temperature and salinity in the poorly fl ushed interior pond. On an annual 

basis there was a net discharge of water from island to the 

exterior lagoon because of precipitation. However, when 

the monthly climatic factors are considered it is apparent 

that during the “dry period” of February to May there is a 

net loss of freshwater in the island water budget, with high 

evaporation creating high-temperature hypersaline water 

in the interior. When the island is in the rainy season, July 

through December, the reverse is true, with the interior 

water becoming cooler and fresher from the rains (see 

Figure 12). In the extreme case, as described by Wolanski 

et al. (1992) for tropical mangrove systems on the coast 

of northern Australia, “The balance between rainfall and 

evaporation, in conjunction with tidal variations, is the 

key factor in determining if the upper levels of the swamp 

are (tidally fl ushed) swamp or (hypersaline) tidal fl at.” A 

further important implication for the shallow pond in the 

south part of West Island is, as stated by Wolanski et al. 

(1992), “rainfall signifi cantly affects porewater salinity 

and it is likely that it also affects nutrient levels within 

the swamp substrate, particularly in areas where regular 

fl ooding by the tides does not occur.” On West Island, 

during the “dry period” of February through May, evapotranspiration is approximately three times that of precipitation. However, during the “wet period” of June through 

December, conditions are reversed with evapotranspiration being approximately one-half that of precipitation 

(see Figure 11). Thus, the net effect on the poorly fl ushed 

interior areas of the West Island mangrove system is that 

of greatly increased salinity during the “dry season” and 

short periods of nearly fresh water from rain storms in the 

wet season (see Figure 12).

The effects of human intrusion into the natural ecosystem are illustrated by Figure 17, an aerial photograph 

showing the survey lines newly cut in 1993. At that time 

the strongest fl ow from the coastal seawater was some 

25 m south of the west– east running survey cut, as identifi ed by the darker, more vigorous vegetation. By 2003 the 

main fl ow had moved north to the survey cut itself as the 

cutting as well as foot traffi c in the cut had deepened that 

area. During the course of the investigations, it was observed that the previous dwarf red mangrove trees alongside these survey lines initiated signs of vigorous growth 

as a result of the increased fl ushing, as illustrated by the 

photograph in Figure 18.

Although previous studies have shown that for the 

past 8,000 years the mangrove growth has managed to 

keep up with rising sea level because of peat accretion, the 

future may be in doubt because of anticipated greatly increasing sea-level rise rates (Mckee et al., 2007). The ability of the island to adjust to rising sea level has important 

implications for a future that will include sea levels rising 

37_Urish_473-490_Lang.indd 487 7_Urish_473-490_Lang.indd 487 9/24/09 10:12/24/09 10:12
488 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

at a rate much greater than that experienced over the past 

8,000 years when mangroves fi rst appeared and fl ourished 

on Twin Cays. As McKee et al. (2007) have stated, “Rates 

of subsurface plus subsurface (root) accretion in fringe, 

transition and interior zones at Twin Cay were 10.4, 6.3, 

and 2.0 mm/year. Fringe mangroves have kept up and could 

accommodate eustatic sea level rise of 4 mm/year if current 

rates of accretion were maintained. If eustatic rates exceed 5 

mm/year then these mangrove islands would not be likely to 

persist, assuming all other conditions remain unchanged.”

The islands of Twin Cays, with a history of comprehensive ecological research, remain an important location 

for measuring and evaluating changes in the mangrove 

and associated ecosystems because they occur in a world 

of dramatic coastal change. Much analytical work remains to link the dynamic hydrology of the mangrove island to the physiological parameters essential to mangrove 

growth. The research site of Twin Cays, with three decades 

of baseline data and research, is a very important asset for 

better understanding the ecosystem of the mangrove. It is 

very important that this work continue and build on the 

substantial foundation of information that now exists.

CONCLUSIONS

Overwashed mangrove islands are extremely complex 

ecosystems. They are essentially self-dependent, and the vitality of the resident mangrove species is primarily a result 

of the tide that produces the essential hydrological functions of fl ushing and nutrient transport. The topography, 

the geomorphology, and even the existence of a mangrove 

island are products of the island vegetation itself. This interaction affecting the island confi guration is constantly 

changing as the mangrove forest with its multiple species 

adjusts to higher sea levels and the resultant changes in 

hydrological fl ow and fl ooding parameters.

The interior of the island is subject to extremes of temperature (20°– 40°C) and salinity (5– 45 ppt) with limited 

fl ushing that may adversely affect the vitality and existence 

of the mangrove, as well as the natural selection of mangrove species. A comparison of the hydrological parameters 

and fl ow regimes in the regions of vigorously growing red 

mangrove with that of dwarf red mangrove strongly suggests 

that enhanced communication with external lagoon water is 

best for the vitality of the red mangrove on Twin Cays.

FIGURE 17. Aerial photograph taken in 1993 (looking south) showing survey lines that were newly cut in 

1993. The original principal tidal fl ow path is evident as the darker green vegetation approximately 30 m 

south of the 1993 east– west survey line.

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NUMBER 38 • 489

The fl ow within the island is strongly infl uenced by 

the substantial frictional resistance of the mangrove root 

system. This dense root system serves to greatly attenuate 

the tidal amplitude as it progresses into the island, creating a reduced hydraulic gradient for water movement. The 

resultant reduced fl ow creates a poorly fl ushed island interior with poor mangrove growth.

Extensive land clearing, especially along the coastal 

margins, has long-term continuing effects of mangrove 

loss from which the island may never recover (Macintyre 

et al., 2009). In contrast, limited incursions such as the observed survey line cutting may shift, but enhance, channel 

fl ow, promoting more vigorous red mangrove growth. In 

extensive fi eld research (Feller et al., 2003), it was found 

that the patterns of nutrient availability within and among 

mangrove ecosystems are complex. Feller et al. (1999) 

showed the dramatic effects of nutrient enrichment on 

mangrove growth as well the changes in nutrient limitations that can take place within relatively short distances 

in swamp ecosystems. At least in the case of the nutrientpoor (P-limitation) condition of the sparse red mangrove 

in the interior of the island, the cause of nutrient limitation 

seems to be poor fl ushing, which limits the refreshing of 

the system with phosphorus-rich lagoon water from tidal 

fl ooding.

A further concern is that of the effect of rising sea 

level on the ability of the mangrove to survive. The hydrodynamics of the mangrove system greatly infl uences the 

mangrove ecosystem both by transport of nutrients and 

sediment and by the direct ability of the geomorphology of 

the island to develop to keep pace with rising sea level as it 

has in the past (McKee et al., 2007). At the least it appears 

that differential growth of mangroves will occur as fl ooding occurs and the hydrodynamics of the system changes.

ACKNOWLEDGMENTS

The authors are grateful to the Smithsonian Institution for the opportunity and research support provided 

over the past twenty years, to the University of Rhode Island for its provision of faculty and staff, especially equipment engineer Brian Gray, in conducting this research, and 

to the many fellow island researchers who have enriched 

our professional lives as a part of a multidisciplinary team. 

We especially thank Klaus Ruetzler, Director of the Smithsonian Caribbean Coral Reef Ecosystem Program, for his 

encouragement in pursuing the hydrological aspect of the 

mangrove ecosystem; Michael Carpenter, Smithsonian Institution (SI), for logistic support that made the fi eldwork 

possible; Molly Ryan (SI) for her most useful and beautiful artwork; and George Venable (SI) for his computeranimated graphics that greatly aided our interpretation of 

the complex water movement in the mangrove swamps. 

We are grateful for fi nancial support that was provided by 

the Exxon Corporation, the National Science Foundation 

Biocomplexity Grant to I. C. Feller (DEB-9981535), and 

the Smithsonian Institution. This is contribution number 

852 of the Caribbean Coral Reef Ecosystems Program, 

Smithsonian Institution, and was supported in part by the 

Hunterdon Oceanographic Research Fund.

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Ecological Characteristics 

of Batis maritima in Florida and Belize

Dennis F. Whigham, Michael C. Whigham, 

Ilka C. Feller, Wilfrid Rodriguez, 

and Ryan S. King

ABSTRACT. Batis maritima, a low-growing perennial species with woody stems and 

succulent leaves, occurs in mangroves and, to a lesser degree, in salt marshes in the 

Neotropics. It spreads by clonal growth, occurs in a wide range of habitats, and at times 

forms monotypic stands. Sites that are permanently fl ooded or are fl ooded regularly by 

tides and salt pans are the only mangrove habitats in which B. maritima does not occur 

or occurs as a few scattered plants. On mangrove-dominated islands in Belize, the coverage and height of B. maritima were highest in open habitats, including sites disturbed by 

human activities. In a mangrove-dominated mosquito impoundment in Florida, B. maritima occurred in all habitats sampled and, similar to observations in Belize, coverage and 

height were greatest in the most open habitats. The abundance and, at times, dominance 

of B. maritima suggests that it may play an important role in the dynamics of mangrove 

ecosystems, especially in the recruitment and establishment of mangrove seedlings. Mangrove seedlings and saplings were present in most of the plots that were sampled in Belize 

and Florida, but there was no relationship between the percent cover of B. maritima and 

the density of seedlings and saplings.

INTRODUCTION

Batis, the only genus in the family Bataceae, has two species. Batis maritima

L. occurs in the Neotropics in coastal salt marshes and mangroves from Georgia 

and Brazil on the Atlantic coast and California to Peru on the Pacifi c Coast of 

North and South America. The species is widely distributed in the Caribbean 

basin. The second species, Batis agrillicola P. Royan, is endemic to coastal areas 

of northern Australia.

Batis maritima, a low-growing C3 perennial species with woody stems and 

succulent leaves, is associated with saline soils and has been described as a species that responds to disturbance in mangroves and salt marshes (Rey et al., 

1990; Pennings and Richards, 1998; Pennings and Callaway, 2000). An important ecophysiological characteristic of B. maritima is the ability to adjust 

photosynthetic rates to increasing soil salinity by making adjustments to leaf sap 

osmolalities (Lüttge et al., 1989). The ability to propagate clonally (Pennings 

and Callaway, 2000) is another characteristic that enables it to respond rapidly 

to altered environmental conditions.

Dennis F. Whigham and Ilka C. Feller, Smithsonian Environmental Research Center, 647 Contees 

Wharf Road, Edgewater, Maryland 21037, USA. 

Michael C. Whigham, Antioch University New 

England (now at University of New Hampshire, 

Natural Resources and Environmental Science, 

Durham, New Hampshire 03824, USA). Wilfrid 

Rodriguez, University of Rhode Island, Kingston, 

Rhode Island 02881, USA. Ryan S. King, Department of Biology, Baylor University, Waco, Texas 

76798, USA. Corresponding author: D. Whigham 

(whighamd@si.edu). Manuscript received 15 August 2008; accepted 20 April 2009.

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492 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Despite its widespread distribution, there have been 

relatively few ecological studies of B. maritima. In Georgia 

salt marshes, Pennings and Richards (1998) found a positive relationship between the presence of wrack (accumulated litter) and the abundance of B. maritima. Pennings 

and Callaway (2000) found that clonal integration was an 

important factor in the ability of the species to colonize 

bare salt pans. The responses of B. maritima to altered 

hydrological conditions appear to vary with differing environmental settings. In hypersaline coastal wetlands in 

Texas, B. maritima cover expanded following inundation 

with freshwater (Alexander and Dunton, 2002). Conversely, the opposite occurred in Baja California (México) 

where its cover increased following the construction of a 

dike that eliminated tidal fl ooding and increased soil salinity (Ibarra-Obando and Poumian-Tapia, 1991). Batis

maritima cover was also dynamic in mangroves in Florida 

that were impounded for mosquito control. The cover of 

all herbaceous halophytic species, including B. maritima, 

decreased following the construction of dikes and the subsequent impoundment and fl ooding of mangroves in the 

Indian River (Rey et al., 1990). Several years later, when 

tidal exchange between the impoundment and estuary 

was restored, B. maritima recolonized areas that were no 

longer fl ooded continuously. Another important ecological feature of B. maritima is its inability to tolerate prolonged periods of shade in mangrove-dominated wetlands 

(López-Portillo and Ezcurra, 1989). Along Florida’s Gulf 

Coast, Milbrandt and Tinsley (2006) observed a greater 

number of black mangrove (Avicennia germinans (L.) 

Stearn) seedlings in existing B. maritima patches compared 

to surrounding mudfl ats. They hypothesized that this improved seedling success was the result of a slight increase 

in elevation provided by the B. maritima root system. In 

contrast, McKee et al. (2007) found that on offshore islands in Belize B. maritima did not appear to have an effect on recruitment of red mangrove (Rhizophora mangle

L.) seedlings.

Other than the experimental research on coastal salt 

marshes (Pennings and Richards, 1998; Pennings and Callaway, 2000), little is known about the ecological role of 

B. maritima in coastal wetlands, especially in mangroves 

where it most frequently occurs. Is it a fugitive species 

that only persists because it is capable of responding to 

changing environmental conditions? Alternatively, is it an 

important species in mangroves because of its impact on 

patterns of nutrient cycling or its ability to infl uence the 

establishment of mangrove trees (i.e., R. mangle, A. germinans, Laguncularia racemosa (L.) Gaertn. f. [white mangrove], Conocarpus erectus L. [buttonwood])? Although 

B. maritima is a common component of mangrove forests 

throughout the Neotropics, there is limited knowledge on 

distribution patterns within the intertidal landscape or on 

the ecological roles of this species across a range of mangrove habitats.

Our objective was to describe the distribution of B. 

maritima in Florida and Belize as part of our overall goal 

to determine its ecological role in mangrove ecosystems. 

Here we describe our initial efforts to characterize the 

ecology of B. maritima at two of the Smithsonian’s longterm research sites (Figure 1) that also represent the range 

of conditions (subtropical and tropical) where this species 

associates with mangroves. For Florida (subtropical), we 

focus on B. maritima in four habitats in a mangrovedominated impoundment along the Indian River Lagoon 

(IRL) that has a history of intervention for purposes of 

mosquito control (Rey et al., 1990). For Belize (tropical), 

we focus on B. maritima in disturbed and undisturbed 

sites on offshore mangrove islands. For both sites, we also 

present data on the relationships between percent cover of 

B. maritima and the density of mangrove seedlings.

STUDY SITES

BELIZE

Twin Cays is the focus of our B. maritima studies 

in Belize. Twin Cays (91.5 ha) is an archipelago of peatbased mangrove islands (Figure 1) located near the crest 

of the barrier reef of central Belize. These islands are located approximately 17 km east of the mainland, and the 

only source of freshwater is precipitation. Vegetation on 

Twin Cays is dominated by the mangroves R. mangle, A. 

germinans, and L. racemosa. The forest structure is heterogeneous and characterized by gradients in hydrology 

and tree height that include a seaward fringe of R. mangle

around the periphery of the islands, along tidal creeks, and 

in perennially fl ooded ponds (Feller et al., 1999). Avicennia germinans and L. racemosa primarily occur in habitats 

that are not water covered at low tide. Vegetation patterns 

on Twin Cays are complex, and the dynamics have been 

the focus of many studies (Feller, 1995; Feller and McKee, 

1999; Rodriguez and Feller, 2004; Lovelock et al., 2006a). 

However, none of the previous research has focused on 

the distribution or ecology of B. maritima even though it 

occurs in almost all habitats except those that do not experience prolonged fl ooding (D. Whigham, personal observation). Human activities have altered parts of Twin Cays 

(Rodriguez and Feller, 2004; McKee et al., 2007), and 

the primary anthropogenic activity has been the clearing 

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NUMBER 38 • 493

FIGURE 1. Approximate locations of SLC24 and Twin Cays (inset map) and IKONOS images of the two study sites. For SLC 24, the white line 

that is seen around the impoundment is a dike. Dark areas within the impoundment are dredged from adjacent subtidal habitats. Darker areas 

on the two large islands are internal tidally infl uenced ponds that are most often shallowly water covered.

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494 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of mangroves with or without the addition of sediments 

dredged from nearby subtidal habitats. In this study, we 

compared the distribution of B. maritima in disturbed and 

undisturbed mangrove habitats at Twin Cays (described in 

further detail below).

FLORIDA

An impounded, mangrove-dominated wetland (SLC 

24) in St. Lucie County in the IRL is the focus of the 

Florida studies (see Figure 1). SLC 24 has been managed 

in a variety of ways since it was diked in 1970. Rey et 

al. (1990) describe management activities and patterns 

of vegetation change in SLC 24 between 1970 and 1987. 

SLC 24 was hydrologically isolated from the IRL by a dike 

(Figure 1) until 1985 when a culvert was installed to remove excess water deposited during two tropical storms. 

Once water levels were lowered, the culvert was sealed, 

and the impoundment remained isolated until 1987 when 

the culvert was reopened and other culverts were installed. 

The cover of all vegetation decreased from 75% to near 

30% following construction of the diked impoundment 

in 1970. Over subsequent years, the cover of herbaceous 

halophytes, including B. maritima, changed in response to 

variations in the timing and duration of fl ooding and the 

establishment and growth of mangroves. Rey et al. (1990) 

concluded that a steady decline in the cover of herbaceous 

halophytes after 1984 was primarily caused by shading 

as the canopies of mangroves developed. Vegetation patterns are also complex in the numerous impoundments 

that have been established in the IRL, and they have been 

the focus of several studies focused primarily on nutrient 

limitation within mangroves (Feller et al., 2003; Lovelock 

and Feller, 2003; Lovelock et al., 2006b). We sampled B. 

maritima in three mangrove-dominated habitats and areas 

associated with salt pans where dwarf A. germinans (sensu 

Feller et al., 2003) occurs as scattered individuals or in 

patches with almost continuous cover. Details of sampling 

locations and methods are given below.

METHODS

BELIZE

We sampled B. maritima in two disturbed sites and six 

undisturbed sites on Twin Cays. One disturbed site is a 2 

ha area on West Island that was cleared of mangroves and 

burned in 1991 and covered with material dredged from 

the adjacent subtidal area in 1995 (Rodriguez and Feller, 

2004; McKee et al., 2007). The other disturbed site was 

clear cut in 2004, but no dredged material was added. In 

both disturbed sites, we sampled B. maritima in 10 randomly located plots (each 1 1 m) in which we made 

visual estimates of its cover, measured its height at fi ve 

randomly chosen locations in each plot, and identifi ed 

and counted all mangrove seedlings and saplings. Seedlings of A. germinans and L. racemosa had cotyledons 

present. Seedlings of R. mangle were individual, with no 

more than one pair of true leaves. Saplings were defi ned 

as individuals less than 50 cm in height with no cotyledons present, or with more than one pair of true leaves in 

the case of R. mangle.

For our undisturbed sites at Twin Cays, we sampled 

B. maritima in three forested habitat types (Fringe, Transition, Interior), which were located at different distances 

from the ecotone between the mangrove forest and open 

water. Fringe habitats, which were dominated by trees 4 to 

5 m tall, were at the outer boundary between mangroves 

and open water, either along ponds located in the interior 

of Twin Cays or along the ocean. Avicennia germinans was 

the dominant tree in the three Fringe habitats adjacent to 

interior ponds. Rhizophora mangle was the dominant tree 

in the three Fringe habitats adjacent to the ocean. Transition and Interior habitats were all dominated by A. germinans. Transition habitats were located approximately 

15 m further into the mangrove forest from the Fringe 

habitats, and Interior habitats were located approximately 

an additional 15 m beyond the Transition habitats. We 

sampled 5 randomly located plots (same procedures as described above) in each of the 90 plots (5 plots 3 habitat 

types 6 sites) in undisturbed mangrove.

FLORIDA

We sampled B. maritima in SLC 24 in four habitat 

types (Fringe  R. mangle, Dense  A. germinans, Sparse 

 A. germinans, Dwarf  A. germinans). The Fringe habitats, dominated by R. mangle 4 to 6 m tall with scattered 

A. germinans, were located at the boundary between mangroves and open water. The two habitats dominated by 

taller (3– 6 m) A. germinans (Dense, Sparse) differed in the 

size and spatial confi guration of the dominant trees. The 

Dense A. germinans habitat had trees that were mostly 4 

to 6 m tall and formed a continuous canopy dominated 

by A. germinans. The Sparse A. germinans habitat was 

also dominated by A. germinans but the trees were usually 

shorter (3– 5 m) and were more widely spaced, resulting 

in a more open canopy. The Dwarf A. germinans habitat 

was always adjacent to salt pans that were mostly unvegetated or only had a few scattered dwarf trees (usually less 

than 1 m tall). We sampled B. maritima in one randomly 

located plot in each of the replicate sites for each habitat 

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NUMBER 38 • 495

type. In each 1 1 m plot, we made the same set of measurements as described above for Belize.

DATA ANALYSIS

Because of the different sampling regimes, we made 

separate statistical comparisons for the Belize and Florida 

data sets. Based on initial screening of the data (Proc Univariate; SAS Institute, 1990), we determined that none of 

the data were normally distributed either in their original 

form or any of the possible transformations. We used the 

nonparametric PROC NPAR1WAY (SAS Institute, 1990) 

to make comparisons of B. maritima data (percent cover, 

height) and the number of mangrove seedlings  saplings 

for the different habitat types at both locations.

RESULTS

BELIZE

Percent cover of B. maritima differed (Figure 2a) 

signifi cantly (df  4, chi-square for Kruskal– Wallis test 

 27.9272, P  0.0001) among the sites on Twin Cays. 

Mean percent cover ranged from 50% to 53% for the two 

disturbed sites and the undisturbed Fringe habitat. Percent 

cover decreased from the Fringe to the Transition ([mean 

 1 SE]  35.5%  4.7%) and Interior (16.9%  2.9%) 

undisturbed sites. The average height of B. maritima also 

differed signifi cantly between sites (Figure 2b; df  4, chisquare for Kruskal– Wallis test  29.0273, P  0.0001). 

Heights were similar at the two disturbed sites (24.4  2.3 

cm  clear-cut  fi ll; 26.4  1.0 cm  clear-cut). At the 

undisturbed sites, height was greatest at the Fringe habitat 

(61.7  18.5 cm) and decreased toward the interior of the 

mangrove forest (40.4  2.2  Transition; 34.7  2.0 

Interior).

The number of mangrove saplings  seedlings also 

differed across sites (Figure 2c), and there were signifi cant 

differences for all three species and for the total of all species (df  4, chi-square for Kruskal– Wallis test  38.9958, 

P  0.0001; 12.5551, P  0.0137; 11.3187, P  0.0232; 

15.5953, P  0.0036 for R. mangle, A. germinans, L. racemosa, and total mangroves, respectively).

The total number of mangrove saplings  seedlings 

was higher at the clear-cut and fi lled site (24.6  13.8 m2) 

compared to the clear-cut site (2.5  0.8 m2) and undisturbed mangrove habitats (mean for all three undisturbed 

sites was 7.3  1.2 m2). Avicennia germinans saplings 

seedlings at the clear-cut and fi lled site were less than 1 m2

(Figure 2c). Rhizophora mangle was the most abundant 

species at the Fringe habitat, whereas A. germinans was 

FIGURE 2. Cover (a), height (b), and sapling  seedling (c) data 

for two disturbed and three undisturbed habitats on Twin Cays 

(Belize). Values are means  1 SE.

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496 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

the most abundant species at the Transition and Interior 

habitats.

FLORIDA

Percent cover (df  3, chi-square for Kruskal– Wallis 

test  38.9252, P  0.0001) and height (df  3, chisquare for Kruskal– Wallis test  33.0923, P  0.0001) 

of B. maritima differed between the four habitat types in 

SLC 24 (Figure 3a). There was no B. maritima in the plots 

that were sampled in the Fringe R. mangle habitat, and 

the cover (2.8%  1.2%) was very low in the Dense A. 

germinans habitat. Percent cover was 42.9  8.1 and 27.8 

 4.6 in the Sparse and Dwarf A. germinans habitats, respectively. Height differences (Figure 3b) among the four 

habitats had the same pattern with the tallest plants occurring in the Sparse A. germinans habitat (48.9  4.5) and 

shortest in the Dense A. germinans habitat (13.1  5.4). 

The total number of saplings  seedlings and the means 

for each mangrove species also differed signifi cantly (Figure 3c) among the four habitat types (df  3, chi-square 

for Kruskal– Wallis test  11.5483, P  0.0091; 12.7678, 

P  0.0052; 16.4377, P  0.0009; 13.4660, P  0.0037 

for R. mangle, A. germinans, L. racemosa, and total mangroves, respectively).

DISCUSSION

The objective of this initial investigation of Batis maritima was to quantify aspects of its distribution in a variety of habitats in mangroves at long-term Smithsonian 

study sites in Belize and Florida. The impetus for the research was the observation that B. maritima is widespread 

in mangroves and, in some habitats, its high abundance 

and cover suggest that it potentially plays an important 

role in these systems. There have, however, been few studies that shed light on its possible ecological importance in 

mangroves. Studies in salt marshes near its northern limit 

found that it was not a dominant species and did not compete well with other marsh plants (Zedler, 1977). There is 

some suggestion that B. maritima may be a fugitive species 

because it is common in disturbed sites (Milbrandt and 

Tinsley, 2006). Pennings and Richards (1998), for example, found that stands of B. maritima were associated with 

areas that were disturbed by wracks of litter in a Georgia 

salt marsh.

Batis maritima has been described as a species that 

does not do well in shaded conditions or under conditions 

of continuous fl ooding (Rey et al., 1990; Alexander and 

Dunton, 2002). However, Keer and Zedler (2002) found 

FIGURE 3. Cover (a), height (b), and sapling  seedling (c) data for 

four habitats in mosquito impoundment SCL 24 in the Indian River 

Lagoon, Florida. Values are means  1 SE.

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NUMBER 38 • 497

that it can tolerate prolonged fl ooding, and it does well in 

waterlogged conditions when light is not limiting (Zedler, 

1980). It also responds positively to increasing salinity 

(Ibarra-Obando and Poumian-Tapia, 1991) but is eliminated under hypersaline conditions (Zedler et al., 1986; 

Dunton et al., 2001).

The only long-term study of B. maritima in changing environmental conditions occurred in one of our 

study sites, SCL 24 in Florida. Rey et al. (1990) examined a sequence of aerial photographs taken over a period 

of time when hydrological conditions varied from years 

when there was continuously fl ooding, to years when the 

impoundment was drained, and to years when there was 

partial tidal exchange with the IRL. Vegetation almost 

completely disappeared when the impoundment was continuously fl ooded. Once the impoundment was opened to 

limited tidal exchange, herbaceous halophytes increased in 

abundance and cover and B. maritima eventually became 

the dominant species. Over time, mangroves recruited and 

eventually dominated the vegetation in most parts of the 

impoundment. As the abundance and size of mangroves 

increased, B. maritima declined along with other herbaceous halophytes in response to increased shading by mangroves (Rey et al., 1990).

Results of our surveys support several of the earlier 

studies and suggest that light levels, regular tidal fl ooding, and soil salinity are three important factors that determine where B. maritima occurs and how abundant it is. 

There have been at least two studies (Pennings and Richards, 1998; Milbrandt and Tinsley, 2006) suggesting that 

B. maritima is a fugitive species that colonizes high-light 

disturbed sites. In Belize, the highest percent cover was at 

the two disturbed sites and the Fringe habitat in the undisturbed mangroves (see Figure 2a). Even though the mean 

cover of B. maritima in the undisturbed sites on Twin Cays 

was lower (34.3%  3.1.9%) than the disturbed sites, the 

highest B. maritima cover (80.3%  2.6%) of any of the 

habitats sampled was in the three Fringe habitats that 

were associated with interior ponds. Edge habitats associated with interior ponds are mostly in full sun and are 

exposed to tidal fl ooding, but the fl ooding is rarely more 

than a few centimeters deep (D. Whigham, personal observations). The substrates are almost always waterlogged, 

and the sediments are soft, mostly composed of fl oc that 

accumulates on the downwind side of the interior ponds. 

The highest B. maritima cover in SLC 24 in Florida also 

occurred at sites that had no overhead mangrove canopy 

or only a discontinuous canopy.

The mean cover of B. maritima was least in the shaded 

habitats in Florida and Belize, supporting the suggestions 

of López-Portillo and Ezcurra (1989) that low light levels 

can limit its abundance and distribution. The absence of 

B. maritima in the sample plots at the Fringe habitat associated with SLC 24 and the lower cover in the Fringe habitats closest to the ocean on Twin Cays (20.9%  2.9%) 

also support the suggestions that regular inundation by 

tidal fl ooding has a negative effect on the species (Alexander and Dunton, 2002).

The mean height of the B. maritima canopy also varied among habitats, and the patterns are most likely the result of variations in light and salinity (Zedler et al., 1986; 

Dunton et al., 2001). In SLC 24, mean height decreased 

from the more open Dwarf and Sparse A. germinans habitats to the shadier Dense A. germinans habitat (Figure 3b). 

At the undisturbed sites in Belize, mean height decreased 

from the Fringe to the Interior, most likely in response to 

decreasing light. The height of the plants was greatest in 

the Fringe habitat associated with the Edge sites that were 

closest to the Interior ponds. Mean height at the Fringe 

habitats associated with the ponds was 85.4  27.1 cm 

compared to 40.4  2.2 at the more shaded Fringe habitats 

closest to the ocean. Taller average height associated with 

the Edge habitats may be the result of higher phosphorus 

concentrations in the sediments. In a separate fertilization 

experiment, we found that B. maritima responded signifi -

cantly to the addition of phosphorus at all the undisturbed 

sites on Twin Cays, but the smallest response was at the 

Edge habitat associated with interior ponds, suggesting 

that phosphorus was more available in those sediments 

(D. Whigham, unpublished data). Compared to the Fringe 

habitats on Twin Cays and the Sparse A. germinans habitat 

in the SLC 24, mean height decreased toward the sites with 

no mangrove canopy (Dwarf A. germinans habitat in SLC 

24 and the two disturbed sites at Twin Cays). Lower mean 

height at the open sites is likely the result of increased salinity as the Dwarf A. germinans site in SLC 24 is hypersaline 

(i.e., soil salinity as high as 100‰; D. Whigham unpublished data). In addition, soil salinity at the clear-cut and 

fi lled site on Twin Cays, while variable during an annual 

cycle, can be more than 60‰ (McKee et al., 2007).

Mangrove seedlings are widely dispersed, and their occurrence varies spatially in response to light levels and their 

ability to withstand fl ooding, salinity, and attacks from 

herbivores (Ellison and Farnsworth, 1993; Olusegun and 

Creese, 1997). If B. maritima facilitates the establishment 

of mangrove seedlings, we would expect a positive relationship between percent cover and the number of seedlings  saplings for one or more of the mangrove species. 

Milbrandt and Tinsley (2006) found that the presence of 

B. maritima had a positive effect on the survival of A. germinans seedlings. McKee et al. (2007), however, found that 

B. maritima had no effect on the recruitment and survival 

38_Whigham_491-500_Lang.indd 497 8_Whigham_491-500_Lang.indd 497 9/24/09 10:19/24/09 10:19
498 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of mangrove seedlings, even though mangrove seedlings 

benefi ted by the presence of other herbaceous species (i.e., 

Distichlis spicata, Sesuvium portulacastrum) at clear-cut 

and fi lled sites sampled in this study. Although there were 

habitat differences in the number of seedlings saplings, 

the presence of seedlings saplings in 88% of the plots 

sampled in Belize and 55% of the plots in Florida indicated that mangrove establishment may have been facilitated by B. maritima. We found no relationship, however, 

between the amount of B. maritima cover and the density 

of seedlings saplings for any of the mangrove species 

(Figure 4). The potential for B. maritima to infl uence the 

distribution and growth of mangroves trees and other 

mangrove plants and animals remains unknown. But, 

given the abundance of the species across a range of habitats, the potential seems high, especially in areas where it 

is the dominant species.

In summary, B. maritima was widespread in most 

mangrove habitats at both our study locations, and there 

were signifi cant interhabitat differences in all the variables 

measured. Mangrove seedlings and saplings were common in areas occupied by B. maritima, but we found no 

evidence that the establishment of mangroves benefi ted 

by increasing cover of this common halophytic species. 

The ubiquitous distribution of B. maritima at all the sites 

sampled, however, indicates that its role in mangrove ecosystems deserves further consideration.

ACKNOWLEDGMENTS

The research was supported by the Smithsonian Marine Science Network. We acknowledge logistical support 

of the station staff at Carrie Bow Cay (Belize) and the 

Smithsonian Marine Station at Ft. Pierce (Florida). Brian 

Miller, project volunteer, assisted with fi eldwork on Twin 

Cays in 2004. This is contribution number 853 of the Caribbean Coral Reef Ecosystems Program (CCRE), Smithsonian Institution, supported in part by the Hunterdon 

Oceanographic Research Fund.

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38_Whigham_491-500_Lang.indd 500 8_Whigham_491-500_Lang.indd 500 9/24/09 10:19

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Sponge Community Dynamics 

on Caribbean Mangrove Roots: 

Signifi cance of Species Idiosyncrasies

Janie L. Wulff

ABSTRACT. Descriptions of the rich sponge faunas inhabiting mangrove roots at various 

Caribbean sites are unanimous in pointing out the heterogeneity of species distribution 

and abundance patterns at all scales, from different portions of a single root to geographic 

subregions. Abiotic factors have often been implicated by correlation, but ecological interactions, and the life history and morphological characteristics of the sponge species, 

may also play key roles. Published studies vary widely in methods used, hampering direct 

comparisons of results, and raising the possibility that conclusions might be infl uenced 

by methods. I have been exploring the processes underlying distribution and abundance 

patterns by applying identical methods to studying community composition and dynamics at two sites in Belize (Twin Cays) and one site in Panama (Bocas del Toro). Established 

communities on roots have been fully censused, by volume and numbers of individuals, 

yearly for three years (i.e., four censuses). Community composition, when evaluated in 

terms of total volume of component species, is very similar at these three sites, although 

abiotic factors differ and geographic distances between sites range from 330 m to 1,200 

km. The nine species found on censused roots at all three sites constituted a total of 89%, 

84%, and 73%, respectively, of the total sponge volume at these sites. In general, species 

exhibited similar patterns of growth, size decrease, and mortality at all sites where they 

were found, suggesting that these are species-level characteristics. Numbers of individuals and volume provide very different assessments of the relative importance of different 

species in these communities. Community change over time appeared to be substantial, 

when measured in terms of shifts in total numbers of individuals or total sponge volume. 

However, taking into account dynamics of individual species provides a very different 

view, as most large changes in numbers or volume were not community wide but tended 

to refl ect life history characteristics typical of early successional stage species or idiosyncratic responses of one or a few species to particular environmental circumstances.

INTRODUCTION

Organisms that live in habitats consisting of discrete patches within an uninhabitable matrix have fascinated biologists who are simultaneously attracted to 

community ecology and to life history evolution. A rich set of conceptual frameworks has developed to explain the dynamics of community assembly and development within each patch in the context of interconnections among patches. 

Theories of, for example, island biogeography (MacArthur and Wilson, 1967), 

multiple stable points (Sutherland, 1974), competitive networks (Jackson and 

Janie L. Wulff, Department of Biological Science, Florida State University, Tallahassee, Florida 

32306-4295, USA (wulff@bio.fsu.edu). Manuscript 

received 29 August 2008; accepted 20 April 2009.

39_Wulff_501-514_Lang.indd 501 9_Wulff_501-514_Lang.indd 501 9/24/09 10:01/24/09 10:01
502 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Buss, 1975), the intermediate disturbance hypothesis (e.g., 

Connell, 1978), and meta-communities (e.g., Mouquet 

and Loreau, 2002) have helped us understand community 

dynamics in patchy habitats ranging from oceanic islands 

and tropical mountaintops to badger mounds, holes in 

mussel beds, and ponds.

Prop roots of Caribbean red mangrove (Rhizophora 

mangle) trees are easily accessible, experimentally tractable, and extraordinarily colorful examples of inherently 

patchy communities. The sessile inhabitants that cover the 

root surfaces colonize in the form of water-borne propagules, and most of them are thereafter confi ned to the root 

on which they landed. Although post-recruitment interactions with neighbors and consumers may have relatively 

deterministic outcomes, a stochastic element, contributed 

by the uncertainty that any particular species will land on 

a particular root, is ever present. Throughout the wider 

Caribbean region sponges are prominent members of the 

prop root communities, and their abundance and diversity of species, color, and forms have inspired time-series 

monitoring and experimental manipulations as well as 

comparative faunal studies (e.g., Sutherland, 1980; Ellison and Farnsworth, 1992; Bingham and Young, 1995; 

Rützler, 1995; Farnsworth and Ellison, 1996; Rützler and 

Feller, 1996; Rützler et al., 2000; Diaz et al., 2004; Diaz, 

2005; Wulff, 2000, 2004, 2005; Engel and Pawlik, 2005). 

Specifi c conclusions relating to how dynamic these sponge 

communities are, and what processes drive the dynamics 

and infl uence distribution and abundance patterns, have 

differed widely among studies, but a consistent theme is 

that the resulting distribution and abundance patterns are 

highly heterogeneous on scales ranging from within individual roots to between geographic subregions.

Sutherland (1980) complemented repeated monitoring of natural communities on prop roots with a study 

of community development on fl at settlement panels suspended among the roots in Venezuela. He concluded that 

these sponge-dominated communities are relatively stable 

over time, and that high diversity could be maintained 

by a trade-off between competitive ability and colonization effi ciency, combined with the continued addition of 

fresh roots that provide refuges for inferior competitors. 

Farnsworth and Ellison (1996) surveyed prop root communities of mangroves in a variety of abiotic settings in 

Belize, focusing on spatial scales of distribution patterns. 

They were able to identify scales of heterogeneity that included backs versus fronts of individual roots, leeward 

versus windward shores, and coastal versus island mangal. At the 11 sites where they sampled twice, their data 

corroborated Sutherland’s (1980) conclusions that community change is minimal. Bingham and Young (1995) 

concluded very differently, from their work in the Florida 

Keys, that dynamics of sponges on mangrove roots can 

be extreme, infl uenced by perturbations from physical 

disturbance, predators, and asexual recruitment. They attributed differences in community dynamics between sites 

in the Florida Keys and Venezuela to differences in seasonality (subtropical versus tropical) and abiotic stressors, 

and suggested that the differences between their study and 

Sutherland’s (1980) study could be explained by equilibrium versus non-equilibrium situations, with the Venezuelan mangrove communities primarily structured by competitive interactions.

Disentangling the effects of biogeography and different suites of abiotic factors by making direct comparisons 

among studies is hampered by the wide variety of approaches that have been applied. Published studies differ 

with respect to units of study, time course and frequency 

of monitoring, and metrics for evaluating abundance. To 

control for technique, I used identical methods to evaluate 

sponge community composition and dynamics for three 

years on mangrove prop roots at three sites in Belize and 

Panama. Following the fates of individual sponges was a 

priority, because my chief interest was in how the morphological and life history strategies of the different sponge 

species constrain or enhance their ability to coexist on the 

prop roots. Rather than focusing on community-level metrics, such as species diversity or primary space occupancy, 

I recorded survival and changes in volume of the same individuals over time and attempted to identify the causes of 

size decrease, fragmentation, or mortality. Two sites near 

each other in Belize differed in abiotic conditions, and a site 

in Panama provided a geographic comparison. My goals 

included (1) assessing the similarity of species composition 

among sites differing in abiotic factors and geographic distance, (2) comparing community dynamics among sites, 

with respect to both numbers of individuals and volume, 

and (3) exploring the possibility that each mangrove sponge 

species adheres to a characteristic approach for maintaining its representation in this community, regardless of the 

specifi c abiotic context and other species present.

METHODS

Three sites characterized by well-developed mangrove 

prop root epiphytic communities were chosen for yearly 

censuses. The three sites were chosen primarily because 

experiments had been established at each several years before, and so regular visits were already required for moni39_Wulff_501-514_Lang.indd 502 9_Wulff_501-514_Lang.indd 502 9/24/09 10:01

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NUMBER 38 • 503

toring. Top priorities in initial site choice had been easy 

access and suffi cient sponge individuals for experimental 

manipulations; species composition was secondary. The 

two Belize sites, both at Twin Cays, near the Smithsonian Institution’s Carrie Bow Cay research station (map 

and further site descriptions in Rützler et al., 2004; Diaz 

et al., 2004), allow comparison of a main channel versus 

a tidal creek near each other (330 m). The Panama site, 

directly across the channel from the Smithsonian Tropical Research Institute marine laboratory on Isla Colon in 

Bocas del Toro (map coordinates and description of the 

overall area are found in Diaz, 2005), adds a geographic 

comparison (1,200 km distant) between two main channel sites. The submerged portions of the prop roots (i.e., 

the portion on which sponges could grow) were from 24 

to 143 cm long, with the majority between 40 and 80 cm 

in length.

At each site, mangrove roots or root clusters were 

chosen that appeared to be healthy (i.e., no signs of rot 

or incipient breakage) and on which it was possible to 

identify and measure all sponges on all sides of each root. 

Root clusters were added to the initial census at each 

site until species accumulation curves had leveled off for 

sponges, and at least 163 sponge individuals (the number of sponges in the fi rst census at the fi rst site) were included: a total of 10 clusters, 1 to 5 roots each (24 roots 

initially) at Hidden Creek; 13 clusters, 1 to 4 roots each 

(37 roots initially), at Sponge Haven; and 15 clusters, 1 to 

3 roots each (42 roots initially), at the Bocas del Toro site. 

Roots were labeled with small plastic tags, coded by color 

and shape, on narrow (1 mm) beaded nylon cable ties. Full 

censuses were made at approximately 1 year intervals, for 

a total of 3 years (i.e., four censuses at each site, except for 

Bocas del Toro, where the 2nd year census was skipped), 

beginning in March 2004 at both Belize sites and in June 

2003 at the Panama site. At each census, every root or 

root cluster was drawn and root lengths measured. Every 

sponge was drawn to scale, in place on the root drawings, and suffi cient dimensions measured to accurately 

estimate volume by conglomerations of appropriate geometric solids. In this way, every sponge could be followed 

for survival, growth, decrease in size, and fragmentation. 

New recruits were added to the root maps as they were 

discovered (recruitment data will be reported in a separate publication), and notes were made on interactions between neighboring sponges and other sessile organisms, as 

well as damage caused by physical disturbance, predation, 

and disease. Some roots at each site were lost by breakage 

during the 3 years. To be able to interpret the time-series 

data clearly, only roots for which at least some portion 

persisted throughout the study were included in the timeseries data analysis, and the only roots added to the study 

were those that branched directly off subtidal portions of 

the originally censused roots.

RESULTS

SPECIES COMPOSITION AND RELATIVE ABUNDANCE, 

BY VOLUME AND NUMBER OF INDIVIDUALS

A total of 21 sponge species were represented by at 

least 0.1% of the total sponge volume on censused roots at 

one or more sites (Table 1). These species represent the demosponge orders Poecilosclerida (8 species), Haplosclerida 

(6 species), Halichondrida (4 species), and Dictyoceratida 

(3 species), in a variety of colors, and with growth forms 

ranging from thinly encrusting to irregularly branching to 

clusters of volcanoes (Figure 1). Of these most abundant 

21 species, 9 were found on censused roots at all three 

sites, and another 6 were found on censused roots at two 

of the three sites (Figure 2). Many of the sponge species 

are relatively rare, and so were present at a site but not on 

a censused root. Adding three cases in which species were 

found at a second or third site on roots directly adjacent to 

at least one censused root increases the number of species 

shared by all three sites to 10, with an additional 7 species shared by two of the three sites. Geographic distance 

was not a strong predictor of the percent of species shared. 

Sponge Haven and Hidden Creek, only 330 m apart, shared 

74% (14/19) of their most common species, and Sponge 

Haven and Bocas del Toro, 1,200 km apart, shared 60% 

(12/20) of their most common species (comparisons not 

signifi cantly different by the G test: 0.1 P 0.5). The 

Hidden Creek and Bocas sites, geographically distant from 

each other and also differing in abiotic factors, shared 55% 

(11/20) of their most common species (comparison with 

the proportion of species shared by Hidden Creek– Sponge 

Haven by the G test: 0.05 P 0.1).

Census data from all years at each site were added 

together for an average relative representation of species, 

with respect to both volume and number of individuals (Figure 3). At all three sites the most abundant species by volume, Tedania ignis, accounted for about half 

(49%– 57%) of the total sponge volume. The nine species 

found on censused roots at all three sites contributed a 

total of 89%, 84%, and 73% of the total volume at, respectively, Hidden Creek (HC), Sponge Haven (SH), and 

Bocas del Toro (BT). Similarity of species representation 

at these sites is also borne out by Morisita’s index of community similarity (using volume as abundance measure), 

39_Wulff_501-514_Lang.indd 503 9_Wulff_501-514_Lang.indd 503 9/24/09 10:01/24/09 10:01
504 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

with similarities of HC– SH  0.977, SH– BT  0.971, and 

HC– BT  0.957. These index values are strongly infl uenced by the similar dominance of T. ignis at all three sites, 

but other species were also consistently either relatively 

abundant or rare at all sites. When sponge species at each 

site are divided into those that rank in the top half by volume versus those that rank in the bottom half, pairwise 

comparisons between sites (see data in Table 1) yield 23 

site pairs in which a species was ranked in either the top 

half or bottom half at both sites and only 7 pairs in which 

a species was ranked in the top half at one site and in the 

bottom half at the other site (signifi cantly different from 

an even distribution by the G test at P 0.005).

At each site species were present on censused roots 

that were represented by volumes of less than 0.1% of 

the total. Among these species were Scopalina ruetzleri

(Wiedenmayer, 1977) at Hidden Creek, Clathrina coriacea

(Montagu, 1818) at Hidden Creek and Sponge Haven, and 

Mycale magnirhaphidifera (van Soest, 1984) at Sponge 

Haven; and Hyrtios violaceus (Duchassaing and Michelotti, 1864), Haliclona vansoesti (de Weerdt, de Kluijver, 

and Gomez, 1999), Haliclona caerulea (Hechtel, 1965), 

and Tethya actinia (de Laubenfels, 1950), all at Bocas del 

Toro, as well as several as yet unidentifi ed species.

In general, number of individuals and total volume 

provide very different views of the relative importance 

of the species in these communities (see Figure 3). This 

discrepancy is strikingly illustrated by the high representation by numbers of individuals of Haliclona manglaris

(15.2%, 27.9%, and 50.1% at HC, SH, and BT, respectively), which also consistently contributed minimal volume (0.06%, 0.08%, and 0.37%). By contrast, Tedania 

ignis, which contributed half the volume at each site, contributed only 8.4% to 20.4% of the individuals.

TABLE 1. Sponge species on censused roots at Hidden Creek and Sponge Haven, both at Twin Cays, Belize; and at Isla Colon, Bocas 

del Toro, Panama. A total of 21 sponge species were represented by at least 0.1% of the total sponge volume on censused roots at one 

or more sites. Species that rank in the top half of the species on censused roots at a site, with respect to volume, are indicated by “XX”, 

and those that rank in the bottom half are indicated by “X”. Species that occurred on censused roots at one site but were only seen on 

a root or roots directly adjacent to at least one censused root at another site are indicated by “x”. A dash (– ) indicates species was not 

found at a site.

Location

Sponge taxon Hidden Creek Sponge Haven Bocas del Toro

Order Dictyoceratida 

 Dysidea etheria de Laubenfels, 1936 X x X

 Spongia tubulifera Lamarck, 1814, and S. obscura Hyatt, 1877 XX XX XX

Order Halichondrida 

 Amorphinopsis sp. XX –– 

 Halichondria magniconulosa Hechtel, 1965 XX XX XX

 Halichondria sp. –XX – 

 Scopalina ruetzleri (Wiedenmayer, 1977) X x – 

Order Haplosclerida 

 Chalinula molitba (de Laubenfels, 1949) XX – X

 Haliclona curacaoensis (van Soest, 1980) X X – 

 Haliclona implexiformis (Hechtel, 1965) XX X X

 Haliclona manglaris Alcolado, 1984 X X X

 Haliclona sp. a X x – 

 Haliclona sp. b ––XX

Order Poecilosclerida 

 Biemna caribea Pulitzer-Finali, 1986 XX X X

 Clathria campecheae Hooper, 1996 X X – 

 Clathria schoenus (de Laubenfels, 1936) ––XX

 Clathria venosa (Alcolado, 1984) X X X

 Lissodendoryx isodictyalis (Carter, 1882) XX XX X

 Mycale microsigmatosa Arndt, 1927 –XX XX

 Tedania ignis (Duchassaing and Michelotti, 1864) XX XX XX

 Tedania klausi Wulff, 2006 –XX XX

39_Wulff_501-514_Lang.indd 504 9_Wulff_501-514_Lang.indd 504 9/24/09 10:01/24/09 10:01
FIGURE 1. Photographs of some of the most common sponge species inhabiting mangrove prop roots at Hidden Creek and Sponge Haven, 

Twin Cays, Belize, and across the channel from the STRI Bocas del Toro Marine Station, Isla Colon, Panama. Top row, from left to right: 

Clathria venosa, Haliclona curacaoensis, Haliclona manglaris (turquoise) and Haliclona sp. b (purple), Dysidea etheria (ethereal blue). Second 

row: Chalinula molitba, Mycale microsigmatosa, Biemna caribea, Tedania ignis (three individuals). Third row: Lissodendoryx isodictyalis, 

Tedania klausi, Haliclona sp. a. Bottom row, from left: Halichondria magniconulosa, Haliclona implexiformis (purple). Authors of species are 

given in Table 1.

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506 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Mean density of numbers of sponge individuals per 

unit length of subtidal prop root was similar for all three 

sites (15, 11, and 15 individuals per meter length of root 

for Hidden Creek, Sponge Haven, and Bocas del Toro, respectively). Refl ecting a relative preponderance of small 

individuals at the Bocas del Toro site, sponge density measured as volume per unit length of subtidal prop root was 

only 5.7 cm3/cm at Bocas, compared with 20.8 cm3/cm 

at Hidden Creek and 15.7 cm3/cm at Sponge Haven. Although variation in root diameter renders root length imprecise as a measure of substratum area monitored, length 

was deemed a better measure than number of roots because of the sixfold variation in root lengths (i.e., from 24 

to 143 cm).

SPONGE COMMUNITY DYNAMICS COMPARED WITHIN AND

BETWEEN SITES, BY VOLUME AND NUMBER OF INDIVIDUALS

During the three years of monitoring, the largest difference between the highest and lowest total sponge volume was 12%, 35%, and 27% at, respectively, Hidden 

Creek, Sponge Haven, and Bocas del Toro; and the largest difference between the highest and lowest number of 

sponge individuals was 50%, 34%, and 39%, respectively 

(Figure 4). Based on these total abundance values, community-wide change appears to be substantial. However, 

comparison over time of abundance of individual species, 

with respect to both volume and numbers of sponge individuals, sheds light on the components of change and 

provides a very different picture. In many cases, large 

overall changes in total volume or numbers in the course 

of a particular year refl ect changes in just one or a few 

species. For example, the drop in total sponge volume between 2005 and 2006 at Sponge Haven (see Figure 4) was 

mostly caused by losses from Halichondria sp., Halichondria magniconulosa (almost to the point of elimination), 

FIGURE 2. Diagram showing sponge species shared among two sites 

in Belize (Hidden Creek and Sponge Haven) and one site in Panama 

(Bocas del Toro). Only the 21 species that each constituted at least 

0.1% of the total sponge volume on censused roots at a minimum of 

one of the three sites are included.

FIGURE 3. Sponge species assemblage composition, with respect to 

total volume contributed by each species, and with respect to the total number of individuals of each species, on mangrove prop roots at 

three Caribbean sites. These average relative abundances were calculated by adding together the volume or numbers of individuals for all 

four yearly census dates (three dates in the case of Bocas del Toro). 

See Table 1 for complete spelling of species names.

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NUMBER 38 • 507

FIGURE 4. Community dynamics for sponges on mangrove prop roots at three Caribbean sites. Relative abundance of the species is represented 

by both total volume and total numbers of individuals. See Table 1 for complete spelling of species names.

39_Wulff_501-514_Lang.indd 507 9_Wulff_501-514_Lang.indd 507 9/24/09 10:02/24/09 10:02
508 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

and T. ignis. For the second and third species these losses 

primarily consisted of size decreases and fragmentations 

of sponges that were subsequently able to regenerate; and 

thus for both of these species, abrupt and dramatic changes 

in volume between the second and third censuses are not 

refl ected in tandem changes in numbers of individuals 

(e.g., H. magniconulosa was represented by 12 individuals 

of total volume 5,518 cm3 in 2005, 14 individuals of total 

volume 187 cm3 in 2006, and 9 individuals of total volume 225 cm3 in 2007). Large differences in maximum size 

achieved by sponges of different species further promote 

asynchronous changes in overall volume and numbers of 

individuals. For example, during this same year in which 

total sponge volume at Sponge Haven decreased by 35%, 

the number of individual sponges there increased by 13%, 

largely the result of a doubling of the number of Haliclona 

manglaris individuals. Yet each H. manglaris individual is 

so small that, even in the aggregate, they scarcely register 

in the overall volume tally (0.2% for the June 2006 census; see Figure 4).

Similarly, progressive loss of individuals of Biemna 

caribea and Haliclona curacaoensis at Hidden Creek resulted in decreases in total numbers of individuals by more 

than half in the course of three years (Figure 5). If these 

species are removed from the “Hidden Creek census –Individuals” graph in Figure 4 (along with the very small 

bodied H. manglaris), the community can be seen to otherwise remain very similar throughout the three years with 

respect to relative representation of the component species 

by numbers of individuals. During this same time period, 

the total volume of all sponges at this site remained very 

similar, although there were large volume changes for individual species (see Figure 4). The Sponge Haven data show 

the same pattern of progressive loss of H. curacaoensis

(see Figure 5) and also B. caribea, although the latter species was not as abundant to begin with at this site.

Not all changes in abundance of particular species 

were abrupt or negative. Volume of Spongia spp. steadily 

increased at all sites (see Figure 5), with little increase in 

numbers, refl ecting high survival of the individuals that 

were present at the fi rst census. Illustrating a third pattern 

of dynamics, the volume of T. ignis fl uctuated at all three 

sites, but at the end of the three years the total volume of 

this species at each site was similar to what it was at the 

start of the study (Figure 5).

Portions of many roots were lost during the three 

years of the study, but new roots sprouting from subtidal 

portions of censused roots nearly balanced the losses during some time periods. Thus the total length of prop roots 

FIGURE 5. Representative population dynamics graphs for three 

sponge species inhabiting mangrove prop roots at sites where yearly 

censuses were made (HC  Hidden Creek; SH  Sponge Haven; 

BC  Bocas del Toro). Total volume of Spongia spp. consistently 

increased between monitoring periods at all three sites; volume of 

Haliclona curacaoensis decreased between monitoring periods at 

both sites in which it was found; Tedania ignis total volume fl uctuated over time but ended up very similar to what it had been at all 

three sites at the start of the study three years earlier.

39_Wulff_501-514_Lang.indd 508 9_Wulff_501-514_Lang.indd 508 9/24/09 10:02/24/09 10:02
NUMBER 38 • 509

included in the census was very similar for the fi rst three 

censuses at Hidden Creek, and for the fi rst two censuses 

at Bocas del Toro and Sponge Haven, and then, after a 

decrease, also for the fi nal two censuses at Sponge Haven. 

Total length (in cm) for the four censuses at Hidden Creek 

was 968, 896, 995, and 562; for Sponge Haven, 1,847, 

1,787, 1,162, and 1,179; and for Bocas del Toro, 1,483, 

1,583, and (after two years) 1,203. Substratum available 

was not necessarily related to sponge abundance with 

respect to either numbers of individuals or total volume 

(compare abundance measures reported in Figure 4 with 

total root lengths censused); for example, sponge volume 

and total root length were inversely associated over the 

three years at the Bocas del Toro site.

VARIATION AMONG SPONGE SPECIES

 IN INDIVIDUAL PERSISTENCE

Because individual sponges were mapped and measured, their fates from one census to the next could be 

recorded as (a) increased in size, (b) fragmented, (c) decreased in size, or (d) disappeared. To characterize each 

species at each site independently of environmental circumstances during a particular time interval, data from all 

1 year intervals between censuses (and one 2 year interval 

in the case of the Bocas del Toro site) were added together 

in Figure 6. Three patterns emerge from these graphs. First, 

fragmentation and size decrease are important aspects of 

persistence for many of these species. The only species represented entirely by individuals that increased in size or 

vanished (i.e., none decreased in size or fragmented) between censuses were Spongia spp. and Amorphinopsis sp. 

Second, at each site variation among species in the degree 

to which individuals persisted was clear. Yearly rates of 

loss ranged from 0% (e.g., Spongia spp.) to 100% (e.g., 

Chalinula molitba). Third, many species exhibited the 

same characteristics at each site where they occurred. For 

example, a set of species characterized by at least 40% of 

the individuals increasing in size from one yearly census to 

the next were evident at each site: Tedania ignis, Haliclona 

implexiformis, Spongia spp., Lissodendoryx isodictyalis, 

and Halichondria magniconulosa. The only exceptions 

were Haliclona implexiformis in Bocas del Toro and Halichondria magniconulosa at Sponge Haven. The reason for 

the H. implexiformis difference at the Bocas site was not 

obvious, but individuals of this species were always very 

small there. At Sponge Haven, both H. magniconulosa

and T. ignis suffered high rates of size decrease and fragmentation between the second and third censuses. These 

FIGURE 6. Proportions of sponge individuals of each species that increased in volume, fragmented, decreased in volume, or disappeared 

entirely between yearly census dates at three Caribbean mangrove 

sites. Although the fate of each individual was recorded in a single 

category at the time of observation, the distinction between “fragmented” and “decreased” can be fuzzy, as it depends on whether or 

not fragments generated survive until the time of observation. See 

Table 1 for complete spelling of species names.

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510 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

departures from their usual pattern (i.e., most individuals 

increasing in size during a year) coincided with the unusual and fl eeting presence of a couple of French angelfi sh 

just before the third census. French angelfi sh have been 

demonstrated to readily consume these two species (Wulff, 

2005) and Halichondria sp. (in preparation), which also 

decreased in volume during the same time interval. Species that only occurred at two sites also exhibited similar 

characteristics with respect to persistence at both sites. For 

example, no Chalinula molitba individuals increased in size 

from year to year at either Hidden Creek or Bocas del Toro, 

and Haliclona curacaoensis, H. manglaris, and Biemna caribea had consistently low survival at each site. In contrast, 

Tedania klausi survived well at Sponge Haven, but suffered 

an extreme decline on censused roots at the Bocas del Toro 

site, coinciding with observed high losses of only this species throughout the site to disease (Wulff, 2006).

DISCUSSION

COMMUNITY COMPOSITION

These three sites that differ in abiotic factors and in 

geographic distance from each other have very similar 

species compositions, not only with respect to species 

present but also with respect to their relative abundance. 

The 9 species that are shared by all three sites constituted 

89%, 84%, and 73% of the total sponge volume at, respectively, Hidden Creek, Sponge Haven, and Bocas del 

Toro. The ubiquity and consistent local dominance of the 

fi re sponge Tedania ignis contributes heavily to similarity among these sites. Previous studies also concur that T. 

ignis is a signature species for this ecosystem throughout 

the wider Caribbean region, and it was the sole species, 

of 23, that was recorded in all eight prop root faunal surveys compiled by Wulff (2000) and in four of fi ve of the 

studies compared by Diaz et al. (2004). Not only does it 

occur at most sites, it tends to be among the most abundant species by any metric. At fi ve sites in Belize (including Hidden Creek and Sponge Haven), Diaz et al. (2004) 

recorded T. ignis as present on 11% to 34% of the roots, 

in the top 3 species ranked by frequency of occurrence. 

By measuring area covered from photographs, Bingham 

and Young (1995) estimated that 16.7% of the root area 

at their Florida Keys site was covered by T. ignis. Using 

line transects, along which the length of root covered by 

each sponge was measured, Sutherland (1980) estimated 

5%– 12% coverage by T. ignis in Bahía de Buche, Venezuela. Evaluating abundance by volume boosts the proportional representation of this species because of its massive 

growth form, and thus in this study T. ignis constituted 

from 49% to 57% of the total sponge volume on censused 

roots. This species not only holds a large proportion of 

the primary substratum space, but it also participates in a 

mutualism with the mangroves, enhancing the persistence 

and health of the entire ecosystem by protecting the roots 

from attacks by boring isopods (Ellison and Farnsworth, 

1990; Ellison et al., 1996).

Tedania ignis is not the only species that is both nearly 

ubiquitous and locally abundant, although it stands out as 

the most extreme. Consistently Lissodendoryx isodictyalis, Halichondria magniconulosa, Spongia spp., Haliclona 

implexiformis, Haliclona manglaris, and Dysidea etheria

appear on faunal lists and, where authors indicate relative 

abundance, by whatever metric, they rank highly (Wulff, 

2000; Diaz et al., 2004).

Although the three sites in this study are similar with 

respect to these widespread typical mangrove root sponge 

species, there are two types of differences among the sites: 

(1) a few species that are abundant at one site but do not 

occur elsewhere (e.g., Amorphinopsis sp. at Hidden Creek), 

and (2) many rare species that appear to differ among sites. 

The virtual lack of overlap of these rarer species on species lists from different sites does not necessarily indicate 

constrained distribution but may simply refl ect their rareness. Diaz et al. (2004) discuss this sampling issue with 

the highly diverse Caribbean mangrove root sponge fauna 

and illustrate it well with their data. Diaz et al. (2004) 

also point out the great degree to which community composition can vary along a particular mangrove fringe. The 

three sites in the present study are known to share additional sponge species if entire contiguous stretches of mangrove are included (Rützler et al., 2000). For example, at 

Sponge Haven, Clathria schoenus is not found near the 

censused roots but appears on roots at this site that are 

further toward the mouth of the main channel.

Sponge species composition differences among sites 

characterized by very different abiotic circumstances have 

been well documented, and some sites are suffi ciently extreme in abiotic factors that sponges are scarcely present 

(Farnsworth and Ellison, 1996) or succumbed to unfavorable conditions while being studied (Pawlik et al., 2007). 

At least some of the differences in species composition 

between Hidden Creek and Sponge Haven, only 330 m 

apart, have already been ascribed to less hospitable abiotic 

factors in the narrow, tidal Hidden Creek. Transplants of 

5 species that are conspicuous at Sponge Haven thrived 

initially in Hidden Creek, but nearly all (61/63) died over 

the course of one year (Wulff, 2004), possibly implicating 

episodically wide fl uctuations in temperature and salinity. 

39_Wulff_501-514_Lang.indd 510 9_Wulff_501-514_Lang.indd 510 9/24/09 10:03/24/09 10:03
NUMBER 38 • 511

The similarity between the three sites in this study is especially interesting, considering that they were chosen for accessibility and overall sponge abundance, rather than for 

species composition, and that they have demonstrated differences in abiotic factors and span a geographic distance 

of 1,200 km.

METHODS FOR STUDYING SPONGES ON MANGROVE

PROP ROOTS CAN INFLUENCE EVALUATIONS 

OF COMMUNITY SIMILARITY BETWEEN SITES 

AND COMMUNITY STABILITY OVER TIME

Methods of studying composition and dynamics of 

sponge communities on mangrove roots have varied with 

respect to metrics for evaluating abundance, sampling unit, 

choice of which units to sample, time interval of sampling, 

and materials, size, and shape of recruitment surfaces. 

This variety refl ects the many different questions posed by 

researchers, and the diffi culty of quantifying sponges; but 

methods may also infl uence conclusions.

Methods for evaluating abundance have included 

analysis of photographs for percent cover, line transects 

down roots with distance covered by each species recorded, 

point counts through acetate sheets, and presence/absence 

on each root, as well as the total numbers of individuals 

and volume of each individual. The advantages and disadvantages of evaluating sponge abundance with respect 

to volume, area covered, or numbers of individuals have 

been previously compared in the context of coral reefs 

(Rützler, 1978; Wulff, 2000, 2001). Choice of metric is 

infl uenced by expediency in the fi eld, and also by whether 

functional roles, life histories, species diversity, or some 

other aspect of these communities is the central focus of 

a study. One advantage to measuring sponge abundance 

by volume is that growth rates can then be calculated if 

the same sponge individuals are followed over time. As 

well, functional roles related to trophic interactions, such 

as fi ltering food particles from the water column and provision of food to spongivores, probably scale with volume. 

Unfortunately, sponge volume is time consuming to measure nondestructively in the fi eld, decreasing the number 

of individuals that can be monitored.

Area can be a problematic measure of sponge abundance, as the amount of sponge tissue under a particular 

point can range over orders of magnitude. At these three 

sites, for example, sponges on prop roots varied in thickness 150 fold, from 0.1 to 15 cm. Evaluating mangrove 

sponge abundance in terms of area is further complicated 

by the prevalence of epizooism, which results in points 

falling simultaneously over more than one sponge species. 

At least one functional role of sponges in mangroves may 

be related to substratum area covered: protection of mangrove roots from boring isopods (Ellison and Farnsworth, 

1990, 1992).

Numbers of individuals are diffi cult to interpret in the 

contexts of sponge population dynamics and functional 

roles, as numbers can increase either by recruitment or 

fragmentation, and individual size can vary over many 

orders of magnitude. The lack of concordance between 

population dynamics of individual species measured 

in terms of numbers of sponges versus total volume on 

the same roots (see Figure 4) underscores how divergent 

conclusions can be when different metrics are chosen for 

evaluating sponge abundance. Evaluating abundance using two or more metrics at the same site can strengthen 

understanding of processes underlying the dynamics. For 

example, data indicating a small increase in numbers of 

individuals of Halichondria magniconulosa at Sponge Haven allowed the coincident large decrease in volume to be 

interpreted as extensive partial mortality and some fragmentation, rather than heavy losses of individuals.

An abundance measure that lends itself well to biodiversity surveys in this inherently fragmented habitat is 

presence/absence of a species on each root. Diaz et al. 

(2004) evaluated relative abundance of sponge species at 

Hidden Creek and Sponge Haven by prevalence on roots. 

Specifi c ranks of the species by prevalence were different from ranks assigned by volume in this study, but the 

match between the 10 most abundant species with respect 

to percent of prop roots inhabited (Diaz et al. 2004) and 

the 10 most abundant species with respect to volume (this 

study) is 80% at Hidden Creek and 60% at Sponge Haven. Resolution of systematic challenges may increase the 

match; for example, a second species of Tedania was only 

formally identifi ed (Wulff, 2006) at Sponge Haven after 

the study by Diaz et al. (2004) was published.

Evaluating abundance by presence/absence can also 

address an important community assembly issue: the 

probability that the community on a root will include a 

particular species. Sutherland (1980) pointed out the great 

importance of habitat division into small discrete patches 

by explicitly comparing the course of community development on prop roots versus on the 20  122 cm asbestos 

panels he deployed for evaluating recruitment. The larger 

area of the panels increased the probability that the competitively dominant, but ineffi ciently recruiting, Tedania 

ignis recruited onto every physically separated substratum 

patch. Once settled on a panel, this species was able to 

continue its growth in every direction, and each panel became quickly dominated by it. Each root had much less 

39_Wulff_501-514_Lang.indd 511 9_Wulff_501-514_Lang.indd 511 9/24/09 10:03/24/09 10:03
512 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

surface area, providing a smaller target for settling larvae 

of competitively dominant species. As predicted, if the 

roots are therefore more reliable refuges for competitively 

inferior species, the species composition on the roots was 

far more heterogeneous (Sutherland, 1980).

For ranking species by relative abundance, the greatest discrepancies between abundance measures (i.e., volume, area, number of individuals, and percent of roots) 

emerge when applied to thinly encrusting species, as their 

volume can be trivial even when they cover large areas 

(e.g., see Wulff, 2001, for an explicit comparison in a coral 

reef sponge community). The possibility that encrusting 

species may be relatively ephemeral because they are easily overgrown is supported by a comparison between the 

pattern of recruitment of the thinly encrusting species 

Clathria campecheae onto initially bare polyvinyl chloride 

(PVC) pipes at Hidden Creek (Wulff, 2004) and its abundance in the established community on prop roots. This 

species was described from coral reefs and had not been 

reported from mangroves, and yet it distinguished itself by 

occurring on more pipes (7/8) than any other species at 20 

months after they were suspended among the mangrove 

roots. Once the possibility of its occurrence on mangrove 

roots was raised, it was discovered at a very low level on 

prop roots at Hidden Creek and Sponge Haven.

This fi nding raises the question of how the successional stage of communities on censused roots might 

infl uence the evaluation of similarity of assemblages between sites and over time. Sutherland (1980) labeled 116 

roots that had not yet entered the water, in addition to 

260 roots that had already been colonized below the water surface. Sponge species that specialize on colonizing 

fresh roots would have therefore been included in his assessment of the total fauna. Because I followed roots with 

already established sponge faunas, and only added new 

roots that sprouted from subtidal portions of previously 

included roots (i.e., new roots that could be colonized by 

sponge growth from already censused portions), the earliest successional stages were not included in my assessment 

of community dynamics. Clathria campecheae, mentioned 

above, was not the only species that was disproportionately well represented on PVC pipes deployed for recruitment at Hidden Creek 20 months earlier. Haliclona curacaoensis, Biemna caribea, and Haliclona manglaris were 

also conspicuous with respect to numbers of individuals, 

percent of pipes colonized, and (for H. curacaoensis and 

B. caribea) volume, in this relatively early stage of community development on initially bare pipes (Wulff, 2004: 

fi g. 3). The pattern of loss of these species from one census 

to the next (see Figures 4– 6) is consistent with the possibility that these are early succession species that are progressively lost from roots as sponge species that are superior 

competitors accumulate over time. These data support 

Sutherland’s (1980) suggestion that the mangrove root inhabitants illustrate a trade-off between colonization rate 

and ability to persist in the community, and raise the possibility that stability of these communities, if measured as 

change over time, will depend on the successional stage 

on the monitored roots. The earlier in succession the assemblage on a root is, the more likely that subsequent censuses will reveal changes in species composition. Apparent 

instability will be further magnifi ed if percent cover is the 

metric chosen for abundance, as thinly encrusting species 

that are effi cient recruiters, but may be eliminated as superior competitors recruit, will initially have very high abundances with respect to area covered.

Observational units in previous studies have ranged 

from camera framer-length segments of roots to root clusters. Bingham and Young (1995) monitored 21 cm long 

root segments at 1 and 2 month intervals. Their analysis revealed how changes in abundance appear at different monitoring intervals, providing insight into the complex and 

rapidly changing dynamics of these communities at particular locations on roots. Their spatial position- focused 

analysis is complementary to the individual organismfocused analysis in the present study. Because the position 

of sponge individuals can shift along the prop roots as 

they increase and decrease in size, it is possible for them 

to move into a particular root segment without a recruitment event and to move out of a root segment while still 

persisting on the root. Thus a sponge assemblage within a 

root segment may appear less stable than the assemblage 

on that entire root. Differences in conclusions of Sutherland and Bingham and Young were attributed by the latter 

authors to greater infl uence of physical disturbance and 

seasonality on a subtropical site (Florida Keys) relative to 

a tropical site (Venezuela), but it is possible that difference 

in choice of observational unit might have also infl uenced 

evaluations of stability.

The balance between numbers of individuals monitored, frequency of monitoring, and method of evaluating 

abundance must be struck with the ultimate aim in mind. 

Following individual sponges over time and evaluating 

their size with respect to volume were essential to the aims 

of this study, which were to understand the life history 

and morphological strategies employed by each species. 

Inevitably the number of individuals and roots that could 

be followed in such detail suffered, as did the frequency of 

39_Wulff_501-514_Lang.indd 512 9_Wulff_501-514_Lang.indd 512 9/24/09 10:03/24/09 10:03
NUMBER 38 • 513

monitoring. Some compensation for these failings is made 

by the detail of the time-series drawings of entire roots. 

Detailed maps of the location of each sponge and comments about its shape and size at each census allowed fragmentation, size decrease, and addition of new recruits to 

be unambiguously distinguished, even when the causes of 

size change were not obvious. It is likely that new sponges 

recruited and vanished, and resident sponges changed in 

size in multiple ways, during the year-long intervals between censuses, and so my data only indicate the net result 

of months of unmonitored dynamics.

SIGNIFICANCE OF ECOLOGICAL

CHARACTERISTICS OF SPONGE SPECIES

Proportions of sponges that increased, decreased, 

fragmented, or disappeared were similar for given species 

among sites, suggesting that these may be species-level 

characteristics. With a few exceptions, the set of species 

that reliably exhibited 40% to 100% of individuals increased between censuses were the same at all three sites 

(Tedania ignis, Haliclona implexiformis, Lissodendoryx 

isodictyalis, Spongia spp., Halichondria magniconulosa), 

and constituted large proportions of the total sponge volume (85%, 82%, and 72% at HC, SH, and BT, respectively) at each site. Numbers of individuals of these species 

found on eight initially bare PVC pipes 20 months after 

they were suspended among prop roots at Hidden Creek, 

ranged from 0 (T. ignis, H. implexiformis, and Spongia

spp.) to 7 (L. isodictyalis) (Wulff, 2004). By contrast, the 

set of species for which only 0% to 30% of the individuals 

increased in size between censuses (i.e., B. caribea, H. curacaoensis, H. manglaris, Clathria campecheae) were each 

represented on the recruitment pipes by 11 to 14 individuals (Wulff, 2006). These patterns hint at the possibility 

of integrated sets of ecological characteristics that help to 

maintain all these species in the mangrove prop root system. Population dynamics of at least some of the typical 

mangrove root sponge species may be tied to their each being most suited to a particular time period in community 

development.

Overall community change, measured by total biomass, 

species diversity, numbers of individuals, and space occupied, can be functionally of great importance on an ecosystem level. However, an exclusive focus on these communitylevel metrics can obscure the components of community 

change— that is, changes in the component species— and 

therefore hamper our understanding of underlying processes. Consideration of the characteristics of individual 

species, such as their probability of persisting from year to 

year; their effi ciency at recruiting; susceptibility to particular biotic mortality sources such as predators, competitors, 

or pathogens; and the frequency with which they fragment 

or suffer partial mortality, may explain much of the community dynamics. Combining these new data on persistence 

with previously reported recruitment data (Wulff, 2004) indicates that some of the heterogeneity in space and time 

among mangrove prop root communities may be the result of the community on each root progressing independently through a successional sequence that is mediated, 

at least in part, by an inverse relationship between ability 

to hold space on mangrove roots and recruitment into the 

community that was fi rst suggested by Sutherland (1980). 

Adding to these life cycle-mediated patterns the observed 

idiosyncratic responses of particular species at a particular 

site, such as Tedania klausi succumbing to disease at the Bocas del Toro site or Halichondria magniconulosa targeted 

for consumption by a pair of French angelfi sh at Sponge 

Haven, allows community dynamics to be understood as 

the result of a complex set of interactions among individual 

sponges representing species that are characterized by specifi c physiological tolerances and morphological and life 

history traits.

ACKNOWLEDGMENTS

I am grateful to the Caribbean Coral Reef Ecosystems 

Program (CCRE), of the National Museum of Natural 

History (NMNH), Smithsonian Institution, for the privilege of being able to do fi eldwork at the Carrie Bow Cay 

fi eld station in Belize; and to Mike Carpenter, Klaus Ruetzler, and the volunteer station managers who make the 

Carrie Bow station an unparalleled resource, supporting 

comprehensive research on tropical marine ecosystems. 

I also thank Gabriel Jacome for always facilitating my 

fi eldwork at the Bocas del Toro station of the Smithsonian Tropical Research Institute. I thank two reviewers 

for helpful comments, and Carla Piantoni (CCRE) and 

Molly K. Ryan (Department of Invertebrate Zoology, 

NMNH) for help with the fi gures. My fi eld research was 

supported by the National Science Foundation under 

Grant No. 0550599, and by the Marine Science Network 

of the Smithsonian Institution, supported in part by the 

Hunterdon Oceanographic Research Endowment. This 

is contribution number 854 of the Caribbean Coral Reef 

Ecosystems Program (CCRE), Smithsonian Institution, 

supported in part by the Hunterdon Oceanographic Research Fund.

39_Wulff_501-514_Lang.indd 513 9_Wulff_501-514_Lang.indd 513 9/24/09 10:03/24/09 10:03
514 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

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— — — . 1980. Dynamics of the Epibenthic Community on Roots of the 

Mangrove Rhizophora mangle, at Bahia de Buche, Venezuela. Marine Biology, 58:75– 84.

Wulff, J. L. 2000. Sponge Predators May Determine Differences in 

Sponge Fauna Between Two Sets of Mangrove Cays, Belize Barrier 

Reef. Atoll Research Bulletin, 477:250– 263.

— — — . 2001. Assessing and Monitoring Coral Reef Sponges: Why and 

How? Bulletin of Marine Science, 69:831– 846.

— — — . 2004. Sponges on Mangrove Roots, Twin Cays, Belize: Early 

Stages of Community Assembly. Atoll Research Bulletin, 519:1– 10.

— — — . 2005. Trade-Offs in Resistance to Competitors and Predators, 

and Their Effects on the Diversity of Tropical Marine Sponges. 

Journal of Animal Ecology, 74:313– 321.

— — — . 2006. Sponge Systematics by Starfi sh: Predators Distinguish 

Cryptic Sympatric Species of Caribbean Fire Sponges, Tedania ignis

and Tedania klausi n. sp. (Demospongiae, Poecilosclerida). Biological Bulletin, 211:83– 94.

39_Wulff_501-514_Lang.indd 514 9_Wulff_501-514_Lang.indd 514 9/24/09 10:03/24/09 10:03
Index

Page numbers for tables are in italics and for fi gures are in bold.

absorption spectra

photosynthetically usable radiation and, 364 (see also photosynthetically usable 

radiation)

seawater and, 363

Acanthais brevidentata, 189– 191, 191, 192, 194

Acartia tonsa, 372. See also copepods

Achatina fulica, 108. See also snails

Acropora, 50– 51, 142, 260– 262, 265– 266, 282– 283, 314– 215, 317, 318, 319, 408, 

440– 441, 449

aspera, 440

cervicornis (staghorn coral), 266, 282, 314, 315, 317, 318, 319, 444

latistella, 441

longicyathus, 408, 440

millepora, 445, 446

muricata, 441

palifera, 445

palmata, 51, 260– 263, 262, 265– 266, 314, 439, 443, 448

tenuis, 442, 445, 449

valida, 441

See also coral

active migration model, 277

adventure tourism, 243

Aetea sica, 232, 233, 235, 236, 237. See also bryozoans

Aeverrillia armata, 233, 234, 236. See also bryozoans

Agaricia, 60, 63, 314– 315, 317, 318, 319, 451

agaricites, 447, 449, 451

growth of, 450

humilis, 445

lamarcki, 447

tenuifolia, 283, 314– 315, 318, 451

undata, 315

See also sponge(s)

40_Index_515-529_Lang.indd 515 0_Index_515-529_Lang.indd 515 9/24/09 10:33/24/09 10:33
516 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Ageratum littorale, 420

Aimulosia

pusilla, 238

uvulifera, 237– 238

See also bryozoans

Aiptasia pallida, 165. See also cnidarian worms; anenomes

algae

benthic, 405

blooms, 4, 16, 32, 35, 63, 66, 170, 405, 409– 410

brown, 285, 446– 447

chemical defense in, 53

coralline, 402, 403, 407, 408, 409, 444– 445, 450, 451

coral mortality and, 447

drift, 234, 236

endosymbionts, 429

fl eshy, 403, 404, 407– 409, 448

green, 31

growth of, 403

indicator species of, 407– 409

macro-, 48, 154– 155, 164, 167– 170, 285, 288, 314– 315, 

402– 405, 407– 410, 440, 446, 448, 451

micro-, 281, 288

red, 445

turf, 405, 409– 410, 446– 447

allelopathy, 447– 448

Amathia

alternata, 232, 233, 235

distans, 232, 233, 235– 236

vidovici, 232, 233, 234, 235, 236– 237, 237

See also bryozoans

American Samoa, 405

Amorphinopsis, 160, 167, 504, 509, 510

atlantica, 167

See also sponge(s)

Amphibalanus

amphitrite 293

eburneus, 293

improvisus barnacle, 293

reticulatus, 293

See also barnacles

Amphimedon erina, 167. See also sponge(s)

amphipods, 275

Anachis fl uctuata, 191, 193. See also snails

anchialine cave(s)

adaptation to, 270, 277– 278

animals, 274, 276, 278– 279

biological signifi cance of, 270

characteristics, 269

chemical characteristics of, 273

ecology of, 270, 272– 273

geology of, 271– 272

lava tubes and, 271, 275, 277

trophic relationships in, 272

See also caves

ANCOVA, 191– 193, 262– 265, 327– 328, 329, 330

anemones, 96– 98, 101, 106, 144, 152, 155, 164– 167, 234, 

255, 430

annelids, 33, 210, 273

Annual Symposium on Sea Turtle Biology and Conservation, 

243. See also marine turtle(s)

ANOVA, 327, 328, 330, 348, 349, 350, 371– 372, 374, 395, 

399, 462

anoxia, 272, 403

Anthozoa, 140, 142, 143.

Antilles. See Netherlands Antilles

Apionsoma, 215– 216. See also sipunculans

Aratus, 66. See also crabs

ARLEQUIN, 222

ascidians, 54, 60, 62, 159, 164, 234, 284, 443

Astyanax fasciatus, 279. See also fi sh

atmosphere

change, 4

CO2 in, 12, 323

enrichment studies of, 399

Australia, 57, 105, 272– 273, 275, 279, 292, 440, 442, 446, 

482, 487, 491

Avicennia germinans, 347, 348, 420, 422– 424, 474, 492, 

494– 497. See also mangrove forest(s)

Axianassa intermedia, 186

Axiopsis serratifrons, 182, 185, 186. See also crabs

Bahalana caicosana, 274. See also isopods

Bahamas, 152

archipelago of, 276

Blue Holes of, 269, 278

coral reefs in, 324

Bahia Almirante, 324– 325, 331– 333, 361

Balanus

improvisus, 253

trigonus, 293

See also barnacles

ballast water, 18, 238, 295

Barbados, 405

barnacles, 249– 250, 251, 254, 255, 293, 293, 296

barrier reef. See coral reef(s)

Batis

agrillicola, 491

distribution, 491

maritima, 420, 491, 492, 496, 498

BayesTraits, 98

Bay Islands of Honduras, 416, 424

Beania

hirtissima, 232, 233, 234, 235

klugei, 232, 233, 235– 237

behavior

caves and, 277

intertidal animals and, 81

Belize

barrier reef of, 6, 45, 47, 51, 53, 111, 283, 287, 288, 316, 

380, 383, 387, 389, 407, 416, 426, 448, 474

40_Index_515-529_Lang.indd 516 0_Index_515-529_Lang.indd 516 9/24/09 10:33/24/09 10:33
NUMBER 38 • 517

blue holes in, 269

central province of, 381

coastal, 46, 389

coral bleaching in, 405, 434

development in, 287, 288

fi sheries in, 287, 289

government, 7, 62, 283

hydrogeomorphic characteristics of, 347

mangrove forest in, 153, 347, 348, 474

microtides of, 382

oceanographic conditions, 153, 156

PAR, 365, 366

seagrass in, 365

seasonal rainfall of, 385

sediment loads and, 389

sponges in, 151– 152, 159, 166, 170, 506

study sites in, 361

surface water absorption spectra of, 364

tourism in, 287

urban and economic growth in, 379

water clarity in, 363

Belize Coastal Zone Management and Fisheries, 62

Belize Lagoon, 283

Belize National Meteorological Service, 381– 382, 385

Bermuda, 60, 135, 136, 238, 272, 274– 276, 278– 279, 

405

Biemna

caribea, 160, 167, 504, 505, 508, 510, 512– 513

maritima 492, 495, 497

See also sponge(s)

Biffarius fragilis, 186

Bifl ustra denticulata, 233, 234, 235

biodiversity, 1, 2, 4, 6– 8, 18, 25, 28, 30, 32– 33, 35– 36, 53, 59, 

74, 87, 230, 241, 287, 452

anchialine cave, 273

in Belize, 283

education programs in, 87

intertidal and subtidal ecosystems, 415

mangroves and, 152, 169, 345

marine, 38, 79, 85, 426

reef, 53, 380, 407

surveys, 511

biofi lms, 424, 445

biological invasions, 291. See also invasive species

black mangrove, 36, 58, 64, 347, 474, 486, 492. See also

mangrove forest(s)

black sea urchin (Diadema antillarum), 78

bleached coral

abundance of, 432, 434, 435

bleached cytoplasm of, 431

environmental stressors and, 435

mechanisms, 79, 82, 88, 260, 314– 315, 319, 389, 430– 435, 

440, 447, 451

rate, 432

seasonal, 434

symbiotic, 435

symptoms of, 435

See also coral

blue crabs, 17, 18. See also crabs

Bocas del Toro, Panama, 75, 151, 154, 170, 347– 348

CARICOMP and 88

research station (BRS), 74, 76, 79, 324, 325, 326

Bochusacea, 275

Bonaire, 450

Bostrycapulus calyptraeformis, 190, 191, 191, 192, 193, 193. 

See also snails

Bostrychietum, 58. See also algae

Bowerbankia, 233, 234, 235– 237

gracilis, 235, 236, 236– 237

maxima, 234

See also bryozoans

box jellyfi shes, 145, 147

Brasiliensis, 420

Brazil, 34, 123, 136

Briareum, 142.

broadcast spawners, 440– 441

bryozoans

branching, 234

colonies, 230

communities, 230

distribution, 233, 235– 236, 237

Buddenbrockia, 140. See also cnidarian worms

Bugula

neritina, 233, 234, 235, 236, 237, 253

stolonifera, 233, 235, 236, 237

turrita, 254

See also bryozoans

Callianidea laevicauda, 186

Callinectes, 182, 183, 184, 185. See also crabs

Callyspongia, 67, 191, 193

Canary Islands, 271, 273, 275– 277, 279

carbon dioxide enrichment studies, 392– 393, 398

carbon production, 17

Caribbean

characteristics, 7, 74

corals in, 57, 59– 60, 62– 63, 66, 314 (see also coral)

epifaunal taxa from, 152 (see also epifauna)

mangroves of (see mangrove forest(s))

tourism, 303, 304, 305

Caribbean Coastal Marine Productivity Program 

(CARICOMP)

Bocas del Toro research station and, 88

Carrie Bow Cay and 380

common methodologies of, 59

seagrass sites, 324, 324, 325– 327, 329–331, 381

Caribbean Coral Reef Ecosystems program (CCRE), 2, 6– 7, 43, 

152, 379

Carijoa riisei, 231– 232. See also coral

40_Index_515-529_Lang.indd 517 0_Index_515-529_Lang.indd 517 9/24/09 10:33/24/09 10:33
518 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Carrie Bow Cay, Belize

bleached coral in, 434

Caribbean coral reef ecosystems program and, 6– 7, 57 (see 

also Caribbean Coral Reef Ecosystems program)

environmental monitoring system of, 380– 382

facilities, 47, 64, 65

fi eldwork in, 181– 184

habitats, 50, 55, 187, 387, 387

history, 44– 45

infrastructure, 59

location, 3, 381

Marine Field Station, 63, 64, 66

meteorological conditions, 381, 383

oceanographic conditions in, 380, 433, 433, 435

physical description of, 380

reef fi shes of, 111

seasonal rainfall of, 385

water clarity, 383, 389, 433

water quality of, 380, 385, 389, 433

water temperature and tidal elevation, 388

wind conditions, 385

Carybdea, 143.

Cassiopea, 143.

Caulerpa verticillata, 156. See also sponge(s)

Caulibugula armata, 232, 233, 236– 237, 237, 238. See also

bryozoans

cave fi sh Typhliasina pearsei, 274

caves

adaptations to, 277– 278

anchialine (see anchialine cave(s))

in Bermuda, 278

limestone, 272

marine, 269

Yucatan, 269, 271, 272, 275, 276

Celleporaria, 235, 237– 238

sherryae, 238

See also bryozoans

Celleporina hassalli, 232, 233

Census of Marine Life (COML), 85

Chalinula molitba, 155, 157, 161, 164, 165, 168, 504, 505, 

509– 510. See also sponge(s)

Charybdis hellerii 182, 183, 184. See also crabs

Chelonibia patula, 108. See also barnacles

Chesapeake Bay, 2, 4, 6, 12, 13, 16, 16– 18, 19– 20, 33, 66, 248, 

250, 360, 369, 370, 371, 375, 392. See also Rhode 

River, Chesapeake Bay

Chironex, 143.

chironomid insect larvae, 53

chlorophyll a, 53, 323, 325–333, 335, 337– 338, 339, 340, 342, 

360, 364, 371, 372, 372– 373, 406, 409

Chondrilla, 60, 68, 68, 159, 167, 315, 405

caribensis, 167

aff. nucula, 315

See also sponge(s)

Chrysaora, 143

quinquecirrha, 370– 372, 372, 374– 376

See also jellyfi sh

ciguatera fi sh poisoning (CFP), 301, 302, 306, 307

ciguatoxins, 301

citrate synthase (CS), 278

Cladonema, 143.

Clathria

campecheae, 504, 512– 513

microchela, 160, 167

schoenus, 157, 160, 163, 164, 165, 166, 167, 168, 169, 

504, 510

venosa, 160, 179, 504, 505

See also sponge(s)

Clathrina

coriacea, 504

primigenia, 167

venosa, 167, 505

See also sponge(s)

Clavelina, 60

puertosecensis, 159, 284

See also ascidians

climate change. See global warming

Cliona, 67. See also sponge(s)

closed-circuit rebreather, 271

cnidarian worms

current classifi cation of, 146

diversity, 139

evolutionary relationships in, 140, 141, 143– 146

subclades of, 140

See also coral; specifi c species

coastal area(s), 11– 12, 19, 30, 356, 359

erosion of, 45, 51, 63, 477

mangrove forests and, 474 (see also mangrove forest(s))

overfi shing and, 16

pollution and, 16

tectonic faults in, 272

Coastal Ecosystem Protection Committee, 243

Codium, 232. See also algae

COI

analysis, 119

sequence, 113, 123, 129, 132, 221

Coiba National Park, 83, 87– 88

Colombia, 53, 87– 88, 152, 174, 176

colonial ciliates, 67

Colpophyllia natans, 318. See also coral

competition-based relative dominance model, 403

Comprehensive Everglades Restoration Plan (CERP), 35

confocal laser scanning microscopy (CLSM), 28, 31

Conocarpus erectus, 420, 492

Conopeum tenuissimum, 234, 236, 294. See also bryozoans

conservation

of cave species, 278– 279

coastal, 81

40_Index_515-529_Lang.indd 518 0_Index_515-529_Lang.indd 518 9/24/09 10:33/24/09 10:33
NUMBER 38 • 519

marine, 4, 25, 86– 88, 260

sea turtle, 8, 242– 244

Consortium for the Barcode of Life (CBOL), 85

Convention on Biological Diversity (CBD), 243

Convention on International Trade in Endangered Species of 

Wild Fauna and Flora (CITES), 243

Convention on the Conservation of Migratory Species of Wild 

Animals (CMS), 243

Coolia, 286, 302, 303. See also dinofl agellates

copepods, 53, 271, 273, 275– 276

coral

bleaching (see bleached coral)

broadcast spawning by, 440– 441

brooding, 445

clonal growth of, 438, 447, 450– 452

Diploria, 67

diseases, 405, 408

egg/sperm, 261

elkhorn, 50, 51, 260, 261, 266, 314

fecundity of, 440

fertilization ecology of, 36, 348, 439, 440

fi re, 50, 51

gametogenesis in, 33, 432, 440

growth, 443

hard, 313

larvae, 35, 260– 261, 263, 266, 408, 438, 442– 443, 444, 

445– 447, 451

metamorphosis, 445

mortality, 263, 313– 314, 443, 449, 451

pathogens, 448

planulae, 409, 442, 445, 451

Porites, 67

post-settlement biology of, 445– 451

recruitment, 438, 440– 441, 451

reefs (see coral reef(s))

reproduction, 438, 439

self-fertilizing, 314

settlement, 438, 443– 447, 450

skeletons, 315, 317

soft, 231– 232

staghorn, 266, 282, 314– 315, 317, 318, 319, 444

white-band disease (WBD) of, 314– 315

Coralaxius nodulosus, 185, 186

Corallianassa longiventris, 184– 185. See also crabs

coral reef(s)

assessment protocols for, 409

biodiversity, 451 (see also biodiversity)

challenges to, 437

characteristics of, 6, 44, 259

cores, 318

cyanobacteria and 446

disturbances of, 380

ecosystems, 44, 313, 402, 409

eutrophication and, 404

Florida, 35

irradiance, 382, 383, 386, 387

management, 403– 407, 410

nutrient concentrations in, 402

recovery, 35

reproduction, 439

rhomboid shoals and, 314– 315, 319, 319

sponges in, 159, 511, 512

structure, 44

upwelling and, 336

water quality and, 324

Coral Reef Development in the Tropical Eastern Pacifi c (TEP), 

81– 82

Coryphopterus, 116, 121

alloides, 112– 113, 125, 130, 138

bol, 112– 113, 115, 123

dicrus, 125, 126, 127, 130

eidolon, 112– 113, 126, 128, 129– 130, 137

glaucofraenum, 112– 113, 115, 119, 120, 121, 125, 126, 

129– 130, 132, 135

hyalinus, 112– 113, 115, 121, 129, 134

kuna, 112– 113, 125, 129– 130, 131, 138

lipernes, 112– 113, 115, 117, 130, 134

personatus, 112– 113, 115, 117, 121, 129, 134

punctipectophorus, 125, 129, 130, 131

thrix, 125, 126, 127, 130

tortugae, 112– 113, 115, 118, 119, 121, 123, 125, 126, 

129– 130, 132, 135

venezuelae, 112– 113, 115, 119, 121, 123, 123, 124, 125, 

129– 130, 132– 133, 136

western Atlantic, 114, 119, 125, 129, 133

western Caribbean, 112

See also fi sh

Costa Rica, 83, 87– 88

crabs

abundance of, 466

fi sheries, 17, 18

intertidal (see Uca)

nursery habitats for, 16

nutrient recycling by, 459

swimming, 182, 183, 183

Crangon crangon, 96. See also crabs

Crepidula cf. nivea, 191, 191, 192, 193, 194, 190

Crisia, 232, 233, 234, 235

elongata, 232, 233, 234

See also bryozoans

Cronius

ruber, 184

tumidulus, 184

See also crabs

crustaceans, 273, 275–276. See also crabs; isopods; shrimps

Cryptocorynetes longulus, 274. See also remipedes

Cryptosula pallasiana, 233, 234, 235, 237

Cuba, 152, 159

40_Index_515-529_Lang.indd 519 0_Index_515-529_Lang.indd 519 9/24/09 10:33/24/09 10:33
520 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Cubozoa, 145, 147.

Culebra Island Education Center, 86

Curacao, 113, 119, 123, 125– 126, 128– 129, 449

cyanobacteria, 35, 152, 404– 405, 408– 409

endosymbionts, 429

mats, 57, 154, 155

Cycloporus variegatus, 31

Cyperus spp, 420

cytochrome c oxidase, 113, 116, 134

Danielopolina, 276. See also ostracods

data loggers, 343, 381

decapod crustaceans, 95, 275–276. See also crabs; shrimps

Deeveya, 276. See also ostracods

deforestation, 325

denaturing gradient gel electrophoresis (DGGE), 174– 175, 175, 

176

Dendronephthya, 142.

Diadema antillarum, 78– 79, 385, 406, 449. See also fi sh

Dichothrix, 448. See also cyanobacteria

Dictyoceratida, 503, 504

Dictyosphaeria cavernosa, 31

Dictyota

caribaea, 284, 448

pulchella, 447

See also algae

dinofl agellates, 5– 6, 33, 63, 283, 286– 288, 301– 302, 302, 303, 

304, 429– 430, 431, 435

Diploria, 448

strigosa, 266, 446

See also coral

Diplosoma listerianum, 253, 443. See also ascidians

dispersal kernels, 442– 443

dissolved oxygen, 4, 16– 17, 269– 270, 272– 273, 278– 279, 326, 

327, 337, 339, 369, 371, 372, 375, 382

Distichlis spicata, 392, 396, 420, 498

DNA

analysis, 34

barcoding, 34, 111, 112, 132

extraction, 220

mitochondrial, 176, 184, 220– 221, 223, 224, 225, 226, 

227

Dominican Republic, 83

dredging operations, 284, 286

dwarf red mangrove, 474, 477, 486, 488. See also mangrove 

forest(s)

Dysidea etheria, 161, 162, 163, 164, 165, 167, 168, 504, 505, 

510. See also sponge(s)

Echinometra viridis, 315, 317

ecology

analysis of, 48, 52

connectivity measurement, 442

diversity patterns in, 247

long-term studies of, 229

recruitment and, 442

eco-tourism, 243, 426. See also tourism

Ecuador, 83, 88

Electra bellula, 235, 236, 236. See also bryozoans

El Niño– Southern Oscillation (ENSO), 7, 74, 260, 380

ENCORE, 405, 408

Encyclopedia of Life (EOL), 86

Endangered Species Act, 260, 266, 314

endemism, 198, 202

endosymbiont densities, 430

Environmental Protection Agency, 16, 28, 76

environmental research, grand challenges in, 12– 19

epifauna

community development, 248, 253, 256, 257

growth rates, 255

recruitment of, 248– 249, 252, 254

spatial variability in, 249

temporal patterns of, 249

Eretmochelys imbricata, 242. See also turtles

Escharoides costifer, 235, 237– 238. See also bryozoans

Eucalliax, 183, 184– 185

Eudendrium carneum, 232

eutrophication, 2, 16– 17, 66, 288, 332– 333, 359– 360, 366, 

391, 402– 406, 408, 410

evapotranspiration, 36, 481, 483, 487

EvoDevo, 210

evolutionary connectivity, 442

Excirolana

antillea, 232, 233, 234, 235, 238

braziliensis, 219– 220, 221, 222, 223, 224, 225, 226, 227

mayana, 221

oplophoroides, 104, 106

See also isopods

Exechonella antillea, 232, 233, 234, 235, 238. See also

bryozoans

Exhippolysmata, 96– 98, 101– 102, 104, 105, 106, 108. See also

shrimps

external transcribed spacer (ETS), 173

Favia

fragum, 444, 446

pallida, 441

See also coral

fertilizer, 349– 350, 380, 396

fi ddler crab. See crabs; Uca

fi re coral, 50, 51. See also coral

fi sh

nursery habitats for, 16

of Panama, 80

Shorefi shes of theTropical Eastern Pacifi c Online 

Information System (SFTEP) and

stygobitic anchialine, 269– 270, 273, 277– 278

FishBase, 112, 202

40_Index_515-529_Lang.indd 520 0_Index_515-529_Lang.indd 520 9/24/09 10:33/24/09 10:33
NUMBER 38 • 521

fi sheries bycatch, 243

Fistulobalanus pallidus, 293. See also barnacles

fl agship species, 241– 242, 244– 245

fl atworms, 31, 33

fl eshy algae, 403, 404, 407– 409, 448

Florida, 446

Atlantic coast of, 36, 230

coral reefs in, 35

impoundments, 460

PAR of, 366

seagrass in, 365 (see also seagrass)

surface water absorption spectra, 364

Florida Bay, 28

Florida Keys, 2, 28, 36, 405, 430– 431, 435, 446, 502, 510, 512

Flower Garden Banks (FGB), 314

Foraminifera. See sponge(s)

Fungia

fungites, 446

larvae of, 263

scutaria, 261, 263, 264

See also coral

Galapagos Islands, 269, 271– 273, 276

Galeta Point Marine Laboratory, 76, 86

Gambierdiscus, 286, 302, 303, 304. See also dinofl agellates

gametes, 211

gametogenesis, 33, 432, 440

gastropods, 191

salinity and, 375

temperature and, 375

See also snails

Gelidiella, 448

gene fl ow, 219, 220, 226– 227, 442

Gesiella jameensis, 273. See also polychaete worms

global warming, 2, 44, 238, 314, 315, 323 

Glovers Reef, Belize, 45, 389, 433

Glypturus acanthochirus, 182, 184– 185

Golfi ngia vulgaris, 210. See also sipunculans

Goniastrea

aspera, 441

favulus, 441

retiformis, 445

Gonionemus, 143.

Goniopora tenuidens, 446. See also coral

Gorgonia mariaei, 174– 175. See also coral

Great Barrier Reef, 405, 429, 443

greenhouse gases, 260, 410

Guadalupe, 152, 159

Guam, 292, 445– 446

Guatemala, 287

Gulf of Chiriquí

chlorophyll a values in, 339

habitat, 7, 337

location, 324, 336

NP ratios in, 343

oxycline in, 343

seasonal nutrients in, 341, 342

SST in, 343

thermocline in, 336

thermohaline structure of, 338

upwelling in, 336, 343

water characteristics of, 338, 339– 340, 340, 341

See also Gulf of Panama; Panama

Gulf of Honduras, 287, 380, 389

Gulf of Mexico, 8, 105, 125, 129, 131, 238, 314, 469

Gulf of Panama, 74, 82, 87, 335– 336, 342– 343

dry seasonal nutrients in, 341, 342, 342

NP ratios in, 343

rainfall patterns in, 337

thermohaline structure of, 338

upwelling in, 342– 343

water characteristics of, 338– 339, 340

water clarity in, 341

See also Panama

Gulf Stream, 6– 7, 34, 73, 435

Halammohydra, 143.

Halichondria magniconulosa, 160, 165, 167, 503, 504, 505, 

506, 508–511, 513

Haliclona, 55, 152, 161, 165, 168, 504, 505, 508

caerulea, 161, 164, 504

curacaoensis, 159, 161, 162, 164– 165, 167, 504, 505, 508, 

510, 512– 513

implexiformis, 161, 165, 167, 513, 504, 505, 509, 510, 513

manglaris, 157, 161, 163– 165, 167, 504, 505, 508, 510, 

512– 513

tubifera, 161, 164, 167

vermeuleni, 157, 161, 162, 164, 165

See also sponge(s)

Haliclystus, 142

Halimeda, 156, 404, 408, 419, 421, 446, 448

opuntia, 446, 448

See also algae: macroHalisarca, 155, 167

caerulea, 162, 168

See also sponge(s)

Halocordyle disticha, 232

Halodule wrightii, 360, 363

Halophila decipiens, 363, 365. See also seagrass

Halosbaena, 276

Haplosclerida, 152, 157, 503, 504

Harbor Branch Oceanographic Institute (HBOI), 26, 33, 35

Hawaii, 60, 260– 261, 271, 276, 292, 404– 405, 407

hawksbill turtle, 242

herbicides, 380

herbivory

coral reef community and, 35

positive effects on reefs of, 449

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522 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

hermaphroditism, 96, 98, 105, 106, 108

in shrimps, 96, 106, 108

simultaneous, 96, 106, 108

Hexacorallia, 140, 142, 144.

Hippolyte, 106

inermis, 98

obliquimanus, 95

williamsi, 95, 98

See also shirmps

Hippopodina, 234

irregularis, 238

verrilli, 233, 236, 237

See also bryozoans

Hipporina, 253. See also bryozoans

historical contingency hypothesis, 98

Honduras, 51, 287

human disease, 35

hurricanes

Belize and, 51

coral mortality and, 406

damage from, 380

effects, 36

Honduras and, 51

Hydra, 146

hydrogen sulfi de, 59, 66– 67, 272, 278

Hydrolithon

boergesenii, 445

onkodes, 445

See also algae: coralline

Hydrozoa, 143, 145.

Hyrtios proteus, 154, 161, 164, 165, 167, 168. See also

sponge(s)

imposex

defi nition of, 189, 194

distribution of, 190– 191, 194

TBT detection with, 195

incident irradiance, 360, 362, 382– 383, 385, 386, 387– 388

Indian River Lagoon (IRL)

ecosystems, 38

fi ddler crab species of, 459 (see also Uca)

habitat, 347

hydrogeomorphic characteristics of, 347, 467

impoundment, 461, 461, 468, 496

location, 230, 361

mangroves in, 347, 348, 350, 352, 354 (see also mangrove 

forest(s))

nutrients in, 352, 353

PAR in, 365

resorption effi ciences, 352

seagrasses in, 234, 236, 360, 361 (see also seagrass)

sediments, 35

Smithsonian Marine Station at Fort Pierce and 6, 28, 35

Indian River Lagoon Species Inventory, 36

Inter-American Tropical Tuna Commission (IATTC), 243

intermediate disturbance hypothesis, 502

internal transcribed spacer (ITS), 173– 174, 175, 176, 177, 202

International Biogeographic Information System, 202

International Taxonomic Information System, 202

International Union for Conservation of Nature (IUCN), 

87– 88, 202, 278, 314

International Year of the Reef, 7, 62, 74

interspecifi c fertilization, 440– 441

inter-tropical convergence zone, 74, 337, 383

Intracoastal Waterway, 238

invasive species

Chesapeake Bay and, 19

marine, 8

Northeastern Pacifi c and, 292

Panama Canal and, 293

recruitment of, 249– 250, 253, 256– 257

research challenges and 18

Iotrochota birotulata, 159. See also sponge(s)

Ipomoea pescaprae, 420

island biogeography, 501

Isochrysis galbana, 191, 219, 220, 274. See also isopods

isopods, 53, 101, 220– 222, 226, 273, 275, 510– 511

Isthmus of Panama, 2, 7– 8, 30, 78– 79, 83– 84, 295, 297, 336. 

See also Panama

Jamaica, 7, 54, 83, 152, 159, 275, 315, 405

Jania, 448

Japan, 142– 143, 216, 273, 275, 442, 484, 487

jellyfi sh, 145, 370

Johnson, Seward Sr, 26

keystone fi sh, 410

KRE (potassium resorption effi ciency), 349, 351, 354

lactate dehydrogenase (LDH), 278

Laguna de Chiriquí, 324

Laguncularia racemosa (white mangrove), 347, 348, 420, 474, 

492. See also mangrove forest(s)

larva(l)

behavior, 445

brachiolarian, 33

brachiopod, 33

coral reefs and, 438

dispersal of 277, 441, 443

fi sh, 67

rearing, 262

settlement, 53, 408, 438, 443– 447, 450

ocean acidifi cation and, 446

oceanic, 33

survival and recruitment, 438

temperature effects on, 446

Lasionectes, 276. See also remipedes

Laurencia papillosa, 446. See also algae

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NUMBER 38 • 523

Lepidophthalmus richardi, 184, 186

Lichenopora, 235, 237. See also bryozoans

Lindra thalassiae, 31

Link, Edwin, 26

Lissoclinum fragile, 234. See also ascidians

Lissodendoryx, 152

colombiensis, 160, 164

isodictyalis, 152, 160, 165– 167, 504, 505, 509, 510, 

513

See also sponge(s)

Lobophora variegata, 446– 447. See also algae

Lyngbya

majuscula, 446

polychroa, 446

See also cyanobacteria

Lysmata

amboinensis, 96, 98, 104

anchisteus, 101, 104

ankeri, 98, 104, 106

argentopunctata, 101, 104

boggessi, 97, 99, 101, 102, 104, 106

californica, 96, 98, 104, 105

chica, 101, 103, 104

galapaguensis, 97, 99, 101, 102, 104

grabhami, 96, 98, 104, 106

kuekenthali, 101, 103, 104

moorei, 101, 103, 104

pederseni, 96, 98, 105

philippinensis, 101, 105

racemosa, 492, 494– 496

rathbunae, 101, 103, 105

seticaudata 98, 105

phylogeny, 107

trisetacea, 101, 103, 105

vittata, 101, 103, 105

wurdemanni, 96, 105, 106, 108

See also shrimps

Lytocarpia, 143.

Madracis auretenra, 318. See also coral

malate dehydrogenase (MDH), 278

Manania, 142.

manatee grass, 234, 360

mangrove crab, 58

mangrove forest(s)

in Belize, 36, 164– 165

black, 36, 474, 347, 348, 420, 424, 492, 494, 495

channel bottom, 58

characteristics, 348, 473

clear cutting, 285, 287, 416, 420, 423, 426– 427, 477

coastal erosion and, 423, 474

dwarf, 36, 474, 477, 486, 488

ecosystems, 345, 480

epifauna of, 168 (see also epifauna)

fl ooding and, 487

forests (see mangrove forest(s))

growth, 350, 355, 356

human effects on, 474, 487

hurricane damage to, 36

loss of, 287

nutrient conservation and, 351, 354

in Panama, 36, 156– 157

peat, 66– 67, 284– 287, 348, 355, 416, 419, 421, 423– 424, 

425, 477

Pelican Cays and, 419

pollution and, 474

prop roots and prop root communities of, 58, 155, 156, 

159, 169, 282, 396, 502, 505, 506, 507, 508, 

513

red, 38, 50, 54, 57, 58, 155, 159, 283, 325, 346, 416, 422, 

474, 477, 480, 486– 489, 492, 502

as reef fi sh nurseries, 345, 415, 426, 474

resorption effi ciences of, 352, 353

root-algal mats, 424

saplings, 495, 497– 498, 498

sea level and, 487, 489

senesced leaves of, 355

sensitivity to sediments, 424

sponge faunas and, 162, 166, 510, 512

stability, 288

surveys, 492, 496

swamp communities, 58

Twin Cays and, 282, 419, 475

white, 347, 348, 420, 474, 492

mangrove oyster, 58

Manning equation, 483

Manning roughness coeffi cient, 483– 484, 484

marine

activities, 87– 88

caves, 269 (see also caves)

ecology, 35– 56

education and outreach, 85– 87

natural products, 32, 35

turtles (see marine turtle(s))

See also ocean; sea

Marine Environmental Sciences Program (MESP) 76

Marine Protected Areas, 410

Marine Science Network (MSN), 1, 2, 4– 6, 8, 19, 30, 36, 66, 

360

marine turtle(s)

conservation, 242– 244

endangered, 242

as food source, 242

outreach and public education, 243

program in Brazil, 242

research, 242– 244

marine zooarchaeology, 80, 87

Markov chain Monte Carlo (MCMC) methods, 98

40_Index_515-529_Lang.indd 523 0_Index_515-529_Lang.indd 523 9/24/09 10:33/24/09 10:33
524 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Meandrina meandrites, 447

Medusozoa, 140, 143– 145

Melinda Forest Station, 477, 481

Menippe, 182, 183

nodifrons, 183

See also crabs

Merguia, 98, 108

rizophorae, 98

See also shrimps

Merhippolyte, 108. See also shrimps

Mesoamerican Barrier Reef System (MBRS), 2, 6, 416, 423– 

424, 426

mesozooplankton, 371, 372, 374– 375

metabolism, 59, 189, 270, 277– 278

meta-communities, 502

metamorphosis, 33– 34, 211– 212, 214– 216, 265, 443, 445– 

446, 451

Mexico, 131, 184, 204, 220, 238, 242, 244, 293, 304, 305

Mictaxius thalassicola, 185. See also crabs

Mictocaris halope, 274, 275

Millepora, 50, 51, 238, 314

complanata, 51, 283

See also coral

Mimocaris, 108. See also shrimps

Mithrax, 182– 183. See also crabs

Mnemiopsis leidyi, 369, 371– 372, 372, 374– 375

Mogula manhattensis, 253. See also tunicates

molecular evolution, 8, 80, 82, 145, 173

Monanchora, 60. See also sponge(s)

Montastrea, 80, 266, 318, 440, 441

annularis, 318, 408, 440– 441, 448, 451

faveolata, 266, 439, 441, 443, 444

franksi, 441

leidyi, 369– 374, 375– 376

Montipora

capitata, 444, 446

digitata, 440

Morone americana, 21. See also fi sh

Morula, 194

Mozambique, 469

Munidopsis polymorpha, 270, 275, 277, 279. 

See also crabs

muricids, 189– 190, 191, 192, 192, 194

Mycale

carmigropila, 160, 162, 164

laevis, 167

magnirhaphidifera, 167, 504

microsigmatosa, 157, 160, 162– 163, 164, 165, 167, 168, 

504, 505

See also sponge(s)

Mycetophyllia aliciae, 447

Myxobolus, 143.

Myxosporea classifi cation, 144

Myxozoa, 140, 143, 143, 145.

Naos Island Laboratory, 76, 80

National Museum of Natural History (NMNH), 2, 3, 4– 6, 26, 

30, 32, 34, 38, 57, 98, 103, 125, 134, 138

National Zoological Park (NZP), 5

Nature Conservancy, 87

Naushonia, 183, 185– 186. See also crabs

nematocyst, 139

nemerteans, 34

Neocallichirus

grandimana, 184– 185

maryae, 184– 185

rathbunae, 185

raymanningi, 185

See also crabs

Nephasoma pellucidum, 210– 211, 212, 214, 215– 216

net ecosystem exchange (NEE), 397

Netherlands Antilles, 152, 324, 442

nitrogen

cycling, 36

discharge, 18, 21

limitation, 346, 355, 404

resorption effi ciency (NRE), 349, 349, 351

resorption profi ciency of, 349

sources, 404

See also nutrient

NOAA (National Oceanic and Atmospheric Administration), 

302– 303

Nolella stipata, 233, 234, 235, 236, 236, 237. See also

bryozoans

non-governmental organizations (NGOs), 86

Nova Scotia, 242

N-resorption effi ciency, 349, 351

N-resorption profi ciency, 354

Nucella lapillus, 189, 194

nutrient

concentrations, 156

pollution from, 346, 406, 409

recycling by crabs, 459

threshold hypothesis, 405, 407

OBIS, 202

ocean

acidifi cation, 260, 446

chlorophyll a concentrations, 323 (see also chlorophyll a)

currents, 66, 248

primary productivity, 323

upwelling, 335, 341

See also marine; sea

Octocorallia, 140, 142, 144, 147.

Oculina, 6, 38

Online BRS Bilingual Biodiversity Database, 87

Online Information System on Tropical Eastern Pacifi c 

Shorefi shes, 87

Ophryotrocha puerulis, 108

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NUMBER 38 • 525

Oreaster, 68. See also starfi sh

ostracods, 272, 273, 274, 275– 276

Ostreopsis, 286, 302, 303. See also dinofl agellates

Ototyphlonemertes, 34

overfi shing, 4, 12, 16, 19, 83, 206, 402, 405– 406, 410

oxygen-defi cient waters, 275

Oxypora lacera, 446, 449

oyster

fi shery, 16

larvae, 376

Padina, 404

Palmer Long-Term Ecological Research Program, 5

Palythoa, 142

Panama

Bocas del Toro Archipelago of (see Bocas del Toro, 

Panama)

Canal (see Panama Canal)

coastal communities of, 74

fi shery resources of, 336

geography of, 73, 74– 76, 77, 336, 337– 338, 361

Gulf of (see Gulf of Panama)

history and ecology of, 7

intertidal community ecology of, 81

invasions in, 80– 81, 295, 298

mangrove forests and, 347 (see also mangrove forest(s))

map of, 77

oceanographic conditions in, 156, 336, 338– 343, 339, 

340, 341, 342

Pacifi c shelf of, 74

Paleontology Project (see Panama Paleontology Project)

seagrass in, 365 (see also seagrass)

shipping history of, 296 (see also Panama Canal)

Smithsonian Tropical Research Institute in (see

Smithsonian Tropical Research Institute (STRI), 

Panama)

sponges in, 159, 166, 506

surface water absorption spectra in, 364, 366

water quality in, 363

Panama Canal, 7, 74, 80– 81, 83, 88, 190

barnacles and, 296

construction of, 294

expansion, 296

marine invasions and, 291, 297

shorefi shes and, 80

transiting, 295, 297

vessel transits, 80, 294

See also Panama

Panama Canal Authority, 296– 297

Panama Canal Zone, 74

Panama Paleontology Project (PPP), 8, 83– 85

Panulirus, 182

Papua New Guinea, 314, 435

Parahippolyte, 108. See also shrimps

Parasmittina, 233, 234, 235, 237– 238. See also bryozoans

Paraspadella anops, 273

Paraxiopsi spinipleura, 185– 186

parrotfi sh, 34, 407, 408. See also fi sh

Paspalum distichum, 420

Pasythea tulipifera, 232, 233, 235

peanut worms, 209. See also sipunculans

peat. See mangrove forest(s): peat

Pectinia paeonia, 441

Pelagomacellicephala iliffei, 273, 274. See also polychaete 

worms

pelagosphera, 33– 34, 210, 212, 214– 216

Pelican Cays, 60, 157, 281, 417

periwinkle, 58

pesticides, 380

Peyssonnelia, 445

Phascolion

cryptum, 33, 215

strombus, 215

Phascolosoma, 215– 216. See also sipunculans

phosphorous limitation, 346, 355, 404

photosynthetically available radiation (PAR), 360, 364– 365, 

365, 365

photosynthetically usable radiation (PUR), 364– 365, 365

Phragmatopoma lapidosa, 232. See also worms

Phragmites australis, 14, 18

physiological ecology, 80– 81

phytoplankton, 62, 286, 323, 325– 327, 332, 360, 406

biomass, 325, 332

dissolved nutrients and, 340

growth, 342, 343

thermocline infl uence on, 344

See also plankton; zooplankton

plankton

ciliates, 33

larvae, 248, 441– 442

mesozoo-, 371, 372, 374– 375

phyto- (see phytoplankton)

productivity, 16

zoo- (see zooplankton)

plate tectonics, 276

Platygyra, 440, 441, 449

daedalea, 441, 446

sinensis, 440

Plaxaura, 142

Pocillopora

damicornis, 408, 446

meandrina, 261, 264– 265, 264

See also coral

Poecilosclerida, 152, 157, 503, 504

pollution, 474

polychaete worms, 53– 54, 210, 234, 249, 253, 255

polychlorinated biphenyls (PCBs), 19, 21

polymerase chain reaction (PCR), 112, 174– 175, 177, 220– 221

40_Index_515-529_Lang.indd 525 0_Index_515-529_Lang.indd 525 9/24/09 10:33/24/09 10:33
526 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Polypodium, 142, 145, 147.

Pomatogebia operculata, 185– 186

Pontonia margarita, 95. See also shrimps

Porifera. See sponge(s)

Porites, 285

astreoides, 283, 317, 318, 439, 446, 451

compressa, 408

cylindrica, 447

damicornis, 408

divaricata, 283, 314

furcata, 283, 314

porites, 283, 407

See also coral

potassium resorption effi ciency (KRE), 349, 351, 354

Pourtalesella incrassata, 233, 235

Processa, 185. See also crabs

Prorocentrum, 286, 302, 303. See also dinofl agellates

protandric simultaneous hermaphroditism (PSH), 96– 98, 

102– 106, 108

protogyny, 96

Pseudopterogorgia bipinnata, 174– 176, 174, 175, 176, 177, 

178. See also coral

public health 307

Puerto Rico, 119, 123, 136, 152, 238, 260– 261, 324

Punta Culebra Nature Center (PCNC), 86

Punta Galeta Laboratory, 76

pyranometer, 382

Pyura chilensis, 108

radiative transfer modeling, 362

rainfall, temporal changes in, 330

Rancheria Island fi eld station, 76, 83

rDNA, 66, 140, 143, 144, 145, 173– 174

reactive oxygen species, 31, 435

rebreathers, 279

Red Sea, 104– 105, 405, 429

red tide, 2, 35, 283, 286

relative dominance model (RDM), 402, 403, 405, 406, 408

remipedes, 273, 274, 275, 276

Reunion Island, 405

Rhabdadenia bifl ora, 420

Rhizophora mangle, 54, 58, 151, 282, 346– 347, 348, 349– 350, 

350, 354, 355– 356, 416, 420, 422, 422, 424, 426, 

461, 474, 492, 494– 496, 502

rhodamine fl uorescent dye, 480, 485

Rhode River, Chesapeake Bay, 4, 12– 19, 13, 14, 15, 18, 

370– 371, 374– 376, 392, 396

Rhynchocinetes typus, 95. See also shrimps

Rypticus, 67. See also fi sh

Salicornia virginica, 420. See also saltmarsh

salt marshes, 12, 14, 15, 16, 18, 346, 399, 491– 492, 496

San Blas Archipelago, 7, 75

San Blas islands, 76, 78

sand dollars, 32

Sarcophyton glaucum, 447

Sargassum, 404, 408

polycystum, 446

See also algae: macroSavignyella lafontii, 232, 233, 235, 236, 237. See also

bryozoans

scanning electron microscopy, 30, 51, 211

Schizoporella

fl oridana, 234, 236, 237

pungens, 238

unicornis, 232, 233, 234, 235

See also bryozoans

Schoenoplectus americanus (formerly Scirpus olneyi), 12, 15, 

392, 396

Scleractinian corals, 437– 438. See also coral

Scopalina ruetzleri, 160, 284, 504. See also sponge(s)

Scripps Institution of Oceanography, 51, 138

Scrupocellaria

bertholletii, 234, 235, 236, 237

regularis, 232, 233, 235

See also bryozoans

sea

grass (see seagrass)

level, 14, 315, 416, 450, 475, 487, 489

seasonal upwelling in, 335

-surface temperatures (SSTs), 260, 303, 338, 343, 376, 

389

warming, 74

See also marine; ocean

seagrass

depth limits, 363, 365

importance of, 359

light absorption by, 360

light requirements of, 360, 366

temperature, 313

as water quality indicator, 359

sea urchin, 78, 406, 449

Secchi depth, 326, 327, 330– 331, 333, 338

chlorophyll a concentration and, 332

climatic variables and, 329

factors affecting, 332

physical variables and, 330

temporal changes in, 328, 329, 330, 331, 331– 332 

See also water clarity

Secchi disc, 16

SECORE, 260

sediment(s)

characteristics of, 466– 468

Gulf of Honduras and, 389

in mangroves, 474, 497

nutrient loads, 389

40_Index_515-529_Lang.indd 526 0_Index_515-529_Lang.indd 526 9/24/09 10:33/24/09 10:33
NUMBER 38 • 527

organic content, 462, 467

reefs and, 387

senescence, 350– 351, 355

sequential hermaphroditism, 106

Sesuvium portulacastrum, 420, 498

Shorefi shes of theTropical Eastern Pacifi c Online Information 

System (SFTEP), 197, 198, 204, 206, 206, 207, 208

shrimps

abundance of, 101

geographic distribution of, 104

hermaphroditism in, 96, 106, 108

ovigerous, 97

population structure of, 101

reproductive organs of, 99

Siderastrea siderea, 283

Sinularia fl exibilis, 447

Siphonosoma cumanense, 215

sipunculans, 33– 34, 60, 209– 211, 214– 216. See also worms

Sipunculus, 215. See also peanut worms

Smithsonian Contributions to the Marine Sciences, 2

Smithsonian Environmental Research Center (SERC), 3, 4, 

12, 14, 16– 19, 30, 32, 60, 249, 250, 251– 252, 

370, 371

grand research challenges of, 12– 19

Smithsonian Foundation of Panama, 86

Smithsonian Institution, 2, 5, 8, 25– 26, 44, 79, 125, 138, 

302– 303, 307, 474, 476– 477, 480

Smithsonian Institution Field Station (Belize), 381

Smithsonian Institution Tropical Environmental Sciences 

Program, 76

Smithsonian Marine Science Network, 3

Smithsonian Marine Science Symposium, 1, 2

Smithsonian Marine Station (SMS), 249

equipment at, 28

at Fort Pierce (SMSFP), 3, 5– 6, 25, 28, 30– 36

at Link Port, 26

marine biodiversity surrounding, 32

Smithsonian Tropical Research Institute (STRI), Panama

bioinformatics offi ce of, 87

coral reef research at, 74

educational programs in, 2, 8

facilities, 8, 76, 77

location, 3, 7, 324

marine invasion studies and, 80

Punta Culebra Nature Center of, 86

research vessels, 83

snails, 108, 193

software, 28, 63, 102, 175, 262, 265, 350

soil

characteristics of, 422

elevation, 394, 393, 394, 399

erosion, 416, 420

measurement, 418– 419

shear strength, 418, 423

stability, 424

surfaces, 421

solar radiation, 330

Sorites dominicensis, 429– 430, 431, 432, 434– 435. See also

sponge(s)

South Water Cay Marine Reserve (SWCMR), 283, 287, 288

Sparisoma viride, 408. See also fi sh

Spartina

patens, 12, 392, 396

spartinae, 420

Spelaeoecia, 276. See also ostracods

Speleophria, 276

spermatophore, 97, 101

spiny lobsters, 182. See also crustaceans

Spirastrella, 60

mollis, 159, 162– 163, 164, 165, 168

See also sponge(s)

sponge(s)

abundance of, 164, 164, 167, 502, 503, 506, 

508–512

disease, 67

distribution of, 159, 165, 166, 167

dredging and, 284

dynamics, 506, 508– 509, 509

ecological characteristics of, 513

mangroves and, 50, 151, 164, 504, 505

methods for studying, 502, 511

population dynamics of, 508

species composition and relative abundance of, 502– 506, 

506, 507, 510– 512

volume, 502–504, 506–513

Spongia, 154, 157, 161, 163– 165, 167– 168, 508– 510, 513. See 

also sponge(s)

Sri Lanka, 244

staghorn coral, 266, 282, 314– 315, 317, 318, 319, 444

stalactites, 272. See also caves

stalagmites, 272. See also caves

starfi sh, 33, 68

crown of thorns, 407

statistics. See ANCOVA; ANOVA

Stephanocoenia intersepta, 319, 439, 447

Stygiomysis, 274

stygofauna, 269– 270, 273– 278

stygoxenes, 270

Stylaraea punctata, 445. See also coral

Stylophora pistillata, 408, 443, 446. See also coral

surface elevation measurement, 394

Symbiodinium microadriaticum, 430

Synnotum aegyptiacum, 232, 233, 235

Syringodium, 234, 238

fi liforme, 234, 360

See also seagrass

40_Index_515-529_Lang.indd 527 0_Index_515-529_Lang.indd 527 9/24/09 10:33/24/09 10:33
528 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

TBT, 189, 190, 194, 195

Tedania

ignis, 157, 159, 160, 162– 163, 164, 165– 166, 167, 

168– 169, 503, 504, 505, 508–510, 513 

(see also sponge(s))

klausi, 504, 505, 510, 513

temperature loggers, 432, 478

Thais, 194

Thaisella kiosquiformis, 191. See also gastropods

Thalamoporella fl oridana, 232– 233, 235

Thalassia, 182, 326

testudinum, 237, 283, 284, 360, 362– 365, 431

See also seagrass

Thalassianthus, 142, 184.

Themiste

alutacea, 215

lageniformis, 215

pyroides, 215

See also sipunculans

Thermosbaenacea, 275. See also crustaceans

Thor, 106. See also shrimps

Thyroscyphus ramosus, 231, 232

Thysanocardia nigra, 215. See also sipunculans

tide

currents, 153, 269, 272, 278, 389

cycle, 269, 477– 478, 480

elevation, 388

fl uctuation, 482, 484, 488

fl ushing, 346, 355

phases, 482

range, 416, 477, 481

wetlands, 391

See also sea

tourism, 11, 86– 87, 243, 287, 289, 303, 325, 332, 380, 426

transmission electron microscopy (TEM), 28, 211, 271

Tributyltin (TBT), 189– 190, 194– 195

Trichoplax, 63

Trinidad, 152

Tubastraea coccina, 442. See also coral

Tulumella, 272, 274. See also shrimps

tunicates, 108, 253

Turbinaria, 404

turbinata, 404

See also coral

turtle grass, 182– 183, 234, 283, 431

turtles

harvesting of, 244

hawksbill, 242

marine (see marine turtle(s))

Twin Cays, Belize

archipelago, 474

bleached coral in, 434

B. maritima studies at, 492, 494

climate, 477

hydrology 480– 486

location, 157, 416, 417, 475, 493

mangroves on, 477

oceanographic conditions, 433, 484

research at, 56, 488

seasonal climatic variations, 481

sponges of, 505

topography, 476, 480

West Island, 418– 419, 474, 476– 478, 479, 480, 481, 483, 

485, 486, 487, 494

two-way analysis of variance, 371, 395. See also ANCOVA; 

ANOVA

Typha, 420

Typhlatya, 272, 276. See also shrimps

Typhliasina pearsei, 274

Uca, 81, 459, 468, 469

abundance and biomass, 462, 463, 464, 465

biomass of, 465minax, 460

burrows, 466, 467, 467

fresh water tolerance of, 467

longisinalis, 469

mordax, 460

pugilator, 460, 466

pugnax, 460

rapax, 460, 462, 465, 466, 468, 469

sex distribution of, 465, 466

size distribution of, 466

speciosa, 460, 462, 465, 466, 468, 469

spinocarpa, 469

substrate and salinity preferences, 468

temperature tolerance of, 469

thayeri, 460, 462, 463, 465, 466, 468, 469

See also crabs

Ulva, 444, 446

UNESCO World Heritage List, 283

United Nations

Convention on the Law of the Sea (UNCLOS), 243

Educational, Scientifi c and Cultural Organization 

(UNESCO), 51

Environmental Programme (UNEP) Regional Seas 

convention, 243

Food and Agriculture Organization (FAO), 244, 303

United States

Antarctic Program (USAP), 5

Army Corps of Engineers, 35

Convention for Migratory Species, 243

Environmental Protection Agency, 16, 28, 76

Geological Survey, 48, 86

National Oceanic and Atmospheric Administration 

(NOAA), 302– 303

National Science Foundation, 45, 182

University National Oceanographic Laboratory System 

(UNOLS), 7

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Upogebia, 185– 186

acanthura, 186

corallifera, 186

missa, 186

vasquezi, 186

See also crabs

Uruguay, 220, 242

Vaughaniella, 404. See also algae: turf

Venezuela, 83, 118– 119, 121, 123, 137– 138, 151, 152, 159, 

166, 324, 405, 502, 510, 512

Virginia Institute of Marine Science (VIMS), 249

water

absorption spectra, 364

clarity (see water clarity)

depths and velocities, 484

mangrove forests and, 485

temperature and bleaching, 432

water clarity, 16, 17, 272, 325, 328, 333, 381, 383, 431

factors affecting, 332, 333

incident solar radiation and, 388

measurement, 361

phytoplankton and, 343

seagrass and, 359

signifi cance of, 323

turbidity and, 387

watershed nutrient discharge, 4, 16

Watersipora, 232

subtorquata, 232, 233, 234, 235

See also bryozoans

wetlands

coastal, 474, 492

mangrove, 346

marginal, 460

restoration 35

tidal, 391

tropical, 473

white mangrove. See mangrove forest(s): white

wind speed, 330

World Heritage Site, 6, 83, 87, 287, 288

World Register of Marine Species (WoRMS), 202

World Trade Organization (WTO), 244

worms

cnidarian (see cnidarian worms)

fl at-, 80

nemertine, 44

peanut, 209

sabellariid, 58, 231– 232, 269

sipuculan, 33– 34, 60, 209– 211, 214– 216

tube (see worms: sabellariid)

WoRMS (World Register of Marine Species), 202

Xestospongia bocatorensis, 152

Yucatan, 324

Yucatan Peninsula, Mexico, 269, 271, 275, 278– 279, 416

zooarchaeology, 82

Zoobotryon verticillatum, 233, 235, 236, 237. See also

bryozoans

zooplankton

egg production, 374– 375

environmental conditions for, 372

gelatinous, 370– 371, 376

polyps, 375

zooplanktivorous, 370

Zoothamnium, 67

zooxanthellae, 6, 82, 241, 265, 430, 435, 439, 440, 442, 446

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SERIES PUBLICATIONS OF THE SMITHSONIAN INSTITUTION

Emphasis upon publication as a means of “diffusing knowledge” was 

expressed by the fi rst Secretary of the Smithsonian. In his formal plan 

for the Institution, Joseph Henry outlined a program that included 

the following statement: “It is proposed to publish a series of reports, 

giving an account of the new discoveries in science, and of the changes 

made from year to year in all branches of knowledge.” This theme of 

basic research has been adhered to through the years by thousands of 

titles issued in series publications under the Smithsonian imprint, commencing with Smithsonian Contributions to Knowledge in 1848 and 

continuing with the following active series: 

Smithsonian Contributions to Anthropology

Smithsonian Contributions to Botany

Smithsonian Contributions in History and Technology

Smithsonian Contributions to the Marine Sciences

Smithsonian Contributions to Museum Conservation

Smithsonian Contributions to Paleobiology

Smithsonian Contributions to Zoology

In these series, the Institution publishes small papers and full-scale 

monographs that report on the research and collections of its various 

museums and bureaus. The Smithsonian Contributions Series are 

distributed via mailing lists to libraries, universities, and similar institutions throughout the world. 

Manuscripts submitted for series publication are received by the 

Smithsonian Institution Scholarly Press from authors with direct affi liation with the various Smithsonian museums or bureaus and are subject 

to peer review and review for compliance with manuscript preparation 

guidelines. General requirements for manuscript preparation are on the 

inside back cover of printed volumes. For detailed submissions requirements and to review the “Manuscript Preparation and Style Guide for 

Authors,” visit the Submissions page at www.scholarlypress.si.edu.

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