Smithsonian Institution

Scholarly Press

Smithsonian Institution

Scholarly Press

Research and Discoveries

The Revolution of Science

through Scuba

Edited by

Michael A. Lang, Roberta L. Marinelli, 

Susan J. Roberts, and Phillip R. Taylor

smithsonian contributions to the marine sciences • number 39
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smithsonian contributions to the marine sciences • number 39

Research and Discoveries 

The Revolution of Science

through Scuba

Edited by

Michael A. Lang, Roberta L. Marinelli, 

Susan J. Roberts, and Phillip R. Taylor

washington d.c.

2013
ABSTRACT

Lang, Michael A., Roberta L. Marinelli, Susan J. Roberts, and Phillip R. Taylor, editors. Research and Discoveries: The Revolution of Science through Scuba. Smithsonian Contributions to the Marine Sciences, number 39, vi + 258 pages, 111 figures, 

7 tables, 2013. The Smithsonian Institution, the National Science Foundation, and the Ocean Studies Board of the National 

Research Council convened the “Research and Discoveries: The Revolution of Science through Scuba” symposium on 24–25 

May 2010 in Washington, D.C., to celebrate the advances and scientific contributions of research using self-contained underwater breathing apparatus (scuba). This volume presents 19 papers by 60 scholars of research findings, with particular 

focus on the scientific contributions accomplished using scuba. It is the first major effort to highlight and validate the use of 

scuba in science by evaluating the output of scientific research in high-impact journal publications. Thirteen papers report 

research findings and discoveries from around the world in environments such as coral reefs, oceanic blue water, under-ice 

polar habitats, and temperate kelp forests, providing perspectives on ecological scales and function, physiology, symbiosis and 

chemistry, biodiversity and behavior, and structured populations. The final six papers are illustrative of underwater research 

that was not only greatly facilitated by scuba, but could perhaps not have been accomplished without it. Topics range from 

biological studies on the coral holobiont to ecological roles of major algal groups on reefs and the functional role of small 

and cryptic metazoans. The research facilitated by scuba and reported in these papers focuses on the scientific results, not 

necessarily on the research methodologies using scuba to obtain those data and observations, and includes several case studies. Where appropriate, laboratory studies complementary to underwater field observations are referenced. The symposium 

showed the strong integration and validation of scientific diving within the overall science domain since the introduction of 

scuba to the science community in 1951. Overarching symposium themes celebrated past, present, and future scientific diving 

contributions, and evaluated the accomplishments and impact of underwater research on the overall understanding of nature 

and its processes. Enduring materials from the symposium, including abstracts, speaker biographies, and webcast videos of 

presentations, have been posted at www.si.edu/sds.

Cover images (left to right): Pseudopterogorgia elisabethae sea fan from Carrie Bow Cay, Belize (photo by Raphael RitsonWilliams); Macrocystis pyrifera kelp from San Diego, California (photo by Michael A. Lang); Leptonychotes weddelli seal 

from McMurdo Station, Antarctica (photo 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

Compilation copyright © 2013 Smithsonian Institution

Text and images in this publication, including cover and interior designs, are owned either by the Smithsonian Institution, 

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Library of Congress Cataloging-in-Publication Data

Research and discoveries : the revolution of science through scuba / edited by Michael A. Lang, Roberta L. Marinelli, Susan 

J. Roberts, and Phillip R. Taylor.

pages cm. — (Smithsonian contributions to the marine sciences number ; 39)

Includes bibliographical references.

1. Scuba diving. 2. Marine sciences. 3. Underwater exploration. I. Lang, Michael A. 

GV838.672.R47 2013

797.2’34—dc23

2013020367

ISSN: 0196-0768 (print); 1943-667X (online)

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.
Contents

EXECUTIVE SUMMARY v

THE REVOLUTION OF SCIENCE THROUGH SCUBA

Scuba Revolutionizes Marine Science 3

Jon D. Witman, Paul K. Dayton, Suzanne N. Arnold, 

Robert S. Steneck, and Charles Birkeland

Diving into the Past: Scuba and the Temporal Dimension of Coral Reefs 13

Ian G. Macintyre and Richard B. Aronson

Diving Physiology and Decompression Sickness: Considerations from 

Humans and Marine Animals 23

Michael A. Lang, Jessica U. Meir, Tanya L. Streeter, 

and Karen B. Van Hoesen

Saturation Diving and Underwater Laboratories: How Underwater 

Technology Has Aided Research on Coral Biology and Reef Ecology 39

Kenneth P. Sebens, Giacomo Bernardi, Mark R. Patterson, 

and Deron Burkepile

Marine Chemical Ecology: A Science Born of Scuba 53

Joseph R. Pawlik, Charles D. Amsler, Raphael Ritson-Williams, 

James B. McClintock, Bill J. Baker, and Valerie J. Paul

Scuba Diving in Blue Water: A Window on Ecology and Evolution 

in the Epipelagic Ocean 71

Laurence P. Madin, William M. Hamner, Steven H. D. Haddock, 

and George I. Matsumoto

Scientific Polar Ice Diving 83

Adam G. Marsh, Amy L. Moran, and James B. McClintock

The Use of Scuba to Study Early Life Histories of Marine Invertebrates 87

Harilaos A. Lessios, Howard R. Lasker, and Don R. Levitan

Behavioral Ecology of Mobile Animals: Insights from In Situ Observations 99

David B. Eggleston, William F. Herrnkind, and Anson H. Hines

Kelp Forests in California 115

Michael S. Foster, Daniel C. Reed, Mark H. Carr, Paul K. Dayton, 

Daniel P. Malone, John S. Pearse, and Laura Rogers-Bennett 
i v • smithsonian contributions to the marine sciences

Kelpbeds as Classrooms: Perspectives and Lessons Learned 133

John S. Pearse, Mark H. Carr, Charles H. Baxter, James M. Watanabe, 

Michael S. Foster, Diana L. Steller, James A. Coyer, Brenda Konar, 

David O. Duggins, and Paul K. Dayton

Rhodoliths and Rhodolith Beds 143

Michael S. Foster, Gilberto M. Amado Filho, Nicholas A. Kamenos, 

Rafael Riosmena-Rodríguez, and Diana L. Steller

How Scuba Changed Our Understanding of Nature: Underwater 

Breakthroughs in Reef Fish Ecology 157

Mark H. Carr, Daniel P. Malone, Mark A. Hixon, Sally J. Holbrook, 

and Russell J. Schmitt

RESEARCH FACILITATED BY SCUBA

INTRODUCTION 171

Michael A. Lang, Roberta L. Marinelli, Susan J. Roberts, 

and Phillip R. Taylor

Understanding the Coral Holobiont through Science and Scuba 173

Steve V. Vollmer, Andrew C. Baker, Mary-Alice Coffroth, 

C. Drew Harvell, and Mónica Medina

The Nature of Macroalgae and Their Interactions on Reefs 187

Mark M. Littler and Diane S. Littler

The Nature of Crustose Coralline Algae and Their Interactions on Reefs 199

Mark M. Littler and Diane S. Littler

The Nature of Turf and Boring Algae and Their Interactions on Reefs 213

Mark M. Littler and Diane S. Littler

The Ecological Significance of Sexual Reproduction by Tropical Green Algae 219

Kenneth E. Clifton

Fine-Scale Interspecific Interactions on Coral Reefs: Functional Roles 

of Small and Cryptic Metazoans 229

Peter W. Glynn

ABOUT THE CONTRIBUTORS 249
Executive Summary

The Smithsonian Institution, the National Science Foundation, and the Ocean Studies Board of the National Research Council convened a symposium in May 2010 

in Washington, D.C., to celebrate the scientific contributions and value of scuba 

as a research methodology. The “Research and Discoveries: The Revolution of Science 

through Scuba” symposium presented research findings by U.S. scholars with particular focus on the scientific contributions accomplished using self-contained underwater 

breathing apparatus. This symposium was the first major effort to highlight and validate 

the use of scientific diving techniques by evaluating the output of scientific research that 

has been presented through high-impact journal publications.

During the two-day event, fifty scholars discussed their research findings and discoveries from around the world on coral reefs, blue-water environments, under-ice polar 

habitats, temperate kelp forests, and other systems of interest. This symposium showed 

the strong integration and validation of scientific diving within the overall science domain since the introduction of scuba to the science community in 1951. Overarching 

symposium themes celebrated past, present, and future scientific diving contributions, 

and evaluated the accomplishments and impact of underwater research on our overall 

understanding of nature and its processes. Exemplars of the first generation of scientific 

diving research include Paul Dayton’s groundbreaking ecological work under Antarctic 

ice sheets; William Hamner’s pioneering studies of gelatinous zooplankton in surficial 

blue waters of the open ocean; Mark and Diane Littler’s multidisciplinary long-term 

phycological studies; William Herrnkind’s crustacean behavioral ecology research; John 

Pearse and Michael Foster’s kelp forest ecological work; and Ian Macintyre, Peter Glynn, 

and Chuck Birkeland’s baseline-establishing coral reef research. 

Approximately thirty years after the advent of scuba another research tool, molecular techniques, became more generally available to marine scientists. Together these two 

tools offer broad techniques to further our understanding of biodiversity, systematics, 

and genomics. The advances in biopharmaceutical work and the understanding of chemical defenses of marine organisms, harmful algal bloom outbreaks, and invasive species 

have encouraged more scientists to don scuba gear and conduct their research under 

water. In an era of increasing occurrences of multiple stressors on such systems as coral 

reefs, deep-time geological studies show patterns and trends of previous episodic events. 

It continues to be difficult to understand ecological processes and interactions and the 

functioning of nature itself in the underwater environment without actually immersing 

oneself in it to make firsthand observations and data collections. 
v i • smithsonian contributions to the marine sciences

Enduring materials from the symposium, including abstracts, speaker bios, and webcast videos of presentations, have 

been posted on the website www.si.edu/sds.

Michael A. Lang

Smithsonian Institution; now at The Ocean Foundation

Roberta L. Marinelli

National Science Foundation, Antarctic Sciences Division, 

Antarctic Organisms and Ecosystems Program; 

now at University of Southern California

Susan J. Roberts

National Research Council, Ocean Studies Board

Phillip R. Taylor

National Science Foundation, Ocean Sciences Division, 

Ocean Section; now at University of Southern California
The Revolution of Science through Scuba

Scuba Revolutionizes Marine Science

Jon D. Witman, Paul K. Dayton, Suzanne N. Arnold, 

Robert S. Steneck, and Charles Birkeland

ABSTRACT. Scuba provides scientists with the capacity for direct observation and experimental 

manipulation in underwater research. Technology allows broader-scale observations and measurements such as satellite detection of coral bleaching up to a global scale and LIDAR determination of 

reef-wide topographic complexity on landscape to regional scales. Scuba-based observations provide 

a means of ground truthing these broad-scale technologies. For example, ground truthing the readings on a scale as small as a video transect taken at 50 cm above the substratum can reveal that the 

previously confident interpretation of the transect data from the video analysis was inaccurate. At 

the opposite end of the spatial continuum, electron microscopy and DNA analysis provide the capacity to determine species traits at a scale too fine for direct observation, while observations made 

during the collection of samples by scuba can provide vital information on the context of the tissue 

sample collection. Using our hands and eyes to set up experiments under water is less expensive and 

more adaptable to the unexpected topographic complexities of hard substratum habitats than doing 

so with submersibles, robots, or via cables from ships. The most profound contribution of scuba to 

underwater science, however, is the otherwise unobtainable insights provided by direct observation. 

Ecology is not always predictable from species traits because the behavioral or interactive characteristics of marine organisms together cause them to function in surprising and often synergistic 

ways. Although our research is often framed around hypotheses developed by deductive reasoning, 

the solutions to research questions cannot always be found by deduction. Data taken by video or 

sensors from satellites, tow-boards, or other vehicles are all incomplete in their context evaluation 

in comparison to direct observation by the human brain. Scuba provides a unique ability to integrate detail with context across small and large scales. The history of marine research has provided 

numerous examples of mysteries that would have been unsolved and findings that would have been 

misinterpreted with confidence if not for direct observation on scuba. We illustrate this aspect of the 

utility of scuba for science with three examples of how direct observation of species in their natural 

habitats has furthered the development of ecological concepts. 

INTRODUCTION

Since the ecological impacts of humans have become global (climate change, lowering of ocean pH, loss of one-third of global topsoil, deforestation, desertification, 

transport of invasive species, etc.), scientists have felt the necessity to measure ecological processes on larger spatial scales. The April 2004 issue of the journal Coral Reefs

was devoted entirely to remote sensing of coral reefs, using sensors from satellites and 

aircraft to assess percentage of living coral cover, percentage of coral bleaching, biomass 

of fleshy algae, rugosity of substratum, transport of dissolved organic matter, transport 

of fine-sediment, and other variables on a large scale. While the focus on global and ecosystem processes is indeed imperative (Dayton and Tegner, 1984; Sala, 2001; Witman and 

Roy, 2009), controlled field experiments and carefully designed surveys and monitoring 

Jon D. Witman, Box G-W, Ecology and Evolutionary Biology, Brown University, Providence, Rhode 

Island 02912, USA. Paul K. Dayton, Mail Code 

0227, Scripps Institution of Oceanography, La 

Jolla, California 92093-0227, USA. Suzanne

N. Arnold, Darling Marine Center, University of 

Maine, 193 Clark’s Cove Road, Walpole, Maine 

04573, USA. Robert S. Steneck, Darling Marine 

Center, University of Maine, 193 Clark’s Cove 

Road, Walpole, Maine 04573, USA. Charles

Birkeland, Department of Biology, University 

of Hawaii at Manoa, Honolulu, Hawaii 96822, 

USA. Correspondence: J. Witman, Jon_Witman

@brown.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
4 • smithsonian contributions to the marine sciences

programs could be completely misinterpreted if analysis of data 

obtained via scuba is not also incorporated.

Scuba created a scientific revolution by providing direct access to underwater habitats composing a large part of the biosphere. While there have been many important specific advances 

(noted in this volume), we believe that the overarching benefit of 

scuba for marine population, community, and ecosystem ecology 

has been to facilitate the direct observation and manipulations of 

individual organisms and their surrounding conditions. Prior to 

scuba, subtidal organisms were studied primarily by peering into 

the water on calm days (e.g., Darwin, 1909; Johnson and Skutch, 

1928) and by analyzing specimens collected by fishing, dredging, 

or plankton nets (e.g., the HMS Challenger expedition). The invention of scuba enabled scientists to observe the behavior and 

ecology of organisms in their natural habitats, quantify patterns, 

study interactions, and conduct experiments to test hypotheses 

about ecological processes. 

Scuba has been associated with an increasing number of 

scientific publications (Figure 1) and the rapid increase in our 

knowledge of marine biodiversity. One example: since the 1950s, 

there has been a consistent increase in the number of newly identified marine fish species per five-year period, from 305 in 1954–

1958 to 846 in 2004–2008. Eschmeyer et al. (2010) documented 

this increase and emphasized the role of scuba.

DISCUSSION

Ground Truthing Theory and

Ground-Breaking Findings

Hypotheses are tested by replicated, controlled, manipulative field or laboratory experiments, or by determining if the 

patterns discerned by surveys or monitoring programs correlate 

with the patterns predicted by the hypotheses. But the hypotheses 

to be tested are created by deductive reasoning of prior concepts. 

Without direct observation by scuba, models can lead to misconceptions. For example, in the 1960s, an unresolved issue in 

the data for coral reef ecosystems was that there was not nearly 

enough plankton to support the large biomass of suspensionfeeding invertebrates and planktivorous fishes. Extensive and repeated surveys only reinforced the existence of this inconsistency 

in the models of required supply for the demand, until Bill Hamner and colleagues on scuba directly observed the behavioral 

and distributional characteristics of zooplankton on coral reefs 

(Hamner and Carleton, 1979). The behavior of the zooplankton indicated that the majority were resident and not drifting 

in from the surrounding waters. The scuba-based observations 

indicated that it was not possible for standard, surface-towed 

plankton nets to adequately quantify zooplankton on coral reefs.

This led to the development of plankton traps that were more 

appropriate for assessing the zooplankton resident on coral reefs 

(Porter and Porter, 1977; Alldredge and King, 1977). The results 

of studies with demersal plankton traps developed and operated 

via scuba totally changed the understanding of the behavior and 

distribution of zooplankton and their role in coral reef ecosystem 

processes. Without scuba, the energy balance of coral ecosystems 

in the oligotrophic mid-ocean would still be a mystery.

Evolution of biotic characteristics is not entirely predictable 

by deductive reasoning, so knowledge of natural history cannot 

be complete without learning from direct observation in nature. 

Deductive reasoning provides a series of alternative hypotheses, 

but the truth might be in none of the hypotheses because we were 

not sufficiently circumspect of key aspects of natural history. We 

might have concluded the study with accepting that the results 

confirmed the best of the available hypotheses, even though the 

FIGURE 1. The use of scuba in the production of scientific papers in biology and oceanography has 

increased exponentially over the past few decades (data from ISI website).
number 39 • 5

closest fit was false. Indeed, many models make the right predictions for the wrong reason because the modelers lack critical natural history (Dayton, 1973) available with scuba. For example, 

until the mid-1970s blue water oceanographers would bemoan 

the ubiquitous slime that fouled the inside of their nets during 

plankton tow surveys. Then, Hamner et al. (1975) published a 

landmark study showing that the slime was in fact a huge predator now categorized as gelatinous zooplankton. 

Scuba allows a more panoramic, multi-dimensional, and unrestricted view than do cameras or other sensors that are developed for a subset of all signals characteristic of the underwater 

world. No instrumentation in the ocean has such detailed perception across large scales as humans with scuba. It is the capacity 

of scuba observers to integrate nearly simultaneous observations 

from the calices of corals to the presence of apex predators that 

makes it possible to verify our perceptions. Although satellites 

and LIDAR from aircraft generate information on a larger scale 

than humans, their perceptions are not fine enough to distinguish 

species. While DNA analysis and electron microscopy record information on a finer scale than possible by humans with scuba, 

the human observer has the essential ability to place the tissue or 

corallite sample in its natural context. It is this unique ability to 

integrate detail with context across small and large scales (e.g., 

from the details of the coral polyp to the community structure 

of apex predators) that makes the observer on scuba absolutely 

vital for the advancement of marine science. 

On the finer scales of direct observation, the species identification of small individuals of corals such as mound-shaped 

Porites and encrusting Montipora in the central and western 

Pacific and Indian Oceans cannot be done reliably from video 

images or from submersibles. Porites randalli, a ubiquitous and 

often most abundant coral on American Samoan reefs (Forsman 

and Birkeland, 2009), is readily recognized by a scuba diver, but 

for decades (1917–1978), specimens of this species had been assumed to be an assortment of small individuals of other species. 

Although specimens can be collected by other means (e.g., hardhat diving, submersibles, dredge, trawl, etc.) for genetic analyses 

of tissue samples and electron microscopy of corallite structure 

for final species descriptions, the awareness of the existence of 

the most abundant coral species would not have occurred without scuba. It is possible that once the distinction of this species 

was recognized by humans through the use of scuba, it might 

also be recognized by video or submersible. Without scuba, data 

analysis from surveys of American Samoan reefs might have 

failed to identify the most common species and mistakenly elevate the abundances of several other less common species of 

Porites. For example, in a 1995 survey that included 140 coral 

species, there were 2,289 recordings of Porites randalli, which 

composed 18% of the coral colonies; spreading these 2,289 data 

over several less common species would have given very misleading survey results (Forsman and Birkeland, 2009).

On the larger scales that apex predators occupy, observers 

with scuba are able to perceive potential biases of underwater 

imaging systems typically used in surveys. When surveying with 

video or other camera systems, the equipment is usually unidirectional with a fixed field of view and is not that sensitive to 

unexpected insights from other dimensions. For example, when 

doing tow-board surveys of large fishes, some species (e.g., the 

large jack Caranx ignobilis and the sharks Carcharhinus amblyrhynchos and C. galapagensis) show a tendency to aggregate 

behind towed divers (Benjamin Richards, NOAA Pacific Islands 

Fisheries Research Center, personal communication). On coral 

reefs, Sphyraena barracuda are known to swim above and behind divers—a commonly noted behavior (C. Birkeland, J. Witman, unpublished observations). These barracuda would not be 

recorded by a forward-facing camera system, which could lead 

to large underestimates of population densities.

Studies of predation on corals in Hawaii provide another 

example of how conclusions would have been very misleading 

without direct observations by scientists on scuba. The most 

common coral on the Hawaiian main islands, Porites compressa,

receives an average of 69 fresh bites/m2

, and these bites were attributed to the common parrot fishes (Jayewardene et al., 2009). 

However, direct observations demonstrated that different corallivorous fishes have characteristically different bites (Jayewardene 

et al., 2009: fig. 2) and that these bites were made by puffers 

(Arothron spp.) that are relatively scarce. This was a conundrum 

until scuba divers observed that less than 2% of the bites of parrot fishes in Hawaii were on living corals and these few exceptions were at the edge of the coral where the coral contacted 

algae (Ong, 2007). Although the puffers rarely showed up on 

survey data, direct observations indicated that the puffers were 

common but were skittish in their behavior and darted for cover 

beneath large Porites colonies or other shelter. Fishes with such 

behavior are not adequately represented in survey data (Jennings 

and Polunin, 1995). It is the capacity of observers with scuba to 

integrate observations from small to large scales that provides us 

with the unique ability to verify our perceptions.

Scuba also provides insight into dimensions of topographically complex benthic habitats that might be missed by other 

survey methods. For example, coral planulae in shallow waters 

(<10 m depth) tend to settle and undergo metamorphosis on 

undersurfaces or on vertical surfaces, sometimes beneath algae 

(Birkeland, 1977). Studies with video transects might conclude 

that the broad spatial extent of the deterioration of the reef to 

rubble by A. planci and bioerosion might have reduced the larval 

supply, whereas scuba-based observations have suggested that 

diverse larval supply was sufficient and that survival of settled 

corals on unstable substrata was low or nonexistent. Subtidal 

surveys or experimental studies without direct observations by 

divers on scuba could render unwarranted conclusions.

In all of our examples above, breakthroughs resulted from 

applying scuba to key ecological questions. Note, however, that 

most of these scientific discoveries occurred around or before 

the late 1970s. Considering the accelerating rate of scientific 

publications that followed (Figure 1), it is clear that the early 

observations primed the pump of the scuba science revolution. 

In the remaining sections, we discuss applications of scuba to 
6 • smithsonian contributions to the marine sciences

management, how it has promoted new insights into natural history, aided paradigm shifts, and contributed to ecological theory 

in a least three key areas of ecological research.

Revealing Heterogeneity for Improved Management

For decades, details of the life history of marine species 

were relatively unknown to biologists charged with managing 

economically important fisheries. Information was acquired primarily through catch data and trawl surveys. Discoveries made 

by scuba in temperate, tropical, and subarctic waters are now 

instrumental in managing fisheries and conserving ecosystems. 

For example, before scuba diving, American lobsters (Homarus 

americanus) in the Gulf of Maine were assumed to have a relatively homogenous population, and no one knew where lobsters 

recruited. Experiments via scuba allowed us to determine that 

this species selects cobblestone habitats as its nursery ground, 

and there it is safe from predators for the first few years of life 

(Wahle and Steneck, 1991, 1992). When the lobsters emerge 

from these early, benthic-phase refugia, they have outgrown their 

predators; thus this species has remarkably low post-settlement 

mortality (Butler et al., 2006; Steneck, 2006a). As a result, populations of this lobster have settlement-driven demography (Palma 

et al., 1999), with “hotspots” fueling high population densities 

(Steneck and Wilson, 2001) that drive intraspecific competition 

pressure (Steneck, 2006b). These experiments show that as population densities increase, competition increases and a counterintuitive thing happens: large, competitively dominant lobsters, 

which have no choice but to fight with every lobster within 

their range of detection, diffuse from the zones of competition 

to where population and trap densities are lower; thus, by default, the chance of being caught declines (Steneck, 2006b). This 

allows numbers of large reproductive lobsters to build up and 

serve as broodstock for future generations (Steneck, 2006a). Annual monitoring via scuba of lobster recruitment along the coast 

of Maine contributes to the American lobster fishery’s status as 

one of the best managed fisheries in the world.

Decades of research via scuba have documented cascading 

processes and shifting baselines on coral and temperate reefs 

(Witman and Sebens, 1992; Dayton et al., 1998; Bellwood et 

al., 2004; Tittensor et al., 2009). Since the 1970s, diving scientists have documented the structuring dynamics of overfishing, 

declining herbivory, increasing algal biomass, and coral recruitment on coral reefs (reviewed in Sandin et al., 2010). The ramifications of overharvesting predators of sea urchins on coral and 

temperate reefs are now well known (Estes and Duggins 1995; 

McClanahan et al., 1999; reviewed in Steneck et al., 2002). In 

sum, this work has influenced the development of many marine 

protected areas, and the establishment of laws restricting fishing gear and the take of certain ecologically critical fish such as 

herbivores. Without spatially explicit scuba-generated data, this 

information would not be available for application to fisheries 

management and policy decisions.

Grasping Natural History

The ability to observe marine life in situ has fostered extensive research on intrinsic variables of organisms. While the 

observational–inductive approach to constructing general scientific theories suffers from the inability to falsify hypotheses (Popper, 1959), in situ observation nonetheless provides a valuable 

grounding in natural history that is required to understand the 

population biology of and interactions among organisms to gain 

a mechanistic understanding of the functioning of marine communities and ecosystems. Addressing many of the most pressing 

societal issues—such as how populations and communities will

react to and recover from climate change and human-induced

disturbances—requires a firm grasp of natural history (Dayton,

2003), without which ecologists may accept the right hypothesis 

for the wrong reason (Dayton, 1973), fail to recognize strong controlling interactions of consumer species, or oversimplify complex 

ecological communities, leading to inaccurate generalizations. Although investigations of climate change effects typically explain 

temporal population and community trends by physical factors 

extrinsic to local populations, substantial temporal variation may 

also be driven by intrinsic variables such as Allee effects, allocation tradeoffs, life history traits, behavior, and physiological 

limitations of organisms. The value of scuba lies in its ability to 

provide a window to view these fundamental attributes. 

As we find ourselves in an age where people are increasingly 

disconnected from nature, scuba can also be a tool to attract 

young people to science. The sheer excitement of breathing under 

water and seeing a hidden world can inspire the next generation of scientists to take an interest in natural history, just as it 

inspired us. 

Paradigm Shifts

The aquatic and marine sciences are relatively unique because most of what is studied is underwater and out of sight. 

Traditionally, this was handled by oceanographers measuring 

particles and concentrations to establish correlations and construct predictive models. In many cases, bottom-up (i.e., resourcedriven) explanations prevailed when the organisms were treated 

as invisible components of the system.

G. E. Hutchinson (1959:147) pointed out that both Wallace (1858) and Elton (1927) asserted that food webs were constructed such that “the predator at each level is larger and rarer 

than its prey.” This pattern became known as the Eltonian food 

pyramid and it developed into the field of trophic dynamics (sensu

Lindeman, 1942). In this view, each trophic level is “successively 

dependent upon the preceding level as a source of energy” (Lindeman, 1942:415). In other words, the primary interactions resulted from lower trophic levels fueling those at the top. Today, 

this is called bottom-up control of community structure (sensu

Power, 1992). Hairston et al. (1960) proposed a decidedly different interpretation of that pattern. Rather than resources at lower 
number 39 • 7

trophic levels fueling higher trophic levels (bottom-up), consumers at higher trophic levels limit the abundance of lower trophic 

levels (top-down) (sensu Power, 1992). This paradigm shift is 

much more than changing terminology. While predators had 

long been considered part of natural communities, they had been 

thought of as “passengers” carried by the resources available in 

the ecosystem. What had been underappreciated was that predators could be “drivers” of the system by limiting the abundance 

of their prey. This new way of thinking opened new avenues of 

ecological theory focused on the community-wide impacts of 

higher-order predators on organisms at lower trophic levels. This 

paradigm shift resonates today in high-impact scientific journals 

(Estes et al., 2011). 

What scuba diving allowed marine ecologists to do was to 

test these differing world views by observing and manipulating 

direct ecological interactions such as predation and competition. With scuba, correlative studies could identify patterns but 

were no longer considered proof of what caused those patterns. 

Quantitative, experimental marine ecology in the broader ocean 

was possible primarily because in situ manipulations could be 

conducted by scuba diving (Witman and Dayton, 2001). In the 

sections below, we discuss how three ecological topics informed 

and enlightened by an in situ experimental approach taken by 

scuba diving ecologists have developed or broadened ecological 

concepts. This is not intended to be an inclusive discussion of the 

topic, but rather a means of illustrating the overarching scientific 

value of scuba. 

Top-­Down Regulation of Food Webs

The importance of both direct (consumptive) and nonconsumptive (behavioral) trophic cascades is becoming well understood in ecology (Peckarsky et al., 2008). Scuba has made it 

possible to observe and understand both important consumptive effects and behavioral responses (Siddon and Witman, 2004) 

to predation that cascade down to lower trophic levels. While 

the sea otter–sea urchin–kelp trophic cascade is well known as 

a classic consumptive cascade (Estes and Palmisano, 1974; Estes 

and Duggins, 1995), behavioral interactions of urchins with their 

predators are sometimes overlooked despite the fact that early 

studies documented strong reactions. For example, escape behaviors from a sea star resulted in the urchins being an important 

part of the diet of anemones in Washington state (Dayton, 1973). 

Using scuba, Mauzey et al. (1968) and Dayton et al. (1977) 

found many examples of effective escape behaviors that critically 

modify our understanding of foraging biology because it forces 

a careful consideration of “catchability” into our interpretation 

of trophic dynamics.

In addition, perceptive observers are able to observe nuances 

of behavior that provide critical understanding to various patterns seen in nature. For instance, clear areas around foundation 

species (Dayton, 1975) were thought to result from allelopathic 

factors as in chaparral-dominated plant communities. However, 

Randall (1965) demonstrated that on coral reefs, they resulted 

from a zone of fear in which grazer foraging was restricted by the 

presence of predators, providing a mechanistic explanation for 

the commonly observed coral reef grazing halos. More recently, 

Siddon and Witman (2004) used scuba in the Gulf of Maine to 

examine variation in the strength of trophic cascades in different but common types of shallow subtidal habitats and found 

that the fear of lobsters prevented rock crabs from foraging on 

urchins, which caused less predation on mussels, providing the 

first example of a non-consumptive trophic cascade in subtidal 

ecosystems. Recent experiments in this system indicated that interspecific competition between the dominant lobster and subordinate crab caused crabs to escape vertically from lobsters by 

climbing up kelp stipes (Wells et al., 2010). Grabowski and colleagues have similarly found strong effects of predator avoidance 

behaviors on trophic cascades in subtidal habitats of Chesapeake 

Bay (Grabowski and Kimbro, 2005; Grabowski et al., 2008). It is 

clear that scuba-based research will continue to stimulate important insight into the role of behavior in driving trophic cascades.

Emergent Properties of Communities Revealed

by Studying Functional Groupings and Guilds

The structure of ecosystems and communities is usually 

described from a simple tally of what is there. Terrestrial and 

aquatic ecologists were occupied with determining number of 

species, how biomass is distributed, and which species dominate 

for nearly a century before the new focus on ecological function 

emerged. Ecosystem function usually relates to driving processes 

such as reproduction, recruitment, growth, productivity, stress, 

competition, predation, and biodiversity. 

In recent decades, several lines of research determined that 

functional attributes of organisms may be more important than 

their relatedness. For example, in the Gulf of Maine, the largest 

crab, Cancer borealis, forages bivalve prey in ways more similar 

to the lobster Homarus americanus than to its closely related 

congener C. irroratus. The latter crab forages identically to an 

unrelated non-native green crab, Carcinus maenus (Moody and 

Steneck, 1993). Similar shared functional attributes have been 

observed among herbivorous mollusks (Steneck and Watling, 

1982), reef fishes (Hixon, 1997; Bellwood et al., 2004), and 

benthic marine algae (Steneck and Dethier, 1994). By observing 

behaviors in situ we come to develop new paradigms on how 

organisms use resources and interact. These new paradigms allows us to advance and test falsifiable hypotheses. As we do this 

we learn new things about these ecosystems, such as the new 

concept of sleeping functional groups (Bellwood et al., 2006). 

Positive Effects of Associated Species

on Habitat Stability and Biodiversity

Naturalists and early ecologists recognized that many species were associated with biogenic habitats such as forests and 
8 • smithsonian contributions to the marine sciences

thickets of vegetation on land and beds of algae and mollusk 

and coral reefs in the sea (Elton, 1927; Thorson, 1957). Indeed, 

much early research in ecology described patterns of species 

associations. Decades of research since have concentrated on 

mechanistic explanations for patterns of species association and 

community assembly. Prominent research efforts were directed 

toward explaining the coexistence of species in these associations 

via competition (Connell, 1961), predation (Paine, 1966), and 

disturbance (Dayton, 1971). While there was a growing recognition of the role of mutualisms in population and community 

ecology, initial work on the subject was more focused on the 

role of coevolution in shaping mutualistic interactions and their 

geographic distribution (Boucher et al., 1982; Futuyma and Slatkin, 1983; Vermeij, 1983; Addicott, 1984) and the biology of 

individual mutualists than on their potential impact on communities and ecosystems. Mutualistic relationships were considered 

dynamically fragile and more prevalent in stable environments 

(May, 1981), an idea that is contradicted by recent research in 

environmentally stressful habitats (Bertness, 1985; Witman, 

1987; Leonard et al., 1999). General predictive models for mutualistic interactions as a specific type of positive interaction 

were developed later (Bertness and Callaway, 1994) and have 

remained an influential component of theoretical ecology (Bruno 

et al., 2003, 2005). 

Scuba-based observations and experiments helped promote 

the idea that positive interactions among species play key roles 

in the maintenance of biodiversity by facilitating the persistence 

of habitats created by foundation species (sensu Dayton, 1975), 

which are now often called physical ecosystem engineers (Jones 

et al., 1994). This critical role was demonstrated for Panamanian 

coral reefs in the early 1970s by elegant experiments following Peter Glynn’s observation that Trapezia crabs and Alpheus 

snapping shrimp living within branching pocilloporid coral colonies prevented the crown of thorns starfish Acanthaster planci

from feeding on the corals (Glynn, 1976; Figure 2A). Pocilloporid colonies where protective symbionts were experimentally 

removed suffered higher rates of destruction by A. planci, and 

coral diversity was higher where the crown of thorns starfish 

was prevented from foraging (Glynn, 1976). Another example of 

positive interactions affecting foundation species, and ultimately, 

species diversity, comes from the Caribbean forereef slope (Wulff 

and Buss, 1979). At a time when much of coral reef ecology was 

focused on the role of competition (Lang, 1973), Wulff and Buss 

(1979) hypothesized that sponges enhance the persistence of foliaceous corals on the steep forereef slope by binding the corals 

to the reef frame (Figure 2B). Corals fell off the reef slope on 

manipulated reefs where divers removed the sponges from the 

coral interstices, resulting in elevated (40% higher) coral mortality compared to controls. Later work in similar habitats showed 

that the underside of foliaceous corals supports an exceptionally high diversity of epifaunal invertebrates (Buss and Jackson, 

1979). Thus, the positive effect of sponges on foliaceous corals 

enhances community-wide biodiversity. The last example comes 

from cold temperate waters where large beds of horse mussels 

(Modiolus modiolus) live on subtidal rocky substrata supporting an associated fauna of benthic invertebrates that Thorson 

(1971:175) called “the most luxuriant society cold temperate 

seas can offer.” Scuba-based sampling and experiments indicated 

that the mussels were foundation species, supporting a highly diverse community of infaunal invertebrates by providing a refuge 

from predation in the mussel beds (Witman, 1985). The subtidal 

zonation at wave-exposed sites in the Gulf of Maine where this 

research was performed showed that the shallow subtidal was 

dominated by Laminarian kelp, giving way to a zone dominated 

by horse mussels at intermediate depths (Witman, 1987). The 

existence of some mussel beds in the shallow kelp zone was enigmatic, considering that dislodgement by kelp overgrowing the 

horse mussels during storms was the most significant source of 

mussel mortality, until divers observed that the mussel beds in 

the kelp zone were packed with green sea urchins (Strongylocentrotus droebachiensis) (Witman, 1987; Figure 2C). Subsequent 

manipulations demonstrated that the horse mussel–sea urchin relationship was a facultative mutualism, as mussel mortality from 

kelp-induced dislodgement was reduced by resident sea urchins 

grazing kelp off the mussels and, in turn, the sea urchins achieved 

a refuge from predation while in the beds (Witman, 1987). 

Taken together, these three case studies clearly demonstrate 

that positive interactions are essential for the persistence of foundation species and for maintaining high levels of biodiversity, an 

area of recent emphasis in ecology (Thomsen et al., 2010). In 

all three cases, the integrity of the foundation species depended 

upon cryptic or semi-cryptic species. The positive feedback would 

not have been revealed without first-hand observations by scuba 

divers who detected positive interactions among the organisms 

because they studied them in their natural environments.

CONCLUSIONS

Scuba has stimulated a revolution in marine science analogous to manned space flight and the microscope. We have been 

able to more carefully construct and repair equipment in space 

since the development of manned space flight. Similarly, a diver’s 

hands are more efficient, more adaptable, and less expensive for 

setting up experiments on a topographically and biologically 

complex substratum than arms from a submersible or a robot. 

The invention of scuba was also a technological advance 

analogous to the invention of the microscope, an instrument that 

revolutionized our study of microbes from deductions to actually 

seeing how cells behave and are constructed. The most profound 

contribution of scuba is having the scientist set up the experiment 

and actually be present to observe any unexpected alternative 

hypotheses that were not available when the otherwise carefully 

designed monitoring program or controlled replicated manipulative experiment was designed (e.g., Dayton, 1973; Brandt et 

al., 2012). Experiments are designed to test specific alternative 

hypotheses we already have in mind by deductive reasoning 

(“all possible alternatives”) when we conceive the experiment. 
number 39 • 9

An apparently successful experiment that “proves” one of the 

preconceived hypotheses might be hiding the truth of a third or 

fourth hypothesis that was not preconceived. However, a diver 

on hand might observe the true situation. One problem with deductive reasoning is that we are convinced that our experiment 

or survey has covered all possible alternative hypotheses. The 

value of observation is that discoveries of natural processes do 

not necessarily require deductive logic, and this is where scuba 

makes a fundamental contribution—providing the means to 

make novel, direct observations.

ACKNOWLEDGMENTS

We thank Michael Lang, Susan Roberts, Phil Taylor, and 

Roberta Marinelli for their hard work in organizing “The 

FIGURE 2. (A) Trapezia crab within a pocilloporid coral colony pinching a crown of thorns starfish Acanthaster planci, which deters it from 

consuming the coral. Red arrow points to chelae of Trapezia (photo from video by P. Glynn). (B) Foliose corals (Agaricia spp.) of the deep 

forereef slope in Jamaica. Sponges bind these corals to the reef frame to prevent them from falling off the slope (photo by J. Witman). (C) A 

mutualism between horse mussels (Modiolus modiolus) and green sea urchins (Strongylocentrotus droebachiensis) in the shallow kelp zone, 

Gulf of Maine. The sea urchins are grazing the kelp off the mussel shell, preventing high mussel mortality from kelp-induced dislodgement

during storms. The sea urchins obtain a refuge from predation while in the mussel beds. The positive interaction enables mussel beds to persist, 

supporting diverse communities of associated invertebrates (photo by J. Witman).
1 0 • smithsonian contributions to the marine sciences

Revolution of Science through Scuba” symposium. We are grateful to the National Science Foundation (Biological Oceanography Program), the Smithsonian Institution, and the National 

Undersea Research Program (NOAA) for funding that made our 

research possible. This paper is dedicated to four outstanding 

pioneers in our field that inspired us and many others to do the 

best possible science in the ocean: Walter Adey, Peter Glynn, Jack 

Randall, and Bob Vadas.

REFERENCES

Addicott, J. F. 1984. Mutualistic interactions in population and community processes. In A new ecology: Novel approaches to interactive systems, ed. P. W. 

Price, C. N. Slobodchikoff, and W. S. Gaud, pp. 437–456. New York: John 

Wiley and Sons.

Alldredge, A. L., and J. M. King. 1977. Distribution, abundance and substrate preference of demersal reef zooplankton at Lizard Island lagoon, Great Barrier 

Reef. Marine Biology, 41:317–335. http://dx.doi.org/10.1007/BF00389098.

Bellwood, D. R., T. P. Hughes, C. Folke, and M. Nystrom. 2004. Confronting the 

coral reef crisis. Nature, 429:827–833. http://dx.doi.org/10.1038/nature

02691.

Bellwood, D. R., T. P. Hughes, and A. S. Hoey. 2006. Sleeping functional group 

drives coral-reef recovery. Current Biology, 16:2434–2439. http://dx.doi.org

/10.1016/j.cub.2006.10.030.

Bertness, M. D. 1985. Fiddler crab regulation of Spartina alterniflora production 

on a New England salt marsh. Ecology, 66:1042–1055. http://dx.doi.org

/10.2307/1940564.

Bertness, M. D., and R. Callaway. 1994. Positive interactions in communities. Trends 

in Ecology and Evolution, 9:191–193. http://dx.doi.org/10.1016/0169-5347

(94)90088-4.

Birkeland, C. 1977. The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits. Proceedings of the Third International Coral Reef Symposium, 1:331–336. 

Boucher, D. H., S. James, and K. H. Keeler. 1982. The ecology of mutualism. Annual 

Review of Ecology and Systematics, 13:315–347. http://dx.doi.org/10.1146

/annurev.es.13.110182.001531.

Brandt, M., J. D. Witman, and A. I. Chiriboga. 2012. Influence of a dominant consumer reverses at increased diversity. Ecology, 93:868–878. 

Bruno, J. F., J. D. Fridley, K. D. Bromberg, and M. D. Bertness. 2005. Insights into 

biotic interactions from studies of species invasions. In Species invasions: Insights into ecology, evolution and biogeography, ed. D. F. Sax, J. J. Stachowicz, 

and S. D. Gaines, pp. 13–40. Sunderland, Mass.: Sinauer Associates, Inc.

Bruno, J. F., J. J. Stachowicz, and M. D. Bertness. 2003. Inclusion of facilitation 

into ecological theory. Trends in Ecology and Evolution, 18:119–125. http://

dx.doi.org/10.1016/S0169-5347(02)00045-9.

Buss, L. W., and J. B. C. Jackson. 1979. Competitive networks: Non-transitive competitive relationships in cryptic coral reef environments. American Naturalist,

112:127–154. 

Butler, M., R. S. Steneck, and W. Herrnkind. 2006. The ecology of juvenile and adult 

lobsters. In Lobsters: The biology, management, aquaculture and fisheries, 

ed. R. Phillips, pp. 263–309. Oxford: Blackwell Publishing Ltd. http://dx.doi

.org/10.1002/9780470995969.ch8.

Connell, J. H. 1961. The influence of interspecific competition and other factors on 

the distribution of the barnacle Chthamalus stellatus. Ecology, 42:710–723. 

http://dx.doi.org/10.2307/1933500.

Darwin, C. 1909. The Voyage of the Beagle. The Harvard Classics, Vol. 29. New 

York: P.F. Collier & Son Company.

Dayton, P. K. 1971. Competition, disturbance and community organization: The 

provision and subsequent utilization of space in a rocky intertidal community. 

Ecological Monographs, 41:351–389. http://dx.doi.org/10.2307/1948498.

———. 1973. Two cases of resource partitioning in an intertidal community: Making the right prediction for the wrong reason. American Naturalist, 107:662–

670. http://dx.doi.org/10.1086/282865.

———. 1975. Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecological Monographs, 45:137–159. http://dx.doi.org

/10.2307/1942404.

———. 2003. The importance of the natural sciences to conservation. American 

Naturalist, 162(1):1–13. http://dx.doi.org/10.1086/376572.

Dayton, P. K., R. J. Rosenthal, L. C. Mahen, and T. Antezana. 1977. Population 

structure and foraging biology of the predaceous Chilean asteroid Meyenaster gelatinosus and the escape biology of its prey. Marine Biology, 39:361–

370. http://dx.doi.org/10.1007/BF00391939.

Dayton, P. K., and M. J. Tegner. 1984. The importance of scale in community ecology: A kelp forest example with terrestrial analogs. In A new ecology: Novel 

approaches to interactive systems, ed. P. W. Price, C. N. Slobodchikoff, and 

W. S. Gaud, pp. 457–481. New York: John Wiley & Sons. 

Dayton, P. K., M. J. Tegner, P. B. Edwards, and K. L. Riser. 1998. Sliding baselines, 

ghosts, and reduced expectations in kelp forest communities. Journal of Applied Ecology, 8:309–322.

Elton, C. 1927. Animal ecology. London: Sidgwick and Jackson, Ltd.

Eschmeyer, W. N., R. Fricke, J. D. Fong, and D. A. Polack. 2010. Marine fish diversity: History of knowledge and discovery (Pisces). Zootaxa, 2525:19–50.

Estes, J. A., and D. O. Duggins. 1995. Sea otters and kelp forests in Alaska: Generality and variation in a community ecological paradigm. Ecological Monographs, 65:75–100. http://dx.doi.org/10.2307/2937159.

Estes, J. A., and J. F. Palmisano. 1974. Sea otters: Their role in structuring nearshore 

communities. Science, 185:1058–1060. http://dx.doi.org/10.1126/science.185

.4156.1058.

Estes, J. A., J. Terbourgh, J. S. Brashares, M. E. Power, J. Berger, W. J. Bond, S. R. Carpenter, T. E. Essington, R. D. Holt, J. B. C. Jackson, R. J. Marquis, L. Oksanen,

T. Oksanen, R. T. Paine, E. K. Pikitich, W. J. Ripple, S. A. Sandin, M. Scheffer, 

T. W. Schoener, J. B. Shurin, A. R. E. Sinclair, M. E. Soule, R. Virtanen, D. A. 

Wardle. 2011. Trophic downgrading of planet Earth. Science, 333:301–306. 

http://dx.doi.org/10.1126/science.1205106.

Forsman, Z. H., and C. Birkeland. 2009. Porites randalli: A new coral species (Scleractinia, Poritidae) from American Samoa. Zootaxa, 2244:51–59.

Futuyma, D. J., and M. Slatkin. 1983. Coevolution. Sunderland, Mass.: Sinauer 

Associates, Inc.

Glynn, P. 1976. Some physical and biological determinants of coral community 

structure in the Eastern Pacific. Ecological Monographs, 45:431–456. http://

dx.doi.org/10.2307/1942565.

Grabowski, J. H., A. R. Hughes, and D. L. Kimbro. 2008. Habitat complexity influences cascading effects of multiple predators. Ecology, 89:3413–3422. http://

dx.doi.org/10.1890/07-1057.1.

Grabowski, J. H., and D. L. Kimbro. 2005. Predator-avoidance behavior extends 

trophic cascades to refuge habitats. Ecology, 86:1312–1319. http://dx.doi.org

/10.1890/04-1216.

Hairston, N. G., F. E. Smith, and L. B. Slobodkin. 1960. Community structure, population control and competition. American Naturalist, 94:421–425. http://

dx.doi.org/10.1086/282146.

Hamner, W. M., and J. H. Carleton. 1979. Copepod swarms: attributes and role in 

coral reef ecosystems. Limnology and Oceanography, 24:1–14. http://dx.doi

.org/10.4319/lo.1979.24.1.0001.

Hamner, W. M., L. P. Madin, A. L. Alldredge, R. W. Gilmer, and P. P. Hamner. 1975. 

Underwater observations of gelatinous zooplankton: Sampling problems, 

feeding biology and behavior. Limnology and Oceanography, 20:907–917. 

http://dx.doi.org/10.4319/lo.1975.20.6.0907.

Hixon, M. A. 1997. Effects of reef fishes on corals and algae. In Life and death of 

coral reefs, ed. C. Birkeland, pp. 230–248. New York: Chapman and Hall. 

http://dx.doi.org/10.1007/978-1-4615-5995-5_10.

Hutchinson, G. E. 1959. Homage to Santa Rosalia: Or, why are there so many 

kinds of animals? American Naturalist, 93:145–159. http://dx.doi.org/10

.1086/282070.

Jayewardene, D., M. J. Donahue, and C. Birkeland. 2009. Effects of frequent fish 

predation on corals in Hawaii. Coral Reefs, 28:499–506. http://dx.doi.org

/10.1007/s00338-009-0475-y.

Jennings, S., and N. V. C. Polunin. 1995. Biased underwater visual census biomass estimates for target-species in tropical reef fisheries. Journal of Fisheries Biology, 47:733–736. http://dx.doi.org/10.1111/j.1095-8649.1995.tb

01938.x.

Johnson, D. S., and A. F. Skutch. 1928. Littoral vegetation on a headland of Mt. 

Desert Island, Maine. I. Submersible or strictly littoral vegetation. Ecology,

9:188–215. http://dx.doi.org/10.2307/1929354.

Jones, C. G., J. H. Lawton, and M. Shackak. 1994. Organisms as ecosystem engineers. Oikos, 69:373–386. http://dx.doi.org/10.2307/3545850.

Lang, J. C. 1973. Interspecific aggression by scleractinian corals. 2. Why the race is 

not only to the swift. Bulletin of Marine Science, 23:260–279. 
number 39 • 1 1

Leonard, G., P. Ewanchuk, and M. D. Bertness. 1999. How recruitment, interspecific interactions and predation control species borders in a tidal estuary. 

Oecologia, 118:492–502. http://dx.doi.org/10.1007/s004420050752.

Lindeman, R. L. 1942. The trophic-dynamic aspect of ecology. Ecology, 23:399–

418. http://dx.doi.org/10.2307/1930126.

Mauzey, K. P., C. Birkeland, and P. K. Dayton. 1968. Feeding behavior of asteroids and escape responses of their prey in the Puget Sound Region. Ecology,

49:603–619. http://dx.doi.org/10.2307/1935526.

May, R. M. 1981. Patterns in multi-species communities. In Theoretical ecology: Principles and applications, 2nd ed., pp. 197–227. Sunderland, Mass.: 

Sinauer Associates, Inc.

McClanahan, T. R, N. A. Muthiga, A. T. Kamukuru, H. Machano, and R. Kiambo. 

1999. The effect of fishing and marine protected areas on the coral reefs of 

northern Tanzania. Biological Conservation, 89:161–182. http://dx.doi.org

/10.1016/S0006-3207(98)00123-2.

Moody, K., and R. S. Steneck. 1993. Mechanisms of predation among large decapod crustaceans of the Gulf of Maine coast: Functional versus phylogenetic 

patterns. Journal of Experimental Marine Biology and Ecology, 168:111–

124. http://dx.doi.org/10.1016/0022-0981(93)90118-8.

Ong, L. 2007. The ecological importance of parrotfish as bioeroders and sediment 

producers in Hawaii and their conservation within small marine protected 

areas. Ph.D. diss., University of Hawaii at Manoa, Honolulu. 

Paine, R. T. 1966. Food web complexity and species diversity. American Naturalist, 

100:65–75. http://dx.doi.org/10.1086/282400.

Palma, A. T., R. S. Steneck, and C. Wilson. 1999. Settlement-driven, multiscale demographic patterns of large benthic decapods in the Gulf of Maine. Journal 

of Experimental Marine Biology and Ecology, 241:107–136. http://dx.doi

.org/10.1016/S0022-0981(99)00069-6.

Peckarsky, B. L., P. A. Abrams, D. I. Bolnick. 2008. Revisiting the classics: Considering nonconsumptive effects in textbook examples of predator–prey interactions. Ecology, 89:2416–2425. http://dx.doi.org/10.1890/07-1131.1.

Popper, K. R. 1959. The logic of scientific discovery. London: Hutchinson and Co.

Porter, J. W., and K. G. Porter. 1977. Quantitative sampling of demersal plankton 

migrating from different coral reef substrates. Limnology and Oceanography,

22:553–556. http://dx.doi.org/10.4319/lo.1977.22.3.0553.

Power, M. E. 1992. Top-down and bottom-up forces in food webs: Do plants have 

primacy? Ecology, 73:733–746. http://dx.doi.org/10.2307/1940153.

Randall, J. E. 1965. Grazing effects on sea grasses by herbivorous reef fishes in the 

West Indies. Ecology, 46:255–260. http://dx.doi.org/10.2307/1936328

Sala, O. E. 2001. Price put on biodiversity. Nature, 412:34–36. http://dx.doi.org

/10.1038/35083676.

Sandin, S. A., S. M. Walsh, and J. B. C. Jackson. 2010. Prey release, trophic cascades, 

and phase shifts in tropical nearshore marine ecosystems. In Trophic cascades: Predators, prey, and the changing dynamics of nature, ed. J. Terborgh 

and J. A. Estes, pp. 71–90. Washington, DC: Island Press. 

Siddon, C. E., and J. D. Witman. 2004. Behavioral indirect interactions: Multiple 

predator effects and prey switching in the shallow rocky subtidal. Ecology,

85:2398–2945. http://dx.doi.org/10.1890/03-0519.

Steneck, R. S. 2006a. Is the American lobster Homarus americanus overfished? A 

review of overfishing with an ecologically-based perspective. Bulletin of Marine Science, 78:607–632.

———. 2006b. Possible demographic consequences to intraspecific shelter competition among American lobsters. Journal of Crustacean Biology, 26:628–638. 

http://dx.doi.org/10.1651/S-2753.1.

Steneck, R. S., and M. N. Dethier. 1994. A functional group approach to the structure of algal-dominated communities. Oikos, 69:476–498. http://dx.doi.org

/10.2307/3545860.

Steneck, R. S., M. H. Graham, B. J. Bourque, D. Corbett, J. M. Erlandson, J. A. 

Estes, and M. J. Tegner. 2002. Kelp forest ecosystem: Biodiversity, stability, 

resilience and their future. Environmental Conservation, 29:436–459. http://

dx.doi.org/10.1017/S0376892902000322.

Steneck, R. S., and L. Watling. 1982. Feeding capabilities and limitations of herbivorous molluscs: A functional group approach. Marine Biology, 68:299–319. 

http://dx.doi.org/10.1007/BF00409596.

Steneck, R. S., and C. J. Wilson. 2001. Long-term and large scale spatial and temporal patterns in demography and landings of the American lobster, Homarus 

americanus, in Maine. Journal of Marine and Freshwater Research, 52:1302–

1319. http://dx.doi.org/10.1071/MF01173.

Thomsen, M. S., A. Altieri, B. Wernberg, F. Tuya, D. Gulbransen, K. McGlathery, 

M. Holmer, and B. R. Silliman. 2010. Habitat cascades: The conceptual 

context and global relevance of facilitation cascades via habitat formation 

and modification. Integrative and Comparative Biology, 50:158–175. http://

dx.doi.org/10.1093/icb/icq042.

Thorson, G. 1957. Bottom communities (sublittoral or shallow shelf). In Treatise 

on marine ecology and paleoecology, ed. J. W. Hedgpeth and H. S. Ladd, pp. 

461–534. Geological Society of America, Memoirs 67. Baltimore: Waverly 

Press.

———. 1971. Life in the sea. New York: McGraw-Hill.

Tittensor, D. P., B. Worm, and R. A. Myers. 2009. Macroecological changes in exploited marine ecosystems. In Marine macroecology, ed. J. D. Witman and 

K. Roy, pp. 310–337. Chicago: University of Chicago Press. http://dx.doi.org

/10.7208/chicago/9780226904146.003.0012.

Vermeij, G. J. 1983. Intimate associations and coevolution in the sea. In Coevolution, ed. D. J. Futuyma and M. Slatkin, pp. 311–327. Sunderland, Mass.: 

Sinauer Associates, Inc.

Wahle, R. A., and R. S. Steneck. 1991. Recruitment habitats and nursery grounds of 

the American lobster (Homarus americanus Milne Edwards): A demographic 

bottleneck? Marine Ecology Progress Series, 69:231–243. http://dx.doi.org

/10.3354/meps069231.

———. 1992. Habitat restrictions in early benthic life: Experiments on habitat selection and in situ predation with the American lobster. Journal of Experimental 

Marine Biology and Ecology, 157:91–114. http://dx.doi.org/10.1016/0022

-0981(92)90077-N.

Wallace, A. R. 1858. On the tendency of varieties to depart indefinitely from the 

original type. Journal of the Proceedings of the Linnean Society (Zoology),

3:53–62.

Wells, R. J. D., R. S. Steneck, and A. T. Palma. 2010. Three-dimensional resource 

partitioning between American lobster (Homarus americanus) and rock crab 

(Cancer irroratus) in a subtidal kelp forest. Journal of Experimental Marine 

Biology and Ecology, http://dx.doi.org/10.1016/j.jembe.2010.01.008.

Witman, J. D. 1985. Refuges, biological disturbance, and rocky subtidal community structure in New England. Ecological Monographs, 55:421–445. http://

dx.doi.org/10.2307/2937130.

———. 1987. Subtidal coexistence: Storms, grazing, mutualism, and the zonation 

of kelps and mussels. Ecological Monographs, 57:167–187. http://dx.doi.org

/10.2307/1942623.

Witman, J. D., and P. K. Dayton. 2001. Rocky subtidal communities. In Marine 

community ecology, ed. M. D. Bertness, S. D. Gaines, and M. Hay, pp. 339–

366. Sunderland, Mass.: Sinauer Associates, Inc.

Witman, J. D., and K. Roy. 2009. Experimental marine macroecology. In Marine 

macroecology, ed. J. D. Witman and K. Roy, pp. 341–356. Chicago: University of Chicago Press. http://dx.doi.org/10.7208/chicago/9780226904146

.003.0013.

Witman, J. D., and K. D. Sebens. 1992. Regional variation in fish predation intensity: A historical perspective in the Gulf of Maine. Oecologia, 90:305–315. 

http://dx.doi.org/10.1007/BF00317686.

Wulff, J. L., and L. W. Buss. 1979. Do sponges help hold coral reefs together? Nature, 281:474–475. http://dx.doi.org/10.1038/281474a0.

Diving into the Past: Scuba and the Temporal 

Dimension of Coral Reefs

Ian G. Macintyre and Richard B. Aronson

ABSTRACT. A variety of sampling techniques afforded by scuba diving have made it possible to

study the Holocene history of coral reefs in detail. This paper describes results of three geological 

techniques and illustrates them with examples from our own work in the Caribbean. First, cores 

extracted with a hydraulic drill from cemented reef frameworks provided the complete history of a 

fringing reef off the Caribbean coast of Panama and documented a relict reef stranded by rising sea 

level off St. Croix. Second, surface samples collected from a coral death-assemblage helped explain 

the demise of an algal-dominated reef off the southern coast of Barbados. Third, push-cores from uncemented reefs in the Belizean barrier-reef lagoon and a coastal lagoon in Panama revealed that 3,000 

or more years of compositional stasis were followed in recent decades by precipitous turnover events, 

in which the previously dominant corals were replaced by a different species. Understanding the geological history of coral reefs over the last several thousand years is critical to predicting their response 

to climate change, alterations in land use, and other natural and anthropogenic perturbations.

INTRODUCTION

Among its many contributions to marine science, scuba diving has enabled researchers to collect vital information on the Holocene history of coral reefs. Historical information can be compared to the reefs’ present-day status to explain current conditions and 

predict the future. In this paper we explore the contribution of scuba to the historical 

analysis of reefs by describing three methods of geological sampling. The geology of coral 

reefs has been reviewed in detail elsewhere (Aronson, 2007; Montaggioni and Braithwaite, 2009); here we focus on scuba-based techniques, which we illustrate with examples from our own research. The salient point is that without the technology of scuba 

diving much of this critical information would remain inaccessible.

ROTARY DRILLING

With the introduction of an underwater, hydraulically powered drill in the early 

1970s (Macintyre, 1978), it became possible to collect cores from cemented frameworks 

across an entire reef, not only above water but underwater on scuba as well (Figure 

1). Drilling revealed the complete Holocene history of a fringing reef off Galeta Point, 

Panama (Macintyre and Glynn, 1976). Cores collected at water depths of 0–10 m showed 

a reef about 14 m thick, with six distinct reef facies (Figure 2).

1. Back-reef sediment facies: This facies consists of skeletal debris composed mainly 

of Acropora palmata, Acropora cervicornis, Porites furcata, Agaricia agaricites, and 

Ian G. Macintyre, Smithsonian Institution, National Museum of Natural History, Department of 

Paleobiology, P.O. Box 37012, Washington, District of Columbia 20013-7012, USA. Richard 

B. Aronson, Florida Institute of Technology, Department of Biological Sciences, 150 West University Boulevard, Melbourne, Florida 32901-6975, 

USA. Correspondence: I. Macintyre, macintyr@

si.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
1 4 • smithsonian contributions to the marine sciences

mollusks in a Halimeda-rich muddy sand. The top of this 

facies grades into a calcareous mangrove peat. 

2. Reef-flat rubble facies: The rubble derives from a variety of 

coral species, including Acropora palmata, Diploria spp., 

Agaricia agaricites, Millepora complanata, and Porites astreoides. Most of this skeletal debris is water-worn, extensively 

bored, and encrusted.

3. Reef Acropora palmata facies: This main structural framework of Galeta Reef ranges from 3 to 11 m thick and consists primarily of well-preserved Acropora palmata. Growth 

patterns indicate that most of the Acropora palmata has not 

been overturned.

4. Fore-reef pavement facies: This facies is heavily indurated 

by submarine cement and extends from the reef crest to the 

drop-off at the outer edge of the reef. It contains a highenergy assemblage consisting of crustose coralline algae, 

Millepora complanata, Agaricia agaricites, and Porites astreoides. Much of this skeletal material has been obliterated 

by multicyclic boring and cementation.

5. Fore-reef coral-head facies: This facies occurs only at the 

base of the outer edge of the reef framework and consists of 

a mixed assemblage of massive corals, including Dichocoenia stokesi, Siderastrea siderea, Porites astreoides, and the 

Orbicella annularis species complex. Most of these corals 

show extensive bioerosion and are in-filled with submarine 

cement.

6. Fore-reef talus facies: The principal components here are 

fragments of coral, crustose coralline algae, bryozoans, mollusks, and Millepora spp. in a matrix of mud and sand.

As confirmed by eighteen radiocarbon dates, the Galeta 

Reef has gone through several stages of development (Figure 3):

a

B

FIGURE 1. Collecting cores from Galeta Reef, Panama, above (A) 

and below (B) the sea surface with a hydraulically operated drill 

(photos courtesy of Ian G. Macintyre).

FIGURE 2. Transect across Galeta Reef showing the six reef facies 

and peat accumulation.
number 39 • 1 5

FIGURE 3. Stages of accumulation of Galeta Reef over the past 7,000 years in relation to the Western Atlantic sea-level curve 

(Lighty et al., 1982). Numbers at top indicate the core-hole locations.
1 6 • smithsonian contributions to the marine sciences

• Beginning slightly more than 7,000 years ago, a small reef 

consisting of Acropora palmata and coral heads established 

on the mid-Miocene siltstone Gatun Formation.

• 6,000 years ago, the reef extended shoreward, taking on the 

relief of the underlying Gatun Formation.

• 5,000 years ago, rapid accumulation of Acropora palmata

masked the substrate relief; the reef-flat rubble facies, backreef sediment facies, and fore-reef talus facies began to form.

• 4,000 years ago, a mature reef with five facies had become 

well developed.

• 3,000 years ago, the reef continued to accumulate with the 

start of the formation of the fore-reef pavement facies.

• 2,000 years ago, all six facies were well developed, but the 

reef framework was no longer accumulating. 

• At present, the mature, emergent reef has mangroves and 

lagoonal sediments transgressing over the reef-flat rubble, 

and the fore reef is characterized by dense pavement and a 

thick talus cover.

Galeta is a classic example of a catch-up reef (Neumann and 

Macintyre, 1985). It has reached sea level and any new vertical 

accretion will depend on the provision of new accommodation 

space through further sea-level rise.

In a subsequent project off the southeast coast of St. Croix 

(Adey et al., 1977), scuba made it possible to collect three cores 

from a shelf-edge system in water depths of 11–15 m (Figure 4). 

These cores all contained a deeper-water coral-head facies with 

radiocarbon dates ranging from 7,000 to 5,000 years BP (before present; see blue sections in Figure 5). The outermost core, 

however contained a section of shallow-water Acropora palmata

below the coral heads, which yielded a date of 9,075 years BP. 

When the date of this core was compared with the positions 

of rising sea level, it became apparent that the shallow-water 

Acropora palmata community died during flooding of the insular shelf about 7,000 years ago (Figure 5). Erosion of the sediment cover on the shelf likely produced turbid conditions at the 

shelf edge, which exceeded the tolerance of the sensitive Acropora palmata. Supporting evidence from X-ray diffraction analysis indicated a marked increase in terrigenous minerals trapped 

in the cement crusts of the coral-head facies, in contrast to the 

clean crusts of the Acropora palmata facies. By the time turbidity had declined and water quality had improved, sea level at 

the shelf edge had risen beyond the depth at which the shallowwater Acropora palmata could become reestablished. As a result, 

the massive-coral (or coral-head) assemblage became dominant 

on the outer shelf. The common occurrence of relict shelf-edge 

reefs in the Caribbean indicates that during the later stages of the 

Holocene Transgression most of these reefs succumbed to stress 

associated with shelf flooding and high turbidity.

The geological patterns illuminated by scuba-based studies 

in Panama and St. Croix hold lessons for the trajectory of reefs 

in our present era of rapid climate change. As rising sea levels 

associated with climate change flood terrestrial habitats, water 

quality will decline as it did off St. Croix 7,000 years ago and we 

can expect similar negative impacts on modern reefs. Continued 

sea-level rise, however, will provide the accommodation space 

necessary for reefs that have caught up with sea level to begin 

growing vertically again.

SURFACE SAMPLING

Geological samples collected from reef surfaces also provide 

valuable information on reef growth and the timing of inimical 

conditions that stop that growth. Another of our scuba-assisted 

studies took place on a “dead,” algae-covered, bank-barrier reef 

off the southeast coast of Barbados (Figure 6). Because the reef 

lies in an area of constant and heavy wave energy driven by the 

trade winds, we could only work on it in September, a time of 

year when storm activity interrupts the otherwise persistent wind 

pattern (Macintyre et al., 2007).

FIGURE 4. Map of the east end of St. Croix showing location of 

core-hole drilling on a bottom of scattered coral heads and octocorals (modified from Adey et al., 1977; photo courtesy of Ian G. 

Macintyre).
number 39 • 1 7

We reached nine study sites along the 15-km crest of this 

bank-barrier reef (Figure 7). We completed ten-meter chaintransect surveys, along with digital photography, and collected 

samples of subfossil corals for radiocarbon dating. Although this 

was clearly a robust, Acropora palmata-dominated reef at one 

time, we found no living colonies. Instead, we encountered occasional small colonies of Porites astreoides, Diploria spp., and 

Millepora complanata (Figure 8). The substrate was dominated 

by macroalgae, crustose coralline algae, and turf algae on dead 

plates of Acropora palmata.

Although the demise of Acropora palmata populations 

in Barbados was previously thought to be partially related to 

human activity in the seventeenth century (Lewis, 1984), radiocarbon dates of 27 samples of Acropora palmata indicated that 

reef accumulation stopped 3,000 years ago, with 11 dates plotting above the sea-level curve (Figure 9). These dates, along with 

the taphonomic observation that the subfossil Acropora palmata

was broken and flattened, indicate that severe storms around 

4,000–3,000 years ago destroyed most of the reef. The few Acropora palmata colonies that survived until 400–300 years ago 

may have been killed off by the clearing of land for sugar cane 

in the late 1600s; however, there has been no reef-framework accumulation for the past 3,000 years. Apparently physical conditions, not human activity, were responsible for the demise of this 

bank-barrier reef.

Why did this reef not recover? There are at least two hypotheses, which are not mutually exclusive. One explanation is 

FIGURE 5. Transect of three core holes across the shelf edge off the south coast of St. Croix. Both coral-head and 

Acropora palmata facies are shown with radiocarbon dates. Note the relationship of the end of Acropora palmata accumulation to the flooding of the shelf 7,000 years ago. X-ray diffraction patterns of cement crusts from the outermost 

core show a marked increase in terrigenous material in the upper coral-head facies (modified from Adey et al., 1977).

FIGURE 6. Satellite photograph of Barbados showing Cobbler’s 

Reef, a bank-barrier reef off the southeast coast (courtesy of DigitalGlobe).
1 8 • smithsonian contributions to the marine sciences

that wave energy in this area may be too high and constant to 

allow herbivores to keep macroalgae in check (Steneck, 1988); 

once the corals died and the macroalgae rose to dominance, the 

macroalgae prevented corals from recruiting successfully. Alternatively, or in addition, the initial flattening of reef topography 

prevented recolonization by Acropora palmata (cf. Precht et al., 

2001), due either to high turbulence or to the loss of sheltered 

microhabitat for herbivores (Szmant, 1997).

PUSH-CORING

Push-coring is an alternative to rotary drilling for reconstructing the Holocene history of coral reefs in lagoonal settings. The 

ribbon reefs, or rhomboid shoals, in the central shelf lagoon of the 

Belizean barrier reef; the patch and fringing reefs in Bahía Almirante, a coastal lagoon at Bocas del Toro in northwestern Panama; 

and certain lagoonal reefs elsewhere in the Caribbean and in the 

Indo-Pacific are uncemented, consisting essentially of accumulations of skeletal fragments of branching and foliose corals packed 

in an unconsolidated, sandy-mud to muddy-sand matrix (Aronson 

et al., 2002, 2004; Wapnick et al., 2004; Toth et al., 2012). Lowenergy conditions and the abundant matrix are primarily responsible for the lack of submarine cementation on these reefs. 

For the push-coring method, divers force a 5 to 6 m aluminum tube into the unconsolidated reef framework, rotating it 

in using adjustable core-slips with handles and pounding with 

a hammer-weight sleeved over the top of the tube (Figure 10). 

Once the tube has penetrated 4–5 m, the free end is sealed with 

a plastic cap and electrical tape. The core is then extracted from 

the reef. Its bottom is sealed and it is then brought to the surface for laboratory analysis. A team of three or four scuba divers can collect a core in a dive of 30–45 minutes. Push-coring is 

an inexpensive, highly portable alternative to drilling and other 

mechanized techniques such as percussion vibracoring (Dardeau 

et al., 2000). Expense and portability are not the sole reasons for 

FIGURE 8. Harrismith site (site C) on Cobbler’s Reef showing scattered and flattened Acropora palmata with a cover of crustose coralline algae, Millepora complanata (M), and macroalgae (modified 

from Macintyre et al., 2007; photo by Allan G. Macintyre).

FIGURE 7. Index map showing the nine study sites (A–I) on Cobbler’s Reef (Macintyre et al., 2007).

FIGURE 9. Radiocarbon dates of Acropora palmata from the crest 

of Cobbler’s Reef plotted in relation to the Western Atlantic sea-level 

curve (Toscano and Macintyre, 2003). Note the samples that plot 

above the sea-level curve, which indicate storm damage. There has 

been no additional reef accumulation for the past 3,000 years (Macintyre et al., 2007). Letters refer to the sites in Figure 7.
number 39 • 1 9

the high value of push-coring in lagoonal environments. Drilling 

is inappropriate because the process itself pulverizes delicate corals and blows them and the unconsolidated fine sediments out 

of the core tube, destroying the very materials that are the focus 

of study.

Thirty-eight push-cores extracted from 20 sites in Belize at 

3–12 m water depth, distributed over 375 km2

 of the central 

shelf lagoon, revealed a striking and remarkably consistent pattern of dominance and turnover during the past 3,000–4,000 

years (as determined by radiocarbon dating). Acropora cervicornis dominated throughout the last several millennia until the 

late 1980s. Turnover events were highly localized in time and 

space, consisting of small-scale shifts in dominance between 

Acropora cervicornis and the lettuce coral Agaricia tenuifolia

(Aronson et al., 2002). After 1986, virtually the entire population of A. cervicornis on the rhomboid shoals was wiped out 

by white-band disease, an infectious bacterial disease that killed 

acroporid populations throughout the Caribbean from the late 

1970s through the early 1990s (Aronson and Precht, 2001). 

High levels of herbivory from the sea urchin Echinometra viridis

controlled algal growth on the dead skeletons of Acropora cervicornis in the Belizean shelf lagoon, so that by the mid-1990s 

the reef surfaces at all 20 sites had switched to dominance by 

Agaricia tenuifolia. This large-scale, recent turnover event was 

recorded as a layer of Agaricia plates at the top of each of the 

cores (Figure 11, left).

The pattern of stasis and turnover was similar in Bahía Almirante in Panama, but the long-term dominant and the cause of 

turnover were different from the Belizean case. Thirty-six cores 

were extracted from 12 sites at 5–10 m water depth, distributed 

over an area of 128 km2

. In this case, branching Porites spp. 

were the continuously dominant corals for the last 3,000–4,000 

years (Figure 11, right). Small-scale turnover events, localized in 

time and space as in Belize, consisted of transitions to Agaricia 

tenuifolia or Acropora cervicornis. Around 1970, the reefs of the 

Bahía switched to dominance by Agaricia tenuifolia. Aronson et 

FIGURE 10. Push-coring technique: (a) two divers rotating a core tube into an uncemented reef, using adjustable core slips with handles (photo 

by Richard B. Aronson); (b) a diver pounding from the top of a core tube using a sliding hammer-weight (photo by Steven V. Vollmer, reproduced courtesy of Richard B. Aronson). Core slips are visible in the background (b), resting on dead coral on the reef surface below the diver. 
2 0 • smithsonian contributions to the marine sciences

al. (2004) attributed the transition in Bahía Almirante to deteriorating water quality from changing patterns of land use in Bocas 

del Toro and surmised that the turnover event was precipitated 

by massive flooding from unusually heavy rains in 1970. These 

hypotheses were corroborated by geochemical analysis (Hilbun, 

2009). The convergence of lagoonal reef systems in Belize and 

Panama on dominance by Agaricia tenuifolia is a remarkable 

example of the biotic homogenization that is affecting marine 

ecosystems worldwide.

The push-cores from the Belizean lagoon and Bahía Almirante consisted of a sandy-mud to muddy-sand matrix containing up to 50% Mg-calcite in the clay-size fractions (<4 mm). The 

consistent mineralogy of 12–13 mole% MgCO3

 and the lack of 

significant Mg-calcite skeletal material in both the silt-size (4–63 

mm) and sand-size (>63 mm) fractions indicate that most of the 

fine Mg-calcite is precipitated (Table 1). By contrast, authors of 

previous studies in Belize had speculated that the fine Mg-calcite 

had a skeletal source. Interestingly, the same Mg-calcite composition found in the lagoonal mud fraction was observed in lithified 

geopetal deposits on serpulid projections in a lagoonal cave in 

Belize (Figure 12). Lithification in the cave suggests that exposed 

sediments may become lithified, whereas the cores indicate that 

trapped sediments may not.

FIGURE 12. (a) Divers sampling serpulid projections on the ceiling of Columbus Cay cave, located in the Belizean barrier reef lagoon. (b) 

Sample of serpulid projection with thick surface deposit of lithified Mg-calcite (after Macintyre, 1984; photos courtesy of Ian G. Macintyre).

FIGURE 11. Generalized logs of push-cores from the central shelf 

lagoon of the Belizean barrier reef and Bahía Almirante, Bocas del 

Toro, Panama. Light green fill indicates a sandy-mud to muddy-sand 

matrix. Blue fill at the tops of the core logs indicates open framework 

that has not yet been in-filled with sediment (adapted from Aronson 

et al., 2002, 2005).

TABLE 1. Concentrations of magnesium calcite in three size fractions of the matrix in lagoonal cores from Belize and Panama 

(from Macintyre and Aronson, 2006). Note Mg-calcite values 

in the clay-size fractions. There was no evidence of a source of 

coarser skeletal Mg-calcite that could break down to form claysize concentrations of Mg-calcite.

Average percent Mg-calcite in substrate

Lagoon location Sand Silt Clay

Belize 9.4% 13.8% 38.2%

Panama 12.6% 16.0% 50.2%
number 39 • 2 1

CONCLUSIONS

The ecological and geological responses of coral reefs to 

natural and human perturbations can only be understood in a 

historical context. We have presented examples of research on 

the Holocene history of Caribbean reefs that could not have been 

accomplished without scuba. The studies highlight the value of a 

millennial-scale perspective for distinguishing signal from noise 

in the trajectories of coral reefs. Predicting how reefs will grow 

and what they will look like in the future will continue to be 

both an ecological and a geological enterprise, with scuba-based 

methodologies figuring prominently.

ACKNOWLEDGMENTS

The research described in this paper benefited from decades 

of support from the Smithsonian Institution, including the Caribbean Coral Reef Ecosystems (CCRE) program, the Smithsonian 

Tropical Research Institute, and, more recently, the Smithsonian Marine Science Network. Additional support was provided 

by a grant to R.B.A. from the National Science Foundation 

(EAR-9902192) and several grants to R.B.A. from the National 

Geographic Society. This is CCRE contribution number 897 

and contribution number 50 from the Institute for Research on 

Global Climate Change at the Florida Institute of Technology. 

REFERENCES

Adey, W. H., I. G. Macintyre, and R. Stuckenrath. 1977. Relict barrier reef off St. 

Croix: Its implications with respect to late Cenozoic coral reef development 

in the western Atlantic. Proceedings of the Third International Coral Reef 

Symposium, Miami, 2:15–21.

Aronson, R. B., ed. 2007. Geological approaches to coral reef ecology. New York: 

Springer-Verlag. http://dx.doi.org/10.1007/978-0-387-33537-7.

Aronson, R. B., I. G. Macintyre, W. F. Precht, T. J. T. Murdoch, and C. M. Wapnick. 2002. The expanding scale of species turnover events on coral reefs in 

Belize. Ecological Monographs, 72:233–249. http://dx.doi.org/10.1890/0012

-9615(2002)072[0233:TESOST]2.0.CO;2.

Aronson, R. B., I. G. Macintyre, C. M. Wapnick, and M. W. O’Neill. 2004. Phase 

shifts, alternative states, and the unprecedented convergence of two reef systems. Ecology, 85:1876–1891. http://dx.doi.org/10.1890/03-0108.

Aronson, R. B., and W. F. Precht. 2001. White-band disease and the changing face 

of Caribbean coral reefs. Hydrobiologia, 460:25–38. http://dx.doi.org/10

.1023/A:1013103928980.

Dardeau, M. R., R. B. Aronson, W. F. Precht, and I. G. Macintyre. 2000. Use of 

a hand-operated, open-barrel corer to sample uncemented Holocene coral 

reefs. In Diving for science in the 21st century: Proceedings of the 20th annual symposium, ed. P. Hallock and L. French, pp. 6–9. St. Petersburg, Fla.: 

American Academy of Underwater Sciences.

Hilbun, N. L. 2009. Land use and reef ecology in the Bocas del Toro Archipelago, 

Panama. Ph.D. diss., University of South Alabama, Mobile.

Lewis, J. B. 1984. The Acropora inheritance: A reinterpretation of the development 

of fringing reefs in Barbados, West Indies. Coral Reefs, 3:117–122. http://

dx.doi.org/10.1007/BF00301955.

Lighty, R. G., I. G. Macintyre, and R. Stuckenrath. 1982. Acropora palmata reef 

framework: A reliable indicator of sea level in the western Atlantic for 

the last 10,000 years. Coral Reefs, 1:125–130. http://dx.doi.org/10.1007

/BF00301694.

Macintyre, I. G. 1978. A hand-operated submersible drill for coring reef substrata. 

In Coral Reefs: Research Methods, ed. D. R. Stoddart and R. E. Johannes. 

UNESCO Monographs on Oceanographic Methodology, 5:75–80.

———. 1984. Extensive submarine lithification in a cave in the Belize barrier reef 

platform. Journal of Sedimentary Petrology, 54:221–235.

Macintyre, I. G., and R. B. Aronson. 2006. Lithified and unlithified Mg-calcite precipitating in tropical reef environments. Journal of Sedimentary Research, 

76:80–89. http://dx.doi.org/10.2110/jsr.2006.05.

Macintyre, I. G., and P. W. Glynn. 1976. Evolution of a modern Caribbean fringing 

reef, Galeta Point, Panama. American Association of Petroleum Geologists 

Bulletin, 60:1054–1072.

Macintyre, I. G., P. W. Glynn, and M. A. Toscano. 2007. The destruction of a large 

Acropora palmata bank-barrier coral reef off Barbados, W. I. Atoll Research 

Bulletin, 545:1–29.

Montaggioni, L. F., and C. J. R. Braithwaite. 2009. Quaternary coral reef systems: 

History, development processes and controlling factors. Amsterdam: Elsevier. 

Neumann, A. C., and I. G. Macintyre. 1985. Reef response of sea level rise: Keep 

up, catch up or give up.  In Proceedings of the Fifth International Coral Reef 

Congress, Tahiti, 3:105–110. Moorea, French Polynesia: Antenne Museum–

EPHE.

Precht, W. F., R. B. Aronson, and D. W. Swanson. 2001. Improving scientific decision-making in the restoration of ship-grounding sites on coral reefs. Bulletin 

of Marine Science, 69:1001–1012.

Steneck, R. S. 1988. Herbivory on coral reefs: A synthesis. Proceedings of the Sixth 

International Coral Reef Symposium, Townsville, Australia, 1:37–49.

Szmant, A. 1997. Nutrient effects on coral reefs: A hypothesis on the importance of 

topographic and trophic complexity to reef nutrient dynamics. Proceedings 

of the Eighth International Coral Reef Symposium, Panama, 2:1527–1532.

Toscano, M. A., and I. G. Macintyre. 2003. Corrected western Atlantic sea-level 

curve for the last 11,000 years based on calibrated 14C dates from Acropora 

palmata framework and intertidal mangrove peat. Coral Reefs, 22:257–270. 

http://dx.doi.org/10.1007/s00338-003-0315-4.

Toth, L. T., R. B. Aronson, S. V. Vollmer, J. W. Hobbs, D. H. Urrego, H. Cheng, I. C. 

Enochs, D. J. Combosch, R. van Woesik, and I. G. Macintyre. 2012. ENSO 

drove 2500-year collapse of eastern Pacific coral reefs. Science, 337:81–84. 

http://dx.doi.org/10.1126/science.1221168.

Wapnick, C. M., W. F. Precht, and R. B. Aronson. 2004. Millennial-scale dynamics 

of staghorn coral in Discovery Bay, Jamaica. Ecology Letters, 7:354–361. 

http://dx.doi.org/10.1111/j.1461-0248.2004.00586.x.

Diving Physiology and Decompression 

Sickness: Considerations from 

Humans and Marine Animals

Michael A. Lang, Jessica U. Meir, Tanya L. Streeter, 

and Karen B. Van Hoesen

ABSTRACT. The objective of scientific divers using scuba as a research tool is to be able to effectively work under pressure without incurring acute or chronic health effects. Chapters in this volume 

address underwater science results achieved through the use of scuba. This particular discussion 

considers physiological and decompression sickness parameters and effects that all humans and marine animals are subject to on a dive. We know that decompression sickness is triggered by a rapid 

reduction of ambient pressure that allows dissolved inert gas in the body to come out of solution in 

gas form (i.e., as bubbles.) Dive computers have been accepted as effective tools in assisting divers 

with the real-time monitoring of their decompression status. Oxygen-enriched air mixtures allow 

extensions of bottom times in certain depth ranges and optimize decompression on ascent. However, 

we continue to search for better tools and methods to take our science deeper. Since the publication 

of Haldane’s “Prevention of Compressed-Air Illness” over 100 years ago, a variety of new research 

directions have attempted to further explain and reduce the occurrence of the decompression sickness syndrome. Humans have ventured under water for at least 2,000 years without the use of an 

external compressed air source. However, observations of physiological adaptations in breath-hold 

diving marine mammals and birds eclipse the capabilities of human breath-hold divers. Nitrogen 

narcosis and neurological decompression sickness on a single breath-hold dive can occur because of 

the depths and durations involved. The consummate divers, marine mammals and diving birds, have 

evolved numerous physiological and morphological adaptations that contribute to such remarkable diving capacity and obviate the two fundamental concerns of diving physiology: oxygen store 

management and the effects of pressure at depth. A more thorough understanding of the physiology underlying these phenomenal divers may also assist in preventing and treating diving-related 

pathologies in humans.

INTRODUCTION

Scuba diving conducted by scientists is an invaluable research tool. Since the advent 

of scuba in the 1950s, placing the trained scientific eye under water on compressed gas 

has provided research value and flexibility that unmanned systems often could not. One 

metric substantiating this value is provided by peer-reviewed scientific publications in 

high-impact journals of research that could not have been performed without the use of 

scientific diving techniques (Lang, 2007). For example, a recent computer search for the 

keyword “scuba” returned 671 articles from all 397 volumes published since 1967 of the 

Journal of Experimental Marine Biology and Ecology (JEMBE, Elsevier).

The purpose of a scientific diving project is the advancement of science requiring 

divers to use scientific expertise in studying the underwater environment. More often 

Michael A. Lang, Smithsonian Institution; now 

at The Ocean Foundation, 1990 M Street NW, 

Suite 250, Washington, District of Columbia 

20036, USA. Jessica U. Meir, University of British Columbia; now at Harvard Medical School, 

Department of Anaesthesia, Massachusetts General Hospital, 55 Fruit Street, Thier 511, Boston, 

Massachusetts 02114, USA. Tanya L. Streeter,

Freediver, Austin, Texas 78378, USA. Karen B.

Van Hoesen, University of California, San Diego 

Medical Center, Diving and Hyperbaric Medicine, 200 W. Arbor Drive, San Diego, California 

92103, USA. Correspondence: Michael A. Lang, 

langm@cox.net.

Manuscript received 25 January 2012; accepted 5 March 2013.
2 4 • smithsonian contributions to the marine sciences

than not this research is conducted in challenging and remote 

environments such as under polar ice, from research vessels at 

sea, or at atolls far removed from immediate medical assistance. 

Yet exposure statistics document that these research activities are 

performed to a remarkable degree of safety and scientific productivity (Lang, 2009; Sayer et al., 2007).

Access to the underwater research site is provided by scuba, 

and we are in continuous pursuit of technology to expand our 

operational window within acceptable safety limits. Safety concerns, however, have gradually eroded our depth limit to what 

has become a 60 m compressed air scuba window for scientific 

diving in the United States with impacts on how and where research is conducted with diving. Our understanding of the ocean 

ecosystem in toto is therefore potentially impaired. For example, 

shallow-water coral reefs are well understood, as are the horizontal linkages between adjacent mangroves and sea grass beds and 

their contributions to the reef ecosystem. But diving limitations 

make vertical linkages and deep systems problematic to investigate. Akin to limiting a tropical rainforest biologist from climbing 

higher than 10 m (thereby missing the majority of biodiversity that 

resides in the canopy), a scientific diver cannot effectively study 

the biodiversity and contributions of the deep reef to the shallowreef system because of current technology and training limitations.

The U.S. Department of Labor’s Occupational Safety and Health 

Administration does not restrict the scientific diving community 

with regard to technology, leaving the operational flexibility to utilize mixed gases, rebreathers, and saturation habitats in research 

methodology to meet the nation’s marine science needs. 

Physiological considerations and the probability of decompression sickness affect humans and marine animals on 

every dive. We know that decompression sickness is triggered 

by a rapid reduction of ambient pressure that allows dissolved 

inert gas in the body to come out of solution in gas form (i.e., 

as bubbles). Since the publication of Haldane’s (1908) “Prevention of Compressed-Air Illness,” a variety of new research 

directions have attempted to further explain and reduce the occurrence of the decompression sickness syndrome. Humans have 

ventured under water for at least two millennia without the use 

of an external compressed air source. However, observations of 

physiological adaptations in breath-hold diving marine mammals and birds eclipse the capabilities of human breath-hold divers. Even the current world-class human depth record of 214 m 

and breath-hold static apnea time of 11 minutes 35 seconds are 

orders of magnitude less than recorded marine mammal dives.

Nitrogen narcosis and neurological decompression sickness on 

a single breath-hold dive can occur because of the depths and 

durations involved. The consummate divers, marine mammals 

and diving birds, have evolved numerous physiological and morphological adaptations that contribute to such remarkable diving capacity and obviate the two fundamental issues of diving 

physiology: oxygen store management and the effects of pressure 

at depth. A more thorough understanding of the physiology underlying these phenomenal divers may also assist in preventing 

and treating diving-related pathologies in humans.

Waking up the aquatic reflexes we harbor as infants is 

perhaps one of the most important elements of freediving, a 

2,000-year-old diving technique still practiced today by the Ama 

of Korea and Japan. In 1967, Robert Croft was the first to practice ‘lung packing,’ the glossopharyngeal breathing technique. 

Today, extreme (No Limits) freediving prompts the question 

as to whether there is a finite limit to the depths a human can 

dive. Some contributing factors involve training and fitness regimen, mental strength, state of relaxation, chest (muscles/ribcage) 

elasticity, partial lung collapse to a residual volume of <0.5 L, 

possible pulmonary edema, glossopharyngeal insufflation that 

can increase pulmonary gas stores to >12 L, alternate equalization modes of sinuses and middle ears, dive times of about 41⁄2 

minutes, and a freediving decompression stop. Physiological phenomena such as nitrogen narcosis and neurological decompression sickness can affect freedivers on a single breath-hold dive 

due to the speed of descent, depths, and durations involved. 

SCIENTIFIC DIVING SAFETY 

AND EDUCATION

Diving Safety Research

The scientific diving community has a traditionally proactive record of furthering diving safety to minimize the risk of 

harm to human health. The first scientific diving safety program 

was established at Scripps Institution of Oceanography in 1952, 

pre-dating the national recreational scuba training agencies. Diving safety programs can be generalized as fulfilling a twofold purpose. The first is a research-support function, which assists the 

diving scientist with specialized underwater equipment, advice, 

and diver support to assist in fulfilling the scientific objectives of 

the diving project. The second is a risk management function that 

protects the safety and health of the individual scientist and the 

liability exposure of the employing organization by providing 

state-of-the-art diving equipment, suitable breathing gases, and 

training and medical surveillance programs. 

Scientific diving safety research by Lang and Hamilton 

(1989) considered a more effective means of decompression 

status monitoring using dive computers. Findings included the 

need for programs to approve specific makes and models of 

dive computers, training, and the operational consideration of 

the buddy pair to follow the most conservative dive computer 

profile. Initiation of appropriate surfacing procedures in case of 

dive computer failure, activation after previous use, and ensuring that complete outgassing has occurred were recommended 

as mitigation procedures. Careful consideration was advised for 

multiple deep dives. An evaluation of the future of dive computers was provided by Lang and Angelini (2009) reporting on 

functionality, features, and configurations. Lang and Egstrom 

(1990) investigated the slowing of ascent rates and performance 

of safety stops to provide scientific divers with a greater margin of decompression safety. Before certification, the diver must 
number 39 • 2 5

demonstrate proper buoyancy, weighting, and a controlled ascent, including a “hovering” stop. Ascent rates are controlled 

at a maximum of 10 m/min from 20 m and are not to exceed 

20 m/min from depth, at the rate specified for the make and 

model of dive computer or table being used. Scientific diving 

programs and many dive computers usually require a stop in 

the 5 m depth range for 3–5 minutes on every dive. Scientific 

divers receive practical training in drysuits, which must have a 

hands-free exhaust valve. A buoyancy compensator, capable of 

horizontal deflation, is required with drysuit use for emergency 

flotation but should not be used under water to avoid uncontrolled buoyancy problems. In the case of any emergency ascent, 

breathing 100% oxygen above water is preferred to in-water air 

procedures for omitted decompression. The effects of multiday, 

repetitive diving on diver physiology were evaluated by Lang 

and Vann (1992), who estimated decompression sickness (DCS) 

incident rates in the USA to be 1 per 1,000 dives in the commercial diving sector, 2 per 10,000 dives for the recreational 

scuba community, and 1 per 100,000 dives in the scientific diving universe. 

Scientific diving programs provide continuous training, 

recertification, and dive site supervision, which helps maintain 

established safe diving protocols. Making repetitive dives over 

multiple days may result in a higher risk of DCS. Increasing 

knowledge regarding the incidence of DCS indicates that the 

ability to predict the onset of DCS on multilevel, multiday diving 

is even less sensitive than the ability to predict DCS on single, 

square-wave-profile dives. There appears to be good evidence 

that there are many variables that can affect the probability of 

the occurrence of DCS symptoms. The ability to mitigate these 

variables through education, supervision, and training appears to 

be possible by promoting good levels of hydration, fitness, rate 

of ascent, and fatigue management. There is adequate technical 

support for the use of oxygen-enriched air (nitrox) and surfaceoxygen breathing in scientific diving where higher gas loadings 

are anticipated in multilevel, multiday dives. Decompression 

sickness is generally recognized as a probabilistic event, which 

tends to steer the scientific diving community toward a more 

conservative approach to occupational diving. 

The order of dive profiles was investigated by Lang and 

Lehner (2000), in part because of the difficulty for scientific divers to adhere to the “dive progressively shallower” rule while on 

projects investigating coral reefs at varying transect depths. More 

importantly, the genesis and physiological validity of the “dive 

deep first” rule was in need of examination. Historically, neither 

the U.S. Navy nor the commercial sector has prohibited reverse 

dive profiles. Reverse-dive profiles are acknowledged as being performed in recreational, scientific, commercial, and military diving. 

The prohibition of reverse-dive profiles by recreational training

organizations cannot be traced to any definite diving experience 

that indicates an increased risk of DCS. There is no convincing 

evidence that reverse-dive profiles within the no-decompression

limits lead to a measurable increase in the risk of DCS. This 

means that there may be no reason for the diving communities 

to prohibit reverse-dive profiles for no-decompression dives less

than 40 m and with depth differentials less than 12 m. 

Oxygen-enriched air (nitrox) has been used in the scientific 

diving community since the early 1970s. Lang (2001, 2006) reported that for entry-level, open-circuit nitrox diving there is no 

evidence that shows an increased risk of DCS with the use of 

oxygen-enriched air (nitrox) compared with compressed air. A 

maximum PO2

 of 1.6 atm is generally accepted based on the history of nitrox use and scientific studies. Routine CO2

 retention 

screening is not necessary for open-circuit nitrox divers. Oxygen 

analyzers should use a controlled flow-sampling device for accurate mix analysis, which should be performed by the blender 

and/or dispenser and verified by the end user. It is important to 

ensure that equipment used with oxygen or mixtures containing 

over 40% oxygen by volume are designed, dedicated, and maintained for oxygen service. 

Operational Diving Procedures

Operational guidelines for remote scientific diving operations were promulgated on a consensual basis by the senior practicing scientific divers for blue-water diving by Heine (1986) and 

for polar diving by Lang and Stewart (1992) and Lang and Sayer 

(2007). A phased approach toward the expansion of the scientific 

diving operational window from 60 m to 90 m was published 

by Lang and Smith (2006), resulting in the evaluation of commercial and military diving methods for the science community 

through surface-supplied diving, rebreathers, mixed gas, and saturation techniques. The most immediately transferable method 

for access to 90 m is surface-supplied diving with mixed gas. This 

would allow for the dive profile management to occur topside, 

and for the scientist at the end of the hose to be able to focus 

on the scientific data collection. There are some disadvantages, 

such as limitations on horizontal mobility, that would make this 

method not applicable to all sites of scientific interest. However, 

surface-supplied training is not overly complicated and would 

allow for a quick transition from scuba to helmet-and-hose diving given the appropriate commercial diving equipment and 

topside management (Lang and Robbins, 2009). Deep-air diving for short-bottom durations under ideal conditions remains a 

possibility for very experienced divers who are cognizant of gas 

management, nitrogen narcosis, decompression strategies, and 

maximum operating depth limits of partial pressure of oxygen. 

Advanced tools such as rebreathers are not new technology, but 

with their surge in popularity in the technical diving community 

we are hopeful that with engineering solutions to support their 

increased reliability and reduce maintenance efforts they will 

evolve into a mainstream tool as well.

The U.S. scientific diving community has long adhered to 

a proven experience-accumulation schedule. Depth certifications 

provide a mechanism to gather diving experience incrementally, 

and scientific dives are planned around the competency of the 

least experienced diver. Diving with compressed air in scientific 

diving operations is not permitted beyond a depth of 58 m. The 
2 6 • smithsonian contributions to the marine sciences

100-hour scientific diver training course consists of theoretical 

training, practical skills training in confined water, and completion of 12 supervised open-water dives in a variety of dive sites 

for a minimum cumulative bottom time of 6 hours. Additional 

training is provided for diving specialties such as decompression 

diving, surface-supplied diving, mixed gas or oxygen-enriched air 

(nitrox) diving, semi- or closed-circuit rebreather diving, saturation diving, blue-water diving, drysuit diving, overhead environment (ice, cave, or wreck) diving, and altitude diving. 

All scientific diving is planned and executed in such a manner as to ensure that every diver maintains constant, effective 

communication with at least one other comparably equipped, 

certified scientific diver in the water. This buddy system is based 

upon mutual assistance, especially in the case of an emergency. 

If loss of effective communication occurs within a buddy team, 

all divers surface and reestablish contact. A dive flag is displayed 

prominently whenever diving is conducted. Scientific diving is 

not conducted unless procedures have been established for 

emergency evacuation of the divers to a hyperbaric chamber or 

appropriate medical facility and these procedures have been approved by the Diving Officer. Diving first aid training is a requisite for scientific diver certification and emergency oxygen kits 

are present at the dive location. Hyperbaric chambers, as a rule, 

are not required to be on site. In the case of an asymptomatic 

diver diving within the dive computer no-decompression limits 

during the previous 48 hours, there should be a minimum 12-

hour delay period with no diving prior to flying. The longer the 

diver delays an ascent to altitude, the lower the probability of 

onset of decompression sickness symptoms. 

Diving Medical Surveillance

Scientific divers who are exposed to hyperbaric conditions 

must possess a current diving medical certification. In passing 

that examination the diver will have been declared by the physician to be medically fit to engage in diving activities as may be 

limited or restricted in the scientific diver medical certification. 

All medical evaluations are performed by, or under the direction 

of, a licensed physician of the applicant diver’s choice, but preferably one trained in diving/undersea medicine. The diver must 

be free of any acute or chronic disabling disease or conditions 

contained in the list of conditions by Bove (1998) for which restriction from diving may be recommended. There are currently 

no fitness standards per se for scientific divers other than during 

the initial scientific diver training course, which includes in-water 

time and distance challenges for swimming. A stress tolerance 

test can be prescribed by a physician based on preliminary 

screening that indicates the potential of a higher than normal 

risk of coronary artery disease. Cardiac events are the proximate 

cause of more than 30% of diving fatalities in the recreational 

diving community (Vann and Lang, 2011). Medical evaluations 

are completed before a diver may begin diving and thereafter at 

five-year intervals up to age 40, three-year intervals after the age 

of 40, and two year-intervals after age 60. Any major injury or 

illness or any condition requiring hospital care requires diving 

medical clearance. If the injury or illness is pressure-related, then 

the clearance to return to diving must be performed by a physician trained in diving medicine. 

DECOMPRESSION SICKNESS

Breathing and Inert Gas

The increased pressure gradient between inspired gas and the 

dissolved gas tension in the body at depth results in an equilibration of the pressure differential leading to saturation. The composition of the air we breathe consists of nitrogen (79%), an inert 

gas that is absorbed and dissolved in the bloodstream and tissues. 

The nitrogen partial pressure (PN2

) at sea level in the lungs and 

surrounding tissues is in equilibrium. Ambient pressure increase 

(on descent) causes denser air in the lungs to be driven into the 

tissues to maintain this equilibrium, a process termed ongassing. 

Ambient pressure decrease (on ascent) causes the increased PN2

 in 

the tissues to be driven into the lungs, called offgassing.

It takes time for nitrogen to enter and to leave the body. Upon 

ascent the body begins to eliminate N2

. If too much N2 is still present after surfacing, the excess nitrogen forms bubbles in the body, 

creating microscopic clots that impair circulation and can damage endothelial linings of vessels. Decompression sickness symptoms range from skin rash, extreme fatigue, coughing, and painful 

joints to paralysis and unconsciousness. Commonly accepted prevention is to stay within dive computer no-decompression limits,

maintain slow ascent rates (<10 m/min), perform safety stops, 

and not run out of breathing gas. 

Haldane and Prevention of “The Bends”

Our fundamental knowledge of decompression was provided 

by Boycott, Damant, and Haldane (1908) in their paper “The Prevention of Compressed Air Illness.” Haldane initially used goats 

and later divers in his decompression experiments to validate his 

dive tables and make some important observations and findings: 

no diver had the bends after rapid decompression from 12.8 m 

(42 ft) to the surface; the general principle that a 2:1 pressure 

difference could be tolerated; the concept of staged decompression; a model using six compartments with different half times; 

and deep compressed-air test dives to 64 m. The tables describing 

uptake and elimination of nitrogen were developed by Haldane’s 

son Jack, aged 13 at the time, who with Ronald Fisher and Sewall 

Wright later became the founder of population genetics (Lang 

and Brubakk, 2009). Validation of Haldane’s tables was followed 

by the Royal and U.S. navies’ adoption of their use in 1908 and 

1912, respectively. They were revised in 1957 and became the 

diving guide for military, commercial, scientific, and recreational 

diving for decades. Subsequently, decompression physiologists 

and modelers modified surfacing ratios, ascent rules, Workman’s 

M-values, Thalmann’s algorithm, probabilistic models, bubble 
number 39 • 2 7

models, and deep stops. Despite these efforts, gas content models 

that are direct descendants of Haldane’s model remain the most 

prevalent approach to decompression (Doolette, 2009).

Decompression Sickness and Bubbles

Decompression sickness is a syndrome caused by a reduction of absolute pressure and a separation of gas in body tissues 

due to inadequate decompression leading to an excessive degree 

of gas supersaturation. In 1879, Paul Bert (1978) demonstrated 

that decompression of animals after a hyperbaric exposure produced bubbles in the blood. The signs and symptoms of DCS and 

treatment with oxygen and recompression are well described. 

However, other aspects of DCS are poorly understood, such as 

the relationship between gas phase separation and DCS injury 

and the large variation in individual susceptibility to DCS. 

Bubbles within the blood and tissues cause vascular obstruction leading to hypoxic tissue damage. Bubbles activate various 

plasma proteins including the coagulation cascade, complement, and kinins (Ward et al., 1987), and are associated with 

aggregation of platelets. Vascular endothelium is a monolayer 

of cells lining blood vessels. The endothelium senses stimuli and 

triggers release of vasoactive substances including nitric oxide 

(NO), which can inhibit adhesion of platelets and leukocytes. In 

response to inflammatory signals initiated by bubbles, endothelial cells become activated, generating endothelial microparticles 

(EMP), which in turn may reduce endothelial function. Vascular 

bubbles can injure endothelium and reduce the vasoactive effects 

of other compounds such as substance P and acetylcholine (Nossum et al., 1999). There is growing evidence that the endothelium may play a key role in the development of DCS. 

Venous gas bubbles (VGB) are found in the vasculature and 

right heart after recreational and professional dives and can be 

monitored and documented with the use of ultrasound by either 

Doppler or echocardiography (Eftedal and Brubakk, 1997). 

There is a statistical relationship between detectable bubbles and 

the risk of DCS (Eftedal et al., 2007). Doppler-detected VGB is 

a useful method of measuring decompression stress and the absence of VGB is a good indicator of decompression safety. 

Exercise has long been thought to be a risk factor for the development of DCS. However, more recent studies have revealed 

that pre-dive exercise and exercise performed during a decompression stop may significantly reduce bubble formation. Wisløff 

and Brubakk (2001) serendipitously found that aerobic endurance exercise training reduced bubble formation in rats exposed 

to hyperbaric pressures. In follow-up studies, an acute bout of 

exercise produced the same protective effect against DCS. Rats 

that were exercised 20 hours prior to a 60 m dive for 45 minutes 

had protection from bubble formation and improved survival 

(Wisløff et al., 2004). Survival time was lengthened even with 

exercise at 48 hours prior to diving. Dujica et al. (2004) found 

that a single bout of high-intensity exercise in humans 24 hours 

prior to a dive significantly reduced the number of bubbles in the 

right heart. In humans, the optimum time to exercise appears to 

be shorter; exercise just 2 hours prior to a dive provides a protective effect (Blatteau et al., 2005).

Mild exercise during decompression decreases the number 

of bubbles, most likely due to increased gas elimination from 

increased alveolar (lung air sacs) ventilation (Dujica et al., 2005). 

In follow-up studies, post-dive exercise caused an eightfold reduction in gas bubbles, presumably due to increased blood flow 

causing a depletion of bubble nuclei at the blood vessel lining 

surface (Dujic, 2009). Hence, exercise performed 24 hours prior 

to decompression, during decompression stops, and after a dive 

is not harmful as previously thought, but appears to protect from 

DCS. The mechanism responsible for these interactions may be 

related to nitric oxide (NO). 

There is growing evidence that the endothelium may play a 

role in the development of DCS. Endothelial nitric oxide (NO) 

is an important vasodilator and can attenuate bubble formation 

and incidence of DCS. Rats that are given an NO blocker exhibit 

far greater bubble formation and minimal survival following a 

dive compared to controls (Wisløff et al., 2003, 2004). Møllerløkken et al. (2006) demonstrated similar findings in a pig model, 

as did Dujica et al. (2006) in humans; pre-dive administration of 

nitroglycerin to humans results in a reduction of bubble formation after diving. Thus, administration of an NO donor (such as 

nitroglycerine) may be a reasonable alternative to exercise and 

may protect against DCS.

Heat stress is a nonpharmacological preconditioning strategy that can lead to protection against various types of insults 

such as ischemia, hypoxia, inflammation, and bubble-induced 

injury. Activation of the heat shock protein HSP70 by mild hyperthermia allows cells to resist subsequent insults that would 

otherwise result in death. This response is referred to as preconditioning. Blatteau et al. (2009) showed that a single pre-dive 

sauna session significantly increased HSP70 and decreased circulating bubbles after a chamber dive. Previous work by the same 

group showed that moderate dehydration and hypovolemia induced by pre-dive exercise could decrease VGB in divers (Blatteau et al., 2007). They hypothesize that heat-exposure-induced 

dehydration and NO pathway could be involved in this protective effect, but further investigation is needed to understand the 

heat-exposure-induced reduction in bubble formation. The role 

of HSP may be more related to the attenuation of tissue reaction 

to vascular bubbles than to direct reduction of bubble formation.

Diving in cold water tends to increase the risk for DCS. 

Previous studies in the 1960s showed that reduced blood flow 

caused by vasoconstriction and the resultant reduction in inert 

gas washout from tissues caused symptoms of DCS. However, 

more recent work by the U.S. Navy (Ruterbusch et al., 2004, 

2005) showed that the risk of DCS could be lowered by keeping 

the diver warm during decompression. It may be beneficial for 

the diver to be cold during the bottom phase of the dive but not 

during decompression. Vasoconstriction can hinder the uptake 

of gas during the dive while increased peripheral tissue perfusion 

from being warm during decompression may result in a greater 

elimination of inert gas (Mueller, 2007).
2 8 • smithsonian contributions to the marine sciences

In a recent article, Møllerløkken and Eftedal (2009) suggested that genetic and epigenetic makeup of individual divers 

may play a role in the variable susceptibility to DCS. Could there 

be genetic links between endothelial dysfunction and DCS? Genes 

involved in NO homeostasis display individual differences in activity. Since NO is an important mechanism in bubble formation, 

genetic links between endothelial dysfunction and DCS may be 

possible. Hence, genetic variations in humans may explain the 

variable susceptibility to DCS. Møllerløkken and Eftedal (2009) 

proposed to study alterations in genetic expression profiles of 

RNA in vascular endothelium following decompression using 

rat models, which may provide further knowledge of genetic 

variability in the physical and biochemical changes experienced 

in diving. By understanding the genetic basis of individual responses to diving, we may be better able to predict individual 

risk of developing DCS with the potential to prevent or relieve 

disease by preconditioning or pharmacological interventions.

FREEDIVING

Decompression Sickness in Breath-­Hold Divers

Breath-hold diving (freediving) is also a method utilized in

underwater research and can also subject scientists to decompression sickness. Unlike scuba divers, breath-hold divers do not

breathe compressed gas; hence the nitrogen that remains in the 

lungs after the last breath before diving is the only inert gas that 

could accumulate in tissues. During a breath-hold dive, compression of the chest increases the nitrogen partial pressure in the 

alveoli, which causes nitrogen to be taken up by the blood. It 

was previously assumed that a breath-hold diver could not accumulate enough nitrogen concentration in the tissues to cause the 

supersaturation that results in decompression sickness. However, 

reports from the 1960s from the Ama divers in Japan describe 

symptoms of decompression sickness in these pearl divers, including partial or complete paralysis, vertigo, and loss of consciousness. Cross (1965) described a syndrome in pearl divers called 

“Taravana,” which means to “fall crazily” and most likely represented decompression sickness. These divers performed frequent 

dives to over 30 msw (100 fsw) with bottom times of 30–60 seconds. They repeated these dives with short surface intervals for 6 

hours per day. Cross (1965) also reported another group of divers 

who had surface intervals twice as long as the Tuamotu divers 

and did not get DCS. Other reports have described decompression sickness in breath-hold divers. Schipke et al. (2006) reported 

90 cases of decompression sickness after repetitive breath-hold

dives. In a recent review of the literature and breath-hold diving,

Lemaitre et al. (2009) reported 141 cases of DCS in 447 divers. 

Lanphier (1965) proposed that repeated deep breath-hold 

dives separated by short intervals at the surface could lead to 

progressive accumulation of enough nitrogen to cause decompression sickness. Short surface intervals do not allow tissue nitrogen to be eliminated. Hence, nitrogen can accumulate in the 

tissues during repeated breath-hold dives equal to the amount 

found in scuba divers. As in scuba diving, repetitive breath-hold 

diving has been reported to produce venous gas emboli detectable with ultrasound Doppler (Spencer and Okino, 1972). A 

single deep breath-hold dive is much less likely to lead to decompression sickness; however, two reports of neurologic symptoms 

occurring after a single deep breath-hold dive may represent 

DCS (Magno et al., 1999; Desola et al., 2000).

Repeated breath-hold dives and short surface intervals are 

factors that predispose to decompression sickness. Fahlman and 

Bostrom (2006) have suggested that increasing the surface interval to at least twice the duration of the dive may help reduce 

accumulated tissue nitrogen and reduce the incidence of DCS in 

breath-hold divers. Understanding how marine mammals avoid 

excessive nitrogen tissue concentrations could help reduce decompression sickness in human breath-hold divers and scuba divers.

Freediving History

For the first nine months of their lives, humans exist in an 

aquatic environment very similar to sea water. If an infant is 

submerged, it instinctively holds its breath for up to 40 seconds 

while swimming breast strokes. It appears that we seem to lose 

this innate diving ability as soon as we commence walking. Waking up these reflexes is one of the most important elements of 

freediving, thus giving humans better abilities to be protected 

at greater depths. Relevant adaptations for freedivers would 

include reflex bradycardia, blood shifts, vasoconstriction, and 

splenic contraction.

The Ama of Japan and Korea are female pearl divers who 

still use a diving technique at least 2,000 years old. Women older 

than 17 years of age use rocks to descend to the bottom where 

they pick up shells and sea weeds; they dive naked 8–10 hours 

per day in water barely over 10°C. Rahn and Yokoyama (1965) 

reviewed the diving physiology of the Ama, which remains the 

baseline of our knowledge of breath-hold diving physiology.

Chatzistathis, a leading sponge diver from Symi, Greece, was 

1.70 m tall and weighed 65 kg. He suffered from remarkable lung 

emphysema, smoked tobacco extensively, and was part deaf from 

a life of diving without proper equalization. In 1913, at age 35, 

Chatzistathis salvaged an anchor from estimated 88 m depth, 

freediving up to three minutes at a time. He was carried down 

by a heavy stone, a primitive diving technique as old as the Greek 

civilization itself. In 1962, Enzo Maiorca was the first to reach the 

fateful 50 m barrier unassisted, despite predictions from scientists 

that beyond 50 m the human lungs would collapse from the pressure. Jacques Mayol was introduced in 1966 and revolutionized 

freediving with his use of Eastern yoga and meditation traditions, 

rather than the previous norm of heavy hyperventilation. 

In 1967, Robert Croft of the U.S. Navy was the first to 

freedive beyond 70 m and his achievements were important in 

establishing most modern scientific conclusions about freediving, 

among them the mammalian diving reflex and the blood shift phenomenon. He was the first record breaker to use “lung packing,” 
number 39 • 2 9

the glossopharyngeal breathing technique first described in polio 

patients by Dail (1951). Loring et al. (2007) measured results of 

glossopharyngeal insufflations and found maximal lung volume 

was increased by 0.13–2.84 L, resulting in volumes 1.5–7.9 SD 

above predicted values. The increased circumference of the thorax and a downward shift of the diaphragm enable a larger filling of the lungs through chest expansion. The amount of gas in 

the lungs after packing increased by 0.59–4.16 L, largely due to 

elevated intrapulmonary pressures of 52–109 cmH2

O that compress gas in the lungs to 100 cmH2

0 (=10 kPa or 10% more air 

compared to 0 kPa). 

By 1999, Francisco Rodriguez (aka Pipin Ferreras) and Umberto Pelizzari pushed each other competitively to 150 m depth 

records in No-Limits. By 2003, Tanya Streeter mirrored Angela 

Bandini’s 1989 feat by breaking the intergender No-Limits world 

record, reaching 160 m depth.

Germonpré et al. (2010) described a technique by Patrick 

Musimu who, by training, was capable of allowing passive 

flooding of the sinuses and middle ear with sea water during 

descent by suppressing protective reflexes during this process. 

Musimu attempted to breach 200 m in No-Limits, but outside 

the supervision of any diving federation. On one last training 

attempt he reached 209 m depth with his sled and successfully 

returned to the surface. Minutes after surfacing, he suffered 

symptoms of decompression sickness and received hyperbaric 

treatment, which canceled the public attempt scheduled a few 

days later.

Modern-­Day Freediving Limits

Herbert Nitsch currently dominates deep freediving and 

aimed to surpass Musimu’s unofficial but widely acknowledged 

209 m dive in this increasingly challenging discipline. On his 41⁄2 

minute 214 m record deep dive, Nitsch used deep-water breathhold decompression by ascending very slowly and making a stop 

to avoid decompression sickness (Figure 1). Table 1 lists current 

FIGURE 1. Profile of Herbert Nitsch’s record no-limit freedive to 214 m in 41⁄2 min, Spetses, Greece, 2007 (from

Lindholm, 2009, courtesy AIDA International, with permission).
3 0 • smithsonian contributions to the marine sciences

world men and women records in eight competitive disciplines.

Streeter (2006) described her training, work-up dives, narcosis symptoms, operational logistics, and actual freedive for the 

2002 No-Limits record to 160 m. She utilized a weighted sled 

for the descent and an inflated lift bag for the ascent. Approximate travel speeds were 1.5–2 m s−1 round trip with a total dive 

time of 3 min, 32 s. Competition freedivers are athletes first with 

performance being the main objective, but they obviously wish 

to perform safely.

We stand to improve freediving performances and learn 

from clinical research on the physiological aspects of breath-hold 

diving and from marine mammal and bird studies.

Considerations

The nitrogen that is available during diving is compressed 

in the lungs and would potentially be the cause of narcosis. This 

amount of nitrogen is not likely to be evenly distributed to the 

body tissues in the short period of freedive time. The body’s diving response vasoconstricts the periphery, forcing the nitrogen to 

go mostly to the brain, which potentially results in an elevated 

brain PN2

. It may not be possible to absorb a significant amount 

of nitrogen from a lung that is severely compressed. The lung 

tissue follows the compression of the air, so that the exchange 

surface area (normally about 70 m2

 between the lung blood and 

the gas space) is reduced to an extremely small area. That could 

support the high-pressure nervous syndrome (HPNS) theory. In 

freedives, nitrogen is being taken up on the way down, but very 

rapidly through a severely shrinking exchange area. It is also possible that nitrogen narcosis may be limited due to reduction in 

gas uptake through atelectasis (lung collapse).

Nitrogen is soluble, allowing pressures to build up substantially, and it is possible that a level of hypoxia exists. The loss 

of lung volume at depth could allow for mixing venous oxygen 

levels. The sensations of nitrogen narcosis and reduced oxygen 

saturations can be quite similar, with increased susceptibility potentially aided by higher CO2

 levels. Comparative physiological 

knowledge seems to indicate that elephant seals’ pre-dive exhalation strategy occurs, in part, to reduce susceptibility to decompression sickness, shallow-water blackout, and nitrogen narcosis. 

Observations of many more dives to these depth ranges would 

be needed to form a more conclusive opinion on nitrogen narcosis and decompression sickness in extreme freedivers. Diving 

physiology in the twilight zone is complicated. There may also 

be a transient hypovolemic (decreased blood volume) effect from 

significant blood pooling, which may interfere with adequate 

perfusion in the tissues for a short period.

PHYSIOLOGY OF THE CONSUMMATE 

DIVERS: MARINE MAMMALS 

AND DIVING BIRDS

The freediving depth records described above are impressive, 

yet even these extreme human performances hardly compare to the 

capabilities of the true consummate divers, marine mammals and 

diving birds. These animals routinely plummet to great depths for 

extended durations (Table 2), yet emerge unscathed by the myriad 

physiological conditions with which human divers must contend. 

Historical studies on diving animals revealed basic physiological and morphological adaptations (e.g., “armored” airways, air 

sinus modifications, thermoregulatory features, enhanced oxygen 

stores) that contributed toward this aptitude, and recent studies 

have shed further light on the remarkable capacity and mechanisms underlying this behavior. Advances in technology, remote 

monitoring, and advanced modeling have provided significant insight into the two fundamental issues of diving physiology: oxygen 

store management and the effects of pressure at depth.

TABLE 1. Current open water and pool world records.

Depth or time: Record holder (date)

Record type Male divers Female divers

Open water

No limits 214 m: Herbert Nitsch (06/07) 160 m: Tanya Streeter (08/02)

Variable weight 142 m: Herbert Nitsch (12/09) 122 m: Tanya Streeter (07/03)

Constant weight 124 m: Herbert Nitsch (04/10) 101 m: Natalia Molchanova (09/09)

Free immersion 116 m: William Trubridge (04/10) 90 m: Natalia Molchanova (09/09)

Constant weight without fins 92 m: William Trubridge (04/10) 62 m: Natalia Molchanova (12/09)

Pool

Static apnea 11 min, 35 s: Stephane Mifsud (06/09) 08 min, 23 s: Natalia Molchanova (08/09)

Dynamic apnea 250 m: Alexey Molchanov (10/08) 214 m: Natalia Molchanova (10/08)

Dynamic without fins 213 m: Tom Sietas (07/08); 160 m: Natalia Molchanova (08/09)

213 m: Dave Mullins (08/08)
number 39 • 3 1

The diving performance of humans is significantly impacted by the effects of pressure, namely via decompression sickness (DCS), N2

 narcosis, and high-pressure nervous syndrome 

(HPNS). Although more commonly associated with breathing 

compressed air, DCS has been reported in human breath-hold 

divers, as discussed above. How, then, do the elite divers of the 

animal kingdom escape the deleterious effects of pressure during their frequent, repetitive, and very deep dives? Several recent reviews detail the morphological and experimental evidence 

of the adaptations of diving animals to the pressures of diving 

(Fahlman, 2009; Lemaitre et al., 2009; Ponganis, 2011) with 

modifications such as the absence of air-filled cranial sinuses in 

seals, middle ear cavities lined with venous plexuses that may 

engorge with blood at depth, anatomical modifications of the 

airways and their responses to compression, and enhanced lung 

surfactants. Scholander’s original model of lung collapse and the 

cessation of gas exchange at depth has been particularly well 

supported by both anatomical and experimental evidence in marine mammals; lung collapse undoubtedly plays a role in limiting 

the accumulation of nitrogen at depth, though the degree and 

depth of collapse are likely variable and dependent on a variety 

of factors (Scholander, 1940; Fahlman, 2009; Ponganis, 2011). 

Cardiovascular adjustments such as reduced heart rates and 

decreased cardiac outputs that occur during diving serve not 

only to conserve oxygen, as discussed below, but also to reduce 

the accumulation of nitrogen. Theoretical and modeling studies have demonstrated that such responses may play a large role 

in limiting the accumulation of nitrogen, at least in certain tissues (Fahlman et al., 2006; Lemaitre et al., 2009). Dive patterns 

(depths, durations, and ascent rates) and dive behavior will also 

dictate the accumulation of nitrogen at depth, though no data 

exist as to how animals might sense or cognitively influence these 

types of parameters.

Despite the protective adaptations of diving animals, relatively recent strandings of beaked whales associated with naval 

sonar exercises and accounts of dysbaric osteonecrosis in sperm 

whales have heightened interest regarding the effects of pressure 

on diving animals, as these findings are consistent with, though 

not diagnostic of, DCS and N2

 absorption at depth (Jepson et al., 

2003; Moore and Early, 2004; Fernandez et al., 2005). If nitrogen loads do reach high levels in diving animals, novel means of 

dealing with this gas burden may exist in the animal kingdom. 

Because of the few actual studies of nitrogen pressures in diving 

animals, more biological data are necessary to further elucidate 

these adaptations.

Oxygen stores in animals are distributed between the respiratory system, blood, and muscle. It is well documented in 

the field of diving physiology that accomplished divers have 

enhanced oxygen stores, mainly attributed to increased blood 

volumes and increased hemoglobin and myoglobin concentrations. For example, an elephant seal has almost twice the hemoglobin concentration, three times the mass-specific blood

volume (Simpson et al., 1970), and 10 to 15 times the myoglobin concentration (Thorson and Le Boeuf, 1994) as compared to 

a human. Equally as important as these increased oxygen stores, 

however, are the rate at which oxygen is depleted and hypoxemic tolerance, or lowest level of oxygen that an animal can 

tolerate. Despite the importance of these latter two parameters, 

few studies have addressed the rate and magnitude of oxygen 

depletion while diving. 

Another hallmark of diving animals is a redistribution of 

oxygen stores among the three compartments (Figure 2). Compared to humans, phocid seals have minimized the percentage 

of oxygen located in the respiratory store, likely an advantage 

toward the avoidance of nitrogen accumulation and decompression sickness. This fits with the fact that phocids dive upon 

expiration and undergo lung collapse at depth, as reviewed previously (Fahlman, 2009). Penguins, otariid seals, and cetaceans, 

however, are thought to dive upon inspiration, and correspondingly have a higher percentage of oxygen stores in the respiratory 

system (Kooyman and Sinnett, 1982; Ponganis et al., 2010; Skrovan et al., 1999). In line with their increased oxygen stores, diving animals have large percentages of their total oxygen within 

the blood and muscle (Figure 2).

In discussing the management of oxygen stores in diving animals, specific examples from the literature highlight three central 

themes: (1) cardiovascular responses, (2) hypoxemic tolerance 

and the rate of oxygen depletion, and (3) energy saving mechanisms such as a hydrodynamic shape and locomotive strategies. 

TABLE 2. Maximum dive depth and duration records for various diving species (Association Internationale pour le Développement de l’Apnée [AIDA International]; Norris and Harvey, 

1972; Watkins et al., 1985; Ridgway, 1986; Le Boeuf et al., 1988; 

Eckert et al., 1989; Lutcavage et al., 1990, 1992; Thorson and Le 

Boeuf, 1994; Kooyman and Kooyman, 1995; Mate et al., 1995; 

Stewart and DeLong, 1995; Ponganis et al., 1997; Kooyman and 

Ponganis, 1998; Kooyman et al., 1999; Southwood et al., 1999; 

Noren and Williams, 2000; Ponganis et al., 2003; Hays et al., 

2004; Tyack et al., 2006; Ponganis et al., 2007).

Depth Duration

Species, record type (holder: year) (m) (min:s)

Human Homo sapiens

Men: No Limits (Nitsch: 2007) 214 4:30

Women: No Limits (Streeter: 2002) 160 3:32

Men: Apnea in pool (Mifsud: 2009) Surface 11:35

Women: Apnea in pool (Molchanova: 2009) Surface 8:23

Leatherback turtle Dermochelys coriacea 1230 67:18

Bottlenose dolphin Tursiops truncatus 390 8

Emperor penguin Aptenodytes forsteri 564 23:06

Northern elephant seal Mirounga angustirostris 1581 119

Beaked whale Ziphius cavirostris 1888 85

Sperm whale Physeter macrocephalus 2250 138
3 2 • smithsonian contributions to the marine sciences

Cardiovascular Responses

Since Scholander’s and Irving’s classic findings during forced 

submersion studies, it has been suggested that reductions in heart 

rate and peripheral perfusion are the principal determinants of 

oxygen depletion (Scholander, 1940; Irving et al., 1941; Scholander et al., 1942). This follows from the fact that the organs accounting for approximately half of O2

 consumption at rest 

are either perfusion dependent or directly related to heart rate 

(Schmidt-Nielsen, 1983; Butler and Jones, 1997; Davis and Kanatous, 1999). Pre- and postdive tachycardias provide optimal loading of O2

 before the dive, and heart rate alterations can result in a 

reduction and redistribution of blood flow during the dive. Most 

diving animals experience a decrease in heart rate upon submersion, the degree varying with species and dive duration (Scholander, 1940; Irving et al., 1941; Butler and Jones, 1997). This can 

be thought of in terms of an energy conservation strategy, as a 

reduced heart rate will result in a slower rate of oxygen depletion, 

consequently yielding increased aerobic dive duration. 

A recent investigation that deployed digital electrocardiogram (ECG) recorders on diving emperor penguins has revealed 

a particularly extreme heart rate response in this elite avian diver, 

documenting the highest and lowest measured heart rates for the 

emperor penguin (Meir et al., 2008). Heart rate decreased to as 

low as 3 bpm during diving, with periods of bradycardia near 

5–6 bpm sustained for over five-minute intervals (Figure 3).

Despite these extreme reductions in heart rate, this diver remains capable of propulsion for active maneuvering and pursuit 

of prey. The mean heart rate during diving was significantly lower 

than the ~70 bpm heart rate of a penguin at rest (heart rates of 

penguins at rest are in the same range as those of humans at rest, 

with these extreme decreases occurring routinely) (Meir et al., 

2008). In contrast, although other diving birds show decreases 

in heart rate upon submersion, this is only relative to their predive tachycardic values (i.e., not lower than resting heart rate) 

(Millard et al., 1973; Butler and Woakes, 1984; Enstipp et al., 

2001; Froget et al., 2004). Heart rates as high as 256 bpm, the 

highest value ever measured in this species, were also measured 

during pre- and post-dive periods (Meir et al., 2008). These extreme highs and lows show the dramatic range of physiological 

responses of which this animal is capable, while its heart rate at 

rest hovers around 70 bpm, not unlike that of our own. In all 

diving animals, heart rate responses can be quite variable, demonstrating the plasticity of oxygen management strategies during 

diving (Thompson and Fedak, 1993; Andrews et al., 1997; Meir 

et al., 2008). 

Oxygen Depletion

Although heart rate responses are indicative of overall oxygen consumption, a more direct approach to understanding the 

management of oxygen stores is to measure oxygen directly 

during the dive. Miniaturized microprocessors, biologging instrumentation, and the novel use of an oxygen electrode have 

recently allowed researchers to document hypoxemic tolerance 

(the lowest tolerable level of oxygen) and oxygen depletion in 

this manner in freely diving emperor penguins and elephant 

seals. This PO2

 (partial pressure of oxygen) electrode has been 

successfully deployed in air sacs and blood vessels in the emperor 

penguin (Stockard et al., 2005; Ponganis et al., 2007; 2009), and 

in blood vessels in the elephant seal (Meir et al., 2009). With the 

recent characterization of the oxygen–hemoglobin dissociation 

curve for these species (Meir et al., 2009; Meir and Ponganis, 

2009), the PO2

 profiles can be converted to hemoglobin (Hb) 

FIGURE 2. The distribution of oxygen stores in humans, elephant 

seals, and emperor penguins (Kooyman, 1989; Kooyman and 

Ponganis, 1998; Kooyman et al., 1999; Ponganis et al., 2003, 

2007, 2009). FIGURE 3. Heart rate and dive profile of an 18.2 min dive of an 

emperor penguin (modified from Meir et al., 2008).
number 39 • 3 3

saturation profiles, providing values for the amount of oxygen 

present in the system at the start of, throughout, and after the 

dive.

These studies have demonstrated exceptional hypoxemic 

tolerance in these species, particularly in the elephant seal. Arterial PO2

 values as low as 12 mmHg (6–8% Hb saturation) at the 

end of the dive were measured in the elephant seal, the lowest 

PO2

 ever measured in a freely diving seal (Meir et al., 2009). This 

is well below the limits of most other mammals, including those 

of mountaineers at the brink of human tolerance at the summit 

of Mt. Everest (Grocott et al., 2009). This value, obtained in a 

voluntary diving setting with unrestricted access to the surface in 

the open ocean, is even nearly equivalent to the critical arterial 

PO2

 of seals in forced submersion studies, as defined by EEG 

criteria marking the threshold of cerebral dysfunction. Venous 

saturation values at the end of the dive were routinely as low 

as 2–10 mmHg (0–4% Hb saturation) in these seals (Figure 4A; 

Meir et al., 2009), and as low as 2–6 mmHg in emperor penguins (Ponganis et al., 2007). Again, these values are well below 

the limits of humans or mammals at maximal exercise, and even 

lower than those of the well-documented hypoxemic extremes of 

horses performing strenuous exercise (Taylor et al., 1987; Bayly 

et al., 1989; Roca et al., 1989; Manohar et al., 2001). Both species demonstrated an arterialization of the venous oxygen store 

(Hb saturations > 90%) (Figure 4A). Combined with the nearcomplete depletion of the venous oxygen store, this illustrates 

highly efficient optimization of the venous oxygen reserves. 

Adaptation at the biochemical level relevant to oxygen management has also been recently revealed in the emperor penguin. 

The hemoglobin of the emperor penguin has a higher affinity 

for oxygen than that of other birds (Meir and Ponganis, 2009), 

similar to that which has been reported for other penguin species and the high-flying bar-headed goose (Lenfant et al., 1969; 

Milsom et al., 1973; Petschow et al., 1977; Black and Tenney, 

1980). This is particularly advantageous for a diving animal that 

experiences low levels of oxygen while diving, as it implies that 

more oxygen is available at any given PO2

. It also allows for 

more complete depletion of the significant respiratory oxygen 

store in this diving bird.

An analysis of results from these studies further highlights 

the differences in the distribution of oxygen stores in different 

species. For example, oxygen profiles of diving emperor penguins 

illustrate that arterial hemoglobin saturation is maintained near 

100% throughout most of the dive, declining only in the final 

portion of the dive when the bird makes its ascent, when ambient 

pressure also declines (Meir and Ponganis, 2009) (Figure 5). This 

keeps oxygen levels high for critical organs like the heart and 

brain, and is consistent with the large respiratory oxygen store 

in this species, the high-affinity hemoglobin of this species, and 

ongoing gas exchange from the lungs to the blood. In contrast, 

arterial hemoglobin saturation values of elephant seals show a 

continuous decline after the start of the dive, often to lower final 

values than those of the emperor penguin at the end of dives 

(Figure 4B; Meir et al., 2009). This is consistent with the fact that 

the elephant seal has only about 4% of its total oxygen stores in 

the respiratory system (Figure 2), undergoes lung collapse, and 

dives upon expiration.

Oxygen depletion patterns in both arterial and venous 

compartments are highly variable, even for dives of the same 

duration. As discussed in relation to heart responses, these investigations further support the plasticity of oxygen management 

strategies during diving. 

FIGURE 4. (A) Venous percent hemoglobin (Hb) saturation and (B) arterial percent Hb saturation and dive profiles for an elephant seal (modified from Meir et al., 2009). In A (venous profile), note the very high % Hb saturation value at the start of the dive (arterialization) and the near 

complete depletion at the end of the dive.
3 4 • smithsonian contributions to the marine sciences

Energy-­Saving Mechanisms

In addition to physiological adaptations and responses, the 

hydrodynamic shape of marine mammals and diving birds (Fish, 

1994) coupled with various locomotor strategies also allows for 

significant energy and oxygen conservation in these animals. Investigations of various species have shown that diving animals 

routinely employ efficient swimming speeds (consistently around 

1–2 m s−1) and optimal stroke frequencies while maneuvering 

through their aquatic habitat (Ponganis et al., 1990; Sato et al., 

2007). Burst and glide swimming strategies and the exploitation 

of buoyancy changes can also result in considerable oxygen savings. It has been estimated that gliding alone could reduce the 

cost of diving by an average of approximately 28% (Williams 

et al., 2000).

DISCUSSION

Given our current operational framework and knowledge of 

human physiology and decompression sickness, we would expect 

the following elements to receive further consideration: a 90 m 

for 30 min operational scientific diving window within acceptable risk parameters; rebreather development with a goal toward 

providing engineering solutions to minimize investment of training time and pre-and post-dive maintenance requirements while 

enhancing reliability through mass production; replacement of 

passive thermal protection strategies with the advent of electrically heated gloves, socks, and undergarments; portable diving 

saturation system development, attainable within the constraints 

of scientific resources, with advantages that outweigh the lower 

cost and relative simplicity of bell diving/surface-supplied systems; and operational and physiological limits of wet diving 

using scuba versus one-man atmospheric diving systems.

Further development of dive computers will better approximate inert gas loads in the diver. Most current units have a diveprofile logging function, downloading capabilities for paperless 

databases, ascent rate monitors, an air-integration mode, and gas 

programmability. Benefits from advances in consumer electronics technology could bring the next generation of dive computers 

high resolution color displays, rechargeable batteries, GPS receivers, underwater communication and navigation, and emergency 

position-indicating radio beacons (EPIRB). Benefits from monitoring technology integrated into the dive computer algorithm 

could provide heart rate monitoring, skin temperature and oxygen saturation measurements, and possibly even inert gas bubble 

detection. Dive computers have for all practical purposes replaced 

dive tables in scientific diving and it would not be unreasonable to 

state that regardless of the number of algorithm variations incorporated within them, they all appear to fall within an acceptable 

window of effectiveness based on available databases of pressurerelated injuries. It is also clear that neither tables nor dive computers can eliminate all decompression problems, but when utilized 

conservatively computers have emerged as an important tool for 

the improvement of scientific diver safety.

In a recent review of DCS in breath-hold diving, Lemaitre et 

al (2009) proposed that if marine mammals could sense low levels of bubbles, they could possibly use behavioral or physiological means to reduce the inert gas burden. The future of human 

diving might entail some type of device that allows for measurement of our own tissue supersaturation and bubble formation.

Understanding the specialized adaptations that reduce decompression sickness in marine mammals and how they avoid excessive blood and tissue PN2

 and prevent bubble formation may 

improve our knowledge of reducing the risk of DCS in human 

breath-hold divers and scuba divers.

How deep can a human go? Avoiding barotrauma of descent and decompression illness and managing nitrogen narcosis are critical in attaining extreme breath-hold depths. Mental 

strength, fitness, and exercise to increase elasticity of the ribcage, 

muscles, and diaphragm are important. Trachea and lungs must 

be able to withstand a collapse to a residual volume of < 0.5 

L. Lindholm (2009) concludes that it is possible for (some) humans to hold their breath for more than 10 minutes or to dive 

to more than 200 m. Special lenses in fluid-filled goggles can be 

used instead of a mask to reduce the non-collapsible air spaces,

and glossopharyngeal insufflations (lung packing) may be used 

to increase pulmonary gas stores to over 12 L. Water equalization of the sinuses and middle ear, while painful, is a useful 

adjunct. Pulmonary edema and partial lung collapse will likely 

occur. Currently, the limits of deep breath-hold diving seem to 

be pulmonary barotrauma of descent causing pulmonary edema 

and nitrogen narcosis incapacitating the diver at depth or causing decompression sickness on ascent. 

FIGURE 5. Arterial percent hemoglobin (Hb) saturation and dive 

profile of four dives of an emperor penguin (modified from Meir and 

Ponganis, 2009).
number 39 • 3 5

Recent advances in technology and continued effort in the 

arena of the diving physiology of marine mammals and birds 

have been fruitful, documenting extreme responses beyond what 

has been traditionally hypothesized for these divers. These insights have implications for a wide variety of topics in diving 

physiology and physiological ecology, with the potential to redefine previous efforts of estimating oxygen utilization, which 

depend on accurate assessments of oxygen storage capacity and 

the extent of depletion while diving. Future work remains in further elucidating the mysteries of the management and exchange 

of gases in marine mammals and diving birds. A complete understanding of the physiology underlying these phenomenal divers and the mechanisms behind these abilities may also assist 

in preventing and treating diving-related pathologies in humans,

as well as human medical situations involving hypoxic damage 

including heart attack, stroke, organ transplant, and reperfusion 

energy.

CONCLUSIONS

The U.S. scientific diving regulatory, medical, training, and 

operational framework has resulted in a remarkably low decompression sickness incidence rate. In this particular segment of the 

diving community, diving safety research on dive computers, ascent rates, multiday repetitive diving, polar diving, reverse-dive 

profiles, oxygen-enriched air, and advanced scientific diving contributes to the conservative risk-management approach of scientific diving. Advances in diving medicine allow for mitigation 

of additional risk while pursuing further understanding of the 

mechanisms of decompression disease. Freediving sheds light on 

the extreme capabilities of human performance, approximating 

the outer limit. Physiological considerations, such as morphological adaptations, and processes, such as management of oxygen 

stores in diving animals, shed light on the remarkable capacity 

and mechanisms that enhance diving capabilities in diving animals. Investigations of cardiovascular responses, oxygen depletion, and energy-saving mechanisms have found further evidence 

in support of the phenomenal capabilities of the consummate 

divers. The importance of scientific diving as a valuable research 

tool that places the trained scientist’s eye under water is illustrated by the quantity of research projects reported in this volume that could otherwise not have been performed, with results 

published in the scientific literature. The peer-review publication 

process validates the viability and effectiveness of scuba as a research methodology. 

ACKNOWLEDGMENTS

We thank the Smithsonian Institution’s Office of the Under 

Secretary for Science, the National Science Foundation, and the 

National Research Council’s Ocean Studies Board for their support of this symposium and the opportunity to contribute. 

REFERENCES

Andrews, R. D., D. R. Jones, J. D. Williams, P. H. Thorson, G. W. Oliver, D. P. Costa, 

and B. J. LeBoeuf. 1997. Heart rates of northern elephant seals diving at sea 

and resting on the beach. Journal of Experimental Biology, 200:2083–2095.

Bayly, W. M., D. R. Hodgson, D. A. Schulz, J. A. Dempsey, and P. D. Gollnick. 1989. 

Exercise-induced hypercapnia in the horse. Journal of Applied Physiology, 

67:1958–1966.

Bert, P. 1978. Barometric pressure (La Pression Barométrique). Bethesda, Md.: Undersea Medical Society. 

Black, C. P., and S. M. Tenney. 1980. Oxygen transport during progressive hypoxia 

in high-altitude and sea-level waterfowl. Respiration Physiology, 39:217–

239. http://dx.doi.org/10.1016/0034-5687(80)90046-8.

Blatteau, J. E., A. Boussuges, E. Gempp, J. M. Pontier, O. Castagna, C. Robinet, 

F. M. Galland, and L. Bourdon. 2007. Haemodynamic changes induced by 

submaximal exercise before a dive and its consequences on bubble formation. British Journal of Sports Medicine, 41(6):375–379. http://dx.doi.org/10

.1136/bjsm.2006.032359.

Blatteau, J. E., E. Gempp, F. M. Galland, J. M. Pontier, J. M. Sainty, and C. Robinet. 

2005. Aerobic exercise 2 hours before a dive to 30 msw decreases bubble formation after decompression. Aviation, Space, and Environmental Medicine,

76:666–669. 

Blatteau, J. E., E. Gempp, J. M. Pontier, C. Balestra, T. Mets, and P. Germonpré. 

2009. Inducing HSP for protection against DCS: Heat exposure before diving 

reduces bubble formation in man. In The future of diving: 100 years of Haldane and beyond, ed. M. A. Lang and A. O. Brubakk, pp. 59–63. Washington, 

D.C.: Smithsonian Institution Scholarly Press. 

Bove, A. A., ed. 1998. Medical examination of sport SCUBA divers. 3rd ed. San 

Antonio, Tex.: Medical Seminars, Inc. 

Boycott A. E., G. C. C. Damant, and J. S. Haldane. 1908. Prevention of compressedair illness. Journal of Hygiene, 8:342–425.

Butler, P. J., and D. R. Jones. 1997. The physiology of diving of birds and mammals. 

Physiological Reviews, 77:837–899.

Butler, P. J., and A. J. Woakes. 1984. Heart rate and aerobic metabolism in Humboldt penguins (Spheniscus humboldti) during voluntary dives. Journal of 

Experimental Biology, 108:419–428.

Cross, E. R. 1965. Taravana: Diving syndrome in the Tuamotu diver. In Physiology 

of breath-hold diving and the Ama of Japan, ed. H. Rahn and T. Yokoyama, 

pp. 207–219. National Research Council Publication 1341. Washington, 

D.C.: National Academy of Sciences.

Dail, C. W. 1951. Glossopharyngeal breathing by paralyzed patients: A preliminary 

report. California Medicine, 75(3):217–218.

Davis, R. W., and S. B. Kanatous. 1999. Convective oxygen transport and tissue 

oxygen consumption in Weddell seals during aerobic dives. Journal of Experimental Biology, 202:1091–1113.

Desola, J., C. E. G. Lundgren, and J. M. Battle. 2000. Thirty neurological accidents 

in Spanish breath-hold divers: Taravana revisited? Undersea and Hyperbaric 

Medicine, 27:92.

Doolette, D. J. 2009. Haldane still rules! In The future of diving: 100 years of Haldane and beyond, ed. M. A. Lang and A. O. Brubakk, pp. 29–32.. Washington, 

D.C.: Smithsonian Institution Scholarly Press. 

Dujica, Ž. 2009. Exercise, endothelium, and diving physiology. In The future of diving: 100 years of Haldane and beyond, ed. M. A. Lang and A. O. Brubakk, pp. 

71–76. Washington, D.C.: Smithsonian Institution Scholarly Press.

Dujica, Ž., D. Duplanc ̇ica, I. Marinovica-Terzica, D. Bakovica, V. Ivanc ̇ev, Z. Valic, 

D. Eterovica, N. M. Petri, U. Wisløff , and A. O. Brubakk. 2004. Aerobic exercise before diving reduces venous gas bubble formation in humans. Journal of Physiology, 555(3):637–642. http://dx.doi.org/10.1113/jphysiol.2003

.059360.

Dujica, Ž., A. Obad, I. Palada, Z. Valic, and A. O. Brubakk. 2006. A single open 

sea air dive increases pulmonary artery pressure and reduces right ventricular function in professional divers. European Journal of Applied Physiology,

97(4):478–485. http://dx.doi.org/10.1007/s00421-006-0203-z.

Dujica, Ž., I. Palada, A. Obad, D. Duplanc ̇ica, D. Bakovica, and Z. Valic. 2005. Exercise 

during a 3-min decompression stop reduces post dive venous gas bubbles.

Medicine and Science in Sports and Exercise, 37:1319–1323. http://dx.doi

.org/10.1249/01.mss.0000174892.27331.ce.

Eckert, S. A., K. L. Eckert, P. J. Ponganis, and G. L. Kooyman. 1989. Diving 

and foraging behavior of leatherback sea turtles (Dermochelys coriacea). 

Canadian Journal of Zoology, 67:2834–2840. http://dx.doi.org/10.1139

/z89-399.
3 6 • smithsonian contributions to the marine sciences

Eftedal, O. S., and A. O. Brubakk. 1997. Agreement between trained and untrained 

observers in grading intravascular bubble signals in ultrasonic images. Journal of Undersea and Hyperbaric Medicine, 24:293–299.

Eftedal, O. S., S. Lydersen, and A. O. Brubakk. 2007. The relationship between venous gas bubbles and adverse effects of decompression after air dives. Journal 

of Undersea and Hyperbaric Medicine, 34:99–105. 

Enstipp, M. R., R. D. Andrews, and D. R. Jones. 2001. The effects of depth on 

the cardiac and behavioral responses of double-crested cormorants (Phalacrocorax auritus) during voluntary diving. Journal of Experimental Biology,

204:4081–4092.

Fahlman, A. 2009. How do marine mammals avoid DCS? In The future of diving: 

100 years of Haldane and beyond, ed. M. A. Lang and A. O. Brubakk, pp. 

129–135. Washington, D.C.: Smithsonian Institution Scholarly Press.

Fahlman, A., and B. Bostrom. 2006. Predicted nitrogen tensions during repeated 

breath-hold diving in humans. In UHMS Annual Scientific Symposium, 

p. 371. Durham, N.C.: Undersea and Hyperbaric Medical Society.

Fahlman, A., A. Olszowka, B. Bostrom, and D. R. Jones. 2006. Deep diving mammals: Dive behavior and circulatory adjustments contribute to bends avoidance. Respiratory Physiology and Neurobiology, 153:66–77. http://dx.doi.org

/10.1016/j.resp.2005.09.014.

Fernandez, A., J. F. Edwards, F. Rodriguez, A. E. de los Monteros, P. Herraez, 

P. Castro, J. R. Jaber, V. Martin, and M. Arbelo. 2005. Gas and fat embolic 

syndrome involving a mass stranding of beaked whales (Family Ziphiidae) 

exposed to anthropogenic sonar signals. Veterinary Pathology, 42:446–457. 

http://dx.doi.org/10.1354/vp.42-4-446.

Fish, F. E. 1994. Influence of hydrodynamic-design and propulsive mode on mammalian swimming energetics. Australian Journal of Zoology, 42:79–101. 

http://dx.doi.org/10.1071/ZO9940079.

Froget, G., P. J. Butler, A. J. Woakes, A. Fahlman, G. Kuntz, Y. Le Maho, and 

Y. Handrich. 2004. Heart rate and energetics of free-ranging king penguins 

(Aptenodytes patagonicus). Journal of Experimental Biology, 207:3917–

3926. http://dx.doi.org/10.1242/jeb.01232.

Germonpré, P., C. Balestra, and P. Musimu. 2010. Passive flooding of paranasal 

sinuses and middle ears as a method of equalization in extreme breath-hold 

diving. British Journal of Sports Medicine, doi:10.1136/bjsm.2010.043679.

Grocott, M. P. W., D. S. Martin, D. Z. H. Levett, R. McMorrow, J. Windsor, H. E.

Montgomery, and Caudwell Xtreme Everest Research Group. 2009. Arterial 

blood gases and oxygen content in climbers on Mount Everest. New England Journal of Medicine, 360:140–149. http://dx.doi.org/10.1056/NEJMoa

0801581.

Hays, G. C., J. D. R. Houghton, and A. E. Myers. 2004. Endangered species: PanAtlantic leatherback turtle movements. Nature, 429:522. http://dx.doi.org/10

.1038/429522a.

Heine, J. N., ed. 1986. Blue water diving guidelines. California Sea Grant Publication No. T-CSGCP- 014. 

Irving, L., P. F. Scholander, and S. W. Grinnell. 1941. Significance of the heart rate 

to the diving ability of seals. Journal of Cellular and Comparative Physiology,

18:283–297. http://dx.doi.org/10.1002/jcp.1030180302.

Jepson, P. D., M. Arbelo, R. Deaville, I. A. P. Patterson, P. Castro, J. D. Baker, 

E. Degollada, H. M. Ross, P. Herraez, A. M. Pocknell, F. Rodríguez, F. E. 

Howie, A. Espinosa, R. J. Reid, J. R. Jaber, V. Martin, A. A. Cunningham, 

and A. Fernández. 2003. Gas-bubble lesions in stranded cetaceans. Nature,

425:575–576. http://dx.doi.org/10.1038/425575a.

Kooyman, G. L. 1989. Diverse divers physiology and behavior. Berlin: SpringerVerlag. http://dx.doi.org/10.1007/978-3-642-83602-2.

Kooyman, G. L., and T. G. Kooyman. 1995. Diving behavior of emperor penguins 

nurturing chicks at Coulman Island, Antarctica. The Condor, 97:536–549. 

http://dx.doi.org/10.2307/1369039.

Kooyman, G. L., and P. J. Ponganis. 1998. The physiological basis of diving to 

depth: Birds and mammals. Annual Review of Physiology, 60:19–32. http://

dx.doi.org/10.1146/annurev.physiol.60.1.19.

Kooyman, G. L., P. J. Ponganis, and R. S. Howard. 1999. Diving animals. In The lung 

at depth, ed. C. E. G. Lundgren and J. Miller, p. 686. New York: Marcel Dekker.

Kooyman, G. L., and E. E. Sinnett. 1982. Pulmonary shunts in harbor seals and sea 

lions during simulated dives to depth. Physiological Zoology, 55:105–111.

Lang, M. A., ed. 2001. Proceedings of the DAN Nitrox Workshop, November 3 and 

4, 2000. Durham, N.C.: Divers Alert Network. 

Lang, M. A. 2006. The state of oxygen-enriched air (nitrox). Journal of Diving and 

Hyperbaric Medicine, 36(2):87–93.

———. 2007. Scientific diving in the United States: The value of scuba as research 

methodology. Journal of the Society for Underwater Technology, 27(3):95–

107. http://dx.doi.org/10.3723/175605407783360044.

———. 2009. Parameters of extreme environment diving. In The future of diving: 

100 years of Haldane and beyond, ed. M. A. Lang and A. O. Brubakk, pp. 

153–159. Washington, D.C.: Smithsonian Institution Scholarly Press.

Lang, M. A., and S. Angelini. 2009. The future of dive computers. In The future of 

diving: 100 years of Haldane and beyond, ed. M. A. Lang and A. O. Brubakk, 

pp. 91–100. Washington, D.C.: Smithsonian Institution Scholarly Press. 

Lang, M. A., and A. O. Brubakk, eds. 2009. The future of diving: 100 years of Haldane and beyond. Washington, D.C.: Smithsonian Institution Scholarly Press.

Lang, M. A., and G. H. Egstrom, eds. 1990. Proceedings of the Biomechanics of 

Safe Ascents Workshop, Sept. 25–29, 1989, Woods Hole, Massachusetts. 

Costa Mesa, Calif.: American Academy of Underwater Sciences.

Lang, M. A., and R. W. Hamilton, eds. 1989. Proceedings of the Dive Computer 

Workshop, USC Catalina Marine Science Center. American Academy of 

Underwater Sciences and California Sea Grant College Program.

Lang, M. A., and C. E. Lehner, eds. 2000. Proceedings of the Reverse Dive Profiles 

Workshop, Oct. 29–30, 1999. Washington, D.C.: Smithsonian Institution.

Lang, M. A., and R. Robbins. 2009. Scientific diving under ice: A 40-year bipolar 

research tool. In Smithsonian at the poles: Contributions to International 

Polar Year science, ed. I. Krupnik, M. A. Lang, and S. E. Miller, pp. 241–252. 

Washington, D.C.: Smithsonian Institution Scholarly Press. http://dx.doi.org/

10.5479/si.097884601X.17.

Lang, M. A., and M. D. J. Sayer, eds. 2007. Proceedings of the International Polar 

Diving Workshop, Svalbard, March 15–21, 2007. Washington, D.C.: Smithsonian Institution.

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

Workshop, February 23–24, 2006. Washington, D.C.: Smithsonian Institution.

Lang, M. A., and J. R. Stewart, eds. 1992. Proceedings of the Polar Diving Workshop, Scripps Institution of Oceanography, May 20–21, 1991. Costa Mesa, 

Calif.: American Academy of Underwater Sciences.

Lang, M. A., and R. D. Vann, eds. 1992. Proceedings of the AAUS Repetitive Diving Workshop, March 18–19, 1991, Duke University Medical Center. Costa 

Mesa, Calif.: American Academy of Underwater Sciences.

Lanphier, E. H. 1965. Applications of decompression tables to repeated breathhold dives. In Physiology of breath-hold diving and the Ama of Japan, ed. 

H. Rahn and T. Yokoyama, pp. 227–236. National Research Council Publication 1341. Washington, D.C.: National Academy of Sciences.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, and S. D. Feldkamp. 1988. Continuous, 

deep diving in female northern elephant seals, Mirounga angustirostris. Canadian Journal of Zoology, 66:446–458. http://dx.doi.org/10.1139/z88-064

Lemaitre, F., A. Fahlman, B. Gardette, and K. Kohshi. 2009. Decompression sickness in breath-hold divers: A review. Journal of Sports Sciences, 27(14):1519–

1534. http://dx.doi.org/10.1080/02640410903121351.

Lenfant, C., G. L. Kooyman, R. Elsner, and C. M. Drabek. 1969. Respiratory function of blood of the Adélie penguin (Pygoscelis adeliae). American Journal of 

Physiology, 216:1598–1600.

Lindholm, P. 2009. The limits of breath-hold diving. In The future of diving: 100 

years of Haldane and beyond, ed. M. A. Lang and A. O. Brubakk, pp. 147–

152. Washington, D.C.: Smithsonian Institution Scholarly Press.

Loring, S. H., C. R. O’Donnell, J. P. Butler, P. Lindholm, F. Jacobson, and M. Ferrigno. 2007. Transpulmonary pressures and lung mechanics with glossopharyngeal insufflation and exsufflation beyond normal lung volumes in competitive breath-hold divers. Journal of Applied Physiology, 102(3):841–846. 

http://dx.doi.org/10.1152/japplphysiol.00749.2006.

Lutcavage, M. E., P. G. Bushnell, and D. R. Jones. 1990. Oxygen transport in the 

leatherback sea turtle Dermochelys coriacea. Physiological Zoology, 63: 

1012–1024.

———. 1992. Oxygen stores and aerobic metabolism in the leatherback sea turtle. 

Canadian Journal of Zoology, 70:348–351.

Magno, L., C. E. G. Lundgren, and M. Ferrigno. 1999. Neurological problems after 

breath-hold diving. Undersea and Hyperbaric Medicine, 26(Suppl.):28–29.

Manohar, M., T. E. Goetz, and A. S. Hassan. 2001. Effect of prior high-intensity 

exercise on exercise-induced arterial hypoxemia in thoroughbred horses. 

Journal of Applied Physiology, 90:2371–2377.

Mate, B. R., K. A. Rossbach, S. L. Nieukirk, R. S. Wells, A. B. Irvine, M. D. Scott, and 

A. J. Read. 1995. Satellite-monitored movements and dive behavior of a bottlenose dolphin (Tursiops truncatus) in Tampa Bay, Florida. Marine Mammal 

Science, 11:452–463. http://dx.doi.org/10.1111/j.1748-7692.1995.tb00669.x.

Meir, J. U., C. D. Champagne, D. P. Costa, C. L. Williams, and P. J. Ponganis. 2009. 

Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant 

seals. American Journal of Physiology - Regulatory, Integrative, and Comparative Physiology, 297:R927–R939. http://dx.doi.org/10.1152/ajpregu.00247

.2009.
number 39 • 3 7

Meir, J. U., and P. J. Ponganis. 2009. High-affinity hemoglobin and blood oxygen saturation in diving emperor penguins. Journal of Experimental Biology, 

212:3330–3338. http://dx.doi.org/10.1242/jeb.033761.

Meir, J. U., T. K. Stockard, C. L. Williams, K. V. Ponganis, and P. J. Ponganis. 2008. 

Heart rate regulation and extreme bradycardia in diving emperor penguins. 

Journal of Experimental Biology, 211:1169–1179. http://dx.doi.org/10.1242

/jeb.013235.

Millard, R. W., K. Johansen, and W. K. Milsom. 1973. Radiotelemetry of cardiovascular responses to exercise and diving in penguins. Journal of Comparative 

Biochemistry and Physiology – Part A: Molecular & Integrative Physiology,

46:227–240. http://dx.doi.org/10.1016/0300-9629(73)90414-3.

Milsom, W. K., K. Johansen, and R. W. Millard. 1973. Blood respiratory properties in some Antarctic birds. The Condor, 75:472–474. http://dx.doi.org/10

.2307/1366574.

Møllerløkken, A., V. J. Berge, A. Jorgensen, U. Wisløff, and A. O. Brubakk. 2006. 

Effect of a short-acting NO donor on bubble formation from a saturation 

dive in pigs. Journal of Applied Physiology, 101:1541–1545. http://dx.doi.org

/10.1152/japplphysiol.01191.2005.

Møllerløkken, A., and I. Eftedal. 2009. Individual risk of decompression sickness: 

Possible effects of genomic or epigenomic variation altering gene expression. 

In The future of diving: 100 years of Haldane and beyond, ed. M. A. Lang 

and A. O. Brubakk, pp. 71–76. Washington, D.C.: Smithsonian Institution 

Scholarly Press.

Moore, M. J., and G. A. Early. 2004. Cumulative sperm whale bone damage and the 

bends. Science, 306: 2215. http://dx.doi.org/10.1126/science.1105452.

Mueller, P. H. J. 2007. Cold stress and decompression sickness. In Proceedings of 

the International Polar Diving Workshop, Svalbard, March 15–21, 2007, ed. 

M. A. Lang and M. D. J. Sayer, pp. 63–72. Washington, D.C.: Smithsonian 

Institution. Pp. 63-72.

Noren, S. R., and T. M. Williams. 2000. Body size and skeletal muscle myoglobin 

of cetaceans: Adaptations for maximizing dive duration. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 126: 

181–191. http://dx.doi.org/10.1016/S1095-6433(00)00182-3.

Norris, K. S., and G. W. Harvey. 1972. A theory of the function of the spermaceti 

organ of the sperm whale (Physeter catodon L.). pp. 397-417. In Animal 

orientation and navigation, ed. S. F. Galler, K. Schmidt-Koenig, G. J. Jacobs, 

and R. E. Belleville, pp. 397–417. Washington, D.C.: National Aeronautics 

and Space Administration.

Nossum, V., S. Koteng, and A. O. Brubakk. 1999. Endothelial damage by bubbles in 

the pulmonary artery of the pig. Journal of Undersea and Hyperbaric Medicine, 26:1–8. 

Petschow, D., I. Wurdinger, R. Baumann, J. Duhm, G. Braunitzer, and C. Bauer. 

1977. Causes of high blood oxygen affinity of animals living at high altitude. 

Journal of Applied Physiology, 42:139–143.

Ponganis, P. J. 2011. Diving mammals. Comprehensive Physiology, 1:447–465.

Ponganis, P. J., M. L. Costello, L. N. Starke, O. Mathieu-Costello, and G. L. Kooyman. 1997. Structural and biochemical characteristics of locomotory muscles 

of emperor penguins, Aptenodytes forsteri. Respiration Physiology, 109:73–

80. http://dx.doi.org/10.1016/S0034-5687(97)84031-5.

Ponganis, P. J., G. L. Kooyman, and S. H. Ridgway. 2003. Comparative diving 

physiology. In Physiology and medicine of diving, ed. A. O. Brubakk and T. S. 

Neuman, pp. 211–226. Edinburgh: Saunders.

Ponganis, P. J., J. U. Meir, and C. L. Williams. 2010. Oxygen store depletion and the 

aerobic dive limit in emperor penguins. Aquatic Biology, 8:237–245. http://

dx.doi.org/10.3354/ab00216.

Ponganis, P. J., E. P. Ponganis, K. V. Ponganis, G. L. Kooyman, R. L. Gentry, and 

F. Trillmich. 1990. Swimming velocity in otariids. Canadian Journal of Zoology, 68:2105–2112. http://dx.doi.org/10.1139/z90-293.

Ponganis, P. J., T. K. Stockard, J. U. Meir, C. L. Williams, K. V. Ponganis, and 

R. Howard. 2009. O2

 store management in diving emperor penguins. Journal of Experimental Biology, 212:217–224. http://dx.doi.org/10.1242/jeb

.026096.

Ponganis, P. J., T. K. Stockard, J. U. Meir, C. L. Williams, K. V. Ponganis, R. P. van 

Dam, and R. Howard. 2007. Returning on empty: Extreme blood O2

 depletion underlies dive capacity of emperor penguins. Journal of Experimental 

Biology, 210:4279–4285. http://dx.doi.org/10.1242/jeb.011221.

Rahn, H. and T. Yokoyama, eds. 1965. Physiology of breath-hold diving and the 

Ama of Japan. National Research Council Publication 1341. Washington, 

D.C.: National Academy of Sciences.

Ridgway, S. H. 1986. Diving by cetaceans. In Diving in animals and man, ed. A. O. 

Brubakk, J. W. Kanwisher, and G. Sundnes, pp. 33–62. Trondheim: Royal 

Norwegian Society of Science and Letters.

Roca, J., M. C. Hogan, D. Story, D. E. Bebout, P. Haab, R. Gonzalez, O. Ueno, and 

P. D. Wagner. 1989. Evidence for tissue diffusion limitation of maximal oxygen uptake in normal humans. Journal of Applied Physiology, 67:291–299.

Ruterbusch, V. L., W. A. Gerth, and E. T. Long. 2004. Diver thermal status as a risk 

factor for decompression sickness (DCS). Undersea and Hyperbaric Medicine, 31(3):95.

———. 2005. Benefits of warm decompression can be realized with hot water suits. 

Undersea and Hyperbaric Medicine, 32(4):33.

Sato, K., Y. Watanuki, A. Takahashi, P. J. O. Miller, H. Tanaka, R. Kawabe, P. J. Ponganis, Y. Handrich, T. Akamatsu, Y. Watanabe, Y. Mitani, D. P. Costa, C.-A.

Bost, K. Aoki, M. Amano, P. Trathan, A. Shapiro, and Y. Naito. 2007. Stroke 

frequency, but not swimming speed, is related to body size in free-ranging seabirds, pinnipeds and cetaceans. Proceedings of the Royal Society, Biological 

Sciences Series B, 274:471–477. http://dx.doi.org/10.1098/rspb.2006.0005.

Sayer, M. D. J., M. A. Lang, and S. Mercer. 2007. The comparative incidence of decompression illness in Antarctic scientific divers. In Proceedings of the International Polar Diving Workshop, Svalbard, March 15–21, 2007, ed. M. A. Lang 

and M. D. J. Sayer, pp. 191–195. Washington D.C.: Smithsonian Institution.

Schipke, J. D., E. Gams, and O. Kallweit. 2006. Decompression sickness following 

breath-hold diving. Research in Sports Medicine, 14:163–178. http://dx.doi

.org/10.1080/15438620600854710.

Schmidt-Nielsen, K. 1983. Animal physiology: Adaptation and environment. London: Cambridge University Press.

Scholander, P. F. 1940. Experimental investigations on the respiratory function in 

diving mammals and birds. Hvalrådets skrifter, 22:1–131.

Scholander, P. F., L. Irving, and S. W. Grinnell. 1942. Aerobic and anaerobic changes 

in seal muscle during diving. Journal of Biological Chemistry, 142:431–440.

Simpson, J. G., W. G. Gilmartin, and S. H. Ridgway. 1970. Blood volume and other 

hematologic values in young elephant seals (Mirounga angustirostris). American Journal of Veterinary Research, 31:1449–1452.

Skrovan, R. C., T. M. Williams, P. S. Berry, P. W. Moore, and R. W. Davis. 1999. 

The diving physiology of bottlenose dolphins (Tursiops truncatus). II. Biomechanics and changes in buoyancy at depth. Journal of Experimental Biology, 202:2749–2761.

Southwood, A. L., R. D. Andrews, M. E. Lutcavage, F. V. Paladino, N. H. West, 

R. H. George, and D. R. Jones. 1999. Heart rates and diving behavior of 

leatherback sea turtles in the eastern Pacific Ocean. Journal of Experimental 

Biology, 202:1115–1125.

Spencer, M. P., and H. Okino. 1972. Venous gas emboli following repeated breathhold dives. Federation Proceedings, 31:355.

Stewart, B. S., and R. L. DeLong. 1995. Double migrations of the northern elephant 

seal, Mirounga angustirostris. Journal of Mammalogy, 76:196–205. http://dx

.doi.org/10.2307/1382328.

Stockard, T. K., J. Heil, J. U. Meir, K. Sato, K. V. Ponganis, and P. J. Ponganis. 

2005. Air sac PO2

 and oxygen depletion during dives of emperor penguins. 

Journal of Experimental Biology, 208:2973–2980. http://dx.doi.org/10.1242

/jeb.01687.

Streeter, T. L. 2006. Nitrogen narcosis during No-Limits freediving world record to 

160 m (525 ft). In Breath-hold diving, ed. P. Lindholm, N. W. Pollock, and 

C. E. G. Lundgren, pp. 17–25. Proceedings of the Undersea and Hyperbaric 

Medical Society/Divers Alert Network Workshop, June 20–21, 2006. Durham, N.C.: Divers Alert Network.

Taylor, C. R., R. H. Karas, E. R. Weibel, and H. Hoppeler. 1987. Adaptive variation in the mammalian respiratory system in relation to energetic demand. II. 

Reaching the limits to oxygen flow. Respiratory Physiology, 69:7–26. http://

dx.doi.org/10.1016/0034-5687(87)90098-3.

Thompson, D., and M. A. Fedak. 1993. Cardiac responses of grey seals during diving at sea. Journal of Experimental Biology, 174:139–164.

Thorson, P. H., and B. J. Le Boeuf. 1994. Developmental aspects of diving in northern elephant seal pups. In Elephant seals: Population ecology, behavior and 

physiology, ed. B. J. Le Boeuf and R. M. Laws, pp. 271–289. Berkeley: University of California Press.

Tyack, P. L., M. Johnson, N. A. Soto, A. Sturlese, and P. T. Madsen. 2006. Extreme 

diving of beaked whales. Journal of Experimental Biology, 209:4238–4253. 

http://dx.doi.org/10.1242/jeb.02505.

Vann, R. D., and M. A. Lang, eds. 2011. Proceedings of the DAN Diving Fatality 

Workshop. Durham, N.C.: Divers Alert Network.

Ward, C. A., D. McCullough, and W. D. Fraser. 1987. Relation between complement 

activation and susceptibility to decompression sickness. Journal of Applied 

Physiology, 62:1160–1166.

Watkins, W. A., K. E. Moore, and P. Tyack. 1985. Sperm whale acoustic behaviors 

in the southeast Caribbean. Cetology, 49:1–15.
3 8 • smithsonian contributions to the marine sciences

Williams, T. M., R. W. Davis, L. A. Fuiman, J. Francis, B. J. Le Boeuf, M. Horning, 

J. Calambokidis, and D. A. Croll. 2000. Sink or swim: Strategies for costefficient diving by marine mammals. Science, 288:133–136. http://dx.doi.org

/10.1126/science.288.5463.133.

Wisløff, U., and A. O. Brubakk. 2001. Aerobic endurance training reduces bubble 

formation and increases survival in rats exposed to hyperbaric pressure. 

Journal of Physiology, 537:607–611. http://dx.doi.org/10.1111/j.1469-7793

.2001.00607.x.

Wisløff, U., R. S. Richardson, and A. O. Brubakk. 2003. NOS inhibition increases 

bubble formation and reduces survival in sedentary but not exercised rats. 

Journal of Physiology, 546:577–582. http://dx.doi.org/10.1113/jphysiol.2002

.030338.

———. 2004. Exercise and nitric oxide prevent bubble formation: A novel approach to the prevention of decompression sickness? Journal of Physiology,

555:825–829. http://dx.doi.org/10.1113/jphysiol.2003.055467.
Saturation Diving and Underwater 

Laboratories: How Underwater 

Technology Has Aided Research 

on Coral Biology and Reef Ecology

Kenneth P. Sebens, Giacomo Bernardi, 

Mark R. Patterson, and Deron Burkepile

ABSTRACT. Despite more than a century of coral reef research, the basic biology of reef corals 

remained poorly understood until the advent of scuba diving and the associated underwater technology that followed. Basic information such as the nature of the coral–algal symbiosis, the importance 

of coral heterotrophy, specialized structures for space competition, the role of mutualistic crustacean 

symbionts, the behavior and dispersal ability of coral larvae, the nature of coral protection from 

ultraviolet radiation and heat stress, and the effects of ocean currents and internal waves on reefs all 

benefited from the ability of scientists to spend time under water observing, making measurements, 

and carrying out experiments. In addition to enhancing our understanding of corals themselves, the 

ability to spend time under water has also provided a huge amount of information about coral reef 

ecosystems and their component species. These benefits were further enhanced by new opportunities 

for saturation diving, and technology such as heated suits and underwater habitats or laboratories. 

One unique example of diving scientists working in concert with underwater technology is the 

Aquarius underwater laboratory (and its predecessors). This asset has allowed hundreds of researchers to spend weeks at a time investigating corals and coral reefs. The availability of underwater 

habitats/laboratories also fostered the development of other new technology for use on coral reefs 

and in other subtidal environments, and this technology is now providing the means to examine how 

changing ocean conditions are likely to impact corals and reefs. 

UNDERWATER RESEARCH ON CORAL REEFS 

AND SUBTIDAL HABITATS

In the early 1800s, naturalists investigating corals reefs had to rely on crude tools 

such as weighted collecting devices lowered from the decks of vessels to explore the reefs 

around coral islands. One example was a hollow, bell-shaped weight filled with wax,

which brought back impressions of the bottom, such as coral surface topographies, and 

even fragments of live coral and algae. Charles Darwin used such methods from the HMS 

Beagle, and his findings were sufficient to produce an elegant theory of reef growth and 

zonation (Darwin, 1842). These naturalists also had a chance to examine corals in the 

shallows and even at low tide when some reefs were exposed for hours. Commercial diving and submarines became available later in the nineteenth century, and had some utility 

Kenneth P. Sebens, Department of Biology 

and Friday Harbor Laboratories, University of 

Washington, Friday Harbor, Washington 98250, 

USA. Giacomo Bernardi, Department of Ecology and Evolutionary Biology, University of 

California at Santa Cruz, Santa Cruz, California 

95076, USA. Mark R. Patterson, formerly of 

Virginia Institute of Marine Science, College of 

William and Mary, Gloucester Point, Virginia; 

now at Marine Science Center, Northeastern University, 430 Nahant Road, Massachusetts 01908, 

USA. Deron Burkepile, Department of Biological Sciences, Florida International University, 

11200 S.W. 8th Street, Miami, Florida 33199, 

USA. Correspondence: K. Sebens, sebens@u

.washington.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
4 0 • smithsonian contributions to the marine sciences

for reef studies and specimen collecting, although there does not 

seem to have been a large number of studies using these methods. 

Despite more than a century of coral reef research using those 

techniques, the basic biology of reef corals remained a mystery 

until the advent of scuba diving and the associated underwater 

technology it made possible. Such fundamental information as 

the nature of the coral–algal symbiosis, the importance of coral 

heterotrophy, specialized structures for space competition, the 

role of mutualistic crustacean symbionts, the behavior and dispersal ability of coral and fish larvae, the nature of coral protection from ultraviolet radiation and heat stress, and the effects 

of ocean currents and internal waves on reefs have all benefited 

from the ability of scientists to spend time under water observing, collecting specimens, making measurements, and carrying 

out experiments. 

Scuba diving has some serious limitations as a research tool 

for diving scientists. At moderate depths, the amount of time one 

can spend on the bottom, or in the water column, is limited, 

from less than an hour to a few hours in a given day. Compare 

this to the situation for terrestrial ecologists, or even intertidal 

researchers who can often spend several hours on each low tide, 

sometimes twice a day, in the relative comfort of the aerial environment. Everything is more difficult under water and often takes 

more time than on land or in the intertidal zone, so anything 

that gives a researcher more time at depth is a huge benefit. One 

option that suffices for some researchers is to work very shallow and thus get more hours without a need for decompression, 

but that only works when their research subjects are available at 

those shallow depths. Another option is extended decompression 

diving, which is generally not supported by university research 

programs, but has been carried out in some cases by working 

with agencies that have this capability (Schmitt, 1987). The same 

is true for mixed-gas diving, which has also had limited availability until the advent of nitrox diving within the scientific (then 

sport) diving community in the 1980s. Use of nitrox can extend 

time working at depths significantly, especially in the range of 

20–40 m depth where bottom time (i.e., time available to work 

at depth) can double (Lang, 2001). However, researchers using 

nitrox are still likely to be limited to less than two hours per day 

of actual working time at such depths. 

Saturation diving offers the advantage of unlimited bottom 

time at saturation depths and greatly extended bottom time at 

depths much below the saturation depth. Time limits become 

more a matter of physical stamina of the divers and their support 

team, and logistical challenges of air delivery and other support. 

Saturation diving for days to weeks also requires the presence 

of an underwater structure, such as a habitat or laboratory, to 

provide comfortable living, sleeping, and eating areas, as well as 

places for research gear and computers. Once such a system is in 

place, divers are able to work for many hours each day, often in 

rotating teams such that even 24-hour studies can be carried out

over many days. Such continuous day and night research is very 

difficult to do from the surface, but becomes relatively routine 

and comfortable using an underwater laboratory. The ability to 

work around the clock has been important for studies of zooplankton behavior and distribution, coral physiology, fish behavior, and many others. The purpose of this paper is to review the 

science that has become possible primarily because of the new 

capabilities offered by saturation diving, underwater laboratories, 

and the associated new technologies that have been developed 

and incorporated by the research teams that have used them. 

UNDERWATER HABITATS 

AND LABORATORIES

The history of saturation diving and underwater habitats 

has been covered elsewhere and will not be part of this review. 

However, a bit of this history is necessary to set the stage. There 

have been a good number and variety of underwater habitats 

designed and put into regular operation for commercial purposes 

such as oil exploration, but relatively few that have been constructed and used primarily as scientific research facilities. Saturation diving is being used at great depths in industry (to over 

500 m), but has been limited to very shallow depths for research 

(under 30 m), mostly to increase safety, but also for ease of operation and supply. 

An early effort was the Conshelf I (Mediterranean) and 

Conshelf II (Red Sea) habitats built for Jacques Cousteau’s explorations and filming during 1962–1965 (Cousteau, 1965). 

These habitats, while shallow (10 m), allowed first two and later 

six aquanauts to stay underwater for seven and thirty days, respectively. In 1965, Conshelf III took six Aquanauts to 100 m for 

three weeks. The path to successful saturation diving was paved. 

During 1965–1969, the U.S. Navy used the Sealab I–III habitats 

for research on diving physiology.

While more than twenty underwater habitats have been 

constructed and used for science, four facilities have had the 

largest scientific research and publication impact: the Tektite I 

and Tektite II habitats in the United States Virgin Islands (USVI; 

1969–1970; Clifton et al., 1970); the Helgoland habitat in the 

cold Baltic Sea (1969–1979); the Hydrolab habitat in the Bahamas (1970–1976) and St. Croix, USVI (1977–1985; Nyden, 

1985; Williams, 1985); and the Aquarius underwater laboratory, 

first in St. Croix, USVI (1987–1989), then on Conch Reef, off 

Key Largo, Florida (1992–present; Shepard et al., 1996). Aquarius has had the longest tenure of these facilities and is still in 

active use at the Florida site as of 2011. Much of the research 

covered in this review was accomplished using the Hydrolab and 

Aquarius laboratories (Figures 1–3).

RESEARCH AREAS

The ability to spend time under water has facilitated a substantial body of work on coral reefs and other subtidal ecosystems and their component species. The Hydrolab and Aquarius 

underwater laboratories have allowed hundreds of researchers 
number 39 • 4 1

FIGURE 1. Hydrolab (left) and Aquarius (right) underwater laboratories (habitats) in Salt River Canyon, St. Croix, USVI (1980s), and at Conch Reef, Key 

Largo, Florida (1990s). Photos by Kenneth Sebens.

FIGURE 2. The Aquarius underwater laboratory (right) at Conch Reef, Florida, and the communications and data center inside the habitat 

during the Jason Project (1996, with A. Grottoli). Photos by Kenneth Sebens.
4 2 • smithsonian contributions to the marine sciences

to spend weeks at a time gathering information on corals and 

coral reef ecosystems. Typically, a research mission in Aquarius

lasts seven to ten days, thus providing longer single observation times (each dive lasts several hours), with a total dive time 

for a mission corresponding, approximately, to six months of 

intensive “classical” diving field work. The availability of these 

laboratories also stimulated the development and adaptation of 

many technologies for use on coral reefs and in other subtidal 

environments. These technologies are now providing the means 

to examine how changing ocean conditions are likely to impact 

corals and reef ecosystems. 

We concentrate on a few research areas that have benefitted 

greatly from the availability of underwater laboratories: coral biology and physiology, coral reef hydrodynamics and flow effects 

on benthos, zooplankton ecology and behavior, fish behavior and 

ecology, and coral reef community and ecosystem ecology. There 

are many other areas of research that have also benefited, including everything from human behavior (as a space station analog) 

and physiology to instrument development and testing (engineering), that will not be covered in this review.

Coral Reef Hydrodynamics and the Effects of Water

Flow on Corals and Other Reef Benthos

Coral reef communities experience a broad range of flow 

conditions, from crashing waves in the surf zone to strong unidirectional currents along deep reef walls and almost-still water in 

some lagoonal and backreef habitats (Sebens and Johnson, 1991; 

Sebens and Done, 1994; Monismith, 2007). Corals and other 

reef organisms must thus deal with limitations imposed on their 

physiology and structure by these flow conditions, as well as by 

the extreme conditions that occur during storm events. Water 

FIGURE 3. Full face mask (K. Sebens, 1999) and helmet (G. Wellington, Jason Project, 1996) systems supplied air from 

Aquarius (left) and from the surface barge above Aquarius (right). Photos by Kenneth Sebens (left) and Karla Heidelberg (with 

permission, right).
number 39 • 4 3

flow also is important for delivery of nutrients and plankton to 

reefs (Leichter et al., 1998, 2003, 2007), and for transport of 

larvae from one reef to another. Current meters can be deployed 

from surface vessels or by divers on no-decompression dives, but 

such meters generally give only mid-depth flows. More recently 

though, acoustic doppler current profilers (ADCPs) have been 

mounted on the bottom to provide comprehensive data on flow 

at all depths above the bottom, but not within centimeters of 

substratum.

More difficult is the characterization of water flow at the 

microscale, from just above the bottom down into the interstices 

of reefs and among tentacles of corals (Reidenbach et al., 2006a, 

2006b, 2007). Getting this type of data involves delicate positioning of instruments and use of video and other technologies 

by divers who reposition their instruments (thermistors, ADVs, 

and electromagnetic flow meters) continuously and move them 

to various habitats and depths (Figure 4). Such studies are often 

paired with physical, biological, and/or chemical sampling over 

the same time period, including temperature, zooplankton, nutrients, coral physiology, and other chemical parameters of the 

water column (Patterson et al., 1991; Sebens and Done, 1994; 

Leichter et al., 1996, 2005).

Flow on reefs originates from a number of sources including 

waves, currents, and internal waves (Monismith, 2007). On reefs 

with strong longshore currents, the biotic communities can experience strong flow at any depth (Sebens and Done, 1994), but 

reefs without such currents often experience the highest flows in 

wave-dominated forereef environments and have a sharp drop in 

flow with depth (Sebens and Johnson, 1991; Sebens, 1997; Sebens et al., 2003). Deep reef and shallow lagoonal habitats with 

very low mean flow conditions are likely to experience reduced 

delivery of particles for suspension feeders (Sebens, 1997) and 

reduced uptake of nutrients by corals and algae (Hearn et al., 

2001). Low flows also affect biological processes such as bleaching, recovery from bleaching, and development of heat shock or 

stress responses (Carpenter and Patterson, 2007; Carpenter et 

al., 2010). As a rough approximation, reef habitats with flow 

speeds normally under 5 cm s-1

 present physiological and nutritional challenges for corals, affecting their photosynthesis, respiration, tissue growth, and calcification (Sebens, 1997). Flows 

in the range of 10–30 cm s-1 may be in the optimal range for 

particle capture and lack of diffusional limitation, whereas flows 

well above that range present challenges for corals in retaining 

particles, keeping tentacles extended, and avoiding mechanical 

damage and dislodgment. 

Moderate to deep reefs can experience variable flow regimes 

when internal waves shoal at those depths, as happens in Florida 

(Leichter et al., 1996, 1998, 2003, 2005, 2007). Benthic suspension feeders experience pulsed periods of high flow, as well as 

pulsed delivery of zooplankton and nutrients, during the wave 

events. This important source of nutrients and particulate material for reefs was first recognized and documented by researchers 

FIGURE 4. An InterOcean S4 electromagnetic current meter in place on a shallow reef, and a Sontek ADV flow meter on a stand that allows 

vertical profiling from just above coral tentacles to 2 m above the bottom. These and several other recently developed instruments have been 

used to characterize flow on coral reefs. Photos by Kenneth Sebens.
4 4 • smithsonian contributions to the marine sciences

using the Aquarius laboratory. In addition to flow magnitude, 

turbulence also affects delivery of dissolved and suspended materials (Monismith, 2007). Davis and Monismith (2011) found 

that turbulence in the reef boundary layer was highly variable 

in time and was modified by near-bed flow and shear, as well as 

stratification concurrent with shoaling internal waves (Davis and 

Monismith, 2011) at Conch Reef.

Coral Physiology and Nutrition

Ideally, researchers would like to understand the physiology 

and nutrition of reef corals under natural reef conditions. Recirculating respirometry chambers deployed on the seafloor next 

to underwater habitats (e.g., Hydrolab, Aquarius) have allowed 

interesting insights into coral ecophysiology that would have not 

been obtained any other way (Patterson et al., 1991). Because 

the chambers are exposed to the same ambient conditions of irradiance, temperature, and water chemistry as nearby corals, the 

perturbation to the test subjects is minimal, a significant advantage when conducting experiments with needed ecological relevance. Chambers developed by Mark Patterson and colleagues 

were used to manipulate flow over coral colonies in a controlled 

fashion. The chambers were the first to be completely computer 

controlled from inside the habitat (Hydrolab), and to our knowledge this was the first use of a desktop computer (Apple IIe) in a 

pressurized underwater environment (Figure 5). A regular CRT 

screen could not be used under pressure, so Patterson acquired 

one of the first flat-screens on loan from the manufacturer, before they were available on laptops. Subsequent experiments in 

Aquarius used an early Apple Macintosh Plus to control experiments, including monitoring the data, performing QA/QC, and 

performing self-diagnostics on the progress of the experiment.

These and later experiments from Aquarius (Figure 6) resulted in data on a diversity of coral species and provided strong 

evidence that flow modulates both respiration and photosynthesis in scleractinians (Patterson et al., 1991; Finelli et al., 2005; 

Carpenter and Patterson, 2007; Carpenter et al., 2010). Aquarius was also used to test gas microelectrodes moved by a micromanipulator under control of a scuba diver to measure diffusive 

boundary layers over individual coral polyps (Patterson, 1992a). 

These data were valuable in constructing a theory of metabolic 

scaling in lower invertebrates and algae that demonstrated the 

effect of shape and flow on the allometric exponent (Patterson, 

1992b) that relates metabolic rate to organism size.

As concern grew about the impact of global warming on 

reefs, experiments were devised to expose corals to elevated water 

temperature in situ using modifications of the prior technology (Figure 7). Thermofoil avionics heaters were applied inside 

the metabolism chambers and precise temperature control was 

achieved from sophisticated industrial controllers inside Aquarius. These experiments would not have been possible without the 

ample power from Aquarius available to run the associated heaters and pumps. More recent work has demonstrated that withincolony variation in photosynthetic performance (Carpenter and 

Patterson, 2007) and heat shock protein expression (Carpenter 

et al., 2010) is modulated by flow in a non-linear, unimodal fashion. The heated chambers also made possible development of a 

new minimally invasive method for measuring the production of 

heat shock proteins in single polyps by carefully excising small 

bits of tissue in situ using a special tool (Bromage et al., 2009). 

Another instrument developed for test and evaluation by 

saturation diving was a handheld profiler for temperature, dissolved oxygen, and pH (Figure 7). This instrument could be precisely emplaced for quick profiling over the bottom 3 m of the 

FIGURE 5. The first computer (Apple II) used in Hydrolab (by M. Patterson and colleagues), including a prototype flat-screen monitor on loan 

from the manufacturer (1984) (left). Chambers used for respirometry and flow studies, deployed adjacent to the reef at Hydrolab (1984) (right). 

Photos by Kenneth Sebens.
number 39 • 4 5

reef, or left in place for 24 hours at a single location. This device 

has gathered valuable data on how a progression toward reef 

heterotrophy in the Florida Keys has impacted the geophysical 

boundary layer dynamics for dissolved oxygen, and how ocean 

acidification affects diurnal variation in pH. Both parameters 

have shown unexpected marked variation over short spatial distances (1 m). 

Coral nutrition is another area of research that has benefited 

greatly from the extended time available to researchers using 

Aquarius, especially for field work at night when most corals are 

feeding on zooplankton. Sebens and Johnson (Johnson and Sebens, 1993; Sebens and Johnson, 1991) used Aquarius to study 

zooplankton availability using a new in situ pump developed for 

this work (Sebens and Maney, 1992; Graham and Sebens, 1996) to 

FIGURE 7. Mark Patterson investigates flow and temperature effects on reef benthos using the Aquarius underwater laboratory in 2002–2003. 

Heated metabolism chambers (left) and dissolved oxygen, pH, and temperature profiling apparatus (right). Photos by Janet Nestlerode.

FIGURE 6. Respirometry chambers used for coral production and respiration measurements at a range of flow speeds being prepared for use in 

Hydrolab by M. Patterson and colleagues (left) (Patterson et al., 1991; photo by Kenneth Sebens), and similar chambers being used for nutrient 

uptake studies (right) (Leichter et al., 2003; photo by James Leichter).
4 6 • smithsonian contributions to the marine sciences

monitor particle capture by several coral species, and to measure 

water flow at the height of corals on the reef over a broad depth 

range. Sebens and colleagues carried out similar studies of zooplankton feeding on a Jamaican reef using the methods developed 

in Aquarius (Sebens et al., 1996a, 1996b, 1997; Sebens, 1997), and 

Mills and Sebens quantified sediment ingestion (Mills and Sebens, 

1997, 2005; Mills et al., 2004). Apparatus developed for these 

studies of coral feeding and growth is illustrated in Figures 8–10.

Heidelberg and colleagues used Aquarius to examine behavior of zooplankton as they approach coral tentacles (Heidelberg 

FIGURE 8. Experimental chambers used for coral feeding studies on top of Aquarius, and on Conch Reef near the underwater laboratory by 

J. Witting, K. Sebens, and colleagues (Witting, 1999; photos by Kenneth Sebens).

FIGURE 9. A large recirculating flume (left) on Conch Reef allowed flow studies of particle and zooplankton capture, and provided both unidirectional and bidirectional flow generated by two electric trolling motors inside the PVC sections. Zooplankton were attracted into the chambers 

using dive lights, then chambers were sealed. Screens prevented plankton from contacting propellors during bidirectional flow runs with live 

zooplankton (K. Sebens, unpublished). Detailed view of working area (right). Photos by Kenneth Sebens.
number 39 • 4 7

et al., 1997), and later to quantify the zooplankton resource 

available to corals (Heidelberg et al., 2010). In a related set of 

experiments, Witting (1999) demonstrated experimentally (Figure 10) that coral growth can be enhanced by added capture of 

zooplankton (attracted by lights directed away from coral transplants), a finding that was later supported by laboratory research 

by Witting and colleagues (Ferrier-Pagès et al., 2003; Houlbrèque 

and Ferrier-Pagès, 2008). The importance of inorganic nutrients 

to reefs and reef corals has also been a focus of research using 

Aquarius (Szmant-Froelich, 1983; Leichter et al., 2003).

Zooplankton on Reefs

Zooplankton are important prey for coral reef fish, corals, 

and other zooplanktivores living on or near reefs. The composition and dynamics of the reef plankton community are interesting in their own right, and zooplankton provide a link between 

primary production in the water column and the reef community. Observation of plankton swarms near reefs and some in situ 

sampling suggested that zooplankton are not homogeneously 

distributed over reefs and do not all originate from offshore 

water flowing over reefs (i.e., some are reef residents). When researchers needed to quantify the plankton resource available to 

near-reef fish, for example, they used divers to swim plankton 

nets along the reef as close as they could maneuver near the reef 

surface (Hobson and Chess, 1976) because they were aware that 

zooplankton assemblages differed nearer to and farther from the 

substratum. 

Observations of crustaceans swimming upward from reef 

surfaces led to the design of emergence traps to quantify those 

demersal plankton that migrate off the reef at dusk (Hobson and 

Chess, 1979; Ohlhorst and Liddell, 1984; Ohlhorst et al., 1985 

[using Hydrolab]; Alldredge and King, 1985) and may return to 

the reef at some later time. These zooplankton provide a link 

between benthic productivity, by reef microalgae for example, 

and both reef fish and sessile invertebrate predators. They are, 

however, a very small fraction of the reef plankton in most places 

(Heidelberg et al., 2003, 2010). The majority of the zooplankton 

over reefs are either open-water plankton advected onto the reef 

or reef-resident plankton that do not live on the reef surfaces but 

maintain themselves near the reef and migrate vertically (Heidelberg et al., 2003, 2010). 

Living on the reef for many days and nights by scientist 

aquanauts using underwater laboratories has allowed the extensive observation necessary to adequately ascertain zooplankton 

behavior, and the interaction of predators with the plankton resource. One recent investigation to quantify zooplankton above 

a coral reef was conducted using Aquarius (Heidelberg et al., 

2010). This team designed a four-inlet plankton sampler made of 

PVC pipe and powered by a large bilge pump (Figure 11). The 

pumps are also inexpensive enough to replace quickly when they 

fail. Each intake pipe, located at 2 m, 1 m, 50 cm, and 5 cm off 

the reef surface, respectively, had a conical plankton net inside 

the PVC pipe end that could be changed easily by divers. There 

was also a separate pump sampler taking zooplankton from 1 m 

below the water surface. Divers were thus able to take samples 

every three hours for 24 hours per day for seven days in a row, 

illustrating how zooplankton assemblages are structured above 

the reef, and thus what type and amount of plankton are available to zooplanktivores on the reef or in the water column near 

the reef. While theoretically possible, this task would have been 

much more difficult, and less safe, working from surface vessels. 

FIGURE 10. Transplant racks for coral growth studies at the Aquarius laboratory (left; Witting, 1999; photo by Kenneth Sebens) and in the 

Mediterranean (right; Cebrian et al., 2012; photo by Joaquim Garrabou). In the assembly at left, a cabled light was added to the center of half 

of the treatments to attract zooplankton at night and thus enhance capture rates by the corals on those racks.
4 8 • smithsonian contributions to the marine sciences

Another excellent example comes from the work of Leichter 

and colleagues, whose observations and measurements using 

Aquarius led to the discovery that internal waves deliver zooplankton (as well as nutrients) from deeper water masses up to 

depths where reef organisms can make use of them (Leichter et 

al., 1998, 2003, 2005, 2007). 

Reef Fish Behavior and Ecology

In the 1980s, the National Oceanic and Atmospheric Administration’s (NOAA) National Undersea Research Program 

had a surface-supplied, hot-water-suit research platform at the 

University of Southern California’s Catalina Marine Science 

Center on Santa Catalina Island. Schmitt used this facility extensively for a shallow subtidal project on fish and other predators 

that could not have been done in any practical way using regular 

scuba.  The experiment tested for predator-mediated, apparent 

competition between two prey types (snail and bivalve) and involved daily censuses of large subtidal areas for the two prey 

types that had been eaten in the previous 24 hours; dead prey 

were removed and replaced daily. The results were the first experimental test of apparent competition (Schmitt, 1987), a process wherein two species affect each other negatively because of 

higher trophic-level influences (i.e., predator effects). It is also the 

project for which Schmitt was awarded the 1989 George Mercer 

Award for Distinguished Research by the Ecological Society of 

America. 

The Schmitt project was important as well in highlighting 

the power (albeit with challenges) of achieving long observation 

times through saturation diving (Schmitt, 1987). Schmitt’s project required six-hour or longer dives to 10 m (33 ft) every day for 

about six weeks; divers used U.S. Navy extreme exposure decompression tables, and each six-hour dive included a decompression 

stop of at least one hour. When a diver reached the limit of multiple days of extreme exposures (i.e., after six consecutive dive 

days), the diver had to stay out of the water for a full day. Obviously this study needed the hot-water suits (with water pumped 

through suits from the surface) to do six-hour dives daily in the 

(cold) summer water temperatures of Catalina Island.

Underwater saturation facilities have greatly facilitated further research on fish ecology and behavior. For example, Levitan 

and Petersen (1995) used a saturation mission in Aquarius to 

investigate fish spawning and fertilization rates under natural 

conditions. Over many years, these researchers collected data 

from 3–12 m using NOAA’s day-boat operation, but the use of 

extended saturation diving allowed them to examine species that 

spawn at greater depths (20–30 m). These were long dives during 

which they examined spawning behavior and then sampled eggs 

after release to obtain an estimate of female fertilization success. 

This team also used Aquarius itself as their working laboratory 

so that they could use a microscope to rapidly score eggs for 

fertilization without the necessity of bringing them to the surface 

and transporting them to shore. 

During 2003–2005, Hay and Burkpile used Aquarius to establish 32 in situ mesocosms (4 m2

 each) where they manipulated 

herbivorous fish species richness to establish the links between 

herbivore identity and richness and benthic community structure on this coral reef. The saturation capabilities of Aquarius

allowed them to perform a labor-intensive study that would have 

taken weeks to accomplish via other means in nine days. The 

amount of time needed at 16–18 m would not have been logistically or financially possible without the capabilities of saturation diving. Consequently, they were able to do some of the first 

direct, long-term assessments of the role of herbivore richness 

on the health of coral reef communities (Burkepile and Hay, 

2007, 2008, 2009, 2010, 2011). For example, Burkepile and Hay 

(2008, 2010) showed that herbivore species richness and identity 

are both important for facilitating the removal of seaweeds and 

the growth of corals. When compared with single-species treatments, mixed-species treatments lowered macroalgal abundance 

by 54%–76%, enhanced cover of crustose coralline algae (preferred recruitment sites for corals) by 52%–64%, increased coral 

cover by 22%, and prevented coral mortality. Complementary 

feeding by different herbivorous fish species drove the herbivore 

FIGURE 11. A plankton sampling array in place near the Aquarius

laboratory on Conch Reef, Florida, used to examine zooplankton 

distribution above the bottom. The center section is 2 m tall and all 

four inlets, at four different heights, are powered by a single large 

submersible pump at bottom left (Heidelberg et al., 2010). Photo by 

Kenneth Sebens.
number 39 • 4 9

richness effects because macroalgae were unable to effectively 

deter fishes with disparate feeding strategies. Ultimately, their 

work suggests that maintaining herbivore species richness appears critical for preserving coral reefs, because complementary 

feeding by diverse herbivores produces positive, but indirect, effects on corals, the foundation species for the ecosystem.

In general, studying fish behavior requires very long observation times. This is why most studies are done in aquaria. 

Research has demonstrated that saturation diving allows for observation times long enough to make more complete and ecologically meaningful observations. Dunlap and Pawlik (1996), for 

example, using the Aquarius habitat as their base, were able to 

observe and video fish feeding on several species of reef sponges 

for several consecutive hours. These observations allowed inference of predatory mechanisms structuring the reef by spongivorous fishes such as trunkfishes and angelfishes. There are many 

other examples where the extended dive times and depths afforded by saturation diving have led to major findings in fish 

ecology and behavior, many more than can be cited here. 

Other Biological and Ecological Insights

about Reefs and Their Inhabitants

Underwater habitats and saturation diving have made it 

possible to follow the behavior of marine animals that must be 

studied in situ. An early example comes from the work of William Herrnkind (1974). Around 1970, it was thought that spiny 

lobsters were randomly nomadic scavengers with a limited social 

repertoire. Based on his observation of mass migration by queuing 

and reports from initial telemetry studies by others, he suspected 

far more complex behavior and sophisticated social and navigational abilities. However, these animals are largely nocturnal and 

adults often occur at depths of ~20 m, at considerable distances 

from shore. In addition, they walk at near-swimming pace and 

roam widely, making it a challenge to observe them by standard 

scuba; their large size and spatial range made it unreasonable to 

infer natural behavior from even large aquaria. Tektite, in particular, and Hydrolab manned undersea habitats provided means 

to substantially overcome these logistical hurdles.

At Tektite I and Tektite II, with successive, lengthy missions 

(three 3-week missions in Tektite II), Herrnkind and colleagues 

were able to daily and repeatedly access the numerous resident 

lobsters within a kilometer of the facility to tag them and identify their den sites (Herrnkind, 1974). Ultrasonic telemetry, then 

in its infancy, allowed them to locate individuals during nocturnal foraging and document movement from dens to feeding 

areas throughout the night. The initial data suggested homing 

to particular favored dens, necessitating accurate orientation 

by non-visual cues. Displacement experiments, sometimes with 

night-long tracking by aquanauts, on telemetered and simple 

color-coded, tagged individuals established that spiny lobsters do 

indeed exhibit accurate non-visual homing from distances of at 

least one kilometer. Further research demonstrated remarkable 

orientation by hydrodynamic, chemical, and geomagnetic senses. 

The previous, inaccurate conceptual premise of lobster natural 

history was replaced as an outcome of that underwater-habitatfacilitated work. The manned habitats enormously facilitated 

access and logistics over standard scuba for this work on the 

typical lifestyle of spiny lobster. In addition, the researchers were 

able to witness behaviors unlikely to occur in captivity, from 

which they developed new hypotheses.

Sessile reef fauna other than corals have also been the target 

of extended saturation diving research. One example is from the 

work of Pawlik (1997, 2011), who used the Aquarius habitat 

to study the demographics of giant barrel sponges, their growth 

rates, re-attachment of sponges after disturbance, and species 

preferences of spongivorous fishes using underwater videography. Sponges as competitors for space on reefs were described 

by Suchanek et al. (1983) for the St. Croix sites. Sponge feeding biology and physiology was also examined by Patterson and 

colleagues using chambers designed specifically for this purpose 

(Trussell et al., 2006). Gorgonian corals have been studied in 

terms of their reproductive biology (West et al., 1993), effects of 

predators (Harvell and Suchanek, 1987; Ruesink and Harvell, 

1990), chemical defenses against predators (Harvell et al., 1993), 

primary production (Miles and Harvell, 1990), and nutrition 

(Lasker et al., 1983). 

Algal biology has also been an important focus of research 

using underwater habitats and laboratories. Using Aquarius, 

James Coyer and colleagues studied the mode of propagation of 

the alga Halimeda, a major carbonate producer in reef system. 

This work was important in understanding the overall dynamics 

of the algal population on the entire reef (Vroom et al., 2003). 

This research required long observation times both for the team 

that studied the algae and for the team that studied the impact 

of fish on the algae. With long observation times, the algae team 

was able to observe Halimeda “spawning,” an event that was 

later described very precisely in Halimeda and other green algae 

by Clifton (1997). 

Earlier work by Hay et al. (1988) using Hydrolab showed 

how diel patterns of growth in Halimeda was an effective strategy to minimize losses to herbivores. They performed essentially 

round-the-clock dives over the course of their saturation mission 

to show that Halimeda produces new, uncalcified tissues that 

are susceptible to herbivores only at night when herbivore activity is low, rather than during the day when herbivory is intense. 

These new, nutrient-rich tissues are flushed with photosynthetic 

pigments only just before sunrise, but they are also increasingly 

resistant to herbivores as the tissues age and become calcified. 

These diel patterns in growth and deployment of energy to constituents of the algal thallus (pigments, carbonate) are cued primarily by the timing of light and dark cycles rather than diel 

changes in seawater chemistry.

Halimeda produces a toxin that mildly affects fishes. Hay 

et al. (1988) observed a number of fishes feeding on Halimeda, 

but invariably they would take just a few bites until finding it 

distasteful. On several occasions, they saw fishes, particularly 

porkfish, Anisostremus virginicus, grab bites of Halimeda, then 
5 0 • smithsonian contributions to the marine sciences

swim off and spit out a few morsels. These morsels were then 

recovered and analyzed to determine if they could reattach and 

regrow, which they did. Thus long observation times afforded by 

saturation diving allowed them to discover sexual and asexual 

propagation of Halimeda at Conch Reef (Walters et al., 2002; 

Herren et al., 2006), and to document variability in ecophysiology of these algae (Beach et al., 2003). Disturbance effects on 

Caulerpa spp. were also examined earlier in deep reef sites at 

St. Croix (Williams et al., 1985), as were disturbances in deep 

seagrass beds (Williams, 1988) and seagrass detritus as a source 

of nutrition in deep habitats (Suchanek et al., 1985).

CONCLUSION

Underwater laboratories and saturation diving techniques 

have also been instrumental, if not transformative, in defining 

the ecosystem parameters of reefs, including their physical oceanography (Shepard and Dill, 1977; Sebens and Johnson, 1991; 

Leichter et al., 1998), effects of extreme storms (Hubbard, 1992; 

Aronson et al., 1994), and geology (Adey and Steneck, 1985; 

Hubbard et al., 1985; Hubbard and Scaturo, 1985). In addition, 

via the longevity of deployment and support, Aquarius and its 

base station on Key Largo have afforded an opportunity for longterm research in the Florida Keys that would otherwise have been

unlikely (Aronson and Swanson, 1997; Miller et al., 2000). The 

overall effect of the various underwater habitat programs (along 

with associated technology they have driven) on our understanding of coral reefs and other subtidal habitats has been enormous. 

With the rapidity of changes in oceans, particularly in shallow 

coastal systems, these technological assets and their development 

will continue to be needed for deriving a greater understanding of 

how best to manage these valuable ecological assets.

ACKNOWLEDGMENTS

We thank Michael Lang, Phil Taylor, Roberta Marinelli, and 

Susan Roberts for organizing the symposium and Michael for 

helping this volume come to be. We also thank several people 

who contributed information for this paper, including Joseph 

Pawlik, William Herrnkind, Russell Schmitt, Howard Lasker, 

Don Levitan, David Eggleston, Steven Miller, Hannah Stewart, 

Joaquim Garrabou, and Karla Heidelberg. Research support 

for many of the projects discussed herein was provided by the 

National Oceanic and Atmospheric Administration’s National 

Undersea Research Program, NURC UNCW, and Aquarius Reef 

Base. Photo credits are provided in the figure captions.

REFERENCES

Adey, W. H., and R. S. Steneck. 1985. Highly productive eastern Caribbean reefs: 

Synergistic effects of biological, chemical, physical, and geological factors. In 

The Ecology of Coral Reefs, ed. M. L. Reaka, pp. 169–187. Symposia Series 

for Undersea Research, Vol. 3, No. 1. Rockville, Md.: NOAA, National Undersea Research Program. 

Alldredge, A. L., and J. M. King. 1985. The distance demersal zooplankton migrate 

above the benthos: Implications for predation. Marine Biology, 84:253–260. 

http://dx.doi.org/10.1007/BF00392494.

Aronson, R. B., J. P. Ebersole, and K. P. Sebens. 1994. Hurricane Hugo’s impact on 

Salt River submarine canyon, St. Croix, U.S. Virgin Islands. In Proceedings of 

the Colloquium on Global Aspects of Coral Reefs: Health, hazards, and history, 1993, ed. W. Ginsburg, pp. 189–195. Miami, Fla.: University of Miami.

Aronson, R. B., and D. W. Swanson. 1997. Video surveys of coral reefs: Uni- and 

multivariate applications. Proceedings of the eighth International Coral Reef 

Symposium, 2:1441–1446. 

Beach, K., L. Walters, P. Vroom, C. Smith, J. Coyer, and C. Hunter. 2003. Variability in the ecophysiology of Halimeda spp. (Chlorophyta, Bryopsidales) on 

Conch Reef, Florida Keys. Journal of Phycology, 39:633–643. http://dx.doi

.org/10.1046/j.1529-8817.2003.02147.x.

Bromage, E., L. Carpenter, S. Kaattari, and M. Patterson. 2009. Quantification of 

coral heat shock proteins from individual coral polyps. Marine Ecology Progress Series, 376:123–132. http://dx.doi.org/10.3354/meps07812.

Burkepile, D. E., and M. E. Hay. 2007. Predator release of the gastropod Cyphoma 

gibbosum increases predation on gorgonian corals. Oecologia, 154:167–173. 

http://dx.doi.org/10.1007/s00442-007-0801-4.

———. 2008. Herbivore species richness and feeding complementarity affect 

community structure and function on a coral reef. Proceedings of the National Academy of Sciences, 105:16201–16206. http://dx.doi.org/10.1073

/pna.0801946105.

———. 2009. Nutrient versus herbivore control of macroalgal community development and coral growth on a Caribbean reef. Marine Ecology Progress Series,

389:71–84. http://dx.doi.org/10.3354/meps08142.

———. 2010. Impact of herbivore identity on algal succession and coral growth 

on a Caribbean reef. PLoS ONE, 5:e8963. http://dx.doi.org/10.1371/journal

.pone.0008963.

———. 2011. Feeding complementarity versus redundancy among herbivorous 

fishes on a Caribbean reef. Coral Reefs, 30:351–362. http://dx.doi.org/10

.1007/s00338-011-0726-6.

Carpenter, L. W., and M. R. Patterson. 2007. Water flow influences the distribution 

of photosynthetic efficiency within colonies of the scleractinian Montastrea 

annularis (Ellis and Solander, 1786): Implications for coral bleaching. Journal of Experimental Marine Biology and Ecology, 351:10–26. http://dx.doi

.org/10.1016/j.jembe.2007.05.022.

 Carpenter, L. W., M. R. Patterson, and E. S. Bromage. 2010. Water flow influences 

the spatiotemporal distribution of heat shock protein 70 within colonies of 

the scleractinian coral Montastrea annularis (Ellis and Solander, 1786) following heat stress: Implications for coral bleaching. Journal of Experimental 

Marine Biology and Ecology, 387:52–59. http://dx.doi.org/10.1016/j.jembe

.2010.02.019.

Cebrian, E., C. Linares, C. Marschal, and J. Garrabou. 2012. Exploring the effects 

of invasive algae on the persistence of gorgonian populations. Biological Invasions, 14:2647–2656. http://dx.doi.org/10.1007/s10530-012-0261-66.

Clifton, E. H., C. V. W. Mahnken, J. C. Van Derwalker, and R. A. Waller. 1970. 

Tektite I, Man-in-the-Sea project: Marine science program. Science, 168:659–

663. http://dx.doi.org/10.1126/science.168.3932.659.

Clifton, K. E. 1997. Mass spawning by green algae on coral reefs. Science, 275: 

1116–1118. http://dx.doi.org/10.1126/science.275.5303.1116.

Cousteau, J. Y. 1965. World without sun. New York: Harper and Row.

Darwin, C. 1842. The structure and distribution of coral reefs. London: Smith, 

Elder, and Co.

Davis, K. A., and S. G. Monismith. 2011. The modification of bottom boundary 

layer turbulence and mixing by internal waves shoaling on a barrier reef. 

Journal of Physical Oceanography, doi: 10.1175/2011JPO4344.1

Dunlap, M., and J. R. Pawlik. 1996. Video-monitored predation by Caribbean reef 

fishes on an array of mangrove and reef sponges. Marine Biology, 126:117–

123. http://dx.doi.org/10.1007/BF00571383.

Ferrier-Pagès, C., J. Witting, E. Tambutté, and K. P. Sebens. 2003. Effect of natural 

zooplankton feeding on the tissue and skeletal growth of the scleractinian 

coral Stylophora pistillata. Coral Reefs, 22:229–240. http://dx.doi.org/10

.1007/s00338-003-0312-7.

Finelli, C. M., B. S. T. Helmuth, N. D. Pentcheff, and D. S. Wethey. 2005. Water flow 

influences oxygen transport and photosynthetic efficiency in corals. Coral 

Reefs, 25:47–57. http://dx.doi.org/10.1007/s00338-005-0055-8.
number 39 • 5 1

Graham, K., and K. P. Sebens. 1996. Distribution of marine invertebrate larvae 

near vertical surfaces in the rocky subtidal zone. Ecology, 77:933–949. http://

dx.doi.org/10.2307/2265513.

Harvell, C. D., W. Fenical, V. Roussis, J. L. Ruesink, C. C. Griggs, and C. H. Greene. 

1993. Local and geographic variation in the defensive chemistry of a West Indian gorgonian coral (Briareum asbestinum). Marine Ecology Progress Series, 

93:165–173. http://dx.doi.org/10.3354/meps093165.

Harvell, C. D., and T. H. Suchanek. 1987. Partial predation on tropical gorgonians 

by Cyphoma gibbosum (Gastropoda). Marine Ecology Progress Series, 38: 

37–44. http://dx.doi.org/10.3354/meps038037.

Hay, M. E., V. J. Paul, S. M. Lewis, K. Gastafson, J. Tucker, and R. N. Trindell. 1988. 

Can tropical seaweeds reduce herbivory by growing at night? Diel patterns 

of growth, nitrogen content, herbivory, and chemical versus morphological 

defenses. Oecologia, 75:233–245. http://dx.doi.org/10.1007/BF00378604.

Hearn, C. J, M. J. Atkinson, and J. L. Falter. 2001. A physical derivation of nutrientuptake rates in coral reefs: Effects of roughness and waves. Coral Reefs, 20: 

347–356. http://dx.doi.org/10.1007/s00338-001-0185-6.

Heidelberg, K. B., K. L. O’Neil, J. C. Bythell, and K. P. Sebens. 2010. Vertical distribution and diel patterns of zooplankton abundance and biomass at Conch 

Reef, Florida Keys (USA). Journal of Plankton Research, 32:75–91. http://

dx.doi.org/10.1093/plankt/fbp101.

Heidelberg, K. B., J. E. Purcell, and K. P. Sebens. 2003. Composition and sources 

of near-reef zooplankton on a Jamaican forereef. Coral Reefs, 23:263–280.

Heidelberg, K. B., K. P. Sebens, and J. E. Purcell. 1997. Effects of prey escape behavior and water flow on prey capture by the scleractinian coral, Meandrina 

meandrites. Proceedings of the eighth International Coral Reef Symposium, 

2:1081–1086.

Herren, L. W., L. J. Walters, and K. S. Beach. 2006. Fragment generation, survival, 

and attachment of Dictyota spp. at Conch Reef in the Florida Keys, USA.

Coral Reefs, 25: 287–295. http://dx.doi.org/10.1007/s00338-006-0096-7.

Herrnkind, W. 1974. Behavior: In situ approach to marine behavioral research. In

Experimental Marine Biology, ed. R. Mariscal, pp. 55–97. New York: Academic Press. 

Hobson, E. S., and J. R. Chess. 1976. Trophic interactions among fishes and zooplankton near shore at Santa Catalina Island, California. Fisheries Bulletin 

U.S., 74:567–598.

———. 1979. Zooplankters that emerge from the lagoon floor at night at Kure and 

Midway Atolls, Hawaii. Fisheries Bulletin U.S., 77:275–280.

Houlbrèque, F., and C. Ferrier-Pagès. 2008. Heterotrophy in tropical scleractinian 

corals. Biological Reviews of the Cambridge Philosophical Society, 81:1–17.

Hubbard, D. K., R. P. Burke, and I. P. Gill. 1985. Accretion in deep shelf-edge reefs,

St. Croix, U.S.V.I. In Deep Water Carbonates, eds. Crevello, P. D., and P. M. 

Harris, pp. 491–527. Tulsa, Okl: SEPM/Society for Sedimentary Geology.

———. 1992. Hurricane-induced sediment transport in open-shelf tropical systems,

an example from St. Croix, U.S. Virgin Islands. Journal of Sedimentary Petrology, 62:946–960. 

Hubbard, D. K., and D. Scaturo. 1985. Growth rates of seven species of scleractinian corals from Cane Bay and Salt River, St. Croix, U.S.V.I. Bulletin of Marine 

Science, 36:325–338. 

Johnson, A. S., and K. P. Sebens. 1993. Consequences of a flattened morphology: Effects of flow on feeding rates of the scleractinian coral Meandrina meandrites. 

Marine Ecology Progress Series, 99:99–114. http://dx.doi.org/10.3354/meps

099099.

Lang, M. A. 2001. Proceedings of the DAN Nitrox Workshop. Durham, N.C.: 

Divers Alert Network.

Lasker, H. R., M. D. Gottfried, and M. A. Coffroth. 1983. Effects of depth on 

the feeding capabilities of two octocorals. Marine Biology, 73:73–78. http://

dx.doi.org/10.1007/BF00396287.

Leichter, J. J., G. B. Deane, and M. D. Stokes. 2005. Spatial and temporal variability 

of internal wave forcing on a coral reef. Journal of Physical Oceanography,

35:1945–1962. http://dx.doi.org/10.1175/JPO2808.1.

Leichter, J. J., A. Paytan, S. Wankel, K. Hanson, S. Miller, and M. Altabet. 2007. 

Nitrogen and oxygen isotopic signatures of subsurface nitrate seaward of the 

Florida Keys reef tract. Limnology and Oceanography, 52:1258–1267. http://

dx.doi.org/10.4319/lo.2007.52.3.1258.

Leichter, J. J., G. Shellenbarger, S. J. Genovese, and S. R. Wing. 1998. Breaking internal waves on a Florida (USA) coral reef: A plankton pump at work? Marine 

Ecology Progress Series, 166:83–97. http://dx.doi.org/10.3354/meps166083.

Leichter, J. J., H. L. Stewart, and S. L. Miller. 2003. Episodic nutrient transport to 

Florida coral reefs. Limnology and Oceanography, 48:1394–1407. http://dx

.doi.org/10.4319/lo.2003.48.4.1394.

Leichter, J. J., S. R. Wing, S. L. Miller, and M. W. Denny. 1996. Pulsed delivery of subthermocline water to Conch Reef (Florida Keys), by internal tide bores. Limnology and Oceanography, 41:1490–1501. http://dx.doi.org/10.4319/lo.1996

.41.7.1490.

Levitan, D. R., and C. Petersen. 1995. Sperm limitation in the sea. Trends in Ecology 

and Evolution, 6:228–231.

Miles, J., and C. D. Harvell. 1990. Primary productivity of Briareum asbestinum over 

depth clines. Report of the National Oceanic and Atmospheric Administration.

Miller, S. L., D. W. Swanson, and M. Chiappone. 2000. Multiple spatial scale assessment of coral reef and hard-bottom community structure in the Florida Keys 

National Marine Sanctuary. Proceedings of the ninth International Coral 

Reef Symposium, 1:69–74. 

Mills, M. M., F. Lipschultz, and K. P. Sebens. 2004. Particulate matter ingestion 

and associated uptake by four species of scleractinian corals. Coral Reefs, 23: 

311–324. http://dx.doi.org/10.1007/s00338-004-0380-3.

Mills, M. M., and K. P. Sebens. 1997. Particle ingestion efficiency of the corals 

Siderastrea siderea and Agaricia agaricites: Effects of flow speed and sediment loads. Proceedings of the eighth International Coral Reef Symposium,

2:1059–1064.

———. 2005. Ingestion and assimilation of nitrogen from benthic sediments by 

three species of corals. Marine Biology, 145:1097–1106. http://dx.doi.org/10

.1007/s00227-004-1398-3.

Monismith, S. G. 2007. Hydrodynamics of coral reefs. Annual Review of Fluid 

Mechanics, 39:37–55.

Nyden, B. B. 1985. Hydrolab: NOAA’s Undersea Research Program at West Indies 

Laboratory. Proceedings of the fifth International Coral Reef Symposium,

5:607–609.

Ogden, J. C., and P. S. Lobel. 1978. The role of herbivorous fishes and urchins 

in coral reef communities. Environmental Biology of Fishes, 3:49–63. http://

dx.doi.org/10.1007/BF00006308.

Ohlhorst, S. L., and W. D. Liddell. 1984. Differing temporal patterns of movement 

into the water column by reef zooplankton. Bulletin of the Ecological Society 

of America, 65:275–276.

Ohlhorst, S. L., W. D. Liddell, and S. K. Boss. 1985. Temporal patterns of migration 

by reef zooplankton. In The Ecology of Coral Reefs, ed. M. L. Reaka, pp. 

117–128. Symposia Series for Undersea Research, Vol. 3, No. 1. Rockville, 

Md.: NOAA, National Undersea Research Program. 

Patterson, M. R. 1992a. A chemical engineering view of cnidarian symbioses. American Zoologist, 32:566–582.

———. 1992b. A mass transfer explanation of metabolic scaling relations in some 

aquatic invertebrates and algae. Science, 255:1421–1423. http://dx.doi.org/10

.1126/science.255.5050.1421.

Patterson, M. R., K. P. Sebens, and R. R. Olson. 1991. In situ measurements of forced 

convection on primary production and dark respiration in reef corals. Limnology and Oceanography, 36:936–948. http://dx.doi.org/10.4319/lo.1991

.36.5.0936.

Pawlik, J. R. 1997. Fish predation on Caribbean reef sponges: An emerging perspective of chemical defenses. Proceedings of the eighth International Coral Reef 

Symposium, 2:1255–1258.

———. 2011. The chemical ecology of sponges on Caribbean reefs: Natural products shape natural systems. Bioscience, 61(11):888–898.

Reidenbach, M. A., J. R. Koseff, and S. G. Monismith. 2007. Laboratory experiments of fine-scale mixing and mass transport within a coral canopy. Physics 

of Fluids, 19(7):075107. http://dx.doi.org/10.1063/1.2752189.

Reidenbach, M. A., J. R. Koseff, S. G. Monismith, J. V. Steinbuck, and A. Genin. 

2006a. Effects of waves, unidirectional currents, and morphology on mass 

transfer in branched reef corals. Limnology and Oceanography, 51:1134–

1141. http://dx.doi.org/10.4319/lo.2006.51.2.1134.

Reidenbach, M. A., S. G. Monismith, J. R. Koseff, G. Yahel, and A. Genin. 2006b. 

Boundary layer turbulence and flow structure over a fringing coral reef. Limnology and Oceanography, 51:1956–1968. http://dx.doi.org/10.4319/lo.2006

.51.5.1956.

Ruesink, J., and C. D. Harvell. 1990. Specialist predation on the Caribbean gorgonian Plexaurella spp. by the ovulid Cyphoma signatum. Marine Ecology 

Progress Series, 65:265–272. http://dx.doi.org/10.3354/meps065265.

Schmitt, R. J. 1987. Indirect interactions between prey: Apparent competition, 

predator aggregation, and habitat segregation. Ecology, 68:1887–1897. 

http://dx.doi.org/10.2307/1939880.

Sebens, K. P. 1997. Adaptive responses to water flow: Morphology, energetics, and 

distribution of reef corals. Proceedings of the eighth International Coral Reef 

Symposium, 2:1053–1058.
5 2 • smithsonian contributions to the marine sciences

Sebens, K. P., and T. J. Done. 1994. Water flow, growth form and distribution of 

sceleractinian corals: Davies Reef (GBR), Australia. Proceedings of the seventh International Coral Reef Symposium, 1:557–568.

Sebens, K. P., B. Helmuth, E. Carrington, and B. Agius. 2003. Effects of water flow 

on growth and energetics of the scleractinian coral Agaricia tenuifolia, in 

Belize. Coral Reefs, 22:35–47.

Sebens, K. P., and A. S. Johnson. 1991. The effects of water movement on prey capture by reef corals. Hydrobiologia, 226:91–101. http://dx.doi.org/10.1007

/BF00006810.

Sebens, K. P., and E. J. Maney, Jr. 1992. A portable diver-operated plankton sampler for 

near-substratum use. In Proceedings of Diving for Science, 1992, ed. L. B. Cahoon, 

pp. 99–114. Wilmington, N.C.: American Academy of Underwater Sciences. 

Sebens, K. P., K. Vandersall, L. Savina, and K. Graham. 1996a. Zooplankton capture 

by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in 

a field enclosure. Marine Biology, 127:303–318. http://dx.doi.org/10.1007/BF

00942116.

Sebens, K. P., J. Witting, and B. Helmuth. 1996b. Effects of water flow and aggregation on particle capture by the reef coral Madracis mirabilis. Journal of 

Experimental Marine Biology and Ecology, 211:1–28. http://dx.doi.org/10

.1016/S0022-0981(96)02636-6.

Shepard, A. N., D. A. Dinsmore, S. L. Miller, C. B. Cooper, and R. I. Wicklund. 

1996. Aquarius undersea laboratory: the next generation. In Methods and 

Techniques of Underwater Research, ed. M. A. Lang and C. C. Baldwin, pp. 

205–212. Washington, D.C.: Smithsonian Institution. 

Shepard, F. P., and R. F. Dill. 1977. Currents in submarine canyon heads off north 

St. Croix, U.S. Virgin Islands. Marine Geology, 24:M39–M45. http://dx.doi

.org/10.1016/0025-3227(77)90025-1.

Suchanek, T. H., R. C. Carpenter, J. D. Witman, and C. D. Harvell. 1983. Sponges 

as important space competitors in deep Caribbean coral reef communities. 

In The Ecology of Deep and Shallow Coral Reefs, ed. M. L. Reaka, pp. 55–

60. Symposia Series for Undersea Research, Vol. 1, No. 1. Rockville, Md.: 

NOAA, National Undersea Research Program.

Suchanek, T. H., S. L. Williams, J. C. Ogden, D. K. Hubbard, and I. P. Gill. 1985. 

Utilization of shallow-water seagrass detritus by Caribbean deep-sea macrofauna: Delta 13C evidence. Deep-Sea Research, 32:201–214. http://dx.doi.org

/10.1016/0198-0149(85)90028-7.

Szmant-Froelich, A. 1983. Functional aspects of nutrient cycling on coral reefs. In 

The Ecology of Deep and Shallow Coral Reefs, ed. M. L. Reaka, pp. 133–

139. Symposia Series for Undersea Research, Vol. 1, No. 1. Rockville, Md.: 

NOAA, National Undersea Research Program.

Trussell, G. C., M. P. Lesser, M. R. Patterson, and S. J. Genovese. 2006. Depthspecific differences in growth of the reef sponge Callyspongia vaginalis: Role 

of bottom-up effects. Marine Ecology Progress Series, 323:149–158. http://

dx.doi.org/10.3354/meps323149.

Vroom, P. S., S. M. Smith, J. A. Coyer, L. J. Walters, C. L. Hunter, K. S. Beach, 

and J. E. Smith. 2003. Field biology of Halimeda tuna (Bryopsidales, Chlorophyta) across a depth gradient: Comparative growth, survivorship, recruitment, and reproduction. Hydrobiologia, 501:149–166. http://dx.doi.org/10

.1023/A:1026287816324.

Walters, L. J., C. M. Smith, J. A. Coyer, C. L. Hunter, K. S. Beach, and P. S. Vroom. 

2002. Asexual propagation in the coral reef macroalga Halimeda (Chlorophyta, Bryopsidales): Production, dispersal and attachment of small fragments. Journal of Experimental Marine Biology and Ecology, 278:47–65. 

http://dx.doi.org/10.1016/S0022-0981(02)00335-0.

West, J. M., C. D. Harvell, and M. Walls. 1993. Morphological plasticity and variation in reproductive traits of a gorgonian coral over a depth cline. Marine 

Ecology Progress Series, 94:61–69. http://dx.doi.org/10.3354/meps094061.

Williams, S. L. 1988. Disturbance and recovery of a deep water Caribbean seagrass 

bed. Marine Ecology Progress Series, 42:63–71. http://dx.doi.org/10.3354

/meps042063.

Williams, S. L., V. A. Breda, T. W. Anderson, and B. B. Nyden. 1985. Growth and 

sediment disturbances of Caulerpa spp. (Chlorophyta) in a submarine canyon. Marine Ecology Progress Series, 21:275–281. http://dx.doi.org/10.3354

/meps021275.

Witting, J. 1999. Zooplankton capture and coral growth: The role of heterotrophy 

in Caribbean reef corals. Ph.D. diss., Northeastern University, Boston.
Marine Chemical Ecology: 

A Science Born of Scuba

Joseph R. Pawlik, Charles D. Amsler, Raphael Ritson-Williams, 

James B. McClintock, Bill J. Baker, and Valerie J. Paul

ABSTRACT. For more than 50 years, organic chemists have been interested in the novel chemical 

structures and biological activities of marine natural products, which are organic compounds that 

can be used for chemical defense and chemical communication by diverse marine organisms. Chemical ecology, the study of the natural ecological functions of these compounds, is an interdisciplinary 

field involving chemistry, biology, and ecology. Examples of ecological functions of marine natural 

products include distastefulness that inhibits feeding by predators, settlement cues for larvae, allelopathic effects that prevent fouling by epiphytes and overgrowth by competitors, and pheromones 

for mate-searching behavior. Much of the research in marine natural products and marine chemical 

ecology has used scuba diving and related undersea technologies as necessary tools. The breadth of 

marine organisms studied and the types of experiments conducted under water have expanded with 

technological developments, especially scuba diving. In this paper, we highlight the importance of 

scuba and related technologies as tools for advancing marine chemical ecology by using examples 

from some of our own research and other selected studies. We trace the origins of marine chemical 

ecology on the heels of marine natural products chemistry in the 1970s and 1980s, followed by the 

development of increasingly sophisticated ecological studies of marine algae and invertebrates in 

Caribbean, tropical Pacific, and Antarctic waters.

INTRODUCTION

Natural products are chemical compounds derived from natural sources, including 

plants, animals, fungi, and bacteria. Marine natural products research involves determining the structure, function, and biosynthesis of these compounds from marine microbes, 

phytoplankton, macroalgae, sponges, tunicates, and corals, among others. Natural products are also called secondary metabolites because they are small molecules with no 

known function in the primary metabolism of the organisms that produce them. As a scientific discipline, marine natural products research is an offshoot of the much older study 

of terrestrial secondary metabolites found primarily in vascular plants, insects, bacteria, 

and fungi. Many marine natural products possess novel functional groups and molecular 

structures compared to those from terrestrial sources. To date, 21,800 natural products 

have been described from marine organisms (MarinLit, 2011; Blunt et al., 2011). 

Marine natural products include diverse classes of compounds, such as terpenes, 

phenols, polyphenolics, acetogenins, peptides, alkaloids, and others. Most research on 

marine natural products focuses on their potential biomedical uses. Metabolites from 

marine organisms have shown antitumor, antiviral, and anti-inflammatory activities,

and several of these are currently in clinical trials to establish their effectiveness as new 

drugs, or are in clinical use (Newman and Cragg, 2004; Molinski et al., 2009; Villa and 

Joseph R. Pawlik, Department of Biology and Marine Biology, UNCW Center for Marine Science, 

5600 Marvin K Moss Lane, Wilmington, North 

Carolina 28409, USA. Charles D. Amsler, Department of Biology, Campbell Hall 464, 1300 

University Blvd, University of Alabama at Birmingham, Birmingham, Alabama 35294-1170,

USA. Raphael Ritson-Williams, Smithsonian 

Marine Station at Fort Pierce, 701 Seaway Drive, 

Fort Pierce, Florida 34949, USA. James B. McClintock, Department of Biology, Campbell 

Hall 464, 1300 University Blvd, University of 

Alabama at Birmingham, Birmingham, Alabama 

35294-1170, USA. Bill J. Baker, Department 

of Chemistry, University of South Florida, 4202 

E. Fowler Ave CHE 205, Tampa, Florida 33620, 

USA. Valerie J. Paul, Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort Pierce, 

Florida 34949, USA. Correspondence: V. Paul, 

paul@si.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
5 4 • smithsonian contributions to the marine sciences

Gerwick, 2010). In addition, some marine natural products may 

realize their biomedical potential by becoming useful molecular 

or biochemical probes (Mayer et al., 2010, 2011). Through detailed mechanistic studies, these biochemical probes may lead 

to the discovery of receptor proteins, enzymes, or other macromolecular targets. The improved understanding of biochemistry and cell and molecular biology that has resulted from 

these studies may ultimately lead to the discovery of new drugs 

(Mayer et al., 2010).

The study of the ecological functions of natural products 

is termed “chemical ecology.” While the roles of natural products in terrestrial plants and insects are relatively well studied, 

much less is known for marine natural products. Examples of 

ecological functions of natural products include distastefulness 

that inhibits feeding by predators, settlement cues for larvae, 

allelopathic effects that prevent fouling by epiphytes and overgrowth by competitors, and pheromones for mate searching 

behavior. Marine chemical ecology relies on chemical and ecological experimentation to determine the individual or suite of 

compounds responsible for driving the observed interactions. 

Determining the compounds responsible for ecological interactions can open a window into other interdisciplinary fields 

that contribute to ecology, including studies of animal behavior, 

neurobiology, sensory ecology, reproduction, predator–prey and 

plant–herbivore interactions, competition, symbiosis, and dispersal and recruitment. 

Much of the research in marine natural products and marine chemical ecology has used scuba diving and related undersea 

technologies as necessary tools. Until the invention of scuba diving, most of the ocean depths were obscured from basic observation, and many marine organisms could not be readily collected. 

Sampling of the benthos at depths greater than a few meters was 

carried out using nets and dredges; this was often compared to 

collecting rainforest insects by pulling a butterfly net behind a 

low-flying plane. Beginning in the 1960s and 1970s, scuba diving 

became an essential tool for the collection of benthic marine organisms, particularly macroalgae and invertebrates, for studies of 

their natural products chemistry (Scheuer, 1990). Also, it was not 

until scientists could use scuba that they could begin to observe 

ecological and behavioral interactions in situ and also conduct 

manipulative experiments to better understand the mechanisms 

underlying marine behavioral and ecological interactions. Marine chemical ecology has now developed into a broad research 

area encompassing studies of the chemical mediation of a variety 

of ecological interactions among marine organisms. The field has 

been comprehensively reviewed on a regular basis (Paul, 1992; 

McClintock and Baker, 2001; Paul and Puglisi, 2004; Paul et al., 

2006, 2007, 2011b; Amsler, 2008; Paul and Ritson-Williams, 

2008; Hay, 2009; Pawlik, 2011), and it is not our intention to 

duplicate these reviews. Instead, we will highlight the importance 

of scuba and related technologies as tools for advancing marine 

chemical ecology by using examples from some of our own research and other selected studies.

HUMBLE BEGINNINGS: 

TOXICITY ASSAYS TO MORE 

RELEVANT TECHNIQUES

The field of marine natural products chemistry experienced 

a “gold rush” in the 1970s and 1980s, when organic chemists 

took advantage of two emerging technologies: scuba diving and 

rapidly advancing spectroscopic methods (mostly nuclear magnetic resonance, or NMR, spectroscopy). The result was a rapid 

increase in the number of publications describing novel metabolites from benthic marine invertebrates and algae (reviewed by 

Faulkner and Fenical, 1977; Scheuer, 1978–1983). Relying on 

the assumption that secondary metabolites must serve some 

function for the organism that produces them, many of these 

publications ascribed ecologically important properties to new 

compounds without empirical evidence; in fact, whole reviews of 

chemical ecology from this period were compiled of references 

with little or no experimental data to support an ecological function for secondary metabolites (Karuso, 1987). 

At about the same time, ecologists were also taking advantage 

of the advent of scuba diving and describing the distributions and 

abundances of benthic animals and plants previously known only 

from much less effective sampling methods, such as dredging (see 

other contributions in this volume). The assumption of many of 

these researchers was that anything sessile and soft-bodied must

be chemically defended to avoid consumption by abundant and 

ever-present predators (Randall and Hartman, 1968; Bakus and 

Green, 1974). In an effort to introduce empiricism to what was 

otherwise descriptive work on species abundances, some ecologists began extrapolating chemical defenses from toxicity assays 

in which fish (usually goldfish or mosquito fish) or invertebrates 

were exposed to aqueous suspensions of crude organic extracts of 

invertebrate tissues (Bakus and Green, 1974; Jackson and Buss, 

1975). Subsequent studies that have compared data from these 

types of toxicity assays with more relevant feeding experiments 

have found no relationship between them (Schulte and Bakus, 

1992; Pawlik et al., 1995; Tarjuelo et al., 2002).

Beginning in the mid to late 1980s, the first publications 

began to appear that employed more ecologically relevant techniques for addressing the biological functions of secondary metabolites from marine animals and plants. These were born of 

collaborations between students and young faculty primarily 

educated in marine biology and ecology and established natural 

products chemists who had developed an interest in the ecological functions of secondary metabolites. Some of this work began 

in the rocky intertidal of Southern California, with members of 

John Faulkner’s natural products group at Scripps Institution of 

Oceanography collaborating with graduate-student marine ecologists to produce some of the first studies of chemical defenses 

of sponges (Thompson, 1985; Walker et al., 1985) and intertidal 

snails (Albizati et al., 1985; Pawlik et al., 1986). However, it was 

scuba diving that allowed these and other researchers unprecedented access to marine organisms in the subtidal environment, 
number 39 • 5 5

where the vast majority of marine biodiversity is found, permitting the collection of rare organisms and large quantities of 

patchily distributed organisms, comparative collections across 

broad geographic regions, and most importantly, manipulative 

experiments to test hypotheses about the functions of secondary metabolites in the field. The following provides a regional 

glimpse of a variety of important chemical ecological studies that 

elucidated the diverse role of secondary metabolites in population and community structure.

INTO THE FIELD

Chemical Ecology in the Caribbean

The transition from toxicity screening to more ecologically 

relevant studies of secondary metabolites from marine organisms began with studies of the chemical defenses of macroalgae from Caribbean coral reefs (Paul and Fenical, 1983, 1986; 

Paul and Hay, 1986). At first, these studies relied on research 

scuba diving for collecting alone; not only were ample volumes 

of algae needed for the isolation of secondary metabolites, but 

these collections had to be separated by species, as in the case 

of the common calcareous algae in the genus Halimeda (Paul 

and Fenical, 1983). Algae of this genus yielded halimedatrial, 

a diterpenoid trialdehyde that was active in a series of antimicrobial, antimitotic, and toxicity assays, but was also tested in 

artificial foods as a feeding deterrent against damselfishes and 

herbivorous mollusks (Paul and Fenical, 1983, 1986). The geographically extensive collections of algae, gathered by diving 

from a research vessel as a mobile diving platform, combined 

with chemical analysis of the concentrations of the metabolites, 

allowed the authors to determine that higher levels of defensive metabolites were correlated with higher levels of herbivory 

(Paul and Fenical, 1986). Field assay methods were developed 

to survey interspecific differences in chemical and morphological defenses in Caribbean macroalgae (Paul and Hay, 1986). In 

what is perhaps the first use of saturation diving in the service of 

marine chemical ecology, researchers using the Hydrolab, then in 

St. Croix, U.S. Virgin Islands, monitored levels of secondary metabolites in Halimeda over the course of the night and day (Hay 

et al., 1988b). Saturation diving from the Hydrolab, and later the 

Aquarius habitat on Conch Reef, near Key Largo, Florida, has 

proven to be a particularly useful technology for time-intensive 

research. Saturation divers live for a week or more at 15 m depth 

in the habitat, essentially a stationary submarine, and can use 

standard scuba diving gear to perform research dives of 6 hours 

or longer per day at the same depth as the habitat. This allows 

research divers to carry out time-consuming observations or manipulations that could never be accomplished by diving from the 

surface. Night- and day-long studies of Halimeda living on the 

coral reef resulted in the discovery that these algae invest high 

concentrations of chemical defenses in the new, unpigmented, 

soft, and nutritionally valuable tissues that grow rapidly at night, 

with a subsequent reduction in chemical defenses in these tissues 

as they turn green and become photosynthetic, age, and become 

protected from herbivores by calcification (Hay et al., 1988b). 

Research on the chemical ecology of macroalgae in the 

Caribbean accelerated rapidly, with defensive roles assigned to 

metabolites from several species in different taxonomic groups 

(Hay et al., 1987, 1988a, 1990; Paul et al., 1987). Again, this research required geographically extensive collections using scuba, 

but also included field observations of species abundances and 

herbivory. Many of these studies introduced novel field and laboratory experiments to assess chemical defenses by using diverse 

consumers, including fishes, sea urchins, sea slugs, polychaete 

worms, and amphipod crustaceans (Hay et al., 1987, 1988a, 

1988c; Hay and Fenical, 1988). These studies tested fundamental hypotheses about plant–herbivore interactions that had previously only been applied to terrestrial systems.

Scores of papers were published over the ensuing two decades that further refined our understanding of the chemical 

ecology of macroalgae on Caribbean reefs (reviews in Hay and 

Steinberg, 1992; Hay, 1997, 2009; Duffy and Hay, 2001; Paul 

et al., 2001, 2006, 2007, 2011a; Paul and Puglisi, 2004; Amsler, 

2008). This knowledge came with new developments in laboratory and field assays designed to test algal chemical defenses 

against a variety of potential threats, including grazers, competitors, and fouling organisms (Hay et al., 1998). Diving technologies were fundamental to the collection of subject and assay 

organisms (Figure 1a), as well as to the field assays themselves 

(Figures. 1b–d). Some recent studies have focused on the antimicrobial and allelopathic effects of Caribbean macroalgae, including the negative effects of macroalgal extracts on adult corals 

(Rasher and Hay, 2010) and settlement of coral larvae (Kuffner 

et al., 2006; Paul et al., 2011a), antimicrobial effects of macroalgal extracts and compounds (Kubanek et al., 2003; Engel 

et al., 2006), and both inhibitive and stimulative effects of algal 

extracts on bacteria cultured from the surfaces of Caribbean corals and macroalgae (Morrow et al., 2011). Recently, saturation 

diving has again been employed to study plant–herbivore interactions at the ecosystem level, with the Aquarius habitat off Key 

Largo, Florida, serving as a base for saturation dives to nearby 

Conch Reef (Burkepile and Hay, 2008, 2010). Large-scale caging 

studies that require long-term saturation dives have revealed that 

the abundance and diversity of herbivores dramatically affects 

macroalgal cover on reefs, with indirect effects on the survival of 

reef-building corals (Burkepile and Hay, 2010).

Investigations of the chemical ecology of Caribbean coral 

reef invertebrates tracked that of macroalgae, with studies focusing on gorgonian corals among the earliest (Gerhart, 1984; 

Pawlik et al., 1987; Harvell et al., 1988; Harvell and Fenical, 

1989; Pawlik and Fenical, 1989; Van Alstyne and Paul, 1992; 

Slattery, 1999). The technical requirements for these studies were 

the same as for those focused on macroalgae, with scuba diving 

figuring prominently in the collection of both subject and assay 
5 6 • smithsonian contributions to the marine sciences

a b

c d

FIGURE 1. Photographs illustrating various field methods that use scuba diving for studies of marine chemical ecology in the Caribbean. (a) A

diver examines and prepares to collect marine cyanobacteria, Lyngbya spp., that are overgrowing a gorgonian (photo by Karen Lane Schroeder); (b) A diver observes fishes feeding during an underwater feeding assay. Paired feeding assays are commonly used to test the palatability of 

algal extracts and natural products. Artificial food made with palatable algae is attached to polypropylene lines, with one line containing control 

food cubes and one containing food with extracts or pure compounds at their natural concentrations (photo by R. Ritson-Williams); (c) Gray

angelfish, Pomacanthus arcuatus, feeds on the palatable sponge Chondrosia collectrix attached to a brick. Angelfishes are major consumers of 

some species of Caribbean sponges (photo by J. Pawlik); (d) Predator exclusion (“caging”) experiment set-up on Conch Reef, Florida. In this 

case, replicate sponge pieces are placed inside and outside of cages to observe net differences in growth after one year for species that are protected by chemical defenses and those that are not (photo by J. Pawlik).
number 39 • 5 7

organisms and in field experiments. Initial surveys of the chemical defenses of gorgonians against generalist predatory fishes 

suggested that there was some interspecific variation in the levels 

of defense (Pawlik et al., 1987), but subsequent experiments after 

assay techniques had been refined revealed that gorgonians were 

broadly defended by secondary metabolites, and that structural 

defenses in the form of small calcareous spicules were likely not 

effective defenses against coral reef consumers that are accustomed to eating limestone when grazing on calcified macroalgae 

and reef-building corals (O’Neal and Pawlik, 2002).

The chemical ecology of a variety of less sedentary Caribbean 

marine invertebrates, ranging from planktonic larvae (Lindquist 

and Hay, 1996; Bullard and Hay, 2002) to hydroids on floating 

mats of Sargassum seaweed (Stachowicz and Lindquist, 1997) to 

crustaceans that co-opt defended algae or invertebrates to protect

themselves by association (Stachowicz and Hay, 2000; Stachowicz, 2001), has been studied. For the beautiful feather-duster

worms (Sabellidae) that are common to some Caribbean reefs, the 

relative speed with which these tube-dwelling worms retract their

feeding radioles correlated to chemical defense, with those that 

retracted more slowly having more potent defenses (Kicklighter 

and Hay, 2007), with the trade-off between defense and escape

speed extending to spaghetti worms (Terebellidae) and others as 

well (Kicklighter et al., 2003; Kicklighter and Hay, 2006).

Caribbean sponges are perhaps the best-understood aquatic 

organisms in terms of their chemical ecology, from the level 

of molecule to ecosystem (Pawlik, 2011), again thanks to the 

various diving technologies that have contributed to their study. 

Sponges are now the dominant habitat-forming organisms on 

many Caribbean reefs, and their populations are increasing (Maliao et al., 2008; McMurray et al., 2010). The earliest studies of 

Caribbean sponge ecology suggested that fish predators had little 

impact on sponge distributions (Randall and Hartman, 1968), an 

idea that was subsequently overturned (Pawlik, 1997). A survey 

approach that considered secondary metabolites as well as structural and nutritional defenses was used to investigate defenses 

against fish predators (Chanas and Pawlik, 1995, 1996; Pawlik 

et al., 1995), with chemical defense clearly playing the dominant 

role (Jones et al., 2005). The secondary metabolites responsible 

for chemical defense were isolated and identified using laboratory and field experiments for most of the common sponge species on Caribbean reefs (Albrizio et al., 1995; Wilson et al., 1999; 

Kubanek et al., 2001; Pawlik et al., 2002); for the oroidin class of 

compounds of the genus Agelas, the molecular basis for chemical 

defense was explored using both natural and synthetic metabolites (Assmann et al., 2000; Lindel et al., 2000). At the same time, 

studies of chemical defenses of Caribbean sponges against other 

potential threats were proceeding, including defenses against invertebrate predators (Waddell and Pawlik, 2000a, 2000b), invertebrate and coral competitors (Engel and Pawlik, 2000; Pawlik et 

al., 2007), fouling (Kubanek et al., 2002), and microbial pathogenesis (Newbold et al., 1999; Kelly et al., 2005).

Technologies more advanced than simple scuba diving, 

including saturation and technical diving, have contributed to 

research into the chemical ecology of Caribbean sponges, and 

these studies have advanced our understanding of how secondary metabolites influence the entire reef community (Pawlik, 

2011). A novel use of the Aquarius habitat on Conch Reef, off 

Key Largo, Florida, was as a platform for long-term videography 

of fish and sea turtle behavior in response to an array of reef, seagrass bed, and mangrove sponges (Dunlap and Pawlik, 1996). It 

was discovered not only that angelfishes and turtles preferred to 

eat sponges that were chemically undefended in feeding experiments with generalist fish predators, such as bluehead wrasses 

(Pawlik et al., 1995) (Figure 1c), but also that parrotfishes, long 

thought of as grazers on only algae and corals, were voracious 

sponge predators (Dunlap and Pawlik, 1996, 1998). These studies led to the determination that sponges on Caribbean reefs 

could be placed into three categories: (1) chemically defended 

species that are left alone by predators, (2) palatable species that 

are consumed by sponge-eating fishes, and (3) preferred species that are removed from the reef and persist only in refuge 

habitats, such as the interstices of the reef or seagrass or mangrove habitats where predators do not forage (Pawlik, 1997). 

Resource trade-offs between investment in chemical defenses and 

reproduction or growth are responsible for the presence of both 

defended and palatable sponge species on Caribbean reefs, a concept that was tested by observing the healing rates of defended 

and palatable sponges (Walters and Pawlik, 2005) by conducting 

long-term growth experiments with sponges inside and outside 

of cages (Leong and Pawlik, 2010) (Figures 1c–d), and by using 

diving to survey patterns of sponge recruitment to a shipwreck 

adjacent to a reef off Key Largo, Florida (Pawlik et al., 2008). 

These studies provide strong evidence that fish predation is the 

dominant force structuring sponge communities in the Caribbean, and that the secondary metabolites produced by chemically defended sponges come at a cost to reproduction, growth, 

or both of these life functions (Pawlik, 2011).

Chemical Ecology in the Tropical Pacific

The earliest investigations of chemical ecology in the tropical 

Pacific were studies of the comparative toxicities of extracts of 

sponges, sea cucumbers, and soft corals (Bakus and Green, 1974; 

Bakus, 1981; Coll et al., 1982). Natural products chemist John 

Coll and ecologist Paul Sammarco developed a collaboration that 

led to some of the earliest field studies of allelopathy and antifouling in marine chemical ecology. Focusing on the taxonomically 

diverse and chemically rich alcyonarians (soft corals) of the Great 

Barrier Reef, this research team discovered that some species of 

soft corals were competitively dominant over both soft and hard 

corals (Labarre et al., 1986; Alino et al., 1992). Subsequent work 

demonstrated that the allelopathic effects of soft corals against 

each other extended to the inhibition of settlement of hard corals (Maida et al., 1995), and evidence of toxic effects of specific 

metabolites from soft corals on hard corals (Aceret et al., 1995). 

More recently, this group has developed more effective methods 

of assessing antifouling activity in the field (Maida et al., 2006).
5 8 • smithsonian contributions to the marine sciences

Studies of the chemical ecology of macroalgae in the tropical Pacific followed those done in the Caribbean by Valerie Paul 

and coworkers. Observations of macroalgal blooms and the 

persistence of macroalgae in the presence of herbivorous fishes 

were made by scuba divers in the field (Figure 2a), suggesting 

that these algae were defended from grazers. Experiments were 

conducted to determine palatability of the natural compounds 

with and without confounding factors of food quality or structural defenses (Paul et al., 1990; Van Alstyne and Paul, 1990; 

Duffy and Paul, 1992; Schupp and Paul, 1994). Often potential 

herbivores had species-specific preferences that allowed them 

to specialize on otherwise chemically defended algae (Hay and 

Steinberg, 1992; Paul et al., 2001). As experiments progressed, 

researchers found that the concept of algal chemical defense was 

more complex. Some algae had variable concentrations or different compounds across space and time (Steinberg and Paul, 1990; 

Meyer and Paul, 1992; Paul and Van Alstyne, 1992; Puglisi and 

Paul, 1997; Van Alstyne et al., 2001). Other compounds found 

in marine algae inhibited the growth of pathogens, suggesting 

that some natural products are important for other functions 

that contribute to survival, such as reducing disease (Puglisi et 

al., 2007; Lane et al., 2009). Extensive research has shown that 

natural products from algae inhibit biofouling on their surfaces 

(reviewed in Fusetani, 2004, 2011; Lane and Kubanek, 2008). 

Halogenated furanones produced by the red alga Delisea pulchra

in Australia inhibited herbivory and also the growth of algae on 

its surface (Wright et al., 2004; Dworjanyn et al., 2006). Chemically rich macroalgae can negatively affect corals through allelopathic interactions when they are in contact (Rasher and Hay, 

2010; Rasher et al., 2011). These types of studies continue today 

and are important for defining how algae can persist in herbivorerich habitats and compete with other benthic organisms.

Although benthic blue-green algae (Cyanobacteria) are not 

related to eukaryotic macroalgae, they fill a similar ecological 

role. Extensive work on the Pacific island of Guam was conducted 

to study the chemical ecology of marine benthic cyanobacteria, 

and also to determine which factors might affect their growth 

and persistence in coral reef habitats (Figure 2b). Cyanobacteria are prolific producers of natural products (Tan, 2010), some 

of which have been tested for their feeding deterrent properties 

(Paul and Pennings, 1991; Pennings et al., 1996, 1997; Thacker 

et al., 1997; Nagle and Paul, 1998, 1999). In situ manipulations, 

including caging experiments, showed that the exclusion of herbivores can sometimes contribute to macroalgal and cyanobacterial bloom formation and growth (Thacker et al., 2001). Benthic 

surveys using scuba showed that some blooms of cyanobacteria 

were regulated by large storms that produced heavy wave action 

that dislodged the cyanobacteria (Becerro et al., 2006). Research 

on benthic cyanobacteria is ongoing around the world, as these 

organisms can form large-scale blooms that kill many benthic 

organisms (Paul et al., 2005, 2007; Watkinson et al., 2005). 

Studies of specialist consumers, especially herbivores that 

specialize on chemically defended algae or cyanobacteria, are 

revealing much about how natural products can influence trophic interactions. Saccoglossans, a group of opisthobranch mollusks, often specialize on green algae, and they can sequester 

algal secondary metabolites, which are then used for their own 

defense against predators (Paul and Van Alstyne, 1988; Hay et 

al., 1990; Becerro et al., 2001). By stealing defensive compounds 

from their food sources, these soft-bodied slugs avoid the costs 

of making chemical defenses. Possibly the best-studied specialists 

are sea hares, which sequester dietary-derived natural products 

primarily in the digestive gland (Pennings and Paul, 1993; de 

Nys et al., 1996; Ginsburg and Paul, 2001). Some sea hares, such 

as species of Dollabela and Stylocheilus, bioaccumulate natural 

products from cyanobacteria (Pennings and Paul, 1993; Pennings 

et al., 1996, 1999, 2001). Demonstrating the potential for studies 

of chemical ecology to generate possible new drugs, the sea hare 

Dolabella auricularia was discovered to contain natural products with anticancer properties (Flahive and Srirangam, 2005; 

Sato et al., 2007). Subsequent collection and isolation required 

huge numbers of sea hares, until it was discovered that the animals were sequestering the compounds from their cyanobacterial 

food (Luesch et al., 2002), illustrating the importance of in situ 

observations of species interactions for discovering the dietary 

source of a natural product. 

A variety of sessile benthic invertebrates from the tropical 

Pacific have been the focus of chemical ecology research. Chemical defenses of Pacific soft corals and gorgonians were studied 

on the reefs of Guam for many years (Wylie and Paul, 1989; 

Van Alstyne et al., 1994; Puglisi et al., 2000, 2002). Slattery and 

coworkers characterized changes in steroids and secondary metabolites over the reproductive period of Sinularia polydactyla, 

and determined that chemical defenses of this soft coral were 

transferred to its eggs and larvae (Slattery et al., 1999). Considerable variation was observed in concentrations of defensive 

terpenes in S. polydactyla and S. maxima at different reefs on 

Guam. Scuba was used to conduct transplant studies and video 

transects that linked higher levels of defensive compounds in soft 

corals that lived on reefs with higher levels of predation by butterflyfishes, suggesting that predation induced greater production 

of the defensive compound pukalide in the corals (Slattery et al., 

2001). The soft coral S. maxima was further studied to determine 

how bleaching might influence its production of defensive compounds. During a natural bleaching event of soft coral colonies in 

the field, concentrations of a defensive compound decreased but 

recovered again after several months. Predation rates increased 

on bleached colonies, and extracts of bleached colonies did not 

deter predation (Slattery and Paul, 2008). Most recently, studies 

of hybridization within the genus Sinularia have revealed that 

hybrid soft corals exhibited greater fitness than the parental species, including stronger allelopathic effects against one parental 

species and stronger antipredatory defenses than either parental 

species (Slattery et al., 2008). 

Sponge chemical defenses have also been investigated in the 

Pacific. One sponge, Dysidea sp., overgrew and killed another 
number 39 • 5 9

FIGURE 2. Photographs illustrating various field methods that use scuba diving for studies of marine chemical ecology in the tropical Pacific. 

(a) A diver examines the chemically rich green alga Chlorodesmis fastigiata before collection (photo by V. Paul); (b) Mixed assemblages of 

cyanobacteria overgrow corals (photo by R. Ritson-Williams); (c) The dorid nudibranch Chromodoris lochi eats an unidentified sponge (photo 

by V. Paul); (d) A feeding assay examines chemical defenses and the role of aposematic coloration in phyllidid nudibranchs (photo by R. RitsonWilliams).

a b

c d
6 0 • smithsonian contributions to the marine sciences

sponge, Cacospongia sp., on Guam. The sponge Dysidea sp. contained the compound 7-deacetoxyolepupuane, which deterred 

fish predators in situ (Thacker et al., 1998). Using scuba, these 

researchers also tested for allelopathic effects of this compound 

by attaching agar strips containing natural concentrations of 

7-deacetoxyolepupuane onto the co-occurring sponge Cacospongia sp. After seven days, the presence of this compound 

alone caused sponge tissue necrosis similar to that observed in 

the sponge–sponge interactions. This chemically mediated competition was first observed by divers in the field, and through 

extensive field-based ecology using scuba it was shown that the 

isolated sponge compound had multiple ecological functions in 

competition and predator defense (Thacker et al., 1998). 

As in the Caribbean, sponge consumers have also been studied in the tropical Pacific, and again, underwater observations 

were critical to understanding predator–prey interactions. Dorid 

nudibranchs are specialized predators on sponges (Figure 2c), but 

in the tropical Pacific sponge diversity is so large that it would be 

impossible to test every possible combination of nudibranch and 

prey. Perhaps the earliest investigation linking a nudibranch to its 

prey did so by demonstrating the presence of structurally complex natural products called macrolides in the dorsal tissues of 

the large Spanish Dancer nudibranch, Hexabranchus sanguineus, 

and in the sponge Halichondria sp., collected by night diving on 

Kwajalein atoll in the Marshall Islands (Pawlik et al., 1988). This 

study went on to demonstrate that the macrolides were “stolen” 

by the nudibranch from its sponge diet and passed on to the egg 

masses of the slug, and that these metabolites were highly effective chemical defenses against co-occurring fish and crab species 

(Pawlik et al., 1988). Observations of another dorid nudibranch, 

Glossidoris palida, determined that the nudibranch was eating 

the sponge Cacospongia sp., from which it would sequester compounds for defense (Avila and Paul, 1997; Becerro et al., 1998). 

Many brightly colored nudibranchs can be observed by divers 

during the day, which appears to be a strategy to advertise their 

chemical defense. The phyllidiid nudibranch Phyllidiella granulatus was frequently seen in Guam, and when the nudibranchs 

were offered alive to fish they were never eaten (Ritson-Williams 

and Paul, 2007). Underwater observations showed that P. granulatus was eating the sponge Acanthella cavernosa, and laboratory analyses found that these two organisms had many of the 

same natural products. In situ feeding assays with the sponge 

compounds showed that they inhibited fish predation at levels 

below natural concentrations (Figure 2d). Using an underwater 

video camera, fish predators were found to avoid these sponge 

compounds without tasting them, demonstrating modification of 

fish behavior by chemical defenses in the field (Ritson-Williams 

and Paul, 2007). This study illustrates not only the potency of 

marine chemical defenses but also the complexity of ecological 

interactions that can only be observed by conducting research 

under water. 

Often, marine natural products from soft bodied invertebrates are assumed to be defensive compounds. While this is 

certainly the best-studied ecological role of natural products, it is 

not their only function. Tetrodotoxin and its analogs are potent 

neurotoxins that have been found in a wide variety of marine 

and terrestrial organisms (Zimmer and Ferrer, 2007), and these 

compounds are typically assumed to have a defensive function. 

Tetrodotoxin and several analogs were found in a planocerid 

flatworm species that eats mobile snails. In situ experiments were 

conducted to see if a natural assemblage of reef fish would eat 

whole live flatworms (Ritson-Williams et al., 2006). Reef fish ate 

almost all of the flatworms offered, suggesting that tetrodotoxin 

is either not defensive or not detected by these predators and 

providing further evidence that toxicity is not the same as antipredatory defense. Further investigation showed that tetrodotoxin was actually used by the flatworm to kill prey items, which 

are mostly gastropod mollusks (Ritson-Williams et al., 2006). 

These experiments show the importance of field experiments 

using scuba to elucidate the function of a secondary metabolite.

Chemical Ecology in Antarctic Waters

The history of chemical ecology in Antarctica is more recent 

than at lower latitudes. The first scientist to use scuba diving 

as a research tool in Antarctica was Michael Neushul in 1958 

(Neushul, 1959, 1961). Neushul described the benthic marine 

communities along the western Antarctic Peninsula currently 

being studied by chemical ecologists, particularly the macroalgal 

flora (Neushul, 1965, 1968). Since Neushul’s time, it has become 

known that chemical defenses against predation are widespread 

in the Antarctic marine flora and fauna (reviewed by Amsler et 

al., 2001a, 2001b, 2008, 2009a; Avila et al., 2008; McClintock 

et al., 2005, 2010; McClintock and Baker, 1997, 1998), which 

is in contrast to predictions made before field studies were initiated in Antarctica that included scuba diving (cf. Amsler et al., 

2000). Diving collections have also facilitated the elucidation of 

many of the secondary metabolites that mediate these ecological 

interactions (Figures 3a–d; Amsler et al., 2001a, 2001b; Lebar 

et al., 2007).

A majority of the diving-based studies of Antarctic marine 

chemical ecology have been conducted from the United States 

Antarctic Program (USAP) facilities at Palmer Station (64°46′S, 

64°03′W) off the western Antarctic Peninsula and at McMurdo 

Station (77°51′S, 164°40′E) in McMurdo Sound, the southernmost extension of the Ross Sea that abuts land. The communities in these two areas differ markedly. Like at other sites 

along the northern half of the western Antarctic Peninsula, at 

Palmer Station qualitative and quantitative diving observations 

reveal that the communities are dominated by forests of large 

brown macroalgae to depths of 30–40 m or greater (Amsler et 

al., 1995; DeLaca and Lipps, 1976). The algal biomass in these 

communities rivals that in temperate kelp forests, particularly in 

the upper 20–30 m (Amsler et al., 1995). At greater depths or, 

beginning at approximately 30 m on vertical rock walls, sessile 

invertebrates dominate the benthos, including sponges, tunicates, 
number 39 • 6 1

FIGURE 3. Marine chemical ecology research in Antarctic waters. (a) Diving through a natural crack next to a small, grounded iceberg in 

McMurdo Sound (photo by C. Amsler); (b) A diver returning to the surface in a melted dive hole within a McMurdo Sound dive hut (photo 

by C. Amsler); (c) A diver collecting amphipods from macroalgae near Palmer Station (photo by B. Baker); (d) A diver collecting the sponge 

Haliclonissa verucossa near Palmer Station (photo by B. Baker).

a b

c d
6 2 • smithsonian contributions to the marine sciences

soft corals, and bryozoans (Figure 3d; C. Amsler and B. Baker, 

personal observations). At McMurdo Station, smaller red macroalgae are present at some but not most dive sites in the 2–20 

m depth range (Miller and Pearse, 1991). Otherwise, sessile, benthic organisms are sparse down to approximately 33 m depth 

due to the formation of anchor ice, which disrupts communities 

by ripping objects, including benthic organisms, from the bottom 

(Dayton et al., 1969, 1970). However, below 33 m qualitative 

and quantitative diving observations have revealed rich benthic 

invertebrate communities dominated by sponges (Dayton, 1979; 

Dayton et al., 1974).

Most current benthic marine research, including chemical ecology, at Palmer Station and other sites along the western 

Antarctic Peninsula is carried out in open water without solid 

overhead ice cover, and the equipment and techniques are very 

much like those used in colder temperate waters. Scientific diving 

in McMurdo Sound is primarily carried out through land-fast 

sea ice. Divers gain access by drilling, melting, or blasting holes 

through the ice or by diving through naturally occurring cracks 

(Figures 3a–b; Lang and Robbins, 2009). Because water visibility 

is commonly in the 100–200 m range in McMurdo Sound, USAP 

regulations do not require divers to be tethered to the surface in 

this overhead diving environment so long as the bottom is within 

the depth limits for the dive, a down-line with strobe lights and 

flags extends from the dive hole all the way to the bottom, and 

water currents are negligible (Lang and Robbins, 2009). In both 

regions, variable volume drysuits with thick undergarments are 

used for thermal protection. Water temperatures along the western Antarctic Peninsula range from approximately −1.5°C to 

+2.0°C and the water temperature in McMurdo Sound is typically −1.8°C during the diving season, so regulator freeze-up is a 

concern, particularly when temperatures are below 0°C. “Slingshot” (“Y”) or “H” valves can be used to allow a diver to mount 

two completely independent regulators on a single tank so that 

the primary regulator can be turned off if it freezes-up and freeflows, thereby allowing the diver to make a controlled ascent 

with the remaining gas. United States Antarctic Program regulations require such a valve system in overhead environments 

such as that in McMurdo Sound (Lang and Robbins, 2009), and 

these are also commonly used along the Antarctic Peninsula as 

an extra safety precaution.

At Palmer Station, a majority of the macroalgal flora is unpalatable to common sympatric animals that include algae in 

their diet (Amsler et al., 2005; Aumack et al., 2010; Huang et 

al., 2006). Overall, nearly half of the macroalgal species have 

been shown to be unpalatable because they produce chemical 

defenses, including all of the large brown macroalgae that dominate the community in terms of biomass, as well as most of the 

more common red macroalgae (Amsler et al., 2005; Aumack et 

al., 2010). Hence, on a biomass basis, well over 90% of the macroalgal flora resists herbivory using chemical defenses. A number 

of the specific secondary metabolites responsible for this bioactivity have been identified (Ankisetty et al., 2004). 

Early in these studies of macroalgal chemical ecology at 

Palmer Station, divers recognized that the dominant macroalgae 

were supporting very dense assemblages of amphipods. Subsequent quantitative diving collections of the amphipods along with 

their host algae revealed densities of 2–20 amphipods g−1 algal 

wet weight (Figure 3c; Huang et al., 2007), which when combined with algal biomass data from this community (Amsler et 

al., 1995) resulted in estimated amphipod densities ranging from 

approximately 30,000 to 300,000 amphipods m2

 of the benthos 

in solid stands of the dominant macroalgae (Amsler et al., 2008). 

These amphipods appear to benefit the macroalgae by keeping 

them relatively clean of epiphytic microalgae and filamentous 

algae, which otherwise would heavily foul them (Aumack et al., 

2011). The amphipods also benefit from the association by gaining 

a refuge from omnivorous fish predators (Zamzow et al., 2010). 

Consequently, these two numerically dominant components of 

the benthic flora and fauna appear to exist in a community-wide,

mutualistic relationship with its basis in the widespread occurrence of chemical defenses in the dominant macroalgae.

On a species-by-species basis, an even higher percentage of 

the sponge species (Figure 3d) at Palmer Station are unpalatable 

to the dominant sea star predator in the community, Odontaster 

validus. Peters et al. (2009) found that 78% of the 27 species examined were unpalatable to the sea star, and in all cases tested the 

unpalatability could be explained by the production of defensive 

metabolites. This prevalence of chemical defense against macropredators is comparable to that observed in Caribbean sponges 

(Pawlik et al., 1995). However, amphipods were deterred from 

feeding by extracts of only 2 of 12 randomly chosen demosponge 

species (Amsler et al., 2009b). With tunicates from this community, even though 100% of 12 species were unpalatable to omnivorous fish and 58% were unpalatable to sea stars, chemical 

defenses explained the unpalatability to fish in only one tunicate 

species (Koplovitz et al., 2009). Either secondary metabolites or 

low tunic pH could explain the unpalatability in five of the seven 

tunicate species unpalatable to sea stars (Koplovitz et al., 2009). 

Similar to sponges, only one of ten tunicate species’ extracts deterred amphipods from feeding (Koplovitz et al., 2009). 

In McMurdo Sound, only two species of fleshy macroalgae 

occur throughout most of the year and both are unpalatable to 

sympatric sea urchins because they produce defensive secondary metabolites (Amsler et al., 1998). Divers commonly observe 

the sea urchins covered with these chemically defended red algae 

(Amsler et al., 1999; Miller and Pearse, 1991). Laboratory studies motivated by these diving observations demonstrated that 

although the urchins do not eat the chemically defended algae, 

they preferentially chose these algae to cover themselves with 

over other available objects. The algae provide urchins with 

a physical defensive barrier against their main predators, two 

large species of sea anemones (Amsler et al., 1999). Moreover, 

the chemically defended algae benefit because the urchins hold 

large amounts of drift algae in the photic zone where they can 

still photosynthesize (Schwarz et al., 2003) and produce spores 
number 39 • 6 3

for the next algal generation (Amsler et al., 1999). Consequently, 

this is a second mutualistic relationship between Antarctic macroalgae and potential herbivores that is based on the common 

occurrence of chemical defenses in Antarctic macroalgae.

Although no comprehensive or randomized-sampling survey of the palatability of sponge species has been completed in 

McMurdo Sound, divers have observed that only relatively few 

sponge species are commonly preyed on by sea stars (Dayton et 

al., 1974; Amsler, Baker, and J. McClintock, pers. obs.). All such 

species for which chemical defenses have been examined were 

undefended (McClintock et al., 1994, 2000) while most other 

sponge species in the community have been shown to elaborate 

defensive metabolites (reviewed by Amsler et al., 2001b). Unlike at Palmer Station, divers do not observe high densities of 

amphipods associated with benthic organisms in this community 

(Amsler, Baker, McClintock, pers. obs.). Sea stars are clearly the 

dominant predators of sponges, although some nudibranchs also 

specialize on sponges (Dayton et al., 1974; Dearborn, 1977; McClintock, 1994). Unlike lower-latitude communities, there are no 

vertebrate or other important visual predators of sponges and 

they have likely been absent for millions of years (Aronson et al., 

2007). Because the sponges do not occur shallower than approximately 30 m depth, sponges are unlikely to be subjected to damaging levels of ultraviolet radiation (Karentz and Lutze, 1990). 

At lower latitudes, sponge pigmentation has been hypothesized 

to be involved in aposematism (warning coloration) (Harrison 

and Cowden, 1976; but see Pawlik et al., 1995) and photoprotection against ultraviolet radiation (Bergquist, 1978; Harrison 

and Cowden, 1976). Neither of these roles would appear to be 

of selective advantage in Antarctica, at least at locations other 

than the western Antarctic Peninsula, particularly if one assumes 

some metabolic cost to production of the pigments (McClintock 

and Baker, 1998). However, all pigments so far identified from 

Antarctic sponges have been found to have chemical defensive 

properties against potential predators, pathogens, or biofoulers 

(McClintock et al., 2005). It has been hypothesized that these 

pigments may originally have been of selective value because of 

other roles but have been maintained in Antarctic sponges because they secondarily took on defensive functions that remain 

advantageous in the modern Antarctic environment (McClintock 

et al., 2005). 

Diving observations in McMurdo Sound also revealed a 

unique symbiotic relationship in the plankton that is mediated 

by chemical defenses. Divers ascending from the benthos noticed 

a pteropod (pelagic mollusk), Clione antarctica, being carried 

on the backs of the amphipod Hyperiella dilatata (McClintock 

and Janssen, 1990). The pteropods are chemically defended from 

fish predation by the polyketide pteroenone (Bryan et al., 1995; 

Yoshida et al., 1995), whereas the amphipods are readily consumed. However, when the amphipods are carrying a captured 

pteropod, they too are rejected as food by the fish (McClintock 

and Janssen, 1990). This is likely detrimental for the pteropods, 

which apparently are unable to feed while being carried by the 

amphipods, and this relationship has been referred to as an “antagonistic symbiosis” by McClintock and Baker (1997). Dead 

pteropods were never detected being carried in situ by amphipods, suggesting that they are periodically released and replaced 

with a fresh individual (McClintock, pers. obs.). 

CONCLUSIONS

Scuba diving and other undersea exploration technologies 

have played a fundamental role in the birth and development 

of both marine natural products research and marine chemical 

ecology. Again, the purpose of this contribution has not been 

to exhaustively review marine chemical ecology, but rather to 

provide insight into the development of this scientific subdiscipline in response to the rise of undersea technologies. Research 

boundaries continue to be expanded, with increasing reliance on 

scuba diving using nitrox mixtures for safer dives and longer bottom times, and mixed-gas technical diving to reach even greater 

depths (Lesser et al., 2009). Moreover, researchers interested in 

marine chemical ecology are now using scuba for field studies 

around the world, including in the North Sea (Toth and Pavia, 

2002), Mediterranean (Tarjuelo et al., 2002; Becerro et al., 2003; 

Haber et al., 2011; Noyer et al., 2011), Red Sea (Ilan, 1995; Kelman et al., 2000; Burns et al., 2003), mid-Atlantic (Ruzicka and 

Gleason, 2009), and temperate South Pacific (Wright et al., 2000; 

Duckworth and Battershill, 2001). This discipline is only a few 

decades old, and vast undersea habitats remain poorly studied 

in terms of the chemical defenses and signals involved in their 

ecology, particularly the open-water plankton, the meiofauna 

and infauna of sandy and muddy benthic habitats, and the deepsea benthos, including hydrothermal vent and seep communities. 

Perhaps new undersea technologies will expand ecological and 

chemical studies to these habitats as well.

ACKNOWLEDGMENTS

J. R. Pawlik thanks the National Science Foundation (NSF) 

for long-term support for his work on the chemical ecology of 

sponges and other invertebrates (most recently through NSF 

grants OCE-0550468 and OCE-1029515) and NOAA’s Coral 

Reef Conservation Program through the NOAA-UNCW Aquarius Reef Base. C. D. Amsler, J. B. McClintock, and B. J. Baker 

also acknowledge the National Science Foundation for support 

of their research on marine chemical ecology in Antarctica for 

many years (current support from NSF grants ANT-0838773 

(CDA, JBM) and ANT-0838776 (BJB)). V. J. Paul also thanks the 

National Science Foundation and National Institutes of Health 

for years of support for research conducted on Guam. V. J. Paul 

and R. Ritson-Williams are grateful to the Smithsonian Marine 

Science Network and the Hunterdon Oceanographic Endowment at the Smithsonian Institution for current support. Current 
6 4 • smithsonian contributions to the marine sciences

funding for their chemical ecology research in Florida and the 

Caribbean has also come from NOAA’s ECOHAB program project NA05NOS4781194, Mote Marine Laboratory Protect Our 

Reefs Grants, and the United States Geological Society Eastern 

Region State Partnership Program. This is contribution #912 of 

the Smithsonian Marine Station at Fort Pierce. 

We dedicate this chapter to the memory of two pioneers in 

marine natural products chemistry, Paul J. Scheuer and D. John 

Faulkner, who collaborated with and inspired marine biologists 

and ecologists to investigate the ecological roles of marine natural products.

REFERENCES

Aceret, T. L., P. W. Sammarco, and J. C. Coll. 1995. Toxic effects of alcyonacean 

diterpenes on scleractinian corals. Journal of Experimental Marine Biology 

and Ecology, 188:63–78. http://dx.doi.org/10.1016/0022-0981(94)00186-H.

Albizati, K. F., J. R. Pawlik, and D. J. Faulkner. 1985. Limatulone, a potent defensive metabolite of the intertidal limpet Collisella limatula. Journal of Organic 

Chemistry, 50:3428–3430. http://dx.doi.org/10.1021/jo00218a044.

Albrizio, S., P. Ciminiello, E. Fattorusso, S. Magno, and J. R. Pawlik. 1995. Amphitoxin, a new high molecular weight antifeedant pyridinium salt from the 

Caribbean sponge Amphimedon compressa. Journal of Natural Products, 58: 

647–652. http://dx.doi.org/10.1021/np50119a002.

Alino, P. M., P. W. Sammarco, and J. C. Coll. 1992. Competitive strategies in soft corals (Coelenterata, Octocorallia). 4. Environmentally induced reversals in competitive superiority. Marine Ecology Progress Series, 81:129–145. http://dx

.doi.org/10.3354/meps081129.

Amsler, C. D., ed. 2008. Algal chemical ecology. Berlin: Springer-Verlag. http://dx

.doi.org/10.1007/978-3-540-74181-7.

Amsler, C. D., K. Iken, J. B. McClintock, M. O. Amsler, K. J. Peters, J. M. Hubbard, F. B. Furrow, and B. J. Baker. 2005. Comprehensive evaluation of the 

palatability and chemical defenses of subtidal macroalgae from the Antarctic 

Peninsula. Marine Ecology Progress Series, 294:141–159. http://dx.doi.org

/10.3354/meps294141.

Amsler, C. D., K. Iken, J. B. McClintock, and B. J. Baker. 2001a. Secondary metabolites from Antarctic marine organisms and their ecological implications. In 

Marine chemical ecology, ed. J. B. McClintock and B. J. Baker, pp. 267–300. 

Boca Raton, Fla.: CRC Press.

———. 2009a. Defenses of polar macroalgae against herbivores and biofoulers. 

Botanica Marina, 52:535–545.

Amsler, C. D., J. B. McClintock, and B. J. Baker. 1998. Chemical defense against herbivory in the Antarctic marine macroalgae Iridaea cordata and Phyllophora 

antarctica (Rhodophyceae). Journal of Phycology, 34:53–59. http://dx.doi.org

/10.1046/j.1529-8817.1998.340053.x.

———. 1999. An antarctic feeding triangle: defensive interactions between macroalgae, sea urchins, and sea anemones. Marine Ecology Progress Series, 183: 

105–114. http://dx.doi.org/10.3354/meps183105.

———. 2000. Chemical defenses of antarctic marine organisms: A reevaluation of 

the latitudinal hypothesis. In Antarctic ecosystems: Models for wider ecological understanding, ed. W. Davison, C. Howard-Williams, and P. Broady, pp. 

158–164. Proceedings of the Seventh SCAR International Biology Symposium. Christchurch: New Zealand Natural Sciences.

———. 2001b. Secondary metabolites as mediators of trophic interactions among 

antarctic marine organisms. American Zoologist, 41:17–26. http://dx.doi.org

/10.1668/0003-1569(2001)041[0017:SMAMOT]2.0.CO;2.

———. 2008. Macroalgal chemical defenses in polar marine communities. In Algal chemical ecology, ed. C. D. Amsler, pp. 91–103. Berlin: Springer-Verlag. 

http://dx.doi.org/10.1007/978-3-540-74181-7.

Amsler, C. D., R. J. Rowley, D. R. Laur, L. B. Quetin, and R. M. Ross. 1995. Vertical distribution of Antarctic Peninsular macroalgae: Cover, biomass, and species composition. Phycologia, 34:424–430. http://dx.doi.org/10.2216/i0031

-8884-34-5-424.1.

Amsler, M. O., J. B. McClintock, C. D. Amsler, R. A. Angus, and B. J. Baker. 

2009b. An evaluation of sponge-associated amphipods from the Antarctic 

Peninsula. Antarctic Science, 21:579–589. http://dx.doi.org/10.1017/S0954

102009990356.

Ankisetty, S., S. Nandiraju, H. Win, Y. C. Park, C. D. Amsler, J. B. McClintock, J. A.

Baker, T. K. Diyabalanage, A. Pasaribu, M. P. Singh, W. M. Maiese, R. D. 

Walsh, M. J. Zaworotko, and B. J. Baker. 2004. Chemical investigation of 

predator-deterred macroalgae from the Antarctic Peninsula. Journal of Experimental Marine Biology and Ecology, 67:1295–1302.

Aronson, R. B., S. Thatje, A. Clarke, L. S. Peck, D. B. Blake, C. D. Wilga, and B. A.

Seibel. 2007. Climate change and invasability of the Antarctic benthos. Annual Review of Ecology and Systematics, 38:129–154. http://dx.doi.org/10

.1146/annurev.ecolsys.38.091206.095525.

Assmann, M., E. Lichte, J. R. Pawlik, and M. Kock. 2000. Chemical defenses of the 

Caribbean sponges Agelas wiedenmayeri and Agelas conifera. Marine Ecology Progress Series, 207:255–262. http://dx.doi.org/10.3354/meps207255.

Aumack, C. F., C. D. Amsler, J. B. McClintock, and B. J. Baker. 2010. Chemically 

mediated resistance to mesoherbivory in finely branched macroalgae along 

the western Antarctic Peninsula. European Journal of Phycology, 45:19–26. 

http://dx.doi.org/10.1080/09670260903171668.

———. 2011. Impacts of mesograzers on epiphyte and endophyte growth associated with chemically defended macroalgae from the western Antarctic Peninsula: A mesocosm experiment. Journal of Phycology, 47:36–41. http://dx.doi

.org/10.1111/j.1529-8817.2010.00927.x.

Avila, C., and V. J. Paul. 1997. Chemical ecology of the nudibranch Glossodoris 

pallida: Is the location of diet-derived metabolites important for defense? Marine Ecology Progress Series, 150:171–180. http://dx.doi.org/10.3354/meps

150171.

Avila, C., S. Taboada, and L. Núñez-Pons. 2008. Antarctic marine chemical ecology: 

What is next? Marine Ecology, 29:1–71. http://dx.doi.org/10.1111/j.1439

-0485.2007.00215.x.

Bakus, G. J. 1981. Chemical defense mechanisms on the Great Barrier Reef, Australia. Science, 211:497–499. http://dx.doi.org/10.1126/science.7455691.

Bakus, G. J., and G. Green. 1974. Toxicity in sponges and holothurians: A geographic pattern. Science, 185:951–953. http://dx.doi.org/10.1126/science.

185.4155.951.

Becerro, M. A., V. Bonito, and V. J. Paul. 2006. Effects of monsoon-driven wave 

action on coral reefs on Guam and implications for coral recruitment. Coral 

Reefs, 25:193–199. http://dx.doi.org/10.1007/s00338-005-0080-7.

Becerro, M. A., G. Goetz, V. Paul, and P. Scheuer. 2001. Chemical defenses of 

the sacoglossan mollusk Elysia rufescens and its host alga Bryopsis sp. 

Journal of Chemical Ecology, 27:2287–2299. http://dx.doi.org/10.1023/A

:1012287105923.

Becerro, M. A., V. J. Paul, and J. Starmer. 1998. Intracolonial variation in chemical 

defenses of the sponge Cacospongia sp. and its consequences on generalist fish 

predators and the specialist nudibranch predator Glossodoris pallida. Marine Ecology Progress Series, 168:187–196. http://dx.doi.org/10.3354/meps

168187.

Becerro, M. A., R. W. Thacker, X. Turon, M. J. Uriz, and V. J. Paul. 2003. Biogeography of sponge chemical ecology: Comparisons of tropical and temperate 

defenses. Oecologia, 135:91–101.

Bergquist, P. R. 1978. Sponges. London: Hutchinson.

Blunt, J. W., B. R. Copp, M. H. G. Munro, P. T. Northcote, and M. R. Prinsep. 2011. 

Marine natural products. Natural Product Reports, 28:196–268. http://dx

.doi.org/10.1039/c005001f.

Bryan, P. J., W. Y. Yoshida, J. B. McClintock, and B. J. Baker. 1995. An ecological role for pteroenone, a novel antifeedant produced by the conspicuous 

Antarctic pteropod Clione antarctica (Gymnosomata: Gastropoda). Marine 

Biology, 122:271–278.

Bullard, S. G., and M. E. Hay. 2002. Plankton tethering to assess spatial patterns of 

predation risk over a coral reef and seagrass bed. Marine Ecology Progress 

Series, 225:17–28. http://dx.doi.org/10.3354/meps225017.

Burkepile, D. E., and M. E. Hay. 2008. Herbivore species richness and feeding 

complementarity affect community structure and function on a coral reef. 

Proceedings of the National Academy of Sciences of the United States of 

America, 105:16201–16206. http://dx.doi.org/10.1073/pnas.0801946105.

———. 2010. Impact of herbivore identity on algal succession and coral growth on 

a Caribbean Reef. PLoS ONE, 5(1):e8963. http://dx.doi.org/10.1371/journal

.pone.0008963n.

Burns, E., I. Ifrach, S. Carmeli, J. R. Pawlik, and M. Ilan. 2003. Comparison of antipredatory defenses of Red Sea and Caribbean sponges. I. Chemical defense. Marine Ecology Progress Series, 252:105–114. http://dx.doi.org/10.3354/meps

252105.
number 39 • 6 5

Chanas, B., and J. R. Pawlik. 1995. Defenses of Caribbean sponges against predatory 

reef fish. 2. Spicules, tissue toughness, and nutritional quality. Marine Ecology 

Progress Series, 127:195–211. http://dx.doi.org/10.3354/meps127195.

———. 1996. Does the skeleton of a sponge provide a defense against predatory 

reef fish? Oecologia, 107:225–231. http://dx.doi.org/10.1007/BF00327906.

Coll, J. C., S. Labarre, P. W. Sammarco, W. T. Williams, and G. J. Bakus. 1982. 

Chemical defenses in soft corals (Coelenterata, Octocorallia) of the Great 

Barrier Reef: A study of comparative toxicities. Marine Ecology Progress Series, 8:271–278. http://dx.doi.org/10.3354/meps008271.

Dayton, P. 1979. Observations of growth, dispersal and population dynamics of 

some sponges in McMurdo Sound, Antarctica. In Sponge biology, Vol. 291, 

ed. C. Levi and N. Boury-Esnault, pp. 271–282. Paris: Centre National de la 

Recherche Scientifique (C.N.R.S.).

Dayton, P., G. Robilliard, and A. DeVries. 1969. Anchor ice formation in McMurdo 

Sound, Antarctica, and its biological effects. Science, 163:273–275. http://dx

.doi.org/10.1126/science.163.3864.273.

Dayton, P. K., G. A. Robilliard, and R. T. Paine. 1970. Benthic faunal zonation as a 

result of anchor ice at McMurdo Sound, Antarctica. In Antarctic ecology, Vol. 

1, ed. M. W. Holgate, pp. 244–258. London: Academic Press.

Dayton, P. K., G. A. Robilliard, R. T. Paine, and L. B. Dayton. 1974. Biological 

accommodation in the benthic community at McMurdo Sound, Antarctica. 

Ecological Monographs, 44:105–128. http://dx.doi.org/10.2307/1942321.

De Nys, R., P. D. Steinberg, C. N. Rogers, T. S. Charlton, and M. W. Duncan. 1996. 

Quantitative variation of secondary metabolite in the sea hare Aplysia parvula and its host plant Delisea pulchra. Marine Ecology Progress Series, 130: 

135–146. http://dx.doi.org/10.3354/meps130135.

Dearborn, J. H. 1977. Foods and feeding characteristics of Antarctic asteroids and 

ophiuroids. In Adaptations within Antarctic ecosystems, ed. G. A. Llano, pp. 

293–326. Proceedings of the Third SCAR Symposium on Antarctic Biology. 

Washington, D.C.: Smithsonian Institution.

DeLaca, T. E., and J. H. Lipps. 1976. Shallow water marine associations, Antarctic 

Peninsula. Antarctic Journal of the United States, 11:12–20.

Duckworth, A. R., and C. N. Battershill. 2001. Population dynamics and chemical 

ecology of New Zealand demospongiae Latrunculia sp. nov. and Polymastia 

croceus (Poecilosclerida: Latrunculiidae: Polymastiidae). New Zealand Journal of Marine and Freshwater Research, 35:935–949. http://dx.doi.org/10

.1080/00288330.2001.9517055.

Duffy, J. E., and M. E. Hay. 2001. Ecology and evolution of marine consumer–prey 

interactions. In Marine community ecology, ed. M. Bertness, M. E. Hay, and 

S. D. Gaines, pp. 131–157. Sunderland, Mass.: Sinauer Associates, Inc.

Duffy, J. E., and V. J. Paul. 1992. Prey nutritional quality and the effectiveness of 

chemical defenses against tropical reef fishes. Oecologia, 90:333–339. http://

dx.doi.org/10.1007/BF00317689.

Dunlap, M., and J. R. Pawlik. 1996. Video monitored predation by Caribbean reef 

fishes on an array of mangrove and reef sponges. Marine Biology, 126:117–

123. http://dx.doi.org/10.1007/BF00571383.

———. 1998. Spongivory by parrotfish in Florida mangrove and reef habitats. 

Marine Ecology, 19:325–337. http://dx.doi.org/10.1111/j.1439-0485.1998.tb

00471.x.

Dworjanyn, S. A., R. de Nys, and P. D. Steinberg. 2006. Chemically mediated antifouling in the red alga Delisea pulchra. Marine Ecology Progress Series, 318: 

153–163. http://dx.doi.org/10.3354/meps318153.

Engel, S., and J. R. Pawlik. 2000. Allelopathic activities of sponge extracts. Marine 

Ecology Progress Series, 207:273–281. http://dx.doi.org/10.3354/meps207273.

Engel, S., M. P. Puglisi, P. R. Jensen, and W. Fenical. 2006. Antimicrobial activities of 

extracts from tropical Atlantic marine plants against marine pathogens and 

saprophytes. Marine Biology, 149:991–1002. http://dx.doi.org/10.1007/s

00227-006-0264-x.

Faulkner, D. J., and W. H. Fenical, eds. 1977. Marine natural products chemistry. 

New York: Plenum Press. http://dx.doi.org/10.1007/978-1-4684-0802-7.

Flahive, E., and J. Srirangam. 2005. The dolastatins: Novel antitumor agents from 

Dolabella auricularia. In Anticancer agents from natural products, ed. G. M. 

Cragg, D. G. I. Kingston, and D. J. Newman, pp. 191–214. Boca Raton, Fla.: 

Taylor and Francis. http://dx.doi.org/10.1201/9781420039658.ch11.

Fusetani, N. 2004. Biofouling and antifouling. Natural Product Reports, 21:94–

104. http://dx.doi.org/10.1039/b302231p.

———. 2011. Antifouling marine natural products. Natural Product Reports, 28: 

400–410. http://dx.doi.org/10.1039/c0np00034e.

Gerhart, D. J. 1984. Prostaglandin A2: An agent of chemical defense in the Caribbean gorgonian Plexaura homomalla. Marine Ecology Progress Series, 19: 

181–187. http://dx.doi.org/10.3354/meps019181.

Ginsburg, D. W., and V. J. Paul. 2001. Chemical defenses in the sea hare Aplysia

parvula: Importance of diet and sequestration of algal secondary metabolites. 

Marine Ecology Progress Series, 215:216–274. http://dx.doi.org/10.3354

/meps215261.

Haber, M., M. Carbone, E. Mollo, M. Gavagnin, and M. Ilan. 2011. Chemical 

defense against predators and bacterial fouling in the Mediterranean sponges 

Axinella polypoides and A. verrucosa. Marine Ecology Progress Series, 422: 

113–122. http://dx.doi.org/10.3354/meps08921.

Harrison, F. W., and R. R. Cowden. 1976. Aspects of sponge biology. New York: 

Academic Press.

Harvell, C. D., and W. Fenical. 1989. Chemical and structural defenses of Caribbean 

gorgonians (Pseudopterogorgia spp.): Intracolony localization of defense. 

Limnology and Oceanography, 34:382–389. http://dx.doi.org/10.4319/lo

.1989.34.2.0382.

Harvell, C. D., W. Fenical, and C. H. Greene. 1988. Chemical and structural defenses of Caribbean gorgonians (Pseudopterogorgia spp.) 1. Development of 

an in situ feeding assay. Marine Ecology Progress Series, 49:287–294. http://

dx.doi.org/10.3354/meps049287.

Hay, M. E. 1997. The ecology and evolution of seaweed-herbivore interactions on 

coral reefs. Proceedings of the eighth International Coral Reef Symposium, 

1:23–32.

———. 2009. Marine chemical ecology: Chemical signals and cues structure marine 

populations, communities, and ecosystems. Annual Review of Marine Science, 1:193–212. http://dx.doi.org/10.1146/annurev.marine.010908.163708.

Hay, M. E., J. E. Duffy, W. Fenical, and K. Gustafson. 1988a. Chemical defense 

in the seaweed Dictyopteris delicatula: Differential effects against reef fishes 

and amphipods. Marine Ecology Progress Series, 48:185–192. http://dx.doi

.org/10.3354/meps048185.

Hay, M. E., J. E. Duffy, V. J. Paul, P. E. Renaud, and W. Fenical. 1990. Specialist herbivores reduce their susceptibility to predation by feeding on the chemically 

defended seaweed Avrainvillea longicaulis. Limnology and Oceanography, 

35:1734–1743. http://dx.doi.org/10.4319/lo.1990.35.8.1734.

Hay, M. E., and W. Fenical. 1988. Marine plant-herbivore interactions: The ecology 

of chemical defense. Annual Review of Ecology and Systematics,19:111–145. 

http://dx.doi.org/10.1146/annurev.es.19.110188.000551.

Hay, M. E., W. Fenical, and K. Gustafson. 1987. Chemical defense against diverse coral reef herbivores. Ecology, 68:1581–1591. http://dx.doi.org/10

.2307/1939850.

Hay, M. E., V. J. Paul, S. M. Lewis, K. Gustafson, J. Tucker, and R. N. Trindell. 

1988b. Can tropical seaweeds reduce herbivory by growing at night? Diel 

patterns of growth, nitrogen-content, herbivory and chemical versus morphological defenses. Oecologia, 75:233–245. http://dx.doi.org/10.1007/BF

00378604.

Hay, M. E., P. E. Renaud, and W. Fenical. 1988c. Large mobile versus small sedentary herbivores and their resistance to seaweed chemical defenses. Oecologia, 

75:246–252. http://dx.doi.org/10.1007/BF00378605.

Hay, M. E., J. J. Stachowicz, E. Cruz-Rivera, S. Bullard, M. S. Deal, and N. Lindquist. 

1998. Bioassays with marine and freshwater macroorganisms. In Methods in 

chemical ecology, Volume 2: Bioassay methods, ed. K. F. Haynes and J. G. 

Millar, pp. 39–141. New York: Chapman and Hall.

Hay, M. E., and P. D. Steinberg. 1992. The chemical ecology of plant-herbivore 

interactions in marine versus terrestrial communities. In Herbivores: Their interaction with secondary metabolites, evolutionary and ecological processes, 

ed. J. Rosenthal and M. Berenbaum, pp. 371–413. San Diego: Academic 

Press. http://dx.doi.org/10.1016/B978-0-08-092545-5.50015-8.

Huang, Y. M., A. O. Amsler, J. B. McClintock, C. D. Amsler, and B. J. Baker. 2007. 

Patterns of gammarid amphipod abundance and species composition associated with dominant subtidal macroalgae along the western Antarctic Peninsula. Polar Biology, 30:1417–1430. http://dx.doi.org/10.1007/s00300-007

-0303-1.

Huang, Y. M., J. B. McClintock, C. D. Amsler, K. J. Peters, and B. J. Baker. 2006. 

Feeding rates of common Antarctic gammarid amphipods on ecologically important sympatric macroalgae. Journal of Experimental Marine Biology and 

Ecology, 329:55–65. http://dx.doi.org/10.1016/j.jembe.2005.08.013.

Ilan, M. 1995. Reproductive biology, taxonomy, and aspects of the chemical ecology of Latrunculidae (Porifera). Biological Bulletin, 188:306–312. http://dx

.doi.org/10.2307/1542307.

Jackson, J. B. C., and L. Buss. 1975. Allelopathy and spatial competition among 

coral reef invertebrates. Proceedings of the National Academy of Sciences 

of the United States of America, 72:5160–5163. http://dx.doi.org/10.1073

/pnas.72.12.5160.
6 6 • smithsonian contributions to the marine sciences

Jones, A. C., J. E. Blum, and J. R. Pawlik. 2005. Testing for defensive synergy in 

Caribbean sponges: Bad taste or glass spicules? Journal of Experimental 

Marine Biology and Ecology, 322:67–81. http://dx.doi.org/10.1016/j.jembe

.2005.02.009.

Karentz, D., and L. H. Lutze. 1990. Evaluation of biologically harmful ultraviolet radiation in Antarctica with a biological dosimeter designed for aquatic 

environments. Limnology and Oceanography, 35:549–561. http://dx.doi.org

/10.4319/lo.1990.35.3.0549.

Karuso, P. 1987. Chemical ecology of the nudibranchs. In Bioorganic marine chemistry, Vol. 1, ed. P. J. Scheuer, pp. 31–60. Berlin: Springer-Verlag. http://dx.doi

.org/10.1007/978-3-642-72726-9_2.

Kelly, S. R., E. Garo, P. R. Jensen, W. Fenical, and J. R. Pawlik. 2005. Effects of Caribbean sponge secondary metabolites on bacterial surface colonization. Aquatic 

Microbial Ecology, 40:191–203. http://dx.doi.org/10.3354/ame040191.

Kelman, D.,Y. Benayahu, and Y. Kashman. 2000. Variation in secondary metabolite 

concentrations in yellow and grey morphs of the Red Sea soft coral Parerythropodium fulvum fulvum: Possible ecological implications. Journal of Chemical Ecology, 26:1123–1133. http://dx.doi.org/10.1023/A:1005423708904.

Kicklighter, C. E., and M. E. Hay. 2006. Integrating prey defensive traits: Contrasts 

of marine worms from temperate and tropical habitats. Ecological Monographs, 76:195–215. http://dx.doi.org/10.1890/0012-9615(2006)076[0195

:IPDTCO]2.0.CO;2.

———. 2007. To avoid or deter: Interactions among defensive and escape strategies in sabellid worms. Oecologia, 151:161–173. http://dx.doi.org/10.1007/s

00442-006-0567-0.

Kicklighter, C. E., J. Kubanek, T. Barsby, and M .E. Hay. 2003. Palatability and defense of some tropical infaunal worms: Alkylpyrrole sulfamates as deterrents 

to fish feeding. Marine Ecology Progress Series, 263:299–306. http://dx.doi

.org/10.3354/meps263299.

Koplovitz, G., J. B. McClintock, C. D. Amsler, and B. J. Baker. 2009. Palatability 

and chemical anti-predatory defenses in common ascidians from the Antarctic Peninsula. Aquatic Biology, 7:81–92. http://dx.doi.org/10.3354/ab00188.

Kubanek, J., W. Fenical, and J. R. Pawlik. 2001. New antifeedant triterpene glycosides from the Caribbean sponge Erylus formosus. Natural Products Letters,

15:275–285. http://dx.doi.org/10.1080/10575630108041292.

Kubanek, J., P. R. Jensen, R. A. Keifer, M. C. Sullards, D. O. Collins, and W. Fenical. 

2003. Seaweed resistance to microbial attack: A targeted chemical defense 

against marine fungi. Proceedings of the National Academy of Sciences of the 

United States of America, 100:6919–6921. http://dx.doi.org/10.1073/pnas

.1131855100.

Kubanek, J., K. E. Whalen, S. Engel, S. R. Kelly, T. P. Henkel, W. Fenical, and J. R.

Pawlik. 2002. Multiple defensive roles for triterpene glycosides from two 

Caribbean sponges. Oecologia, 131:125–136. http://dx.doi.org/10.1007/s

00442-001-0853-9.

Kuffner, I. B., L. J. Walters, M. A. Becerro, V. J. Paul, R. Ritson-Williams, and K. S. 

Beach. 2006. Inhibition of coral recruitment by macroalgae and cyanobacteria. Marine Ecology Progress Series, 323:107–117. http://dx.doi.org/10.3354

/meps323107.

Labarre, S. C., J. C. Coll, and P. W. Sammarco. 1986. Competitive strategies of soft 

corals (Coelenterata, Octocorallia). 3. Spacing and aggressive interactions 

between alcyonaceans. Marine Ecology Progress Series, 28:147–156. http://

dx.doi.org/10.3354/meps028147.

Lane, A. L., and J. Kubanek. 2008. Secondary metabolite defenses against pathogens and biofoulers. In Algal chemical ecology, ed. C. D. Amsler, pp. 229–243.

Berlin: Springer-Verlag. http://dx.doi.org/10.1007/978-3-540-74181-7_11.

Lane, A. L., L. Nyadong, A. S. Galhena, T. L. Shearer, E. P. Stout, R. M. Parry, 

M. Kwasnik, M. D. Wang, M. E. Hay, F. M. Fernandez, and J. Kubanek. 

2009. Desorption electrospray ionization mass spectrometry reveals surfacemediated antifungal chemical defense of a tropical seaweed. Proceedings of 

the National Academy of Sciences of the United States of America, 106:7314–

7319. http://dx.doi.org/10.1073/pnas.0812020106.

Lang, M. A., and R. Robbins. 2009. Scientific diving under ice: A 40-year bipolar 

research tool. In Smithsonian at the poles: Contributions to International 

Polar Year science, ed. I. Krupnik, M. A. Lang, and S. E. Miller, pp. 241–252. 

Washington, D.C.: Smithsonian Institution Scholarly Press. http://dx.doi.org

/10.5479/si.097884601X.17.

Lebar, M. L., J. L. Heimbegner, and B. J. Baker. 2007. Cold-water marine natural 

products. Natural Product Reports, 24:774–797. http://dx.doi.org/10.1039

/b516240h.

Leong, W., and J. R. Pawlik. 2010. Evidence of a resource trade-off between growth 

and chemical defenses among Caribbean coral reef sponges. Marine Ecology 

Progress Series, 406:71–78. http://dx.doi.org/10.3354/meps08541.

Lesser, M. P., M. Slattery, and J. J. Leichter. 2009. Ecology of mesophotic coral reefs. 

Journal of Experimental Marine Biology and Ecology, 375:1–8. http://dx.doi

.org/10.1016/j.jembe.2009.05.009.

Lindel, T., H. Hoffmann, M. Hochgurtel, and J. R. Pawlik. 2000. Structure-activity 

relationship of inhibition of fish feeding by sponge-derived and synthetic 

pyrrole-imidazole alkaloids. Journal of Chemical Ecology, 26:1477–1496. 

http://dx.doi.org/10.1023/A:1005591826613.

Lindquist, N., and M. E. Hay. 1996. Palatability and chemical defense of marine invertebrate larvae. Ecological Monographs, 66:431–450. http://dx.doi.org/10

.2307/2963489.

Luesch, H., G. G. Harrigan, G. Goetz, and F. D. Horgen. 2002. The cyanobacterial origin of potent anticancer agents originally isolated from sea hares. 

Current Medicinal Chemistry, 9:1791–1806. http://dx.doi.org/10.2174

/0929867023369051.

Maida, M., P. W. Sammarco, and J. C. Coll. 1995. Preliminary evidence for directional allelopathic effects of the soft coral Sinularia flexibilis (Alcyonaria, 

Octocorallia) on scleractinian coral recruitment. Bulletin of Marine Science, 

56:303–311.

———. 2006. A diffusion chamber for assessing efficacy of natural anti-fouling 

defenses in marine organisms. Journal of Experimental Marine Biology and 

Ecology, 337:59–64. http://dx.doi.org/10.1016/j.jembe.2006.06.008.

Maliao, R. J., R. G. Turingan, and J. Lin. 2008. Phase-shift in coral reef communities 

in the Florida Keys National Marine Sanctuary (FKNMS), USA. Marine Biology, 154:841–853. http://dx.doi.org/10.1007/s00227-008-0977-0.

MarinLit. 2011. MarinLit: A Marine Literature Database. http://www.chem.canter

bury.ac.nz/marinlit/marinlit.shtml.

Mayer, A. M. S., K. B. Glaser, C. Cuevas, R. S. Jacobs, W. Kem, R. D. Little, J. M. 

McIntosh, D. J. Newman, B. C. Potts, and D. E. Shuster. 2010. The odyssey of 

marine pharmaceuticals: A current pipeline perspective. Trends in Pharmacological Sciences, 31:255–265. http://dx.doi.org/10.1016/j.tips.2010.02.005.

Mayer, A. M. S., A. D. Rodriguez, R. G. S. Berlinck, and N. Fusetani. 2011. Marine 

pharmacology in 2007–8: Marine compounds with antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiprotozoal, antituberculosis, and antiviral activities: Affecting the immune and nervous system, and 

other miscellaneous mechanisms of action. Comparative Biochemistry and 

Physiology, Part C, 153:191–222.

McClintock, J. B. 1994. Trophic biology of Antarctic echinoderms. Marine Ecology 

Progress Series, 111:191–202. http://dx.doi.org/10.3354/meps111191.

McClintock, J. B., C. D. Amsler, and B. J. Baker. 2010. Overview of the chemical 

ecology of benthic marine invertebrates along the western Antarctic Peninsula. Integrative and Comparative Biology, 50:967–980. http://dx.doi.org/10

.1093/icb/icq035.

McClintock, J. B., C. D. Amsler, B. J. Baker, and R. W. M. van Soest. 2005. Ecology 

of Antarctic marine sponges: An overview. Integrative and Comparative Biology, 45:359–368. http://dx.doi.org/10.1093/icb/45.2.359.

McClintock, J. B., and B. J. Baker. 1997. A review of the chemical ecology of shallowwater Antarctic marine invertebrates. American Zoologist, 37:329–342.

———. 1998. Chemical ecology in Antarctic seas. American Scientist, 86:254–263.

———, eds. 2001. Marine chemical ecology. Boca Raton, Fla.: CRC Press.

McClintock, J. B., B. J. Baker, C. D. Amsler, and T. L. Barlow. 2000. Chemotactic 

tube-foot responses of the spongivorous sea star Perknaster fuscus to organic 

extracts of sponges from McMurdo Sound, Antarctica. Antarctic Science, 12: 

41–46. http://dx.doi.org/10.1017/S0954102000000067.

McClintock, J. B., B. J. Baker, M. Slattery, M. Hamann, R. Koptizke, and J. Heine. 

1994. Chemotactic tube-foot responses of a spongivorous sea star Perknaster 

fuscus to organic extracts from Antarctic sponges. Journal of Chemical Ecology, 20:859–870. http://dx.doi.org/10.1007/BF02059583.

McClintock, J. B., and J. Janssen. 1990. Pteropod abduction as a chemical defense in a pelagic Antarctic amphipod. Nature, 346:424–426. http://dx.doi

.org/10.1038/346462a0.

McMurray, S. E., T. P. Henkel, and J. R. Pawlik. 2010. Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida 

Keys. Ecology, 91:560–570. http://dx.doi.org/10.1890/08-2060.1.

Meyer, K. D., and V. J. Paul. 1992. Intraplant variation in secondary metabolite 

concentration in three species of Caulerpa (Chlorophyta: Caulerpales) and its 

effects on herbivorous fishes. Marine Ecology Progress Series, 82:249–257. 

http://dx.doi.org/10.3354/meps082249.

Miller, K. A., and J. S. Pearse. 1991. Ecological studies of seaweeds in McMurdo 

Sound, Antarctica. American Zoologist, 31:35–48.

Molinski, T. F., D. S. Dalisay, S. L. Lievens, and J. P. Saludes. 2009. Drug development from marine natural products. Nature Reviews Drug Discovery, 8:69–

85. http://dx.doi.org/10.1038/nrd2487.
number 39 • 6 7

Morrow, K. M., V. J. Paul, M. R. Liles, and N. Chadwick. 2011. Allelochemicals 

produced by Caribbean macroalgae and cyanobacteria have species-specific 

effects on reef coral microorganisms. Coral Reefs, 30:309–320. http://dx.doi

.org/10.1007/s00338-011-0747-1.

Nagle, D. G., and V. J. Paul. 1998. Chemical defense of a marine cyanobacterial 

bloom. Journal of Experimental Marine Biology and Ecology, 225:29–38. 

http://dx.doi.org/10.1016/S0022-0981(97)00205-0.

———. 1999. Production of secondary metabolites by filamentous tropical marine 

cyanobacteria: Ecological functions of the compounds. Journal of Phycology, 

35:1412–1421. http://dx.doi.org/10.1046/j.1529-8817.1999.3561412.x.

Neushul, M. 1959. Biological collecting in Antarctic waters. Veliger, 2:15–17.

———. 1961. Diving in Antarctic waters. Polar Record, 10:353–358. http://dx.doi

.org/10.1017/S0032247400051470.

———. 1965. Diving observation of sub-tidal Antarctic marine vegetation. Botanica Marina, 8:234–243.

———. 1968. Benthic marine algae. Antarctic Map Folio Series, 10:9–10, plates 

14–15.

Newbold, R. W., P. R. Jensen, W. Fenical, and J. R. Pawlik. 1999. Antimicrobial activity of Caribbean sponge extracts. Aquatic Microbial Ecology, 19:279–284. 

http://dx.doi.org/10.3354/ame019279.

Newman, D., and G. Cragg. 2004. Marine natural products and related compounds 

in clinical and advanced preclinical trials. Journal of Experimental Marine 

Biology and Ecology, 67:1216–1238.

Noyer, C., O. P. Thomas, and M. A. Becerro. 2011. Patterns of chemical diversity in 

the Mediterranean sponge Spongia lamella. PLoS ONE, 6(11):e20844. http://

dx.doi.org/10.1371/journal.pone.0020844.

O’Neal, W., and J. R. Pawlik. 2002. A reappraisal of the chemical and physical defenses of Caribbean gorgonian corals against predatory fishes. Marine Ecology Progress Series, 240:117–126. http://dx.doi.org/10.3354/meps240117.

Paul, V. J., ed. 1992. Ecological roles of marine natural products. Ithaca, N.Y.: 

Comstock Publishing Associates.

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. http://dx.doi.org/10.2307/25066642.

Paul, V. J., E. Cruz-Rivera, and R. W. Thacker. 2001. Chemical mediation of 

macroalgal-herbivore interactions: Ecological and evolutionary perspectives.

In Marine chemical ecology, ed. J. B. McClintock and B. J. Baker, pp. 227–

266. Boca Raton, Fla.: CRC Press.

Paul, V. J., and W. Fenical. 1983. Isolation of halimedatrial: Chemical defense adaptation in the calcareous reef-building alga Halimeda. Science, 221:747–749. 

http://dx.doi.org/10.1126/science.221.4612.747.

———. 1986. Chemical defense in tropical green algae, order Caulerpales. Marine Ecology Progress Series, 34:157–169. http://dx.doi.org/10.3354/meps

034157.

Paul, V. J., and M. E. Hay. 1986. Seaweed susceptibility to herbivory: Chemical 

and morphological correlates. Marine Ecology Progress Series, 33:255–264. 

http://dx.doi.org/10.3354/meps033255.

Paul, V. J., M. E. Hay, J. E. Duffy, W. Fenical, and K. Gustafson. 1987. Chemical 

defense in the seaweed Ochtodes secundiramea (Montagne) Howe (Rhodophyta): Effects of its monoterpenoid components upon diverse coral reef 

herbivores. Journal of Experimental Marine Biology and Ecology, 114:249–

260. http://dx.doi.org/10.1016/0022-0981(88)90141-4.

Paul, V. J., I. B. Kuffner, L. J. Walters, R. Ritson-Williams, K. S. Beach, and M. A.

Becerro. 2011a. Chemically mediated interactions between macroalgae 

Dictyota spp. and multiple life-history stages of the coral Porites astreoides. 

Marine Ecology Progress Series, 426:161–170. http://dx.doi.org/10.3354

/meps09032.

Paul, V. J., S. Nelson, and H. Sanger. 1990. Feeding preferences of adult and juvenile 

rabbitfish Siganus argenteus in relation to chemical defenses of tropical seaweeds. Marine Ecology Progress Series, 60:23–34. http://dx.doi.org/10.3354

/meps060023.

Paul, V. J., and S. C. Pennings. 1991. Diet-derived chemical defenses in the sea hare 

Stylocheilus longicauda (Quoy and Gaimard 1824). Journal of Experimental 

Marine Biology and Ecology, 15:227–243. http://dx.doi.org/10.1016/0022

-0981(91)90126-H.

Paul, V. J., and M. P. Puglisi. 2004. Chemical mediation of interactions among 

marine organisms. Natural Product Reports, 21:189–209. http://dx.doi.org

/10.1039/b302334f.

Paul, V. J., M. P. Puglisi, and R. Ritson-Williams. 2006. Marine chemical ecology. 

Natural Product Reports, 23:153–180. http://dx.doi.org/10.1039/b404735b.

Paul, V. J., and R. Ritson-Williams. 2008. Marine chemical ecology. Natural Product Reports, 25:662–695. http://dx.doi.org/10.1039/b702742g.

Paul, V. J., R. Ritson-Williams, and K. Sharp. 2011b. Marine chemical ecology in benthic environments. Natural Product Reports, 28:345–387. http://dx.doi.org

/10.1039/c0np00040j.

Paul, V. J., R. Thacker, K. Banks, and S. Golubic. 2005. Benthic cyanobacterial 

bloom impacts the reefs of South Florida (Broward County, USA). Coral 

Reefs, 24:693–697. http://dx.doi.org/10.1007/s00338-005-0061-x.

Paul, V. J., and K. L. Van Alstyne. 1988. Use of ingested algal diterpenoids by Elysia 

halimedae Macnae (Opisthobranchia: Ascoglossa) as antipredator defenses. 

Journal of Experimental Marine Biology and Ecology, 119:15–29. http://dx

.doi.org/10.1016/0022-0981(88)90149-9.

———. 1992. Activation of chemical defenses in the tropical green algae Halimeda

spp. Journal of Experimental Marine Biology and Ecology, 60:191–203.

Pawlik, J. R. 1997. Fish predation on Caribbean reef sponges: An emerging perspective of chemical defenses. Proceedings of the eighth International Coral Reef 

Symposium, 2:1255–1258.

———. 2011. The chemical ecology of sponges on Caribbean reefs: Natural 

products shape natural systems. Bioscience, 61:888–898. http://dx.doi.org

/10.1525/bio.2011.61.11.8.

Pawlik, J. R., K. F. Albizati, and D. J. Faulkner. 1986. Evidence of a defensive role 

for limatulone, a novel triterpene from the intertidal limpet Collisella limatula. Marine Ecology Progress Series, 30:251–260. http://dx.doi.org/10.3354

/meps030251.

Pawlik, J. R., M. T. Burch, and W. Fenical. 1987. Patterns of chemical defense among 

Caribbean gorgonian corals: A preliminary survey. Journal of Experimental 

Marine Biology and Ecology, 108:55–66. http://dx.doi.org/10.1016/0022

-0981(87)90130-4.

Pawlik, J. R., B. Chanas, R. J. Toonen, and W. Fenical. 1995. Defenses of Caribbean 

sponges against predatory reef fish. 1. Chemical deterrency. Marine Ecology 

Progress Series, 127:183–194. http://dx.doi.org/10.3354/meps127183.

Pawlik, J. R., and W. Fenical. 1989. A re-evaluation of the ichthyodeterrent role of

prostaglandins in the Caribbean gorgonian coral Plexaura homomalla. Marine 

Ecology Progress Series, 52:95–98. http://dx.doi.org/10.3354/meps052095.

Pawlik, J. R., T. P. Henkel, S. E. McMurray, S. Lopez-Legentil, T. L. Loh, and 

S. Rohde. 2008. Patterns of sponge recruitment and growth on a shipwreck 

corroborate chemical defense resource trade-off. Marine Ecology Progress 

Series, 368:137–143. http://dx.doi.org/10.3354/meps07615.

Pawlik, J. R., M. R. Kernan, T. F. Molinski, M. K. Harper, and D. J. Faulkner. 1988. 

Defensive chemicals of the Spanish dancer nudibranch Hexabranchus sanguineus and its egg ribbons: Macrolides derived from a sponge diet. Journal 

of Experimental Marine Biology and Ecology, 119:99–109. http://dx.doi

.org/10.1016/0022-0981(88)90225-0.

Pawlik, J. R., G. McFall, and S. Zea. 2002. Does the odor from sponges of the 

genus Ircinia protect them from fish predators? Journal of Chemical Ecology,

28:1103–1115. http://dx.doi.org/10.1023/A:1016221415028.

Pawlik, J. R., L. Steindler, T. P. Henkel, S. Beer, and M. Ilan. 2007. Chemical warfare on coral reefs: Sponge metabolites differentially affect coral symbiosis in 

situ. Limnology and Oceanography, 52:907–911. http://dx.doi.org/10.4319

/lo.2007.52.2.0907.

Pennings, S. C., S. Nastisch, and V. J. Paul. 2001. Vulnerability of the sea hare Stylocheilus striatus to fish predators: Importance of diet and fish species. Coral 

Reefs, 20:320–324. http://dx.doi.org/10.1007/s003380100178.

Pennings, S. C., S. R. Pablo, and V. J. Paul. 1997. Chemical defenses of the tropical 

benthic marine cyanobacterium Hormothamnion enteromorphoides: Diverse 

consumers and synergisms. Limnology and Oceanography, 42:911–917. 

http://dx.doi.org/10.4319/lo.1997.42.5.0911.

Pennings, S. C., and V. J. Paul. 1993. Sequestration of dietary secondary metabolites 

by three species of sea hares: Location, specificity and dynamics. Marine Biology, 117:535–546. http://dx.doi.org/10.1007/BF00349763.

Pennings, S. C., V. J. Paul, D. C. Dunbar, M. T. Hamann, W. A. Lumbang, B. Novack, 

and R. S. Jacobs. 1999. Unpalatable compounds in the marine gastropod 

Dolabella auricularia: Distribution and effect of diet. Journal of Chemical 

Ecology, 25:735–755. http://dx.doi.org/10.1023/A:1020832414766.

Pennings, S. C., A. M. Weiss, and V. J. Paul. 1996. Secondary metabolites of the 

cyanobacterium Microcoleus lyngbyaceus and the sea hare Stylocheilus longicauda: Palatability and toxicity. Marine Biology, 126:735–743. http://dx.doi

.org/10.1007/BF00351340.

Peters, K. J., C. D. Amsler, J. B. McClintock, R. W. M. van Soest, and B. J. Baker. 

2009. Palatability and chemical defenses of sponges from the western Antarctic Peninsula. Marine Ecology Progress Series, 385:77–85. http://dx.doi

.org/10.3354/meps08026.

Puglisi, M. P., S. Engel, P. R. Jensen, and W. Fenical. 2007. Antimicrobial activities of extracts from Indo-Pacific marine plants against marine pathogens 
6 8 • smithsonian contributions to the marine sciences

and saprophytes. Marine Biology, 150:531–540. http://dx.doi.org/10.1007/

s00227-006-0376-3.

Puglisi, M. P., and V. J. Paul. 1997. Intraspecific variation in secondary metabolite 

production in the red alga Portieria hornemannii: Monoterpene concentrations are not influenced by nitrogen and phosphorus enrichment. Marine Biology, 128:161–170. http://dx.doi.org/10.1007/s002270050079.

Puglisi, M. P., V. J. Paul, J. Biggs, and M. Slattery. 2002. The co-occurrence of chemical and structural defenses in the gorgonian corals of Guam. Marine Ecology 

Progress Series, 239:105–114. http://dx.doi.org/10.3354/meps239105.

Puglisi, M. P., V. J. Paul, and M. Slattery. 2000. Biogeographic comparisons of chemical and structural defenses of the Pacific gorgonians Annella mollis and Annella reticulata. Marine Ecology Progress Series, 207:263–272. http://dx.doi

.org/10.3354/meps207263.

Randall, J. E., and W. D. Hartman. 1968. Sponge-feeding fishes of the West Indies. 

Marine Biology, 1:216–225. http://dx.doi.org/10.1007/BF00347115.

Rasher, D. B., and M. E. Hay. 2010. Chemically rich seaweeds poison corals when 

not controlled by herbivores. Proceedings of the National Academy of Sciences of the United States of America, 107:9683–9688. http://dx.doi.org

/10.1073/pnas.0912095107.

Rasher, D. B., E. P. Stout, S. Engel, J. Kubanek, and M. E. Hay. 2011. Macroalgal 

terpenes function as allelopathic agents against reef corals. Proceedings of the 

National Academy of Sciences of the United States of America, 108:17726–

17731. http://dx.doi.org/10.1073/pnas.1108628108.

Ritson-Williams, R., and V. J. Paul. 2007. Marine benthic invertebrates use multimodal cues for defense against reef fish. Marine Ecology Progress Series, 340: 

29–39. http://dx.doi.org/10.3354/meps340029.

Ritson-Williams, R., M. Yoshi-Yamashita, and V. J. Paul. 2006. Ecological functions 

of tetrodotoxin in a deadly polyclad flatworm. Proceedings of the National 

Academy of Sciences of the United States of America, 103:3176–3179. http://

dx.doi.org/10.1073/pnas.0506093103.

Ruzicka, R., and D. F. Gleason. 2009. Sponge community structure and antipredator defenses on temperate reefs of the South Atlantic Bight. Journal of 

Experimental Marine Biology and Ecology, 380:36–46. http://dx.doi.org/10

.1016/j.jembe.2009.08.011.

Sato, M., M. Sagawa, T. Nakazato, Y. Ikeda, and M. Kizaki. 2007. A natural peptide, dolastatin 15, induces G2/M cell cycle arrest and apoptosis of human 

multiple myeloma cells. International Journal of Oncology, 30:1453–1459.

Scheuer, P. J., ed. 1978–1983. Marine natural products: Chemical and biological 

perspectives. Volumes 1–5. New York: Academic Press.

———. 1990. Some marine ecological phenomena: Chemical basis and biomedical 

potential. Science, 248:173–177. http://dx.doi.org/10.1126/science.2183350.

Schulte, B. A., and G. J. Bakus. 1992. Predation deterrence in marine sponges: Laboratory versus field studies. Bulletin of Marine Science, 50:205–211.

Schupp, P. J., and V. J. Paul. 1994. Calcification and secondary metabolites in tropical seaweeds: Variable effects on herbivorous fishes. Ecology, 75:1172–1185. 

http://dx.doi.org/10.2307/1939440.

Schwarz, A. M., I. Hawes, N. Andrew, A. Norkko, V. Cummings, and S. Thrush. 

2003. Macroalgal photosynthesis near the southern global limit for growth; 

Cape Evans, Ross Sea, Antarctica. Polar Biology, 26:789–799. http://dx.doi

.org/10.1007/s00300-003-0556-2.

Slattery, M. 1999. Fungal pathogenesis of the sea fan Gorgonia ventalina: Direct 

and indirect consequences. Chemoecology, 9:97–104. http://dx.doi.org/10

.1007/s000490050039.

Slattery, M., G. A. Hines, J. Starmer, and V. J. Paul. 1999. Chemical signals in 

gametogenesis, spawning, and larval settlement and defense of the soft coral 

Sinularia polydactyla. Coral Reefs, 18:75–84. http://dx.doi.org/10.1007/s00

3380050158.

Slattery, M., H. N. Kamel, S. Ankisetty, D. J. Gochfeld, C. A. Hoover, and R. W. 

Thacker. 2008. Hybrid vigor in a tropical Pacific soft-coral community. Ecological Monographs, 78:423–443. http://dx.doi.org/10.1890/07-1339.1.

Slattery, M., and V. J. Paul. 2008. Indirect effects of bleaching on predator deterrence in the tropical Pacific soft coral Sinularia maxima. Marine Ecology 

Progress Series, 354:169–179. http://dx.doi.org/10.3354/meps07200.

Slattery, M., J. Starmer, and V. J. Paul. 2001. Temporal and spatial variation in 

defensive metabolites of the tropical Pacific soft corals Sinularia maxima and 

S. polydactyla. Marine Biology, 138:1183–1193. http://dx.doi.org/10.1007

/s002270100540.

Stachowicz, J. J. 2001. Chemical ecology of mobile benthic invertebrates: Predators 

and prey, allies and competitors. In Marine chemical ecology, ed. J. B. McClintock and B. J. Baker, pp. 157–194. Boca Raton, Fla.: CRC Press. http://

dx.doi.org/10.1201/9781420036602.sec2.

Stachowicz, J. J., and M. E. Hay. 2000. Geographic variation in camouflage specialization by a decorator crab. American Naturalist, 156:59–71. http://dx.doi

.org/10.1086/303366.

Stachowicz, J. J., and N. Lindquist. 1997. Chemical defense among hydroids on 

pelagic Sargassum: Predator deterrence and absorption of solar UV radiation 

by secondary metabolites. Marine Ecology Progress Series, 155:115–126. 

http://dx.doi.org/10.3354/meps155115.

Steinberg, P. D., and V. J. Paul. 1990. Fish feeding and chemical defenses of tropical 

brown algae in Western Australia. Marine Ecology Progress Series, 58:253–

259. http://dx.doi.org/10.3354/meps058253.

Tan, L. T. 2010. Filamentous tropical marine cyanobacteria: A rich source of natural products for anticancer drug discovery. Journal of Applied Phycology, 22: 

659–676. http://dx.doi.org/10.1007/s10811-010-9506-x.

Tarjuelo, I., S. Lopez-Legentil, M. Codina, and X. Turon. 2002. Defence mechanisms of adults and larvae of colonial ascidians: Patterns of palatability and 

toxicity. Marine Ecology Progress Series, 235:103–115. http://dx.doi.org/10

.3354/meps235103.

Thacker, R. W., M. A. Becerro, W. A. Lumbang, and V. J. Paul. 1998. Allelopathic 

interactions between sponges on a tropical reef. Ecology, 79:1740–1750. 

http://dx.doi.org/10.1890/0012-9658(1998)079[1740:AIBSOA]2.0.CO;2.

Thacker, R. W., D. W. Ginsburg, and V. J. Paul. 2001. Effects of herbivore exclusion 

and nutrient enrichment on coral reef macroalgae and cyanobacteria. Coral 

Reefs, 19:318–329. http://dx.doi.org/10.1007/s003380000122.

Thacker, R. W., D. G. Nagle, and V. J. Paul. 1997. Effects of repeated exposures to 

marine cyanobacterial secondary metabolites on feeding by juvenile rabbitfish and parrotfish. Marine Ecology Progress Series, 147:21–29. http://dx.doi

.org/10.3354/meps147021.

Thompson, J. E. 1985. Exudation of biologically-active metabolites in the sponge 

Aplysina fistularis. 1. Biological evidence. Marine Biology, 88:23–26. http://

dx.doi.org/10.1007/BF00393039.

Toth, G. B., and H. Pavia. 2002. Intraplant habitat and feeding preference of two 

gastropod herbivores inhabiting the kelp Laminaria hyperborea. Journal 

of the Marine Biological Association of the United Kingdom, 82:243–247. 

http://dx.doi.org/10.1017/S0025315402005416.

Van Alstyne, K. L., M. N. Dethier, and D. O. Duggins. 2001. Spatial patterns in macroalgal chemical defenses. In Marine chemical ecology, ed. J. B. McClintock 

and B. J. Baker, pp. 301–324. Boca Raton, Fla.: CRC Press. 

Van Alstyne, K. L., and V. J. Paul. 1990. The biogeography of polyphenolic compounds in marine macroalgae: Temperate brown algal defenses deter feeding 

by tropical herbivorous fishes. Oecologia, 84:158–163.

———. 1992. Chemical and structural defenses in the sea fan Gorgonia ventalina: 

Effects against generalist and specialist predators. Coral Reefs, 11:155–159. 

http://dx.doi.org/10.1007/BF00255470.

Van Alstyne, K. L., C. R. Wylie, and V. J. Paul. 1994. Antipredator defenses in tropical Pacific soft corals (Coelenterata: Alcyonacea). II. The relative importance 

of chemical and structural defenses in three species of Sinularia. Journal of 

Experimental Marine Biology and Ecology, 178:17–34. http://dx.doi.org/10

.1016/0022-0981(94)90222-4.

Villa, F. A., and L. Gerwick. 2010. Marine natural product drug discovery: Leads 

for treatment of inflammation, cancer, infections, and neurological disorders. 

Immunopharmacology and Immunotoxicology, 32:228–237. http://dx.doi

.org/10.3109/08923970903296136.

Waddell, B., and J. R. Pawlik. 2000a. Defenses of Caribbean sponges against invertebrate predators. I. Assays with hermit crabs. Marine Ecology Progress 

Series, 195:125–132. http://dx.doi.org/10.3354/meps195125.

———. 2000b. Defenses of Caribbean sponges against invertebrate predators. II. 

Assays with sea stars. Marine Ecology Progress Series, 195:133–144. http://

dx.doi.org/10.3354/meps195133.

Walker, R. P., J. E. Thompson, and D. J. Faulkner. 1985. Exudation of biologicallyactive metabolites in the sponge Aplysina fistularis. 2. Chemical evidence. 

Marine Biology, 88:27–32. http://dx.doi.org/10.1007/BF00393040.

Walters, K. D., and J. R. Pawlik. 2005. Is there a trade-off between wound-healing 

and chemical defenses among Caribbean reef sponges? Integrative Comparative Biology, 45:352–358. http://dx.doi.org/10.1093/icb/45.2.352.

Watkinson, A. J., J. M. O’Neil, and W. C. Dennison. 2005. Ecophysiology of the marine 

cyanobacterium, Lyngbya majuscula (Oscillatoriaceae) in Moreton Bay, Australia. Harmful Algae, 4:697–715. http://dx.doi.org/10.1016/j.hal.2004.09.001.

Wilson, D. M., M. Puyana, W. Fenical, and J. R. Pawlik. 1999. Chemical defense 

of the Caribbean reef sponge Axinella corrugata against predatory fishes. 

Journal of Chemical Ecology, 25:2811–2823. http://dx.doi.org/10.1023/A

:1020811810223.
number 39 • 6 9

Wright, J. T., R. de Nys, A. G. B. Poore, and P. D. Steinberg. 2004. Chemical defense 

in a marine alga: Heritability and the potential for selection by herbivores. 

Ecology, 85:2946–2959. http://dx.doi.org/10.1890/03-4041.

Wright, J. T., R. de Nys, and P. D. Steinberg. 2000. Geographic variation in halogenated furanones from the red alga Delisea pulchra and associated herbivores 

and epiphytes. Marine Ecology Progress Series, 207:227–241. http://dx.doi

.org/10.3354/meps207227.

Wylie, C. R., and V. J. Paul. 1989. Chemical defenses in three species of Sinularia

(Coelenterata, Alcyonacea): Effects against generalist predators and the 

butterflyfish Chaetodon unimaculatus Bloch (Perciformes). Journal of Experimental Marine Biology and Ecology, 129:141–160. http://dx.doi.org/10

.1016/0022-0981(89)90053-1.

Yoshida, W. Y., P. J. Bryan, B. J. Baker, and J. B. McClintock. 1995. Pteroenone: 

A defensive metabolite of the abducted Antarctic pteropod Clione antarctica. Journal of Organic Chemistry, 60:780–782. http://dx.doi.org/10.1021

/jo00108a057.

Zamzow, J. P., C. D. Amsler, J. B. McClintock, and B. J. Baker. 2010. Habitat choice 

and predator avoidance by Antarctic amphipods: The roles of algal chemistry and morphology. Marine Ecology Progress Series, 400:155–163. http://

dx.doi.org/10.3354/meps08399.

Zimmer, R. K., and R. P. Ferrer. 2007. Neuroecology, chemical defense and the 

keystone species concept. Biological Bulletin, 213:208–225. http://dx.doi

.org/10.2307/25066641.

Scuba Diving in Blue Water: 

A Window on Ecology and 

Evolution in the Epipelagic Ocean

Laurence P. Madin, William M. Hamner, Steven H. D. Haddock, 

and George I. Matsumoto

ABSTRACT. Conventional methods of zooplankton sampling have serious limitations for the study 

of soft-bodied gelatinous animals, which are easily damaged or destroyed in nets and trawls. An 

alternative approach is scuba diving in the upper waters of the open ocean to make observations, 

measurements, and collections in situ. With appropriate safety measures, this method has proved 

highly effective in revealing natural behavior of a variety of animals, as well as in allowing collection 

of live specimens for experimental work or detailed taxonomic examination. Simple precautions and 

protocols have allowed blue-water diving to be conducted safely and productively for the last 40 

years. It has provided insight into both the biology of individual species and the structure and functioning of epipelagic communities in tropical, temperate, and polar oceans. It has further revealed 

the occurrence and effects of nonliving material like marine snow, as well as the microstructure 

created by density layers and convergences. The direct experience of the water column environment 

that blue-water diving can provide is a valuable key to understanding the lives of its inhabitants.

INTRODUCTION

The study of zooplankton has been based historically on the results of pulling nets 

of various configurations through the water column and taking what was collected as 

representative of the zooplankton community. It is obvious, though frequently ignored, 

that different nets capture different categories of organisms depending on their mouth 

diameter, mesh size, bridle configuration, and towing speed. Crustaceans are usually well 

represented in net samples, along with other small- to medium-sized animals with hard 

bodies and slow swimming speeds. Trawls with very large mouth openings and coarse 

mesh size capture faster and larger epipelagic animals, such as fish and squid. Other 

sampling devices, like Niskin bottles, retrieve an intact water sample with everything in 

it, and in principle provide a comprehensive picture of all planktonic organisms present. 

But the necessarily small sample size of a water bottle (typically 1–30 L) with its small 

opening (centimeters in diameter) makes it unlikely to catch anything that is rare or large, 

or that would avoid a bottle moving through the water on a wire. With nets or water 

samplers, it is possible to get a fairly representative sample of small organisms ranging 

from microbes, phytoplankton, and protozoa up through the smaller crustaceans and 

other mesozooplankton. What is typically missing from these samples are alert, fastswimming animals like euphausiid and decapod crustaceans, squid, and fish, and also the 

Laurence P. Madin, Woods Hole Oceanographic 

Institution, 266 Woods Hole Road, Woods Hole, 

Massachusetts 02543, USA. William M. Hamner, University of California, Los Angeles, Department of Ecology and Evolutionary Biology, Box 

951606, Los Angeles, California 90095-1606,

USA. Steven H. D. Haddock and George I. 

Matsumoto, Monterey Bay Aquarium Research 

Institute, 7700 Sandholdt Road, Moss Landing, California 95039, USA. Correspondence:

L. Madin, lmadin@whoi.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
7 2 • smithsonian contributions to the marine sciences

gelatinous animals that are often sparsely distributed, relatively 

large and fragile, and usually damaged or destroyed by plankton 

nets and trawls.

Many oceanographers and marine biologists unfortunately 

still think of the upper water column of the open ocean as a 

biological desert, a misconception related to the fact that most 

epipelagic zooplankton are effectively invisible, either transparent or too small to be seen. Nonetheless, net zooplankton are always present in blue, seemingly empty surface waters. One need 

only tow a net for five to ten minutes to collect a valid sample 

of net zooplankton, but short net tows grossly undersample rare 

species, and small-diameter nets underestimate the abundance of 

larger taxa, most of which are gelatinous and transparent. As 

blue-water diving research has shown, epipelagic waters contain 

a rich spectrum of larger gelatinous zooplankton that is rarely 

represented in net collections.

BLUE-WATER SCUBA DIVING

We know now that many aspects of animal biology are best 

understood by observing undisturbed animals in the environments where they live and evolve. Terrestrial biologists are not 

constrained physiologically from conducting most field investigations, but comparable field studies of undisturbed oceanic animals are surprisingly recent because humans are not adapted for 

underwater work. William Beebe used hard-hat surface-supplied

air to observe fish and zooplankton under water in 1926 (Beebe, 

1926), and he later used a bathysphere a half-mile down (Beebe,

1935) to observe midwater fish and invertebrates. Although the 

aqualung was invented in 1943, publications about underwater 

behavior of fish did not appear until the 1960s (Randall and Randall, 1960; Hobson, 1963, 1965). Use of scuba to investigate demersal fish and invertebrates is now routine (see other chapters 

herein), with long-term in situ investigations possible under water

day after day at the exact same site, often on the same individual 

organisms. In the open sea, however, one cannot return day after 

day to investigate the same individuals or population of pelagic 

animals because zooplankton drift and pelagic fishes swim away. 

According to Haddock (2004:553), “With the exception of pioneers like Bieri (1966) and Ceccaldi (1972), few people attempted 

to observe plankton in their natural environment before Hamner 

and students pioneered the technique of blue-water scuba diving

(Hamner, 1975; Hamner et al., 1975).” Subsequently, many biologists have spent thousands of hours using scuba in blue water 

to observe undisturbed, mostly gelatinous animals in their own 

environment. It is important to emphasize that our review of discoveries about epipelagic animals via use of scuba since 1972 is 

concerned with only those creatures that are found routinely in 

the upper 40 m of the water column. Many gelatinous animals 

occur also in much deeper water where they have been investigated via bathysphere, research submersible, and remotely operated vehicles (ROVs) (Beebe, 1935; Nishizawa et al., 1954; Mills 

et al., 1996; Johnsen, 2001; Haddock, 2004; Robison, 2004).

Blue-water scuba diving was formalized during a research 

program in 1971–1972 in the Florida Current near Bimini in 

the Bahamas (Hamner, 1974; Hamner et al., 1975). Although 

primarily a scuba-oriented exercise, the work also included sampling of zooplankton with 30-cm-diameter nets every month 

for 15 months. Specimens of only the most common gelatinous 

species were captured with nets, although gelatinous animals 

were clearly present in the water column because they were 

observed almost every day by scuba divers. Ctenophores were 

often strained through the mesh of the net or damaged almost 

beyond recognition. Other gelatinous taxa, delicate but also fastswimming, actively avoided nets. For example, the pseudothecosome mollusks Gleba, Corolla, and Cymbulia are especially 

sensitive to turbulence. They are vulnerable to predators when 

feeding motionless with mucus structures, and they swim away 

rapidly when disturbed by the bridle of a plankton net (Gilmer, 

1972). Planktonic mollusks sometimes even evade capture by 

divers and it is not surprising that they had not been collected 

previously in large numbers (Gilmer, 1974). However, given 

good visibility, a group of divers can examine thousands of cubic 

meters during a dive, locating individuals of many of the larger 

gelatinous animals within that volume. 

The gelatinous zooplankton studied via scuba in the Florida Current were, at that time, poorly known taxa such as 

foraminifera, radiolarians, hydromedusae, siphonophores, scyphomedusae, ctenophores, heteropods, pteropods, salps, and appendicularians (Hamner et al., 1975). Most of these gelatinous 

zooplankton have evolved convergent attributes: they are all 

mostly transparent, delicate, relatively large (>1 cm), neutrally 

buoyant, slow-swimming, tactile, and nonvisual. Most do not 

react to scuba divers unless physically disturbed, enabling scuba 

divers to observe undisturbed, undamaged specimens from all 

these taxonomic groups at very close range in the upper sunlit 

regions of tropical seas. Though many gelatinous taxa are transparent and hard to see against a uniform blue background, there 

are ways to enhance their contrast by looking at them from certain angles relative to down-welling sunlight and, with practice, 

divers sometimes can spot and identify species from meters away. 

Like birdwatchers who recognize a species from a flash of color 

or movement, experienced blue-water divers can often identify 

animals by their characteristic swimming attitudes or motions or 

a gestalt impression, even without a clear, close-up view. 

Plankton nets and trawls damage or destroy gelatinous zooplankton, so scuba divers collect individual, undamaged animals 

by hand in wide-mouthed jars for subsequent identification and 

laboratory study. Oceanic zooplankton live in the water column 

away from the sea floor, rarely encounter the seabed or shallow 

reefs, and have not evolved behavioral responses for avoiding 

rigid surfaces. In standard rectangular laboratory aquaria, therefore, these animals often sink to the bottom and become trapped 

in the corners, or are embolized by air bubbles. Some taxa can 

be cultured or maintained in the laboratory via use of circular 

planktonkreisels (Hamner, 1990) or other taxon-specific aquaria 

(Raskoff et al., 2003), but it is difficult to know how much 
number 39 • 7 3

physical confinement alters their behavior. Blue-water diving is 

without question the best way to learn how undisturbed pelagic 

animals behave naturally (Hamner, 1985; Haddock, 2004).

Different sampling procedures can mislead, but they can also 

corroborate and confirm the nature of biodiversity in a marine 

community. Thus, in a study of the western Mediterranean Sea 

(Mills et al., 1996), use of scuba in blue water generated a list of 

gelatinous organisms that was as rich in species as the taxa collected with the Johnson Sea Link submersible, yet few of these species are ever present in plankton tows in the same waters. Many 

new gelatinous species are yet to be described; some, such as the 

ctenophores Tinerfe cyanea (Chun, 1889) and Deiopea kaloktenota (Chun, 1879), not seen since the nineteenth century, were 

recently “rediscovered” in the Mediterranean by blue-water divers.

Studies of bio-optical properties of open-ocean animals have 

benefitted greatly from blue-water collections by scuba divers.

Blue-water collections of individual, undamaged, hand-collected 

specimens are especially critical for studies of physiology and 

bioluminescence. A series of recent papers has cataloged the 

distribution and physical properties of transparency of scubacollected specimens (e.g., Johnsen and Widder, 1998, 1999, 

2001; Johnsen, 2001). Examinations of bio-optical properties of 

these species have included luminescence spectra (Haddock and 

Case, 1999) and the discovery and cloning of a green-fluorescent 

protein from a ctenophore (Haddock et al., 2010).

LOGISTICS AND SAFETY AT SEA

Blue-water divers are neutrally buoyant in a featureless open 

sea. There are no landmarks for orientation, the sea floor is far 

below and out of sight, and it is possible to become disoriented 

and drift too far from other divers or descend too deep. To avoid 

these potential hazards and ensure the safety and productivity 

of blue-water diving, simple operational procedures for use of 

scuba at sea have been employed (Hamner, 1975; Haddock and 

Heine, 2005). 

Blue-water divers usually work at sea from a small boat 

launched from a mother ship or driven offshore from a marine 

lab. At the research location, the divers tie a surface float to the 

boat with a 10 m line. A weighted (1–2 kg) 30–40 m down-line 

with a small trapeze is suspended from the surface float. One 

person acts as a safety diver and stays close to the trapeze, which 

is a central hub for organizing the divers’ lines. Lightly weighted 

10 m safety lines (tethers) slide up and down through clips on 

the trapeze, and each diver attaches the free end of a tether to 

his or her buoyancy vest. With tethers attached to the trapeze, 

the divers descend, moving the trapeze to the desired working 

depth, where they are then free to search for animals within a 10 

m radius from the down-line without danger of drifting away or 

going too deep.

Blue-water dives typically last from 30 to 60 minutes. Maximum dive depths depend on the certification levels of the divers 

but rarely exceed 40 m (130 ft), with dive time dependent on 

water temperature, the depth at which the divers work, and how 

hard they swim. Usually no-decompression diving is practiced,

with mandatory safety stops as the divers ascend. As with other 

types of scuba diving, dive computers help determine dive parameters. Enriched air nitrox gas has been used, and GPS technology 

allows divers to make accurate records of their dive location and 

drift rate when landmarks are not available. Specialized bluewater diving methods have been adapted for use at night and 

also for operations under Antarctic ice (Hamner, 1982).

TROPICAL AND TEMPORATE 

EPIPELAGIC ECOLOGY

Physical Characteristics of a Liquid

Three-­Dimensional World

The waters of the world’s oceans are the largest known living 

space in the solar system: at over 1.37 billion km3

 and extending to an average depth of 3.7 km, they comprise 98% of all 

the water on Earth. The open ocean stretches from the surface 

to the bottom—a vast, three-dimensional, fluid environment that 

presents some extreme challenges for all inhabitants. The organisms that occupy this vast space are among the most numerous of 

Earth’s creatures but also some of the most unfamiliar to us landdwellers; they are sometimes called “aliens from inner space.” 

This liquid environment has permitted the evolution of organisms 

quite unlike any terrestrial species, which are restricted by gravity to life primarily in two dimensions. Blue-water diving allows

humans to briefly experience what life in the upper waters of the 

largest biome of Earth is like, enhancing our understanding of 

the open ocean environment and the daily lives of its inhabitants.

The liquid, three-dimensional nature of the water column is 

perhaps its most significant difference from terrestrial environments. Reduced gravity has allowed for the evolution of the largest animal on Earth, the blue whale, and gelatinous zooplankton 

with bizarre shapes and without rigid support structures. Pelagic 

organisms are released from the physical constraints imposed by 

gravity on terrestrial animals, swimming or floating neutrally 

buoyant in the ocean. The opportunity to observe the beauty and 

grace of gelatinous invertebrates is a splendid reward for those 

scientists fortunate enough to have dived in blue water.

The water column is divided by subtle yet important vertical 

gradients and discontinuities that affect the distribution, behavior, and life histories of the organisms that inhabit it. Temperature is an important structuring gradient in the open ocean. In 

the blue water of the tropics and subtropics, heating from the 

sun often creates a thin, very warm layer of water just below 

the surface, which can be a unique habitat for small animals like 

radiolarians, ctenophores, and calycophoran siphonophores. An 

upper, mixed layer of uniform temperature is usually bounded 

by a lower thermocline where temperature changes several degrees over a few meters or less. This sharp boundary creates 

a density difference, or pycnocline, that often is within diving 
7 4 • smithsonian contributions to the marine sciences

range. Organisms sensitive to the temperature difference may 

be restricted to above or below the thermocline. Food particles, 

grazers, and their predators often accumulate at the pycnocline 

between lighter and denser water masses (Hamner et al., 1987). 

Particulates like marine snow and clumps of inorganic and organic materials are also sometimes trapped within density layers. 

Sometimes multiple layers of water with different densities can 

occur within the top tens of meters, creating a layer-cake structure that sorts organisms according to size, density, and behavior. 

These discontinuities can be visible to divers, whether through 

a difference in refractive index, which is seen as a shimmering 

or hazy layer, or through the presence of dense phytoplankton 

layers that visually indicate the subsurface chlorophyll maximum, which is typically measured by oceanographers through 

its fluorescence. 

A second pervasive gradient throughout the water column 

is hydrostatic pressure. The monotonic increase in pressure with 

depth is almost certainly of ecological significance to organisms 

in the water column and may be an important sensory cue regulating depth distributions and diel or ontogenetic migrations, 

but little is known about mechanisms of pressure sensitivity in 

zooplankton.

Light is strongest at the surface and the photosynthetic zone 

typically extends to about 200 m. However, some light penetrates 

to about 1,000 m at intensities that allow animals to detect the 

difference between day and night. This mesopelagic zone is home 

to a wide variety of predatory and scavenging animals, most of 

them bioluminescent, and with many that make daily vertical migrations. At night in the open ocean the gradients of temperature, 

density, and pressure remain, but light is gone and the composition and activity of the biological community in the epipelagic 

zone often change dramatically, with the arrival of diel migrators 

and an increased level of feeding. Use of scuba at night in the 

open sea has begun to provide insight into the behavior and ecology of midwater migratory animals (Graham et al., 2009).

The movement of water in the open ocean also creates horizontal as well as vertical discontinuities and boundaries. Fronts 

between water masses, such as the west wall of the Gulf Stream, 

can create distinct barriers that separate adjacent horizontal 

water masses and accumulate large and small organisms at the interface. Wind-driven down-welling structures like Langmuir cells

can also concentrate passively and actively swimming organisms, 

as can areas of shear at the boundaries between different currents 

(Rakow and Graham, 2006). The scale of these discontinuities is 

sometimes small enough to be observable by divers.

The Nature of Cover in Open Water

Recent textbooks on biological oceanography assume that 

pelagic ecosystems are controlled almost exclusively by the flow 

of materials and energy and microbial processes. Alternately, 40 

years of blue-water diving have shown us that although epipelagic communities are affected on a daily and seasonal basis by 

flows of energy and materials and by microbial processes, over 

geological time these communities have been shaped primarily 

by convergent evolution related to the attenuation and diurnal 

pattern of sunlight, an absence of cover in the open sea, and 

predation. 

Charles Elton (1939:336) noted that terrestrial animals use 

the presence of cover on land as a refuge from predators, but that 

refuge can be achieved also through the “influence of the physical qualities and behavior of the prey, such as size, speed, color, 

and quickness of sense,” as well as nocturnal behavior, camouflage, running, and flying. Thus, according to Elton (1939), there 

are a limited number of broad but nonetheless discrete categories of terrestrial animals that hide, burrow, fly, or run quickly; 

that are large, aggressive, nocturnal, small, or dangerous; or that 

aggregate for protection as in herds, flocks, and schools. All of 

these attributes are part of Elton’s (1939:334) “protective system 

of the prey.” We recognize a similar ecological taxonomy for the 

creatures of the surface of the sea (Hamner et al., 1975; Hamner, 

1995; see also Zaret, 1975, for freshwater). Epipelagic animals 

cluster due to convergent evolution into seven major oceanic assemblages based on the absence of cover at sea and the necessity 

for refuge from predators. We describe these categories of adaptation below. 

Plants on land are large and rooted in the soil, they structure the ambient light environment through foliage density and 

shade, and they provide lots of cover where animals can hide 

from predators. In the epipelagic ocean, however, the primary 

producers are phytoplankton, single-celled algae. Phytoplankton 

cannot provide cover for oceanic animals because they are too 

small, and in the water column there are no rocks beneath which 

animals can hide nor soils into which they can burrow. In the 

epipelagic zone light is attenuated primarily by the absorption 

spectrum of water rather than by shade from the primary producers. In the open ocean, quite simply, there is no place to hide 

from predators.

In the absence of cover, species interactions are governed 

dramatically by predators, as we learned for ourselves when our 

University of California (UC), Davis, research group began bluewater diving in Bimini, Bahamas, in 1972. As we observed and 

collected many types of gelatinous zooplankton in the surface 

waters of the Gulf Stream, suspended in clear blue water over a 

sea floor thousands of feet below, we felt vulnerable to large predators. Our first three weeks of blue-water diving were uneventful,

but then one morning a large shark suddenly appeared. None of 

the scuba divers reacted calmly, but instead everyone tried unsuccessfully to get into the boat at once. We subsequently developed 

better protocols for responding to the presence of sharks.

Just as noted by Elton (1939) for terrestrial animals, a surprisingly limited number of effective antipredatory evolutionary 

options are also available for oceanic animals. In the open sea 

there has been convergent evolution for

1. transparency: relatively large (0.5–20 cm), slow, nonvisual, 

gelatinous animals (e.g., medusae, ctenophores, siphonophores, salps, and pteropods);
number 39 • 7 5

2. small size: below visual resolution of the vertebrate eye (less 

than 0.2 mm; e.g., copepods, appendicularians, fish eggs, 

and invertebrate larvae);

3. schooling behavior: individuals identical in size and color 

(2–20 cm, fast and silvery) in schools (e.g., clupeid fishes, 

small squid, and krill);

4. nekton: fast swimming, large size(20 cm–20 m), and aggressive (e.g., tuna, billfish, sharks, penguins, and seals and other 

mammals);

5. vertical diurnal migration: relatively fast swimmers, micronekton, intermediate in size (2–10 cm; e.g., euphausiids, 

midwater fish, and squid);

6. neuston: sea-surface dwellers (e.g., Physalia and Velella); and

7. “cheaters”: 20–200 cm, slow, conspicuous, armored or 

tricky (e.g., turtles, Mola mola, remoras, and flying fish).

The epipelagic ocean is therefore a rich mixture of transparent zooplankton, microplankton, schooling species, nekton, 

vertical diurnal migrators, and neuston, but transparent gelatinous animals are by far the easiest group of animals for bluewater divers to study because humans are poorly designed to 

keep pace with faster swimming animals. Many taxa of relatively large, slow, gelatinous invertebrates are almost always 

present in blue water near the sea surface. They are protected 

from fast-swimming predators during the day because most visual predators cannot see them. Blue-water scuba divers can see 

these creatures by hovering in place, focusing for close-up vision,

and looking upward to enhance side- and back-lighting of the 

organisms against the sea surface. Excellent vision is required to 

collect effectively in blue-water research. Since many gelatinous 

zooplankton are unrelated genetically, it is certain that tissue 

transparency is a highly selected feature and has evolved quite 

independently in many taxonomic groups via convergent evolution. In the future, we anticipate that additional cladograms 

similar to that constructed by Johnsen (2001) for tissue transparency will demonstrate that epipelagic transparent animals also 

have converged evolutionarily for relatively large body size, slow 

swimming speeds, and reduction of sense organs. 

Food Resources and Trophic Structures

In situ scuba observations of feeding behavior and mechanisms have provided many new insights into how epipelagic 

animals obtain food. Some animals such as thecosome and 

pseudothecosome pteropods (Gilmer, 1972, 1974) and some 

medusae, siphonophores, and ctenophores (Swanberg, 1974; 

Harbison et al., 1978; Matsumoto and Hamner, 1988; Haddock, 

2007) can be observed only in situ because they do not behave 

normally in captivity. Even animals that can be used in lab experiments, such as salps and some medusae and ctenophores, give 

the best results when collected by divers (Madin, 1974; Hamner 

et al., 1975 [for prey selection and avoidance], 1987 [for ctenophores]; Matsumoto and Harbison, 1993; Madin and Deibel, 

1998). Information on the potentially important role that the 

“jelly web” might play in oceanic trophic structure was provided 

by Robison (2004) and Condon et al. (2011). It should be noted 

that both laboratory and in situ observations are often required 

to determine the full suite of feeding behavior. There are behaviors observed in the field that are not typically seen in the laboratory, and if actually observed in the laboratory, they could not 

have been understood without corroborative field evidence (e.g., 

foraging behavior); but there also are behaviors observed in the 

laboratory that are never or infrequently observed in open sea. 

Recent advances in technology have elicited some very detailed 

water flow mechanics used for feeding both in the field (Dabiri et 

al., 2005) and in the laboratory (Colin et al., 2010).

Our observations of epipelagic gelatinous zooplankton 

using blue-water scuba in the Florida Current and the Gulf of 

California showed us three trophic levels: grazer-herbivores,

primary carnivores, and secondary carnivores (Hamner et al., 

1975). These zooplankton constitute a distinct evolutionary assemblage based on shared, convergent attributes of large size, 

neutral buoyancy, tissue transparency, slow swimming speeds, 

and tactile sensory abilities, but they also constitute an ecological assemblage that exchanges nutrient resources via competition 

and predation (Alldredge and Madin, 1982). One of our most 

unexpected early findings regarding trophic relationships was 

that, in contrast to a rigidly layered trophic pyramid wherein 

small herbivorous crustaceans use tiny appendages and fine setae 

to select and capture a narrowly restricted size of phytoplankton, 

large gelatinous grazers instead use mucus structures to capture 

and consume a broad range of sizes and types of food particles 

across different trophic levels, including algae, live net zooplankton, and detritus. We observed for the first time how mucus 

sheets, nets, and strands were used to collect, concentrate, and 

transport food particles by pteropods (Gilmer, 1972, 1974; Lalli 

and Gilmer, 1989), thaliaceans (salps, doliolids, and pyrosomes; 

Madin, 1974), prosobranch veliger larvae (R. Gilmer, UCLA, 

unpub. observation), polychaete larvae (Hamner et al., 1975), 

and free-swimming appendicularians (Alldredge, 1972, 1976a). 

These large gelatinous grazers filter commensurately large volumes of water. For example, a single chain of a large oceanic 

salp, Pegea confoederata, composed of 200 individual zooids 

filters as much water per minute as 90,000 copepods/1,000 m3

(Harbison and Gilmer, 1976). Thus, although not nearly as abundant numerically as net zooplankton, large gelatinous animals 

are disproportionately effective grazers and predators in the 

water column. 

The use of mucus for food capture by epipelagic grazers, 

along with phytoplankton aggregations, produces copious quantities of marine snow, a primary mechanism for carbon flux (Alldredge, 1972; Wangersky, 1974; Hamner et al., 1975; Silver et al., 

1978; Alldredge and Silver, 1988). Feeding filters and mucus webs 

become clogged, discarded, and heavy with unwanted materials 

and feeding wastes, and this material sinks rapidly away from 

surface waters. These macroparticles can be collected by hand in 

syringes by divers and used in a variety of studies (Silver et al., 

1978; Villareal et al., 1999). The constituents of the marine snow 
7 6 • smithsonian contributions to the marine sciences

and associated microbial or invertebrate populations may also 

be observed. During the 38 years since our description of marine 

snow in the blue waters of the Florida Current, we have learned 

much about how microbes process particulate and dissolved organic carbon and transparent exopolymer particles (Alldredge, 

1989; Alldredge et al., 1993). There are more than 1,600 literature entries for marine snow in ISI Web of Science since 1975, 

but none prior to this, not even the unfortunately ignored initial 

description of marine snow by Nishizawa et al. (1954).

Recently we have learned that salp-mucus feeding webs

can capture an even greater size-range of particulates than we

thought initially, including submicrometer particles. According to 

Sutherland et al. (2010:15129), “Although particles larger than 

1 μm (e.g., flagellates, small diatoms) represent a larger carbon 

pool, smaller particles in the 0.1- to 1-μm range (e.g., bacteria, 

Prochlorococcus) may be more quickly digestible because they 

present more surface area, and we find that particles smaller than 

the mesh size (1.4 μm) can fully satisfy salp energetic needs” (see 

Figure 1). Epipelagic offshore waters are frequently dominated by 

microplankton that are too small to be captured by mechanical 

sieving (Riisgård and Larsen, 2010), yet salps apparently can fulfill their entire energetic requirements through an exclusive diet of 

submicrometer particles, including viruses, bacteria, and colloids. 

It was known that small copepods are size-specific herbivores,

and we knew from observations made while blue-water diving

(Hamner et al., 1975) that the much larger salps and pteropods 

were generalized grazers that fed on particulates that sometimes 

differed in size by two to three orders of magnitude, thereby blurring the distinctiveness of discrete trophic levels. We learn now, 

however, from controlled laboratory and field experiments that 

“salps and other pelagic tunicates remove particles that are four 

to five orders of magnitude smaller than themselves, thereby bypassing several trophic levels” (Sutherland et al., 2010:15132).

Direct observations under water have provided exciting and 

previously unknown details of parasitic or commensal relationships. One of the most common involves hyperiid amphipods 

and some copepods living on or in a variety of gelatinous hosts 

(Harbison et al., 1977; Madin and Harbison, 1977; Laval, 1980), 

and that often rear their broods on the bodies of gelatinous animals (Gasca and Haddock, 2004). These associations rarely are 

apparent in net-collected samples, yet constitute an important 

ecological niche occupied by major groups of otherwise nonpelagic crustaceans. Similar behavior is also seen in some juvenile 

cephalopods and fishes. 

There are also many kinds of predatory gelatinous zooplankton in the water column. In our initial blue-water publications 

from Bimini we described predation by medusae, siphonophores, 

ctenophores, heteropods, pteropods, and chaetognaths (Hamner 

et al., 1975). Medusae, siphonophores, and ctenophores feed 

directly on small copepods via tentacles with nematocysts and 

colloblasts; some siphonophores consume surprisingly large 

prey (Pagès and Madin, 2010). Narcomedusae and ctenophores 

can also specialize, capturing specific types of gelatinous prey, 

including other ctenophores, medusae, appendicularians, or 

salps (Harbison et al., 1978; Madin, 1988; Haddock, 2007). In 

many simple oceanic food pyramids or linear food chains, herbivorous copepods are directly preyed upon by primary carnivores. But chaetognaths also eat copepods, and many medusae, 

siphonophores, and ctenophores eat chaetognaths, thus feeding 

as secondary carnivores higher on the food chain. Tuna, flying 

fish, cod, sea turtles, and albatross (Madin, 1974) sometimes 

eat salps, and salps capture and consume copepods along with 

diatoms, yet salps apparently can also consume viruses, colloids, 

and bacteria (Sutherland et al., 2010). Consequently it is often 

difficult to assess trophic status at any given time without simultaneous analysis of gut contents. 

During the past 38 years we have learned an enormous 

amount about predatory relationships within the gelatinous epipelagic assemblage beyond our initial observations in the Gulf 

Stream and Gulf of California (Madin, 1988). It is now clear 

that the gelatinous assemblage of blue-water zooplankton is not 

a “dead end” to the flow of energy and materials in the open 

sea, but instead is a complex, often-changing food web, with 

surprising and strange trophic interactions and links to everything from the microbial web to fish, whales, turtles, and birds. 

Gelatinous grazers and predators can sometimes unexpectedly 

overwhelm entire pelagic ecosystems and become keystone species, such as when a single species of introduced ctenophore ate 

all the fish larvae in the Black Sea, eliminating most commercial fishing (Kideys, 2002; Ghabooli et al., 2011). Recently it 

has been shown that blooms of medusa and ctenophores also 

FIGURE 1. Size distribution of living and nonliving particles in 

the upper ocean, including viruses, colloids, submicron particles, 

bacteria, Prochlorococcus, Synechococcus, nanoplankton, and microplankton. Diagonal line is regression of microphytoplankton 

concentration versus cell diameter.
number 39 • 7 7

produce large quantities of dissolved and colloidal organic material that both stimulates and alters the composition of the microbial community, potentially with broad consequences for the 

biogeochemistry of entire habitats (Condon et al., 2011).

Behavior

Blue-water diving allows observation of many aspects of 

behavior, one of the most obvious of which is locomotion. Although the word plankton means “drifting,” in fact zooplankton, including most gelatinous taxa, can swim by various means. 

Swimming behavior can be difficult to study in the laboratory 

because confined tank volumes and the delicate construction of 

many species often lead to artifacts of behavior and misleading 

observations or measurements. Constraining animals with tethers and other devices to restrict their movements, while effective 

for small, hard-bodied forms like copepods, is usually impractical with larger gelatinous animals and can create problems with 

natural fluid flow. Tanks large enough to minimize these effects 

make it hard to observe animals closely. 

Direct observations by divers at sea are preferred to ensure 

accurate documentation of swimming behavior, but these can 

be difficult to obtain under uncontrolled field conditions. The 

tethered-diver safety system for blue-water scuba allows divers 

to maintain good visual distance and continuous visual contact 

with a subject animal without disturbing them, but this is only 

effective for fairly large and slow-swimming species. Besides by 

direct visual observation, behavior can be recorded on video 

and fluid flow visualized with dye tracers (Madin, 1990; Sutherland and Madin, 2010). Estimates of swimming speed in situ 

have been made by timing the transit of animals over known 

distances, measured with depth gauges or by marking start and 

end points with dye and measuring distance (Madin, 1990); fluid 

flow patterns and rates can be measured from video of dye traces 

(Sutherland and Madin, 2010). Recently the development of a 

Self-Contained Underwater Velocimetry Apparatus (SCUVA; 

Katija and Dabiri, 2008) makes possible in situ digital particle 

image velocimetry measurements that provide information on 

swimming energetics. 

Medusae were thought to swim by jet propulsion but work 

by Costello, Colin, and colleagues (Colin et al., 2003; Costello et 

al., 2008) has shown that there are different modes of fluid manipulation by different species that combine jetting with swimming and feeding currents created by the “rowing” action of the 

bell margin. Early studies of siphonophore locomotion (Mackie, 

1964) were made in aquaria, with subsequent lab and field studies by Purcell (1980, 1981). Swimming of ctenophores has also 

been studied in tanks, but the size and fragility of many lobates 

and cestids makes in situ observations critical (Harbison et al., 

1978; Matsumoto and Hamner, 1988; Matsumoto and Harbison, 1993). While some early studies of swimming by salps were 

done only in lab tanks (Bone, 1984), later studies combined lab 

and field observations and measurements to observe both smalland large-scale aspects of swimming behavior by single salps and 

chains of various species (Madin, 1990; Sutherland and Madin, 

2010). Blue-water diving also enables study of complex swimming behavior of animals relative to their environment or in 

schools or swarms.

Complex behavior of the moon jellyfish (Aurelia aurita) was 

investigated using scuba in Saanich Inlet, Vancouver Island, British Columbia, Canada (Strand and Hamner, 1988; Hamner et 

al., 1994). Dense swarms of Aurelia can be found in Saanich Inlet 

in late summer. Jellyfish dispersed across Saanich Inlet at night 

via tidal currents, but when direct sunlight hit the water in the 

morning the medusae began to swim horizontally at the surface 

and directionally to the southeast, producing massive swarms 

along the southeastern sides of the fjord in the afternoon. Jellyfish that had greater distances to swim also swam directionally 

southeast in the afternoon, demonstrating that horizontal navigation is controlled by a time-compensated sun compass. When 

the jellyfish reached the sides of the fjord, they ceased swimming 

horizontally and instead swam vertically, and thereafter male 

medusae released sperm strands into the water column. The 

dense swarms of Aurelia in Saanich Inlet, therefore, are breeding 

aggregations, something that could only have been determined 

from direct observations via use of scuba. Similar swarms of 

moon jellies with trailing sperm strands have been seen in the 

waters off California (G. Matsumoto, Monterey Bay Aquarium 

Research Institute, pers. obs.).

Taxon-­Specific Observations

A broad diversity of organisms have become gelatinous as 

they evolved to live suspended in the water column. These span a 

taxonomic range from single-celled organisms to large jellies and 

colonies of tunicates. Many larvae of fish, worms, mollusks, and 

others also spend a portion of the life cycle as semitransparent 

meroplankton. 

Macroscopic protists, such as radiolarians and foraminifera, 

and other protists, such as the giant dinoflagellate Noctiluca, can 

reach high numbers in surface waters. Radiolarians and foraminifera are amoeboid but bear siliceous (radiolaria) or calcareous (foraminifera) “shells” or spicules. Some of these feed by 

snagging marine snow on spicule tips, where it is enveloped by 

the cell membrane. Inactive particles and live microzooplankton 

also adhere to the sticky surface of the cell membrane. Noctiluca

feeds with an external mucus web (Omori and Hamner, 1982). 

Shallow polycystine radiolarians contain algal symbionts, and 

while their molecular phylogeny has been examined (Amaral 

Zettler et al., 1997), little is known of their ecological impact 

(Swanberg, 1983). Some species are small enough to be collected 

with syringes, while other colonial forms (often mistaken for egg 

masses) may reach a meter in length. These gelatinous colonies 

trap small zooplankton like copepods on their surfaces, and digest them within vacuoles. Yet at the same time, hyperiid amphipods of similar size roam freely over the colonies as commensals. 

The observation and collection of these colonial radiolarian in 

situ has only been possible with blue-water diving. Foraminifera 
7 8 • smithsonian contributions to the marine sciences

are important indicators of past climate change. Their shells hold 

a record of the isotopic composition of the seawater in which 

they were formed, and thus they are of great interest to paleooceanographers. Divers have collected live forams in snap-cap 

vials so they can be cultured and studied in the laboratory (Spero 

et al., 1997).

Many planktonic cnidarians, principally hydromedusae, 

have been investigated in the field, collected using scuba, and 

studied further in the laboratory (Colin et al., 2003; Costello et 

al., 2008). Siphonophores, fragile colonial forms that are rarely 

seen intact, are especially suitable for blue-water collection (Biggs 

et al., 1986) and have contributed to a recent molecular phylogeny of this group (Dunn et al., 2005). Hydromedusae, smaller 

scyphomedusae, and cubozoans are all readily collected in jars; 

larval anemones (particularly cerianthid larvae) and larval corals 

may be encountered.

Comb jellies are among the most fragile gelatinous zooplankton. Only the hardiest species, such as Pleurobrachia and 

Beroe, could be found in plankton net collections or were figured 

in older textbooks. Scuba divers, however, now collect even the 

most fragile of lobate and cestid ctenophores by hand in individual jars, and ctenophores collected through blue-water diving have revealed new facets of their ecology (Swanberg, 1974; 

Harbison et al., 1978) and molecular phylogenetics (Podar et al., 

2001). Rarely seen forms sometimes appear common to bluewater divers; many new species have been discovered in surface 

waters (Madin and Harbison, 1978; Matsumoto, 1988).

Pelagic tunicates (salps, doliolids, pyrosomes, and appendicularians) feed directly at low trophic levels, demonstrate 

rapid population explosions, and form an important component 

of many highly productive food webs (Madin, 1974; Alldredge, 

1977). While many salps are hardy enough to be enumerated 

from plankton tows, their physiology and ecology is difficult to 

study without in situ observation and hand-collected live specimens for laboratory experiments. Doliolids are even more fragile 

and difficult to maintain in the laboratory (Madin and Deibel, 

1998). Appendicularians (also called larvaceans) build elaborate 

feeding webs (or “houses”) that, until recently, could only be observed in situ (Alldredge, 1976b; Deibel, 1986). A few species 

of appendicularians have been successfully cultured (Paffenhöfer, 

1973; Fenaux et al., 1986), but the great majority of species are 

poorly known and not amenable to laboratory observation. 

Pelagic mollusks, such as pteropods, heteropods, and nudibranchs, have been investigated using blue-water scuba techniques. Pteropods (Limacina, Corolla, and Clione) may occur 

in large numbers, along with diverse species of heteropods and 

other pelagic mollusks (Lalli and Gilmer, 1989). Holoplanktonic 

nudibranchs such as Phylliroe prey on planktonic cnidaria. Ommastrephid squid may occasionally be observed with their large 

gelatinous egg masses (Staaf et al., 2008).

Arrow worms (phylum Chaetognatha) are sometimes large 

enough to be observed by divers. They are among the most important net zooplankton predators, feeding particularly on copepods. A diverse array of polychaetes are found both free-living 

and in association with other gelatinous plankton. Alciopid 

polychaetes, for example, are often predators or parasites of 

ctenophores. 

Open-ocean adult fish, such as the sunfish Mola mola, as 

well as sharks, billfish, and some schooling pelagic species, can be 

occasional, charismatic visitors during scuba dives in blue water; 

larval fish are frequently encountered at night. In addition, some 

pelagic fish hide behind the veil of large gelatinous species such 

as scyphomedusae or the siphonophore Physalia.

epipelagic polar oceans

In polar regions, the light regime of the epipelagic zone differs from that in all other parts of the ocean. Instead of experiencing a diurnal light/dark regime, surface waters at high latitudes 

remain sunlit for most or all of a 24-hour day in summer, and the 

opposite in winter. Polar oceans are also unique in that sea ice 

provides cover for epipelagic organisms, year-round in the Arctic 

and seasonally in the Antarctic. We have used blue-water scuba 

extensively in the open sea in the Antarctic, Arctic, and subpolar 

oceans to investigate epipelagic euphausiids, salps, ctenophores, 

and medusae, but we have been able to study euphausiids near 

the sea surface during the day only in polar oceans. “In polar 

oceans in summer, diurnal vertical migration [is not necessarily 

advantageous] . . . for an herbivore such as Euphausia superba

because all phytoplankton production occurs quite near the 

surface and pelagic herbivores either feed there or they starve. 

Rather than swimming down into deep water to evade predators, 

Euphausia superba engages in schooling behavior in the epipelagic zone, . . . electing a modal survival strategy that is quite different from the diurnal vertical migratory solution so effective 

for most tropical euphausiids. Thus, when the temporal periodicity of the 24-hour light environment changes, so must the nature 

of the convergent adaptive solutions change to permit survival in 

an illuminated, three-dimensional environment devoid of cover”

(Hamner, 1995:75).

For behavioral research on Antarctic krill Euphausia superba near the Antarctic Peninsula, we used tethered, blue-water

scuba protocols modified for dry-suit diving (Hamner, 1982). In 

most parts of the world euphausiids are vertical diurnal migrators, near the surface only at night, but surface schools of Antarctic krill had been seen previously in summer at the surface by 

Hardy and Gunther (1935) around the docks at South Georgia 

Island and by Marr (1962) from aboard ship; density of krill in 

schools was estimated at about 64,000/m3 (1 krill/in3

), which was 

later confirmed photographically under water via scuba by Ragulin (1969), Hamner and colleagues (Hamner et al., 1983; Hamner, 1984a), and O’Brien (1987). These observations of schooling 

behavior by Antarctic krill are of central importance for understanding the ecology of the entire Antarctic water column (Hamner et al., 1983; Hamner, 1984b; Hamner and Hamner, 2000).

The behavior of Euphausia superba changes during ontogeny from a dispersed solitary larva to larvae clumped within 
number 39 • 7 9

swarms and then to uniformly polarized furciliae close-packed 

into schools. We directly observed this behavioral transition for 

krill larvae in the Gerlache Strait, Antarctica, while blue-water 

diving (Hamner et al., 1989). In open ocean without sea ice, isolated furciliae at the surface were at very low densities (0.003/

m3

). In the presence of sea ice, individual, free-swimming furciliae were more abundant (0.3/m3

), but tiny schools of furciliae 

also were found below the sea ice at densities of about 3×109

/

m3

. Sea ice provides larval krill with concentrated epontic algal 

food and protection from predators, and it facilitates formation 

first of swarms of nonpolarized individuals and then of small, 

ice-oriented polarized schools. “Euphausia superba makes an 

abrupt behavioral transition after the last larval molt from an 

individualistic, planktonic lifestyle to that of a highly social, nektonic juvenile. Then and throughout the rest of its life, most aspects of krill behavior are expressed within the context of highly 

organized, polarized schools” (Hamner and Hamner, 2000:192).

The large cydippid Antarctic ctenophore Callianira antarctica captures and digests Antarctic krill. Near the Antarctic Peninsula we saw ctenophores with feeding tentacles fully extended 

and with partly digested krill in their guts, but only when there 

were no krill schools in the immediate vicinity, although krill 

were clearly nearby as evidenced by krill acoustic signatures 

and krill fecal pellets and molts in the water column (Hamner 

and Hamner, 2000). When C. antarctica was seen within krill 

schools, ctenophore guts were empty and fishing tentacles were 

completely retracted. Callianira antarctica captures prey with 

colloblasts and stretchy tentacles that reel in prey one at a time, 

which often takes several minutes. Schooling, therefore, protects 

most krill from C. antarctica because it is physically impossible 

for cydippid ctenophores to fish with delicate, extended tentacles 

within schools of tens of thousands of krill/m3

. 

At least one large lobate ctenophore, probably a new species 

in the genus Eurhamphaea, has been observed and collected by 

blue-water divers in the Antarctic. This species also appears to 

be a predator on krill or their larvae. Also present is Beroe cucumis, the species that preys on other ctenophores and attains a size 

of 25 cm in the Antarctic. In the Arctic, the cydippid Mertensia 

ovum occupies a similar niche to Eurhamphaea’s, but preys on 

large copepods as well as krill (e.g., Matsumoto, 1991; Swanberg and Bamstedt, 1991). Mertensia ovum appears to store lipids

derived from crustacean prey in numerous droplets contained 

within the mesoglea, presumably as an energy store (Larson and 

Harbison, 1989). Other ctenophores observed by diving in the 

Arctic include Bolinopsis infundibulum, which attains a size of 20 

cm or more, Beroe cucumis, and Dryodora (Purcell et al., 2010).

Pelagic tunicates have an unusual asymmetric distribution 

in polar seas. While appendicularians are common in the Arctic, 

salps are absent (Deibel and Daly, 2007), yet salps are extremely 

abundant in the Southern Ocean where they often alternate with 

krill as the dominant grazing species (Loeb et al., 1997; Atkinson 

et al., 2004). The dominant species of salps in most of the Southern Ocean is Salpa thompsoni, with smaller populations of the 

very similar S. gerlachei reported nearer the Antarctic continent. 

Two other species, Ihlea racovitzai and I. magalhanica also occur 

in the region, but usually in smaller numbers. Three of these species appear restricted in distribution to south of the Antarctic 

Convergence, with I. magalhanica found in the vicinity of the 

Falkland Islands. Blue-water divers have provided material for 

studies of salp energetics and fecal pellet production (Phillips et 

al., 2009).

CONCLUSIONS

Although study of gelatinous animals of the plankton began 

in the nineteenth century when naturalists like Chun, Mayer, and 

Bigelow dipped specimens from the sea, major progress in understanding the functional morphology, behavior, and ecological 

roles of these organisms has depended on the ability afforded by 

blue-water diving to observe and collect gelatinous fauna from 

their natural oceanic environment. Blue-water diving is simply 

field biology carried out in a field that has become accessible 

with scuba in the last four decades. It has allowed biologists to 

do the kind of research that was done a century ago on land, but 

in one of the largest and least known habitats on Earth, populated by diverse, abundant, and largely unknown animals. While 

the method has clear limitations, it is a powerful complement to 

other approaches to the study of open-ocean organisms, and deserves to be more widely used by a new generation of oceanographers. In addition to its value as a means of observing, collecting, 

and experimenting with planktonic animals in situ, blue-water 

diving gives oceanographers and marine biologists a personal,

immersive experience of the nature of the open ocean environment that cannot be achieved by towing nets, looking at instrument readouts, or even watching video from an ROV. We believe 

this is a valuable experience for all ocean scientists. 

REFERENCES

Alldredge, A. L. 1972. Abandoned larvacean houses: A unique food source in the pelagic environment. Science, 177:885–887. http://dx.doi.org/10.1126/science

.177.4052.885.

Alldredge, A. L. 1976a. Discarded appendicularian houses as sources of food, surface habitats and particulate organic-matter in planktonic environments.

Limnology and Oceanography, 21:14–23. http://dx.doi.org/10.4319/lo.1976

.21.1.0014.

Alldredge, A. L. 1976b. Field behavior and adaptive strategies of appendicularians 

(Chordata: Tunicata). Marine Biology, 38:29–39. http://dx.doi.org/10.1007/

BF00391483.

Alldredge, A. L. 1977. House morphology and mechanisms of feeding in the Oikopleuridae (Tunicata, Appendicularia). Journal of Zoology, 181(2):175–188. 

Alldredge, A. L. 1989. The significance of suspended detrital aggregates of marine 

snow as microhabitats in the pelagic zone of the ocean. In Recent advances in 

microbial ecology, ed. T. Hattori, Y. Ishida, M. Yoshiharu, R. Y. Morita, and 

A. Uchida, pp. 108–112. Proceedings of the 5th International Symposium on 

Microbial Ecology. Tokyo: Japan Scientific Societies Press.

Alldredge, A. L., and L. P. Madin. 1982. Pelagic tunicates: Unique herbivores in the 

marine plankton. BioScience, 32:655–663. http://dx.doi.org/10.2307/1308815.

Alldredge, A. L., U. Passow, and B. E. Logan. 1993. The abundance and significance 

of a class of large, transparent organic particles in the ocean. Deep-Sea Research, 40:1131–1140. http://dx.doi.org/10.1016/0967-0637(93)90129-Q.
8 0 • smithsonian contributions to the marine sciences

Alldredge, A. L., and M. W. Silver. 1988. Characteristics, dynamics and significance of marine snow. Progress in Oceanography, 20:41–82. http://dx.doi

.org/10.1016/0079-6611(88)90053-5.

Amaral Zettler, L., M. L. Sogin, and D. A. Caron. 1997. Phylogenetic relationships 

between the Acantharea and the Polycystinea: A molecular perspective on 

Haeckel’s Radiolaria. Proceedings of the National Academy of Sciences, 94: 

11411–11416. 

Atkinson, A., V. Siegel, E. Pakhomov, and P. Rothery. 2004. Long-term decline in 

krill stock and increase in salps within the Southern Ocean. Nature, 432:100–

103. http://dx.doi.org/10.1038/nature02996.

Beebe, W. 1926. The Arcturus adventure. New York: G. B. Putnam’s Sons. 

———. 1935. Half mile down. London: The Bodley Head.

Bieri, R. 1966. Feeding preferences and rates of the snail, Ianthina prolongata, the 

barnacle, Lepas anserifera, the nudibranchs Glaucus atlanticum and Fiona 

pinnata, and the food web in the marine neuston. Publications of the Seto 

Marine Biological Laboratory, 14:161–170.

Biggs, D. C., P. Laval, J.-C. Braconnot, C. Carré, J. Goy, M. Masson, and P. Morand. 1986. In situ observations of Mediterranean zooplankton by scuba 

and bathyscaphe in the Ligurian Sea in April 1986. In Diving for science . . . 

86, proceedings of the 6th annual Scientific Diving Symposium, Tallahassee, 

ed. C. T. Mitchell, pp. 153–161. Costa Mesa, Calif.; American Academy of 

Underwater Sciences.

Bone, Q. 1984. Jet propulsion in Doliolum (Tunicata: Thaliacea). Journal of Experimental Marine Biology and Ecology, 76:105–118. http://dx.doi.org/10

.1016/0022-0981(84)90059-5.

Ceccaldi, H. J. 1972. Observations biologiques de Cestus veneris. Tethys, 4:707–

710.

Colin, S. P., J. H. Costello, L. J. Hansson, J. Titelman, and J. O. Dabiri. 2010. Stealth 

predation and the predatory success of the invasive ctenophore Mnemiopsis 

leidyi. Proceedings of the National Academy of Sciences, 197(40):17223–

17227. http://dx.doi.org/10.1073/pnas.1003170107.

Colin, S. P, J. H. Costello, and E. Klos. 2003. In situ swimming and feeding behavior 

of eight co-occuring hydromedusae. Marine Ecology Progress Series, 253: 

305–309. http://dx.doi.org/10.3354/meps253305.

Condon, R. H., D. K. Steinberg, P. A. del Giorgio, T. C. Bouvier, D. A. Bronk, W. M.

Graham, and H. W. Ducklow. 2011. Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. Proceedings of the National Academy of Sciences, http://dx.doi.org/10.1073/ pnas.1015782108.

Costello, J. H., S. P. Colin, and J. O. Dabiri. 2008. Medusan morphospace: Phylogenetic constraints, biomechanical solutions, and ecological consequences. 

Invertebrate Biology, 127:265–290. http://dx.doi.org/10.1111/j.1744-7410

.2008.00126.x.

Dabiri, J. O., M. Gharib, S. P. Colin, and J. H. Costello. 2005. Vortex motion in the 

ocean: In situ visualization of jellyfish swimming and feeding flows. Physics 

of Fluids, 17:091108. http://dx.doi.org/10.1063/1.1942521.

Deibel, D. 1986. Feeding mechanism and house of the appendicularian Oikopleura vanhoeffeni. Marine Biology, 93:429–436. http://dx.doi.org/10.1007

/BF00401110.

Deibel, D., and K. L. Daly. 2007. Zooplankton processes in Arctic and Antarctic 

polynyas. In Polynyas: Windows into polar oceans, ed. W. O. Smith, Jr., and 

D. Barber, pp. 271–322. Elsevier Oceanography Series 74. Amsterdam: Elsevier Publishing.

Dunn, C. W., P. R. Pugh, and S. H. Haddock. 2005. Molecular phylogenetics of 

the siphonophora (Cnidaria), with implications for the evolution of functional specialization. Systematic Biology, 54:916–935. http://dx.doi.org/10

.1080/10635150500354837.

Elton, C. 1939. On the nature of cover. Journal of Wildlife Management, 3:332–

338. http://dx.doi.org/10.2307/3796305.

Fenaux, R., A. Bedo, and G. Gorsky. 1986. Premières données sur la dynamique d’une 

population d’Oikopleura dioica Fol, 1872 (Appendiculaire) en élevage. Canadian Journal of Zoology, 64:1745–1749. http://dx.doi.org/10.1139/z86-263.

Gasca, R., and S. H. D. Haddock. 2004. Associations between gelatinous zooplankton and hyperiid amphipods (Crustacea: Peracarida) in the Gulf of California. Hydrobiologia, 530/531:529–535. http://dx.doi.org/10.1007/s10750

-004-2657-5.

Ghabooli, S., T. A. Shiganova, A. Zhan, M. E. Cristescu, P. Eghtesadi-Araghi, H. J. 

MacIsaac. 2011. Multiple introductions and invasion pathways for the invasive ctenophore Mnemiopsis leidyi in Eurasia. Biological Invasions, 13:679–

690. http://dx.doi.org/10.1007/s10530-010-9859-8.

Gilmer, R. W. 1972. Free-floating mucus webs: A novel feeding adaptation for the 

open ocean. Science, 176:1239–1240. http://dx.doi.org/10.1126/science.176

.4040.1239.

———. 1974. Some aspects of feeding in thecosomatous pteropod molluscs. Journal of Experimental Marine Biology and Ecology, 15:127–144. http://dx.doi

.org/10.1016/0022-0981(74)90039-2.

Graham, W. M., J. H. Costello, S. P. Colin, A. Malej, D. Lucic, V. Onofri, and A. Benovic. 2009. In situ manipulation of vertically migrating gelatinous zooplankton using nighttime blue-water scuba in the south-central Adriatic Sea. Annales Serie Histoire Naturelle, 19(Suppl. 2):19–24. 

Haddock, S. H. D. 2004. A golden age of gelata: Past and future research on planktonic ctenophores and cnidarians. Hydrobiologia, 530/531:549–566. http://

dx.doi.org/10.1016/0022-0981(74)90039-2.

———. 2007. Comparative feeding behavior of planktonic ctenophores. Integrative 

Comparative Biology, 47:847–853. http://dx.doi.org/10.1093/icb/icm088.

Haddock, S. H. D., and J. F. Case. 1999. Bioluminescence spectra of shallow and 

deep-sea gelatinous zooplankton: Ctenophores, medusae and siphonophores. 

Marine Biology, 133:571–582. http://dx.doi.org/10.1007/s002270050497.

Haddock, S. H. D., and J. N. Heine. 2005. Scientific blue-water diving. La Jolla, 

Calif.: California Sea Grant.

Haddock, S. H. D., N. Mastroianni, and L. M. Christianson. 2010. A photoactivatable green-fluorescent protein from the phylum Ctenophora. Proceedings of 

the Royal Society, London, B: Biological Sciences, 277:1155–1160. http://

dx.doi.org/10.1098/rspb.2009.1774.

Hamner, W. M. 1974. Blue-water plankton. National Geographic, 146:530–545.

———. 1975. Underwater observations of blue-water plankton: Logistics, techniques, and safety procedures for divers at sea. Limnology and Oceanography, 20:1045–1051. http://dx.doi.org/10.4319/lo.1975.20.6.1045.

———. 1982. Procedures for in situ observations of krill schools in the Southern 

Ocean. Antarctic Journal of the United States, 8:165. 

———. 1984a. Aspects of schooling in Euphausia superba. Journal of Crustacean 

Biology, 4(Spec. No. 1):67–74.

———. 1984b. Krill: Untapped bounty? National Geographic, 165:626–643.

———. 1985. The importance of ethology for investigations of marine zooplankton. Bulletin of Marine Science, 37:414–424.

———. 1990. Design developments in the planktonkreisel, a plankton aquarium 

for ships at sea. Journal of Plankton Research, 12:397–402. http://dx.doi.org

/10.1093/plankt/12.2.397.

———. 1995. Predation, cover, and convergent evolution in epipelagic oceans. Marine and Freshwater Behavior and Physiology, 26:71–89. http://dx.doi.org

/10.1080/10236249509378930.

Hamner, W. M., and P. P. Hamner. 2000. Behavior of Antarctic krill (Euphausia 

superba): Schooling, foraging, and antipredatory behavior. Canadian Journal of Fisheries and Aquatic Science, 57(Suppl. 3):192–202. http://dx.doi.org

/10.1139/f00-195.

Hamner, W. M., P. P. Hamner, B. S. Obst, and J. H. Carleton. 1989. Field observations on the ontogeny of schooling of Euphausia superba furcilia and 

their relationship to ice in Antarctic waters. Limnology and Oceanography,

34:451–456. http://dx.doi.org/10.4319/lo.1989.34.2.0451.

Hamner, W. M., P. P. Hamner, and S. W. Strand. 1994. Sun compass migration 

by Aurelia aurita (Scyphozoa): Population persistence versus dispersal in 

Saanich Inlet, British Columbia. Marine Biology, 119:347–356. http://dx.doi

.org/10.1007/BF00347531.

Hamner, W. M., P. P. Hamner, S. W. Strand, and R. W. Gilmer. 1983. Behavior of 

Antarctic krill, Euphausia superba: Chemoreception, feeding, schooling, 

and molting. Science, 220:433–435. http://dx.doi.org/10.1126/science.220

.4595.433.

Hamner, W. M., L. P. Madin, A. L. Alldredge, R. W. Gilmer, and P. P. Hamner. 1975. 

Underwater observations of gelatinous zooplankton: Sampling problems, 

feeding biology, and behavior. Limnology and Oceanography, 20:907–917. 

http://dx.doi.org/10.4319/lo.1975.20.6.0907.

Hamner, W. M., S. W. Strand, G. I. Matsumoto, and P. P. Hamner. 1987. Ethological observations on foraging behavior of the ctenophore Leucothea sp. 

in the open sea. Limnology and Oceanography, 32:645–652. http://dx.doi

.org/10.4319/lo.1987.32.3.0645.

Harbison, G. R., D. C. Biggs, and L. P. Madin. 1977. The association of amphipods 

Hyperiidea with gelatinous zooplankton. II. Associations with Cnidaria, Ctenophora and Radiolaria. Deep-Sea Research, 24:465–488. http://dx.doi.org

/10.1016/0146-6291(77)90484-2.

Harbison, G. R., and R. W. Gilmer. 1976. The feeding rates of the pelagic tunicate Pegea confoederata and two other salps. Limnology and Oceanography,

21:517–528. http://dx.doi.org/10.4319/lo.1976.21.4.0517.

Harbison, G. R., L. P. Madin, and N. R. Swanberg. 1978. On the natural history and 

distribution of oceanic ctenophores. Deep-Sea Research, 25:233–256. http://

dx.doi.org/10.1016/0146-6291(78)90590-8.
number 39 • 8 1

Hardy, A. C., and E. R. Gunther. 1935. The plankton of the South Georgia whaling 

grounds and adjacent waters, 1926–1927. Discovery Reports, 11:1–377. Cambridge: Cambridge University Press. 

Hobson, E. S. 1963. Feeding behavior in three species of sharks. Pacific Science,

17:171–194.

———. 1965. Diurnal–nocturnal activity of some inshore fishes in the Gulf of California. Copeia, 1965:291–302. http://dx.doi.org/10.2307/1440790.

Johnsen, S. 2001. Hidden in plain sight: The ecology and physiology of organismal 

transparency. Biological Bulletin, 201:301–318. http://dx.doi.org/10.2307

/1543609.

Johnsen, S., and E. A. Widder. 1998. The transparency, visibility and ultrastructure 

of gelatinous zooplankton. American Zoologist, 38:99A. 

———. 1999. The physical basis of transparency in biological tissue: Ultrastructure and the minimization of light scattering. Journal of Theoretical Biology, 

199:181–198. http://dx.doi.org/10.1006/jtbi.1999.0948.

———. 2001. Ultraviolet absorption in transparent zooplankton and its implications for depth distribution and visual predation. Marine Biology, 138:717–

730. http://dx.doi.org/10.1007/s002270000499.

Katija, K., and J. O. Dabiri. 2008. In situ field measurements of aquatic animal–

fluid interactions using a Self-Contained Underwater Velocimetry Apparatus 

(SCUVA). Limnology and Oceanography Methods, 6:162–171. http://dx.doi

.org/10.4319/lom.2008.6.162.

Kideys, A. 2002. Fall and rise of the Black Sea ecosystem. Science, 297:1482–1484. 

http://dx.doi.org/10.1126/science.1073002.

Lalli, C., and R. W. Gilmer. 1989. Pelagic snails: The biology of holoplanktonic 

gastropod mollusks. Palo Alto, Calif.: Stanford University Press. 

Larson, R. J., and G. R. Harbison. 1989. Source and fate of lipids in polar gelatinous zooplankton. Arctic, 42:339–346. 

Laval, P. 1980. Hyperiid amphipods as crustacean parasitoids associated with gelatinous 

zooplankton. Oceanography and Marine Biology Annual Review, 18:11–56.

Loeb, V., V. Siegel, O. Holm-Hansen, R. Hewitt, W. Fraser, W. Trivelpiece, and 

S. Trivelpiece. 1997. Effects of sea-ice extent and krill or salp dominance on 

the Antarctic food web. Nature, 387(6636):897–900. http://dx.doi.org/10

.1038/43174.

Mackie, G. O. 1964. Analysis of locomotion in a siphonophore colony. Proceedings 

of the Royal Society of London, B: Biological Sciences, 159(975):366–391. 

http://dx.doi.org/10.1098/rspb.1964.0008.

Madin, L. P. 1974. Field observations on the feeding behavior of salps (Tunicata: 

Thaliacea). Marine Biology, 24:143–147. http://dx.doi.org/10.1007/BF003

89262.

———. 1988. Feeding behavior of tentaculate predators: In situ observations and a 

conceptual model. Bulletin of Marine Science, 43:413–429.

———. 1990. Aspects of jet propulsion in salps. Canadian Journal of Zoology,

68:765–777. http://dx.doi.org/10.1139/z90-111.

Madin, L. P., and D. Deibel. 1998. Feeding and energetics of Thaliaceans. In The biology of pelagic tunicates, ed. Q. Bone, pp. 43–64. London: Oxford University 

Press.

Madin, L. P., and G. R. Harbison. 1977. The associations of amphipods Hyperiidea with gelatinous zooplankton. I. Association with Salpidae. Deep-Sea 

Research, 24:449–463. http://dx.doi.org/10.1016/0146-6291(77)90483-0.

———. 1978. Thalassocalyce inconstans gen. n. sp. n. an enigmatic ctenophore 

representing a new family and order. Bulletin of Marine Science, 28:680–687.

Marr, J. W. S. 1962. The natural history and geography of the Antarctic krill (Euphausia superba). Discovery Report, 32:33–464.

Matsumoto, G. I. 1988. A new species of lobate ctenophore, Leucothea pulchra sp. 

nov., from the California Bight. Journal of Plankton Research. 10(2):301–

311. http://dx.doi.org/10.1093/plankt/10.2.301.

Matsumoto, G. I. 1991 Functional morphology and locomotion of the Arctic ctenophore Mertensia ovum Fabricius. Sarsia, 76:177–185. 

Matsumoto, G. I., and W. M. Hamner. 1988. Modes of water manipulation by the 

lobate ctenophore Leucothea sp. Marine Biology, 97:551–558. http://dx.doi

.org/10.1007/BF00391051.

Matsumoto, G. I., and G. R. Harbison. 1993. In situ observations of feeding, foraging, and escape behavior in three orders of oceanic ctenophores: Lobata, Cestida, and Beroida. Marine Biology, 117:279–288. http://dx.doi.org/10.1007

/BF00345673.

Mills, C. E., P. R. Pugh, G. R. Harbison, and S. H. D. Haddock. 1996. Medusae, 

siphonophores and ctenophores of the Alborán Sea, south western Mediterranean. Scientia Marina, 60:145–163. 

Nishizawa, S., M. Fukuda, and N. Inowe. 1954. Photographic study of suspended 

matter and plankton in the sea. Bulletin of Pacific Fisheries, Hokkaido University, 5:36–40.

O’Brien, D. P. 1987. Direct observations of the behavior of Euphausia superba and 

Euphausia crystallorophias (Crustacea: Euphausiacea) under pack ice during the Antarctic spring of 1985. Journal of Crustacean Biology, 7:437–448. 

http://dx.doi.org/10.2307/1548293.

Omori, M., and W. M. Hamner. 1982. Patchy distribution of zooplankton: Behavior, population assessment and sampling problems. Marine Biology, 72:193–

200. http://dx.doi.org/10.1007/BF00396920.

Paffenhöfer, G. A. 1973. The cultivation of an appendicularian through numerous 

generations. Marine Biology, 22:183–185. http://dx.doi.org/10.1007/BF003

91782.

Pagès, F., and L. P. Madin. 2010. Siphonophores eat fish larger than their stomachs. Deep-Sea Research II, 57:2248–2250. http://dx.doi.org/10.1016/j.dsr2

.2010.09.026.

Phillips, B., P. Kremer, and L. P. Madin. 2009. Defecation by Salpa thompsoni

and its contribution to vertical flux in the Southern Ocean. Marine Biology,

156:455–467. http://dx.doi.org/10.1007/s00227-008-1099-4.

Podar, M., S. H. D. Haddock, M. Sogin, and G. R. Harbison. 2001. A molecular 

phylogenetic framework for phylum Ctenophora. Molecular Phylogenetics 

and Evolution, 21:218–230. 

Purcell, J. E. 1980. Influence of siphonophore behavior upon their natural diets: 

Evidence for aggressive mimicry. Science, 209:1045–1047. http://dx.doi.org

/10.1126/science.209.4460.1045.

———. 1981. Dietary composition and diel feeding patterns of epipelagic siphonophores. Marine Biology, 65:83–90. http://dx.doi.org/10.1007/BF00397071.

Purcell, J. E., R. R. Hopcroft, K. N. Kosobokova, and T. E. Whitledge. 2010. Distribution, abundance, and predation effects of epipelagic ctenophores and jellyfish in the western Arctic Ocean. Deep Sea Research II, 57:127–135. http://

dx.doi.org/10.1016/j.dsr2.2009.08.011.

Ragulin, A. G. 1969. Underwater observations on krill. Trudy Vsesoiuznogo 

Nauchno-Issledo-vatel’skogo Instituta Morskogo Rybnogo Khoziaistiva i 

Okeanografi (VNIRO) 66:223–230. 

Rakow, K. C., and W. M. Graham. 2006. Orientation and swimming mechanics by 

the scyphomedusae Aurelia sp. in shear flow. Limnology and Oceanography, 

51:1097–1106. http://dx.doi.org/10.4319/lo.2006.51.2.1097.

Randall, J. E., and H. A. Randall. 1960. Examples of mimicry and protective resemblance in tropical marine fishes. Bulletin of Marine Science of the Gulf and 

Caribbean, 10:444–480.

Raskoff, K. A., F. A. Sommer, W. M. Hamner, and K. M. Cross. 2003. Collection and 

culture techniques for gelatinous zooplankton. Biological Bulletin, 204:68–

80. http://dx.doi.org/10.2307/1543497.

Riisgård, H. U., and P. S. Larsen. 2010. Particle capture mechanisms in suspensionfeeding invertebrates. Marine Ecology Progress Series, 418:255–293. http://

dx.doi.org/10.3354/meps08755.

Robison, B. H. 2004. Deep pelagic biology. Journal of Experimental Marine Biology and Ecology, 300(1–2):253–272. http://dx.doi.org/10.1016/j.jembe

.2004.01.012.

Silver, M. W., A. J. Shanks, and J. D. Trent. 1978. Marine snow: Microplankton 

habitat and source of small-scale patchiness in pelagic populations. Science, 

201:371–373. http://dx.doi.org/10.1126/science.201.4353.371.

Spero, H. J., J. Bijma, D. W. Lea, and B. E. Bemis. 1997. Effect of seawater carbonate concentration on planktonic foraminiferal carbon and oxygen isotopes. 

Nature, 390:497–500. http://dx.doi.org/10.1038/37333.

Staaf, D., S. Camarillo-Coop, S. Haddock, A. Nyack, J. Payne, C. Salinas-Zavala,

B. Seibel, L. Trueblood, C. Widmer, and W. Gilly. 2008. Natural egg mass 

deposition by the Humboldt squid (Dosidicus gigas) in the Gulf of California 

and characteristics of hatchlings and paralarvae. Journal of the Marine Biological Association of the United Kingdom, 88:12. http://dx.doi.org/10.1017

/S0025315408001422.

Strand, S. W., and W. M. Hamner. 1988. Predatory behavior of Phacellophora 

camtschatica and size-selective predation upon Aurelia aurita (Scyphozoa: 

Cnidaria) in Saanich Inlet, British Columbia. Marine Biology, 99:409–414. 

http://dx.doi.org/10.1007/BF02112134.

Sutherland, K. R., and L. P. Madin. 2010. Comparative jet wake structure and 

swimming performance of salps. Journal of Experimental Biology, 213:2967–

2975. http://dx.doi.org/10.1242/jeb.041962. 

Sutherland, K. R., L. P. Madin, and R. Stocker. 2010. Filtration of submicrometer 

particles by pelagic tunicates. Proceedings of the National Academy of Sciences, 107:15129–15134. http://dx.doi.org/10.1073/pnas.1003599107.

Swanberg, N. R. 1974. The feeding behavior of Beroe ovata. Marine Biology,

24:69–76. http://dx.doi.org/10.1007/BF00402849.

———. 1983. The trophic role of colonial radiolaria in oligotrophic oceanic environments. Limnology and Oceanography, 30:646–652. 
8 2 • smithsonian contributions to the marine sciences

Swanberg, N. R., and U. Bamstedt. 1991. Ctenophora in the Arctic: The abundance, distribution and predatory impact of the cydippid ctenophore Mertensia ovum (Fabricius) in the Barents Sea. Polar Research, 10:507–524. http://

dx.doi.org/10.1111/j.1751-8369.1991.tb00669.x.

Villareal, T. A., C. H. Pilskaln, M. Brzezinski, F. Lipschultz, M. Dennett, and G. B.

Gardner. 1999. Upward transport of oceanic nitrate by migrating diatom 

mats. Nature, 397:423–425. http://dx.doi.org/10.1038/17103.

Wangersky, P. J. 1974. Particulate organic carbon: Sampling variability. Limnology and Oceanography, 19:980–984. http://dx.doi.org/10.4319/lo.1974.19

.6.0980.

Zaret, T. M. 1975. Strategies for existence of zooplankton prey in homogeneous 

environments. Verhandlungen des Internationalen Verein Limnologie, 19: 

1484–1489.
Scientific Polar Ice Diving

Adam G. Marsh, Amy L. Moran, and James B. McClintock

ABSTRACT. Early ecological descriptions of under-ice benthic communities in McMurdo Sound 

were made over 40 years ago by wetsuit divers Paul Dayton and John Pearse, resulting in seminal 

papers. Polar diving equipment has evolved since then in areas of life-support breathing apparatus 

and thermal protection. Scientific polar ice diving has developed into a research tool for intensive 

sampling and experimental programs by marine ecologists describing under-ice ecosystem structure,

and provided insights into how benthic communities respond to disturbance. Direct scuba observations have established the remarkable continuity that exists in species distribution and abundances. 

The ability to scuba dive in a stable, marine benthic community in polar habitats provides researchers with a unique opportunity to understand the structuring forces at a population level and selective 

adaptations at an organismal level. Research by Moran and Woods using cutting-edge methods in 

underwater environmental measurement developed and tested a sophisticated model for metabolic 

regulation in embryos developing on the sea floor. Work by Marsh in understanding energy utilization during development in an Antarctic sea urchin highlighted a novel mechanism of metabolic energy conservation associated with protein metabolism. A current research focus is on environmental 

imprinting via epigenetic modifications to genomic DNA, which could have a large impact on cellular physiological activities. This could possibly function as a mechanism for regulating large-scale 

shifts in cellular energy utilization, perhaps serving as the key mechanism by which organisms have 

adapted to polar life in the cold and dark. McClintock and coworkers’ discovery regarding feeding 

deterrents in an Antarctic sponge has fueled an extraordinary understanding of chemically mediated 

defense in polar benthic communities.

INTRODUCTION

Polar marine ecosystems are vastly understudied. In general, they possess unique 

features related to extremes of temperature, photoperiod, and the frequent occurrence of 

a sea ice layer at the ocean–atmosphere boundary. It is this latter feature of sea ice dynamics that makes these habitats particularly challenging for studying benthic macroorganisms (both animals and plants). Surface ice conditions confound the collection of living 

specimens and constrain logistics for in situ experimental manipulations. Consequently, 

scientific research activities in polar coastal margins focusing on benthic organisms require well-organized and -trained scuba diving teams for direct observations, collections, 

and experiments. Scientific research on polar marine organisms poses many challenges. 

In areas where sea ice coverage is significant in terms of either a solid layer or high ice 

floe densities, great skill and caution must be exercised by dive teams engaged in scuba 

diving activities. Scientific ice diving in polar regions has yielded a wealth of information 

that could not have been obtained by any other sampling methods. The ability of a diver 

to make direct under-ice observations and the delicate skill with which critical samples 

can be collected or experimental arrays handled have yielded critical new knowledge 

of the richly diverse and ecologically complex polar habitats. In short, polar ice diving 

Adam G. Marsh, School of Marine Science, University of Delaware, Lewes, Delaware 19958, 

USA. Amy L. Moran, Department of Biological Sciences, Clemson University, Clemson, South 

Carolina 29634, USA. James B. McClintock,

Department of Biology, University of Alabama 

at Birmingham, Birmingham, Alabama 35294, 

USA. Correspondence: A. Marsh, amarsh@

udel.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
8 4 • smithsonian contributions to the marine sciences

has developed as a mature branch of scientific diving that is irreplaceable in terms of the discoveries that have been made and 

will continue to be made.

DIVING

Techniques and strategies for diving in polar ice environments have received considerable expert attention in recent years 

(Lang and Sayer, 2007; Lang, 2009). Local dive-site conditions 

can be variable and require unique solutions to mitigate risk.

However, there are some aspects to polar ice diving that all scientific divers face, which we briefly summarize below to provide 

an overview of the challenges that are involved with scientific ice 

diving in polar coastal zones. Readers should consult Lang and 

Sayer (2007) and Krupnik et al. (2009) for more details specific 

to ice diving research activities.

The biggest challenge to ice diving can be limited options 

for water entry and exit. In floe environments, dynamic interactions of winds and currents can establish significant risks for 

the ability of a diver under water to navigate back to a safe exit 

point. In conditions with a solid sea ice surface, divers operate 

as if in an underwater cavern with restricted access. Diving is 

not conducted under conditions where there is any doubt about 

the ability to return to the exit location. Once all the risk factors have been identified and mitigated, then underwater work 

can commence. A second significant challenge is thermal protection for the diver while under water. Drysuits are standard 

equipment now and there are a variety of commercial designs 

using heavy-duty, tear-resistant outer-layer materials to make the 

suits durable under harsh field conditions. Drysuits need to be 

fitted to the diver’s body, with sufficient extra space to allow for 

several layers of insulating undergarments. A third challenge for 

working in water under ice is buoyancy control. Maintaining a 

larger air volume in the drysuit to accommodate the insulating 

undergarments results in more potential for large air pockets to 

move around within the suit and cause sudden shifts in balance 

points and trim levels. More air necessitates more lead weight, 

and so a larger total mass of the diver plus equipment requires 

greater attention to suit-volume regulation for maintaining neutral buoyancy. A fourth challenge is ensuring that the diver has 

the appropriate equipment for a safe dive. This mostly means 

that divers must have first- and second-stage regulators that are 

designed for use in sea water at -2°C without developing internal 

ice crystals that could result in a free-flow event. A great deal of 

scrutiny must be exerted to ensure that any regulator used under 

the ice is not prone to free-flow events.

SCIENCE

Some of the most important work involving early ecological descriptions of under-ice benthic communities in McMurdo 

Sound were made by wetsuit divers in the mid-sixties and resulted 

in seminal papers by Paul Dayton and John Pearse (Pearse, 1966, 

1967; Dayton et al., 1969, 1974). Dayton and Pearse were pioneers in making detailed underwater observations and experiments, and continued productive Antarctic research careers with 

their students by utilizing scuba as the first tool for observation 

and collection (Dayton and Oliver, 1977; Oliver, 1984; McClintock and Pearse, 1986, 1987; Pearse et al., 1991; Pearse 

and Lockhart, 2004). Scientific ice diving became the primary 

mechanism for intensive sampling and experimental programs 

by marine ecologists describing under-ice ecosystem structure 

(Slattery and Oliver, 1986; Brey et al., 1995; Slattery and McClintock, 1995; Blight et al., 2010). The ability to perform direct 

experimentation under the ice has provided many insights into 

how benthic communities respond to disturbance (Lenihan et al., 

2003; Conlan et al., 2004; Kim et al., 2007; Conlan et al., 2010; 

Kim et al., 2010) and the delicate balance that exists between 

abiotic selection pressures and population survival (growth, reproduction, and recruitment) in marine communities subjected 

to continuous harsh environmental conditions.

We now have a much better understanding of the longevity 

of polar benthic communities and how shifts in trophic organization may proceed over much more gradual time scales than 

in other marine ecosystems (Brey et al., 1995; McClintock and 

Pearse, 1986, 1987). Direct scuba observations and research diving activities for the last 40 years have established the remarkable 

continuity that exists over this time frame in species distribution 

and abundances. This level of system equilibrium is only possible because of the seasonally and annually stable ecosystem 

structure. The only other comparable marine ecosystems are the 

abyssal plains of the deep oceans, where direct observations are 

only possible via deep submergence vehicles. The ability to scuba 

dive and directly observe, collect, and manipulate a stable marine 

benthic community in polar habitats provides researchers with 

a unique opportunity to understand the structuring forces at a 

population level and selective adaptations at an organismal level. 

The majority of the biosphere on this planet, 75% by volume, 

consists of a single habitat type: cold (~2o

C), dark sea water. One 

of the few places where this habitat type is accessible by scuba is 

along the coastal margins of Antarctica. 

Ongoing research by the coauthors of this paper continues a 

tradition of strong scientific diving programs in coastal Antarctic 

habitats. The observation, collection, and experimentation that is 

afforded from a first-person perspective by actively engaging in

under-ice research constantly fuels new discoveries and new questions (McClintock et al., 2010b). As the field of biology has been 

moving more and more toward molecular-level understandings

based on increasingly sophisticated technologies, scientific diving 

remains an important tool for collecting organisms necessary for 

physiological, biochemical, and molecular genetic research. 

Work by Amy Moran, in collaboration with Art Woods, has 

used cutting-edge methods in underwater environmental measurement to develop and test a sophisticated model for metabolic regulation in embryos developing on the sea floor (Woods 

and Moran, 2008a, 2008b; Woods et al., 2009; Moran and 
number 39 • 8 5

Woods, 2010). In general, the availability of oxygen in seawater 

and the rate of oxygen consumption by an organism is a critical 

balance (supply versus demand) that is unique in polar environments. One facet where this is particularly important is for the 

egg capsules of nudibranchs (Mollusca). Here, the deposition of 

numerous embryos into a single capsule is under a tight selective 

constraint of ensuring that sufficient oxygen is available in the 

center of the capsule so that all embryos can survive through 

development. The research of Woods and Moran has made many 

interesting discoveries of embryo size, egg-capsule size, capsule 

density, and capsule geometry that are associated with adaptations for survival of nudibranch embryos in polar habitats. Questions of oxygen transport, growth regulation, metabolic energy 

utilization, and developmental period remain key questions for 

understanding the life-history adaptations of many polar marine 

invertebrate species. Pursuing this work will require additional in 

situ work under the ice.

Work by Adam Marsh has focused on understanding energy 

utilization during development in an Antarctic sea urchin (Marsh 

and Manahan, 1999; Marsh et al., 1999; Marsh and Manahan, 

2000; Marsh et al., 2001). Metabolic efficiency is an overriding feature of many species in polar ecosystems where primary 

production is severely limited to only a small portion of each 

year. Many invertebrate larval forms have feeding structures and 

rely on the capture of exogenous food for their nutrition. However, in polar ecosystems, there is very little food available in the 

water column throughout most of the austral spring and summer 

developmental periods. Work in the Manahan laboratory has 

demonstrated a fascinating and novel mechanism of metabolic 

energy conservation associated with protein metabolism: the net 

cost of protein accumulation (net of synthesis and degradation) 

is much less in the embryos of the Antarctic sea urchin than in 

any other known marine organism (Marsh et al., 2001). 

Recent work by Marsh is delving into genomic-level responses to temperature stress (Fielman and Marsh, 2005; Ulrich 

and Marsh, 2009) and the potential for salinity stress to become 

an important selection force in the future (Cowart et al., 2009). 

We are now focusing on environmental imprinting via epigenetic modifications to genomic DNA, which could have a large 

impact on cellular physiological activities. This would function 

as a major mechanism for regulating large-scale shifts in cellular energy utilization, perhaps serving as the key mechanism by 

which organisms have adapted to polar life in the cold and dark. 

Despite the molecular focus of ongoing studies, diving operations under the ice for collections and observations remain an 

important component of this field work. 

Work by Jim McClintock has been prolific, particularly in 

collaboration with marine natural products chemist Bill Baker 

and phycologist Charles Amsler. A simple discovery regarding 

feeding deterrents in an Antarctic sponge has fueled an extraordinary understanding of chemically mediated defense in polar 

benthic communities (McClintock and Vernon, 1990; McClintock and Gauthier, 1992; Peters et al., 2009, 2010; Aumack 

et al., 2010). The revolutionary discovery here was McClintock’s 

shattering of a paradigm that asserted that chemical defense 

in polar environments was not important because of the lack 

of predation pressures in comparison to tropical coral reefs 

(where chemical defense was well documented; Slattery and McClintock, 1995). This work completely shifted our perspective 

of the role of predation in shaping polar benthic communities. 

Subsequent work on identifying chemical deterrents that exist 

in polar organisms (both plants and animals) has led to a better 

understanding of the precarious balance in oligotrophic systems 

that exists among predators and their sessile prey or herbage. 

Knowing about these biochemical-level interactions that exist 

among species has led to a much broader understanding of processes that shape polar benthic community structure, particularly 

in terms of the interactions between consumers and producers 

(Amsler et al., 2009a, 2009b; McClintock et al., 2010a). 

SUMMARY

There is no substitute for direct observation. Much of what 

we know today about polar benthic communities was derived 

from questions that scientific divers asked based on their own 

observations. In truth, we know much less about benthic coastal 

habitats below polar sea ice than other marine systems (perhaps 

with the exception of the deep sea). Even after 50 years of scuba 

exploration there remains a host of research questions to ponder. 

The limited access to the environment imposed by sea ice coverage substantially reduces the observation time often taken for 

granted when exploring a rocky intertidal pool or snorkeling on 

a coral reef. Scientific diving by principal investigators is an essential component of establishing a working knowledge of what 

“normal” looks like under the ice in Antarctica, and a key focus 

of future polar diving is to provide basic information that will 

help to identify and evaluate the impact of environmental change 

on these unique habitats. 

ACKNOWLEDGMENTS

The authors gratefully recognize funding from the National 

Science Foundation for their Antarctic research over the years 

(for example, ANT-0838773 to JBM and Charles Amsler) and 

appreciate all the logistical and diving operations support they 

have received at McMurdo and Palmer Stations, Antarctica, especially from diving officers Jimmy Stewart, Michael Lang, and 

Rob Robbins. JBM also acknowledges the support of an Endowed Professorship in Polar and Marine Biology provided by 

the University of Alabama at Birmingham. 

REFERENCES

Amsler, C. D., M. O. Amsler, J. B. McClintock, and B. J. Baker. 2009a. Filamentous algal endophytes in macrophytic Antarctic algae: Prevalence in hosts 
8 6 • smithsonian contributions to the marine sciences

and palatability to mesoherbivores. Phycologia, 48:324–334. http://dx.doi

.org/10.2216/08-79.1.

Amsler, C. D., K. Iken, J. B. McClintock, and B. J. Baker. 2009b. Defenses of polar 

macroalgae against herbivores and biofoulers. Botanica Marina, 52:535–545. 

http://dx.doi.org/10.1515/BOT.2009.070.

Aumack, C. F., C. D. Amsler, J. B. McClintock, and B. J. Baker. 2010. Chemically 

mediated resistance to mesoherbivory in finely branched macroalgae along 

the western Antarctic peninsula. European Journal of Phycology, 45:19–26. 

http://dx.doi.org/10.1080/09670260903171668.

Blight, L. K., D. G. Ainley, S. F. Ackley, G. Ballard, T. Ballerini, R. L. Brownell, Jr., 

C.-H. C. Cheng, M. Chiantore, D. Costa, M. C. Coulter, P. K. Dayton, A. L. 

Devries, R. Dunbar, S. Earle, J. T. Eastman, S. D. Emslie, C. W. Evans, R. A. Garrott, S. Kim, G. Kooyman, A. Lescroel, M. Lizotte, M. Massaro, S. Olmastroni, 

P. J. Ponganis, J. Russell, D. B. Siniff, W. O. Smith, Jr., B. S. Stewart, L. Stirling, 

J. Willis, P. Wilson, and E. J. Woehler. 2010. Fishing for data in the Ross Sea. 

Science, 330:1316. http://dx.doi.org/10.1126/science.330.6009.1316.

Brey, T., J. Pearse, L. Basch, J. McClintock, and M. Slattery. 1995. Growth and production of Sterechinus neumayeri (Echinoidea: Echinodermata) in McMurdo 

Sound, Antarctica. Marine Biology, 124:279–292. http://dx.doi.org/10.1007

/BF00347132.

Conlan, K. E., S. L. Kim, H. Lenihan, and J. Oliver. 2004. Benthic changes during 10 

years of organic enrichment by McMurdo Station, Antarctica. Marine Pollution Bulletin, 49:43–60. http://dx.doi.org/10.1016/j.marpolbul.2004.01.007.

Conlan, K. E., S. L. Kim, A. R. Thurber, and E. Hendrycks. 2010. Benthic changes at 

McMurdo Station, Antarctica following local sewage treatment and regional 

iceberg-mediated productivity decline. Marine Pollution Bulletin, 60:419–

432. http://dx.doi.org/10.1016/j.marpolbul.2009.10.009.

Cowart, D. A., P. N. Ulrich, D. C. Miller, and A. G. Marsh. 2009. Salinity sensitivity 

of early embryos of the Antarctic sea urchin, Sterechinus neumayeri. Polar 

Biology, 32:435–441.

Dayton, P. K., and J. Oliver. 1977. Antarctic soft-bottom benthos in oligotrophic 

and eutrophic environments. Science, 197:55–58. http://dx.doi.org/10.1126

/science.197.4298.55.

Dayton, P. K., G. A. Robilliard, and A. L. Devries. 1969. Anchor ice formation in 

McMurdo Sound, Antarctica and its biological effects. Science, 163:273–274. 

http://dx.doi.org/10.1126/science.163.3864.273.

Dayton, P. K., G. A. Robilliard, R. Paine, and L. Dayton. 1974. Biological accommodation in benthic community at McMurdo Sound, Antarctica. Ecological 

Monographs, 44:105–128. http://dx.doi.org/10.2307/1942321.

Fielman, K., and A. G. Marsh. 2005. Genome complexity and repetitive DNA in 

metazoans from extreme marine environments. Gene, 362:98–108. http://dx

.doi.org/10.1016/j.gene.2005.06.035.

Kim, S. L., K. K. Hammerstom, K. E. Conlan, and A. R. Thurber. 2010. Polar ecosystem dynamics: Recovery of communities from organic enrichment in McMurdo Sound, Antarctica. Integrative Comparative Biology, 50:1031–1040. 

http://dx.doi.org/10.1093/icb/icq058.

Kim, S. L., A. Thurber, K. K. Hammerstrom, and K. E. Conlan. 2007. Seastar response to organic enrichment in an oligotrophic polar habitat. Journal of 

Experimental Marine Biology and Ecology, 346:66–75. http://dx.doi.org/10

.1016/j.jembe.2007.03.004.

Krupnik, I., M. A. Lang, and S. E. Miller, eds. 2009. Smithsonian at the poles: Contributions to International Polar Year science. Washington D.C.: Smithsonian 

Institution Scholarly Press.

Lang, M. A. 2009. Parameters of extreme environment diving. In The future of diving: 100 years of Haldane and beyond, ed. M. A. Lang and A. O. Brubakk, pp. 

153–159. Washington, D.C.: Smithsonian Institution Scholarly Press.

Lang, M. A., and M. D. J. Sayer, eds. 2007. Proceedings of the International Polar 

Diving Workshop, Svalbard, March 15–21, 2007. Washington, D.C.: Smithsonian Institution.

Lenihan, H., C. Peterson, S. L. Kim, K. E. Conlan, R. Fairey, C. McDonald, 

J. Grabowski, and J. Oliver. 2003. Variation in marine benthic community 

composition allows discrimination of multiple stressors. Marine Ecology 

Progress Series, 261:63–73. http://dx.doi.org/10.3354/meps261063.

Marsh, A. G., P. Leong, and D. Manahan. 1999. Energy metabolism during embryonic development and larval growth of an Antarctic sea urchin. Journal of 

Experimental Biology, 202:2041–2050.

Marsh, A. G., and D. Manahan. 1999. A method for accurate measurements of the 

respiration rates of marine invertebrate embryos and larvae. Marine Ecology 

Progress Series, 184:1–10. http://dx.doi.org/10.3354/meps184001.

———. 2000. Metabolic differences between “demersal” and “pelagic” development of the Antarctic sea urchin Sterechinus neumayeri. Marine Biology, 

137:215–221. http://dx.doi.org/10.1007/s002270000364.

Marsh, A. G., R. Maxson, and D. Manahan. 2001. High macromolecular synthesis 

with low metabolic cost in Antarctic sea urchin embryos. Science, 291:1950–

1952. http://dx.doi.org/10.1126/science.1056341.

McClintock, J. B., C. D. Amsler, and B. J. Baker. 2010a. Overview of the chemical ecology of benthic marine invertebrates along the western Antarctic 

peninsula. Integrative and Comparative Biology, 50:967–980. http://dx.doi

.org/10.1093/icb/icq035.

McClintock, J. B., C. D. Amsler, A. L. Moran, H. A. Woods, and B. J. Baker. 2010b. 

Introduction to the symposium: Advances in Antarctic marine biology. Integrative and Comparative Biology, 50:948–949. http://dx.doi.org/10.1093

/icb/icq005.

McClintock, J. B., and J. Gauthier. 1992. Antimicrobial activities of Antarctic 

sponges. Antarctic Science, 4:179–183. http://dx.doi.org/10.1017/S095410

2092000270.

McClintock, J. B., and J. S. Pearse. 1986. Organic and energetic content of eggs and 

juveniles of Antarctic echinoids and asteroids with lecithotrophic development. Comparative Biochemistry and Physiology, A. Physiology, 85:341–345. 

http://dx.doi.org/10.1016/0300-9629(86)90259-8.

———. 1987. Biochemical composition of Antarctic echinoderms. Comparative Biochemistry and Physiology, B. Biochemistry and Molecular Biology, 

86:683–687. http://dx.doi.org/10.1016/0305-0491(87)90211-2.

McClintock, J. B., and J. Vernon. 1990. Chemical defense in the eggs and embryos 

of Antarctic sea stars (Echinodermata). Marine Biology, 105:491–495. http://

dx.doi.org/10.1007/BF01316320.

Moran, A. L., and H. A. Woods. 2010. Limits to diffusive O2

 transport: Flow, form, 

and function in nudibranch egg masses from temperate and polar regions. 

PLoS One, 5:1–8. http://dx.doi.org/10.1371/journal.pone.0012113.

Oliver, J. 1984. Selection for asexual reproduction in an Antarctic polychaete 

worm. Marine Ecology Progress Series, 19:33–38. http://dx.doi.org/10.3354

/meps019033.

Pearse, J. S. 1966. Antarctic asteroid Odontaster validus: Constancy of reproductive periodicities. Science, 152:1763–1764. http://dx.doi.org/10.1126/science

.152.3730.1763.

———. 1967. Coelomic water volume control in Antarctic sea-star Odontaster 

validus. Nature, 216:1118–1119. http://dx.doi.org/10.1038/2161118a0.

Pearse, J. S., and S. Lockhart. 2004. Reproduction in cold water: Paradigm changes 

in the 20th century and a role for cidaroid sea urchins. Deep Sea Research 

Part II: Topical Studies in Oceanography, 51:1533–1549. http://dx.doi.org

/10.1016/j.dsr2.2004.06.023.

Pearse, J. S., J. B. McClintock, and I. Bosch. 1991. Reproduction of Antarctic benthic marine invertebrates: Tempos, modes, and timing. American Zoologist, 

31:65–80.

Peters, K. J., C. D. Amsler, J. B. McClintock, and B. J. Baker. 2010. Potential chemical defenses of Antarctic sponges against sympatric microorganisms. Polar 

Biology, 33:649–658. http://dx.doi.org/10.1007/s00300-009-0741-z.

Peters, K. J., C. D. Amsler, J. B. McClintock, R. W. M. van Soest, and B. J. Baker. 

2009. Palatability and chemical defenses of sponges from the western Antarctic Peninsula. Marine Ecology Progress Series, 385:77–85. http://dx.doi

.org/10.3354/meps08026.

Slattery, M., and J. B. McClintock. 1995. Population structure and feeding deterrence in three shallow-water Antarctic soft corals. Marine Biology, 122:461–

470. http://dx.doi.org/10.1007/BF00350880.

Slattery, P., and J. Oliver. 1986. Scavenging and other feeding-habits of lysianassid 

amphipods (Orchomene spp.) from McMurdo Sound, Antarctica. Polar Biology, 6:171–177. http://dx.doi.org/10.1007/BF00274880.

Ulrich, P. N., and A. G. Marsh. 2009. Thermal sensitivity of mitochondrial respiration efficiency and protein phosphorylation in the clam Mercenaria 

mercenaria. Marine Biotechnology, 11:608–618. http://dx.doi.org/10.1007

/s10126-009-9177-2.

Woods, H. A., and A. L. Moran. 2008a. Oxygen profiles in egg masses predicted 

from a diffusion-reaction model. Journal of Experimental Biology, 211:790–

797. http://dx.doi.org/10.1242/jeb.014613.

———. 2008b. Temperature–oxygen interactions in Antarctic nudibranch egg 

masses. Journal of Experimental Biology, 211:798–804. http://dx.doi.org/10

.1242/jeb.014621.

Woods, H. A., A. L. Moran, C. P. Arango, L. Mullen, and C. Shields. 2009. Oxygen 

hypothesis of polar gigantism not supported by performance of Antarctic 

pycnogonids in hypoxia. Proceedings of the Royal Society, B: Biological Sciences, 276(1659):1069–1075. http://dx.doi.org/10.1098/rspb.2008.1489.
The Use of Scuba to Study Early Life 

Histories of Marine Invertebrates

Harilaos A. Lessios, Howard R. Lasker, and Don R. Levitan

ABSTRACT. Scuba has permitted in situ research of the early life histories of subtidal marine invertebrates, limited only by the small size of early stages. Investigators have used scuba to observe, 

among other things, coral spawning, including the spectacular mass spawns on the Great Barrier 

Reef, which established that most corals are hermaphroditic broadcast spawners. Observations and 

experiments have been conducted to measure fertilization rates of free-spawning species, such as 

octocorals, sea cucumbers, sea urchins, and sea stars. Experiments have measured relative male reproductive success and the gamete traits that influence it in sea urchins. Finally, in tunicates, which 

produce larvae large enough to be seen by the naked eye and short-lived enough to be followed on 

a single dive, scuba has allowed direct observation from release to settlement, thus helping to shed 

some light on this process, which otherwise can only be studied indirectly.

INTRODUCTION

The reproductive biology of marine organisms was, during the nineteenth century, 

the realm of zoologists and embryologists. Dissection and histological analysis of adults 

identified reproductive cycles, and careful study of the morphology of embryos and their 

metamorphoses into adults was a hallmark of “nineteenth century biology.” The products 

of those efforts—expansive, often beautifully illustrated monographs—form the basis 

of our understanding of the reproductive biology of many marine invertebrates. This 

foundation was skewed toward taxa that could be studied in the laboratory or could be 

readily collected and observed. Entering the water and finding out what these organisms 

do in nature is an essential additional component to this foundation. If the American 

baseball player Yogi Berra’s dictum, “You can observe a lot by watching,” is correct, then 

it is scuba that has allowed researchers to “watch.”

For over a century it has been recognized that understanding the early life history 

stages of marine organisms is critical to understanding their population dynamics. Yet it 

was only in the 1980s that researchers took to the field to observe these stages. With the 

advent of scuba, investigators were able to conduct careful observations on the relative 

importance of different life stages and determine what traits made individuals more or 

less likely to survive through these transitions. Observations and experiments took time, 

patience, and a careful hand, requirements that provided an excellent match between the 

research question and the use of scuba.

In this chapter we consider how in situ observations and experiments have provided 

information on spawning behavior, fertilization, larval survivorship, and settlement of 

several marine invertebrates. Our aim is to illustrate how the use of scuba has permitted the acquisition of critical knowledge connected to early life histories in the natural 

environment.

Harilaos A. Lessios, Smithsonian Tropical Research Institute, Box 0843-03092, Balboa, Panama. Howard R. Lasker, Graduate Program in 

Evolution, Ecology and Behavior, Department 

of Geology, University at Buffalo, Buffalo, New 

York 14260, USA. Don R. Levitan, Department 

of Biological Science, Florida State University, Tallahassee, Florida 32306, USA. Correspondence:

H. Lessios, Lessiosh@si.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
8 8 • smithsonian contributions to the marine sciences

THE USE OF SCUBA TO STUDY 

THE REPRODUCTIVE BIOLOGY 

OF MARINE INVERTEBRATES

Spawning Observations

A striking example of the role of scuba in facilitating new 

knowledge is the reproductive biology of corals. At the start of 

the twentieth century, few data were available about coral reproductive biology. Reports characterized scleractinians as brooders 

that released fully developed planula larvae. Although there were 

data indicating that some species broadcast gametes (see references in Fadlallah and Pearse, 1982), the suggestion that scleractinians were primarily brooders (Marshall and Stephenson, 

1933; Yonge, 1940) persisted until the 1980s.

This perception was corrected when a group of researchers 

from James Cook University discovered a mass spawning event 

on the Great Barrier Reef (Harrison et al., 1984). In that first 

publication on the mass spawning, the number of scleractinians 

known to broadcast spawn grew from eight to over sixty. The 

in situ observations of spawning behavior and characterizations 

of the extent and timing of the event were the product of scuba 

use. Similarly, the microscopic examination of tissue and the 

laboratory observations, which were also an important component of the research, were dependent on scuba for the collection 

of specimens. Scuba allowed the study of reproductive biology 

to expand from those species that could be readily collected in 

shallow pools and exposed tidal flats to species in the full extent of the reef. The images of the spawning event electrified a 

generation of researchers who proceeded to search for similar 

events at other locations. The data from the Great Barrier Reef 

mass spawning continued to grow (Babcock et al., 1986), and 

additional reports from the Pacific and the Caribbean (Szmant, 

1986; Van Veghel, 1993) led to the conclusion that the majority 

of scleractinian taxa are hermaphroditic and broadcast spawners (Richmond and Hunter, 1990; Carlon, 1999). The most 

recent review of the literature (Harrison, 2011) identifies 367 

broadcast-spawning species compared to 75 that brood planulae. It is difficult to imagine that our understanding would be as 

complete without the use of scuba.

Although many species exhibit some degree of synchrony 

among individuals, observations of spawning are rare. An event 

that lasts minutes to hours and occurs on only a few days each 

year is not readily observed. Perhaps the greatest contribution 

of scuba to increasing our knowledge of spawning is that it enables researchers to spend large amounts of time in the water and 

serendipitously observe spawning events. For instance, Hendler 

and Meyer (1982), Lessios (1984), Pearse et al. (1988), McEuen 

(1988), Lamare and Stewart (1998), and Himmelmann et al. 

(2008) all report observations of spawning events in a variety 

of echinoderms. In a study of reproduction of Strongylocentrotus spp., Levitan (2002a) twice observed natural spawning by 

S. franciscanus, and was able to incorporate data from these 

events into a study that otherwise relied on induced spawning. 

Serendipity is a key factor in discovering spawning events, but 

the good fortune in all of these studies was facilitated by many 

hours of diving. 

The discovery of the mass spawning event on the Great 

Barrier Reef led to observations of other taxa (Babcock et al., 

1986; Alino and Coll, 1989; Babcock et al., 1992) and inspired 

efforts to discover similar events in the Caribbean (Gittings et al., 

1992; Van Veghel, 1993; de Graaf et al., 1999). Other studies in 

which divers have identified spawning times and patterns have 

their origins in observations of tissue samples that indicate the 

general timing of spawning. For instance, observations of tissue 

samples led Lindquist et al. (1997) to place covers over colonies 

of two species of Caribbean sponges to collect their gametes and 

characterize the timing of their spawning. While scuba provides a 

window on spawning events, it does not always produce dramatic 

results. For instance, Beiring and Lasker (2000) used the presence 

of gonad in collected specimens to predict spawning of Eunicea 

(Plexaura) flexuosa in Panama, but were able to observe spawning in only a small number of colonies relative to the number 

of colonies that were believed to spawn over the weeks of their 

observations. Similarly, many of the spawning events reported by 

Babcock et al. (1992) involved only small numbers of individuals.

Species with well-synchronized and predictable spawning 

events have been particularly amenable to study using scuba.

Once the basic information on spawning has been elucidated, 

scuba has provided researchers with the ability to make detailed 

observations and conduct elaborate experiments to study various aspects of reproductive biology. For instance, a variety of 

studies have investigated the role of the timing of spawning in 

reproductive isolation of closely related species with both intraspecific and interspecific differences being observed (Van Veghel, 

1993; Sanchez et al., 1999; Van Oppen et al., 2002; Levitan et 

al., 2004). 

Fertilization Success

Mortensen (1938) considered fertilization to be a significant 

obstacle in the life history of broadcast spawners. In contrast, in 

a paper that for decades was one of the guiding forces of benthic ecology, Thorson (1946) considered and rejected the likelihood of variation in successful production of embryos. These 

hypotheses were examined in a series of experiments by Pennington (1985). Working with the sea urchin Strongylocentrotus 

droebachiensis, Pennington was able to show that in natural settings sperm released by males in induced spawning events were 

rapidly diluted. As sperm were advected, the probability of fertilization decreased dramatically within meters of the spawning 

male. These experiments, which were conducted by scuba divers in 10 m depths, were followed by theoretical papers (Denny, 

1988; Denny and Shibata, 1989) that underscored the difficulty 

of achieving high fertilization rates in some environments. Subsequent work with sea urchins has raised a number of methodological questions about the appropriate manner to assess 

fertilization success (Thomas, 1994; Yund and Meidel, 2003; 
number 39 • 8 9

Yund et al., 2005). However, regardless of the precise values 

of fertilization rates, Pennington’s study changed the paradigm 

to one in which fertilization success was not necessarily high. 

Where, when, and how marine species achieve high fertilization 

success is a fundamental question in their reproductive biology 

that relates to the fitness of individuals, the sustenance of populations, and even the efficacy of such conservation approaches as 

marine protected areas.

Assessing fertilization rates in the field requires access to 

benthic organisms as they spawn, which (with the exception of 

intertidal or very shallow habitats) requires the use of scuba. Fertilization probabilities measured in the field vary widely among 

studies. While cases of sperm limitation have been reported, most 

studies include at least some examples of high probabilities of 

fertilization. This may reflect the importance of fertilization rates 

and thus of strong selection for mechanisms that enhance fertilization, or alternately it may be a reflection of the life history of 

organisms that have been studied. 

The first series of reports of in situ measurements of fertilization rates appeared in 1992 (Babcock and Mundy, 1992; Babcock et al., 1992; Brazeau and Lasker, 1992; Oliver and Babcock, 

1992; Sewell and Levitan, 1992). Babcock et al. (1992) based 

their estimates of fertilization success on collections of eggs from 

the water column following their release from several Great Barrier Reef holothurians. They reported fertilization success ranging from 0% to 96%. The proportion of eggs fertilized in the 

spawning events varied among species, by day, time of day, and 

number and proximity of spawning individuals. Most of the values were well over 50%, with the sea cucumber Bohadshia argus

having fertilization success ranging from 86% to 96% during the 

same night. Most studies suggest eggs are fertilized at the peak 

of spawning events: eggs spawned early in the event, late in the 

event, or by relatively isolated individuals can have low, sometimes near-zero fertilization rates. Sewell and Levitan (1992) 

found high fertilization success in a spawning sea cucumber. The 

octocoral Plexaura kuna exhibits fertilization success that varies 

with day of the spawning event and current speed (Lasker et al., 

1996). Individual samples had fertilization success ranging from 

0% to 100%, and the monthly means for the multi-day synchronous spawning events ranged from 0% to 60.4%. Similarly collected data for Pseudoplexaura porosa found overall fertilization 

success to be 67%, but the rates varied with day and position on 

the reef (Coma and Lasker, 1997). Up to 83% of Acanthaster 

planci eggs were fertilized (Babcock and Mundy, 1992). Eggs 

released by individuals that were over 60 m from the nearest 

male still had fertilization success rates of 23%. All of the eggs 

collected in these studies were obtained using scuba. Eggs of octocorals (which are large and positively buoyant) could possibly 

have been collected on the surface downstream of the spawning 

colonies, but counting the numbers of colonies spawning and 

characterizing the fine-scale variation that was observed would 

have been impossible without scuba.

Fertilization success has also been measured in several 

species that brood. Brazeau and Lasker (1992) estimated 

fertilization rates of the octocoral Briareum asbestinum on two 

reefs in the San Blas Islands, Panama. The estimates of Brazeau 

and Lasker (1990) were based on comparisons between the number of mature eggs present in the polyps and the numbers of 

embryos produced by the colonies. Values of fertilization success 

on reefs that had relatively low abundances of B. asbestinum are 

among the lowest reported in natural spawning events. In many 

instances none of the eggs were fertilized, and in the best of three 

years the average success was only 20%. As might be expected 

in a system with low fertilization success, colonies with nearby 

males did better. In contrast, estimates of fertilization success are 

markedly higher for Pseudopterogorgia elisabethae, a Caribbean 

octocoral that also surface broods (Lasker, 2006), and for the 

scleractinian Goniastrea favulus (Miller and Mundy, 2005). Fertilization occurs on the colony surface in both of these species 

and in both, the fertilization of released eggs approached 100% 

in some samples.

Estimating Male Reproductive Success

Most work on fertilization ecology has focused on the percentage of eggs that are fertilized. Female success provides key 

information on the demographic effects of sperm availability and 

how females with different traits might be under differential selection. Estimates of male fertilization success are also critical for 

understanding selection on male traits and for determining the 

relative intensity of sexual selection between males and females. 

Measures of male reproductive success have lagged behind female estimates because they are more difficult to obtain. As the 

use of genetic markers has become more efficient, more affordable, and possible with tiny embryos, estimates of male reproductive success have started to emerge. 

The first estimates of male reproductive success focused on 

species that brood offspring. In these species, females retain eggs 

and collect sperm for fertilization from the water column. Estimating parentage from brooders is somewhat simplified because 

maternity is known and only paternity must be estimated. In addition, embryos can be collected more simply from the brood 

chamber. Divers do not need to be on hand during the moment of 

spawning to collect eggs and embryos in the sea during brief and 

often unpredictable spawning events. The first study of male success was conducted on the ascidian Botryllus schlosseri (Grosberg, 1991). Colonies bred to be homozygous for rare alleles 

were explanted, and their sperm were allowed to disperse. After 

two weeks, samples from adult colonies at marked distances 

from these source colonies were collected, and embryos were 

analyzed for these rare alleles. The results showed that paternity 

rapidly diminished over the first 50 cm from the focal colony, 

suggesting that effects of sperm on gene flow are highly localized. Further experimental work with brooding species of both 

Botryllus and the bryozoan Celleporella hyalina has investigated 

how the presence of nearby mates influences the likelihood of 

mating with more distant mates and also the likelihood of selfing 

versus outcrossing (Yund and McCartney, 1994).
9 0 • smithsonian contributions to the marine sciences

Work using scuba to place and retrieve experimental arrays 

of sessile brooding invertebrates examined the consequences of 

egg versus sperm allocation on reproductive success in hermaphroditic species. The hypothesis was that hermaphrodites should 

allocate much more energy toward eggs than sperm if fertilization requires a one to one interaction between sperm and egg, 

and if sperm are smaller than eggs. Empirical data, however, indicated that energy allocation was much more even between the 

male and female gametes than predicted. Subtidal experiments 

showed that under conditions of competition, individuals allocating more energy to sperm garnered higher success (McCartney, 

1997; Yund, 1998). More recent work also demonstrated that 

even in the absence of competition, increased allocation to sperm 

allowed individuals to overcome sperm limitation when mates 

were distantly located (Johnson and Yund, 2009). Combined, 

these findings provide a potential explanation for similar levels 

of investment to male and female gametes in hermaphrodites.

Patterns of paternity, and multiple parentage in natural populations of brooding invertebrates, has also been explored using 

scuba. Studies on both ascidians (Johnson and Yund, 2007) and 

soft corals (Lasker et al., 2008) suggest that multiple paternity is 

common, and that patterns of paternity are not clearly related to 

mate distance, body size, or density. It may be that the timing of 

release of sperm may influence paternity more than differences 

in mate distance; nearby mates have no chance at fertilization 

if they release sperm when eggs are not available. Experiments 

conducted on broadcast-spawning individuals indicate that male 

timing is critical to fertilization and paternal success (Levitan, 

2005). In addition to timing effects, there is some evidence indicating that increases in the number of males contributing 

sperm can influence the fraction of fertilized eggs (Purchase et 

al., 2007), presumably because eggs vary in their compatibility 

with different kinds of sperm. High multiple paternity across 

gradients of adult density (Johnson and Yund, 2007) or distance 

(Lasker et al., 2008) may reflect the importance of both timing 

and gametic compatibility that results in genetic variation within 

a brood across these demographic conditions.

Paternity from natural spawning has been measured in one 

system of a broadcasting marine invertebrate. Coffroth and 

Lasker (1998) established long-term studies of male and female 

reproductive success in the broadcast spawning soft coral Plexaura kuna. This species often fragments asexually. Male reproductive success was examined as a function of distance from a 

focal female to each male genotype and the number of colonies 

that belonged to each genotype (clone size). Plexaura kuna predictably broadcasts gametes 3 to 9 days following the full moon, 

releasing eggs large enough to be seen by divers. Egg samples 

were collected into syringes by divers located downstream of 

spawning female colonies. Embryos were reared for several days 

and then frozen for genetic analysis using RAPD markers. Most 

variation in male reproductive success could be attributed to 

their distance from the female. In addition, clone size might indirectly influence paternal success by spreading individuals across 

a larger area, thus decreasing the distance to potential mates.

The Use of Scuba to Determine if Gamete Traits

Influence Fertilization in the Sea

Gamete interactions have been studied in the laboratory for 

the past hundred years (e.g., Lillie, 1915). Gamete traits such 

as egg size (Levitan, 1993; Marshall et al., 2002), egg accessory 

structures (Podolsky, 2002; Farley and Levitan, 2001), chemical attractants (Miller, 1966; Riffell et al., 2004), sperm velocity (Levitan, 2000a; Kupriyanova and Havenhand, 2002), and 

sperm-egg compatibility (Hagström and Lönning, 1967; Evans 

and Marshall, 2005) have been shown in the laboratory to influence the rate of fertilization within species and the likelihood of 

hybridization across species. However, to understand the fitness 

consequences of variation in sperm and egg traits it is necessary 

to study it in the sea. There is reason to doubt the importance of 

variation in these traits because the velocity of water flow (cm to 

m per second; Denny, 1988) can be orders of magnitude greater 

than sperm velocity (~200 micrometers per second; Levitan et al., 

1991), and because mate density and distance exert large effects 

on the local concentration of sperm (Pennington, 1985; Levitan, 

2002a). These variables could perhaps swamp the consequences 

of subtle variation in traits such as sperm velocity or egg receptivity. Determining how gamete traits influence reproductive success in the sea provides support for the numerous theories on 

how sperm availability influences gamete morphology (Levitan, 

2000b; Podolsky, 2004; Luttikhuizen et al., 2004) and compatibility (Swanson and Vacquier, 2002; Zigler et al., 2005).

Field studies conducted along the shores of Vancouver 

Island, British Columbia have investigated the influence of sperm 

availability and gamete traits on fertilization in three congeneric 

subtidal sea urchins: Strongylocentrotus droebachiensis, S. franciscanus, and S. purpuratus. Gamete traits vary in these three 

species. Strongylocentrotus purpuratus has the smallest eggs and 

requires the highest sperm concentrations to achieve fertilization; 

it is also the species with eggs most resistant to polyspermy and 

has the fastest, but shortest-lived sperm. Strongylocentrotus droebachiensis has the opposite traits: large eggs that require the least 

amount of sperm to achieve fertilization but are the most susceptible to polyspermy, and the slowest, but longest-lived sperm.

Strongylocentrotus franciscanus is intermediate in all these traits 

(Levitan, 1993; Levitan et al., 2007). This gradient in gamete 

traits is consistent with S. purpuratus having gamete traits best 

adapted to high levels of sperm availability and S. droebachiensis having traits best adapted to low levels of sperm availability. 

Field surveys using scuba documented that along the outer west 

coast of Vancouver Island these traits match the level of aggregation and population density seen among these three species; 

average nearest-neighbor distances (Levitan, 2002b) and local 

densities (Levitan, 2002a) indicate that S. purpuratus lives in 

the most crowded populations and S. droebachiensis lives in the 

most sparse ones.

Subtidal field experiments have examined how gametes from 

these three species perform under a range of conditions of sperm 

availability. The first set of experiments was intended to isolate 
number 39 • 9 1

gametes from the adults to see how within- and among-species

variation in gamete performance in the field could be predicted 

by how well they performed in the laboratory. The protocol was 

to induce sea urchins to spawn in the laboratory and measure 

gamete traits and gamete performance. Then the protocol was to 

bring these gametes into the field and release them, wait for fertilization to occur, and then collect eggs with a subtidal plankton 

pump. Collected eggs were then brought back to the laboratory to 

determine the fertilized fraction. The results of these studies documented that individuals that produced gametes that performed 

well in the laboratory also produced gametes that performed 

well in the ocean; the subtle differences in gamete traits noted 

in the laboratory translated into fitness differences in the ocean 

(Levitan, 1996). The results also documented that each species 

produced gametes that performed best under conditions of sperm 

availability that were typical for that species (Levitan, 1998).

A second set of field experiments attempted to reflect spawning in nature more accurately. Sea urchins were induced to spawn 

in situ via an injection of 0.55 mol/L KCl solution and then 

placed back into their natural locations across a range of population densities and flow conditions (Levitan, 2002a). In these experiments, a 5×5 meter grid was established on the bottom over

a range of sea urchin abundances. All the sea urchins from one 

species within the grid were injected with KCl to induce spawning. After 30 minutes, the position of all individuals was mapped 

and a sample of eggs was collected above each female with a 

subtidal plankton pump. Patterns of water flow and depth were 

measured with a S4 current meter, which recorded flow and water 

depth every 0.5 s. The results indicated strong effects of population density and abundance, but also revealed species differences 

as suggested by the previous study, which had examined gamete 

traits independently of adult spawning behavior; S. purpuratus

performed best at high population densities, but S. droebachiensis

performed best at low densities (Levitan, 2002a). Manipulation 

of S. purpuratus to lower densities than typical resulted in that 

species doing poorly relative to the other two species (Levitan, 

2002a). Further tests, examining how S. franciscanus performed 

at higher densities, indicated that this species was much more 

susceptible to embryo death caused by polyspermy compared 

to S. purpuratus (Levitan, 2004). In sum, the field studies suggest that these species have gamete traits that perform best under 

typical conditions and also suggest density-dependent selection of

gamete traits based on levels of sperm availability.

Investigations of patterns of sexual selection and the influence of selection on gamete traits (specifically on gamete recognition proteins) used the same field protocols as above, with the 

addition that the developing embryos were cultured for three 

days, and then frozen for parentage analysis (Levitan, 2004; 

2008). In addition, tube foot samples were collected from all 

adults in the experiment for genetic analysis to determine their 

reproductive success, but also to sequence sperm bindin, a protein on the head of the sperm that binds to a receptor on the surface of the egg (Levitan and Ferrell, 2006; Levitan and Stapper, 

2010). These experiments were conducted with S. franciscanus

and S. purpuratus, species that differ in their susceptibility to 

polyspermy. The results of the parentage analysis indicated that 

in S. franciscanus the level of male competition for eggs was similar across male densities. Across densities ranging from sperm 

limitation to polyspermic conditions the variance in reproductive 

success was relatively high and constant; there were male winners and losers at all densities. 

The pattern in females was more complex. At low sperm 

densities, there was high variance in female success caused by 

sperm limitation. As male density increased, female fertilization 

success increased to the point where all females were saturated 

with sperm and the variance among females was very low; all 

females were successful. However, as densities increased further, 

variance in female reproductive success increased again, driven 

by variation in polyspermy among eggs produced by different 

females. These results suggest very different selective pressures at 

high and low sperm densities. At low densities both males and 

females are selected to produce gametes with the capacity for a 

high rate of fertilization. However, at high densities, eggs suffer 

from polyspermy, so that females producing eggs less compatible with sperm avoid embryo death. Males, on the other hand, 

should compete for fertilization and be selected for higher fertilization rates. This produces sexual conflict over fertilization rate 

(and gametic compatibility) at high densities (Levitan, 2004).

Individuals from this same experiment were then sequenced 

to determine their sperm bindin genotype. The results indicated 

that males with a common form of the protein had a fertilization 

advantage over males with a rarer form of the protein, while 

females with the rarer genotypes were more successful. Further 

analysis indicated that males that matched females at the sperm 

bindin locus were most successful at low densities when sperm 

were limited, while mismatched individuals had higher success 

at high densities when polyspermy was common (Levitan and 

Ferrell, 2006). These findings and similar results noted in S. purpuratus (Levitan, 2008; Levitan and Stapper, 2010) suggest that, 

in spite of the large influences of water flow and distance on 

reproductive success, subtle within-species differences in gametic 

compatibility can be important in determining fertilization success in the sea.

The Use of Scuba to Follow

the Fate of Planktonic Larvae

Many benthic marine organisms display dual life cycles. The 

adults are sessile or sedentary, but they produce planktonic larvae that are released in the water column, where they stay for 

different lengths of time ranging from a few minutes to several 

months, and travel with the currents to distant locations (Scheltema, 1988) where they settle to complete the life cycle. The fate 

of such larvae is an important parameter, both in the study of the 

life history of particular species (Stearns, 1977) and in our understanding of the factors that affect marine community composition 

(Lewin, 1986; Underwood and Fairweather, 1989; Grosberg and 

Levitan, 1992; Roughgarden et al., 1994). However, given their 
9 2 • smithsonian contributions to the marine sciences

microscopic size, often unpredictable release, and frequently long 

planktonic stages, larvae are difficult or impossible to observe directly in nature. Thus in most instances investigators have had to 

rely on indirect methods of assessing the mode and rate of larval 

influx into benthic ecosystems. Such methods include radioactive 

labeling and release of larvae into their native habitat (Arnold et 

al., 2005); comparison of larval supply (determined by plankton 

sampling) to quantities of metamorphosing juveniles (Grosberg, 

1982; Yoshioka, 1982; Lamare, 1998; Lamare and Barker, 1999; 

Doherty et al., 2004; Mariani et al., 2005; Pineda et al., 2010); or 

identification of paternity using genetic markers (Grosberg and 

Quinn, 1986; Mackie et al., 2006). Though the study of the larval lives of most organisms has necessarily relied on such indirect 

methods or on laboratory observations, the larvae of a few organisms are large enough to be seen with the naked eye, and the 

planktonic phase is short enough to be followed by divers on a 

single tank of air. Through the use of scuba, a handful of studies 

have taken advantage of these properties to elucidate important 

aspects of larval behavior and their consequences for successful 

establishment events.

Olson (1983; 1985) was able to follow the larval fate of the 

ascidian Diademnum molle at Lizard Island, Australia. Diademnid larvae remain in the plankton for a matter of minutes or 

hours and are large enough to be seen by the naked eye. Species 

of the family Diademnidae also release their larvae at a predictable time every day of the year. Variation in the timing of release 

among species appears to depend on whether a species contains 

symbiotic algae. Species that lack algae release larvae around 

dawn, whereas those that possess algae release larvae near the 

middle of the day. Diademnum molle larvae are 2.5 mm long and 

contain algae of the genus Prochloron sufficient to add color and 

thus be visible under water. Olson (1983) was able to track 89 

larvae, 14 of them from release to settlement. Newly released larvae displayed positive phototaxis and swam toward the surface. 

After one to ten minutes, the phototaxis was reversed, and the 

larvae appeared to be attracted by dark surfaces, including divers’ wetsuits. The planktonic stage of the 14 larvae that could be 

followed from release to settlement ranged from 40 seconds to 6 

minutes. Larvae that swam longer were often lost from observation before they settled, but laboratory experiments showed that 

in general they settle 20 minutes to 2 hours after release, with 

90% settling within 30 minutes. When a patch reef was denuded 

of adult colonies, recruitment ceased on a downstream reef that 

the larvae could reach within these times, but continued almost 

unaffected on a more distant downstream reef (Olson, 1985).

Monitoring of settling panels showed that the larvae overwhelmingly preferred to settle in dark spaces, and that the newly 

formed colonies died if exposed to bright light. Given that light 

appears to be lethal to the newly settled juveniles, a larval release 

in the middle of the day appears paradoxical, but it may well be 

an adaptation for allowing the larvae to choose spaces appropriate for adult growth by avoiding overly bright spots. The best 

time to choose a spot likely to remain shady for most of the day 

is during the period of most abundant light. Even though adult 

colonies can move over small distances, there is a clear advantage 

in choosing the proper habitat during the larval stage.

Davis (1987) also took advantage of the large size of ascidian 

larvae to perform direct observations of their behavior. He studied 

the settlement preferences of the colonial ascidian Podoclavella 

cylindrica, which releases 4 mm long larvae with easily observed 

bright blue coloration. Monitoring of natural recruitment showed 

that it was higher than expected by chance on bare space and on 

the sponge Euryspongia, but lower than expected on three other 

genera of sponges. Davis observed larvae approaching bare space 

and four kinds of sponges and scored how many settled on each 

substratum versus how many touched it and then released. Eighty 

four larvae could be followed from release to settlement. They 

showed a preference for settling on bare space or on unfouled 

surfaces of Euryspongia, with a high percentage of rejection of 

three other sponges. Davis also quantified post-settlement survival of recruits for 30 days, and found a tight correlation between larval substrate preference and juvenile survivorship. In a 

different study, Davis and Butler (1989) followed 100 larvae of 

Podoclavella moluccensis to assess how far they traveled before 

settlement. The distance ranged from 5 cm to 13.4 m, with nearly 

80% settling within 2.5 m of the point of release.

Potential sources of mortality could also be determined by 

following the larvae of both Diademnum molle (Olson 1983) 

and of Podoclavella moluccensis (Davis and Butler, 1989). Stony 

corals and hydroids often entangled the ascidian larvae. Entangled larvae usually were able to break free, but in some cases 

were ingested. Fishes that put the larvae in their mouth invariably spit them out, presumably because they are unpalatable. 

Such high rejection rates were not observed in a study conducted 

by Stoner (1990; 1994) in Hawaii on the larvae of the ascidian 

Diplosoma similis.

In Stoner’s (1990; 1994) study, 259 larvae of Diplosoma 

similis were followed in Kaneohe Bay, at the island of Oahu in 

Hawaii. Like Diademnum molle, Diplosoma similis is host to 

algal cells of the genus Prochloron. Larvae are approximately 

2 mm long and are released predictably in the morning hours, so 

they could be followed by divers. Stoner found that larvae swim 

for an average of 3.8 minutes and disperse at an average distance 

of 2.2 m from the parental colony. At approximately 42 seconds 

after release, the larvae swam down toward the substratum, 

maintaining a distance of a few centimeters from it. At a mean 

time of approximately two minutes after release, they contacted 

the surface of the reef. Dead coral, an unidentified sponge, and 

the green algae Dictyosphaeria were preferred points of contact. 

After contact, they moved along the bottom for a distance of 

20 cm before losing their tails and settling to form new colonies 

(Stoner, 1994). Of the total number of larvae that were followed 

by divers, 34% were lost from observation. Of the remaining 

171 larvae, 71% settled successfully, and 49% were either eaten 

by planktivores or became ensnared in mucus sheaths of coral 

and the larvacean Oikopleura, an important difference from the 

larvae of Diademnum molle observed by Olson (1983) and of 

Podoclavella cylindrica observed by Davis (1987). 
number 39 • 9 3

Predation by pomacentrids and coral was also high on 

another ascidian, Lissoclinum patella (Olson and McPherson, 

1987). Post-settlement mortality of Diplosoma similis was much 

higher than mortality in the larval stage: 50% of the newly metamorphosed individuals perished within one day of metamorphosis, and none survived longer than a month (Stoner, 1990).

These studies, along with a few others (e.g., Young and 

Chia, 1984) have greatly increased our knowledge of events that 

occur in the larval life stage of ascidians and of the factors that 

influence their rate of entering benthic communities. The extent 

to which information from ascidians can be generalized to other 

organisms with much longer periods in the plankton, particularly planktotrophic ones, remains to be determined. Scuba cannot be used for direct observations of larvae that measure less 

than 1 mm or that stay in the water column for long periods of 

time, but it is still useful in documenting the beginning of their 

lives (i.e., their release) and the stage at which they are transformed to their sedentary stage (i.e., settlement).

The Use of Scuba to Determine Larval Settlement

Settlement, the selection of substrate and metamorphosis 

into the sedentary phase, is a critical phase in the lives of many 

marine organisms. However, it can be observed only when larvae 

are large enough to be seen as they settle (see section on larval observations). For most organisms we can study only recruitment, 

the addition of individuals to an arbitrary age class as they grow. 

Each study of recruitment attempts to concentrate on recruitment 

to the smallest size that can be observed within sampling intervals (dictated by logistic considerations) in order to deduce as 

accurately as possible the processes that affect settlement. Stoner’s 

(1990) finding that 50% of newly metamorphosed ascidian colonies perished within a day after larval settlement suggests that 

the window provided by recruitment for a realistic view of settlement may be very narrow. Although this is expected to vary with 

the type of organism (Hunt and Scheibling, 1997), 30 studies on 

bivalves, gastropods, barnacles, ascidians, bryozoans and echinoderms, reviewed by Gosselin and Qian (1997), all suggest that 

juvenile mortality is generally quite high. High mortality before 

the first observation of recruiting juveniles can lead to erroneous 

estimates of settlement, particularly if mortality is not random, 

though the unknowable distortions do not necessarily affect all 

studies. For example, studies that seek to quantify the number of 

juveniles of a particular species that enter the benthic community 

at a given time can accommodate net recruitment without knowledge of pre- versus post-settlement mortality.

Without scuba, recruitment of juvenile marine organisms 

can be studied in only the intertidal (e.g., Crisp, 1961; Connell, 

1972; Strathmann et al., 1981; Grosberg, 1982; Connell, 1985) 

or on panels that can be suspended in the water and then retrieved (e.g., Osman and Whitlatch, 1995). With the ability of 

divers to remain under water for long periods of time, the study 

of recruitment of both sessile and mobile juvenile marine organisms has blossomed and has resulted in more studies than can be 

reviewed here. Scuba has allowed non-destructive quantification 

of organisms that appear on a given natural or artificial substrate 

in pre-determined intervals, as well as comparisons and manipulations intended to uncover factors that affect the entrance of 

juveniles into benthic communities as the result of larval settling 

preferences (Highsmith, 1982; Snelgrove et al., 1999; Mariani et 

al., 2005), oceanographic conditions (Stoner et al., 1997), predation (Sammarco, 1980; 1982; Yoshioka, 1982; Doherty et al., 

2004), depth (Hurlbut, 1991), and other physical parameters 

(Yoshioka, 1982). 

Occasionally, the fortuitous occurrence of a major ecological shift during the period of monitoring has resulted in the opportunity to study a phenomenon of even wider importance than 

recruitment itself. An example of such a case has been the study 

of Bak (1985) of recruitment of the sea urchin Diadema antillarum during mass mortality suffered by this species. Bak (1985) 

studied the recruitment of juvenile Diadema to plastic grates suspended over the reef in Curaçao from 1982 to 1984. Diadema 

antillarum was, until 1983, a dominant component of Caribbean 

coral reefs, affecting community composition through its grazing 

of algae (Sammarco, 1982; Carpenter, 1986), predation on live 

coral (Bak and van Eys, 1975; Sammarco, 1980), and bioerosion 

of the calcium carbonate substrate (Scoffin et al., 1980). Starting 

in April 1983, D. antillarum suffered mass mortality, which was 

first noticed on the Caribbean coast of Panama, and was then 

followed as it affected all populations in the Caribbean and the 

western Atlantic (Lessios et al., 1984) one by one. Population 

densities in all studied localities were reduced by more than 97% 

(Lessios, 1988). The mass mortality front, traveling along coastal 

currents, reached Curaçao in October 1983 (Bak et al., 1984).

In Bak’s (1985) study, divers examined the small cells of the 

plastic grates similar to the ones shown in Figure 1 every two 

weeks and were able to locate juvenile sea urchins 1–3 mm in diameter. The number of recruits at each plate over time established 

that (1) recruitment was higher where the resident adult populations of the species were dense; (2) there were seasonal peaks 

of recruitment; and (3) a certain amount of growth of coralline 

algae on the grates was necessary for sea urchin recruitment, but 

excessive fouling of the plastic by algae depressed the number of 

juveniles observed by the divers. The number of small Diadema

located by Bak at each sampling interval between June 1982 and 

February 1984 was impressive. Maximum densities of juveniles 

were 102–188/m2

 recruited in a fortnight in June 1983. After 

February 1984, practically no juveniles recruited on the plastic 

grates through December 1984, when monitoring stopped. Thus, 

Diadema larvae were arriving at Curaçao for four months following the decimation of the adult populations on this island in 

October 1983. These larvae could have only come from other 

populations that had not yet been affected by the mass mortality. 

Indeed, D. antillarum populations on the coast of Venezuela died 

off in late November 1983 and at Barbados, upstream of Curaçao on the Caribbean Current, in early December 1983 (Lessios 

et al., 1984). In the laboratory, larvae of this species settle 34 to 

90 days after fertilization (Carpenter, 1997; Eckert, 1998), so the 
9 4 • smithsonian contributions to the marine sciences

cessation of recruitment in Curaçao in March 1984 is consistent 

with the hypothesis that larvae continued to arrive from as far 

as Barbados, then stopped after the Barbados populations were 

decimated. Bak’s study thus demonstrated not only factors that 

are important for eliciting settlement, but also the geographical 

extent of linkages between populations and the significance of 

events at distant places for settlement of a prominent component 

of the coral reef community.

Diadema antillarum populations in the Caribbean continued to remain low for the next quarter of a century (Lessios, 

2005; Chiappone et al., 2008; Miller et al., 2009). Vermeij et 

al. (2010) followed up on Bak’s (1985) study by setting up the 

same plastic grates on leeward reefs at Curaçao and monitoring 

recruitment from March to July 2005. They found that 22 years 

after the decimation of resident populations, the recruitment rate 

had increased by a factor of 56 relative to what it was immediately after the mass mortality, but was still half of what it was 

before this event. Despite this increase in recruitment, adult populations around the island remained low, indicating that settlement and recruitment are necessary but not sufficient causes for 

population recovery.

CONCLUSIONS

As the examples we presented in this chapter indicate (and 

they are only a small part of underwater research), much has 

been accomplished through scuba to study reproductive biology 

and early life histories of marine invertebrates. Some of the data 

that have been gathered have been the result of systematic or 

serendipitous observations, but a large part of marine research 

involves actual experimentation that was probably never envisioned in the days before autonomous diving became a reality. 

The study of biology will never be as easy under water as it is on 

land, but technological advancements that permit longer, deeper 

dives with less need for infrastructural support will, in the future, 

provide new insights into the life histories of marine organisms.

REFERENCES

Alino, P., and J. C. Coll. 1989. Observation of the synchronized mass spawning and 

postsettlement activity of octocorals on the Great Barrier, Australia: Biological aspects. Bulletin of Marine Science, 45:697–707.

Arnold, W. S., G. L. Hitchcock, M. E. Frischer, R. Wanninkhof, and Y. P. Sheng. 2005. 

Dispersal of an introduced larval cohort in a coastal lagoon. Limnology and 

Oceanography, 50:587–597. http://dx.doi.org/10.4319/lo.2005.50.2.0587.

Babcock, R. C., G. D. Bull, P. L. Harrison, A. J. Heyward, J. K. Oliver, C. C. Wallace, 

and B. L. Willis. 1986. Synchronous spawnings of 105 scleractinian coral 

species on the Great Barrier Reef. Marine Biology, 90:379–394. http://dx.doi

.org/10.1007/BF00428562.

Babcock, R. C., and C. N. Mundy. 1992. Reproductive biology, spawning and field 

fertilization rates of Acanthaster planci. Australian Journal of Marine and 

Freshwater Research, 43:525–534. http://dx.doi.org/10.1071/MF9920525.

Babcock, R. C., C. Mundy, J. Keesing, and J. Oliver. 1992. Predictable and unpredictable spawning events: In situ behavioural data from free-spawning coral 

reef invertebrates.Invertebrate Reproduction and Development, 22:213–228. 

http://dx.doi.org/10.1080/07924259.1992.9672274.

Bak, R. P. M. 1985. Recruitment patterns and mass mortalities in the sea urchin 

Diadema antillarum. Proceedings of the fifth International Coral Reef Congress, 5:267–272.

Bak, R. P. M., M. J. E. Carpay, and E. D. de Ruyter van Steveninck. 1984. Densities 

of the sea urchin Diadema antillarum before and after mass mortalities on the 

coral reefs of Curaçao. Marine Ecology Progress Series, 17:105–108. http://

dx.doi.org/10.3354/meps017105.

Bak, R. P. M., and G. van Eys. 1975. Predation of the sea urchin Diadema antillarum Philippi on living coral. Oecologia, 20:111–115. http://dx.doi.org/10

.1007/BF00369023.

Beiring, E. A., and H. R. Lasker. 2000. Egg production by colonies of a gorgonian coral. Marine Ecology Progress Series, 196:169–177. http://dx.doi.org

/10.3354/meps196169.

Brazeau, D. A., and H. R. Lasker. 1990. Sexual reproduction and external brooding by the Caribbean gorgonian Briareum asbestinum. Marine Biology, 104: 

465–474. http://dx.doi.org/10.1007/BF01314351.

———. 1992. Reproductive success in the Caribbean octocoral Briareum asbestinum. Marine Biology, 114:157–163.

Carlon, D. B. 1999. The evolution of mating systems in tropical reef corals. Trends 

in Ecology and Evolution, 14:491–495. http://dx.doi.org/10.1016/S0169

-5347(99)01709-7.

FIGURE 1. Larval collector similar to the one used in Bak’s (1985) 

study of Diadema recruitment (photo by H. Lessios).
number 39 • 9 5

Carpenter, R. C. 1986. Partitioning herbivory and its effects on coral-reef algal 

communities. Ecological Monographs, 56:345–363. http://dx.doi.org/10

.2307/1942551.

———. 1997. Invertebrate predators and grazers. In Life and death of coral reefs, 

ed. C. Birkeland, pp. 198–248. New York: Chapman and Hall. http://dx.doi

.org/10.1007/978-1-4615-5995-5.

Chiappone, M., L. M. Rutten, D. W. Swanson, and S. L. Miller. 2008. Population 

status of the urchin Diadema antillarum in the Florida Keys 25 years after the 

Caribbean mass mortality. Proceedings of the eleventh International Coral 

Reef Symposium, 2:712–716.

Coffroth, M. A., and H. R. Lasker. 1998. Larval paternity and male reproductive 

success of a broadcast-spawning gorgonian, Plexaura kuna. Marine Biology, 

131:329–337. http://dx.doi.org/10.1007/s002270050326.

Coma, R., and H. R. Lasker. 1997. Effects of spatial distribution and reproductive 

biology on in situ fertilization rates of a broadcast-spawning invertebrate.

Biological Bulletin, 193:20–29. http://dx.doi.org/10.2307/1542733.

Connell, J. H. 1972. Community interactions on marine rocky intertidal shores. 

Annual Reviews of Ecology and Systematics, 3:169–192. http://dx.doi.org/10

.1146/annurev.es.03.110172.001125.

———. 1985. The consequences of variation in initial settlement vs. postsettlement mortality in rocky intertidal communities. Journal of Experimental Marine Biology and Ecology, 93:11–45. http://dx.doi.org/10.1016/0022-0981

(85)90146-7.

Crisp, D. J. 1961. Territorial behaviour in barnacle settlement. Journal of Experimental Biology, 38:429–446.

Davis, A. R. 1987. Variation in recruitment of the subtidal colonial ascidian Podoclavella cylindrica (Quoy and Gaimard): The role of substatum choice and 

early survival. Journal of Experimental Marine Biology and Ecology, 106:57–

71. http://dx.doi.org/10.1016/0022-0981(87)90147-X.

Davis, A. R., and A. J. Butler. 1989. Direct observations of larval dispersal in the 

colonial ascidian Podoclavella moluccensis Slutter: Evidence of closed populations. Journal of Experimental Marine Biology and Ecology, 127:189–203. 

http://dx.doi.org/10.1016/0022-0981(89)90184-6.

de Graaf, M., G. J. Geertjes, and J. J. Videler. 1999. Observations on spawning of 

scleractinian corals and other invertebrates on the reefs of Bonaire (Netherlands Antilles, Caribbean). Bulletin of Marine Science, 64:189–194.

Denny, M. W. 1988. Biology and the mechanics of the wave-swept environment. 

Princeton, N.J.: Princeton University Press.

Denny, M. W., and M. F. Shibata. 1989. Consequences of surf-zone turbulence for 

settlement and external fertilization. American Naturalist, 134:859–889. 

http://dx.doi.org/10.1086/285018.

Doherty, P. J., V. Dufour, R. Galzin, M. A. Hixon, M. G. Meekan, and S. Planes. 

2004. High mortality during settlement is a population bottleneck for a 

tropical surgeonfish. Ecology, 85:2422–2428. http://dx.doi.org/10.1890/04

-0366.

Eckert, G. L. 1998. Larval development, growth and morphology of the sea urchin 

Diadema antillarum. Bulletin of Marine Science, 63:443–451.

Evans, J. P., and D. J. Marshall. 2005. Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution, 59:106–112.

Fadlallah, Y. H., and J. S. Pearse. 1982. Sexual reproduction in solitary corals: Synchronous gametogenesis and broadcast spawning in Paracyathus stearnsii. 

Marine Biology, 71:233–239. http://dx.doi.org/10.1007/BF00397040.

Farley, G. S., and D. R. Levitan. 2001. The role of jelly coats in sperm-egg encounters, fertilization success, and selection on egg size in echinoids. American 

Naturalist, 157:626–236. http://dx.doi.org/10.1086/320619.

Gittings, S. R., G. S. Boland, K. J. P. Deslarzes, C. L. Combs, B. S. Holland, and T. J. 

Bright. 1992. Mass spawning and reproductive viability of reef corals at the 

East Flower Garden Bank, Northwest Gulf of Mexico. Bulletin of Marine 

Science, 51:420–428.

Gosselin, L. A., and P. Y. Qian. 1997. Juvenile mortality in benthic marine invertebrates. Marine Ecology Progress Series, 146:265–282. http://dx.doi.org

/10.3354/meps146265.

Grosberg, R. K. 1982. Inter-tidal zonation of barnacles: The influence of planktonic 

zonation of larvae on vertical distribution of adults. Ecology, 63:894–899. 

http://dx.doi.org/10.2307/1937228.

———. 1991. Sperm-mediated gene flow and the genetic structure of a population 

of the colonial ascidian Botryllus schlosseri. Evolution, 45:130–142. http://

dx.doi.org/10.2307/2409488.

Grosberg, R. K., and D. R. Levitan. 1992. For adults only: Supply side ecology and 

the history of larval biology. Trends in Ecology and Evolution, 7:130–133. 

http://dx.doi.org/10.1016/0169-5347(92)90148-5.

Grosberg, R. K., and J. F. Quinn. 1986. The genetic control and consequences of 

kin recognition by the larvae of a colonial marine invertebrate. Nature, 322: 

456–459. http://dx.doi.org/10.1038/322456a0.

Hagström, B. E., and S. Lönning. 1967. Experimental studies of Strongylocentrotus 

droebachiensis and S. pallidus. Sarsia, 29:165–176.

Harrison, P. L. 2011. Sexual reproduction of scleractinian corals. In Coral reefs: An 

ecosystem in transition, ed. Z. Dubinsky and N. Stambler, pp. 59–85. Berlin: 

Springer. http://dx.doi.org/10.1007/978-94-007-0114-4_6

Harrison, P. L., R. C. Babcock, G. D. Bull, J. K. Oliver, C. C. Wallace, and B. L. 

Willis. 1984. Mass spawning in tropical reef corals. Science, 223:1186–1189. 

http://dx.doi.org/10.1126/science.223.4641.1186.

Hendler, G., and D. L. Meyer. 1982. Ophiuroids flagrante-delicto and notes on the 

spawning behavior of other echinoderms in their natural habitat. Bulletin of 

Marine Science, 32:600–607.

Highsmith, R. C. 1982. Induced settlement and metamorphosis of sand dollar 

(Dendraster excentricus) larvae in predator-free sites: Adult sand dollar beds. 

Ecology, 63:329–337. http://dx.doi.org/10.2307/1938950.

Himmelman, J. H., C. P. Dumont, C. F. Gaymer, C. Vallieres, and D. Drolet. 2008. 

Spawning synchrony and aggregative behaviour of cold-water echinoderms 

during multi-species mass spawnings. Marine Ecology Progress Series, 361: 

161–168. http://dx.doi.org/10.3354/meps07415.

Hunt, H. L., and R. E. Scheibling. 1997. Role of early post-settlement mortality in 

recruitment of benthic marine invertebrates. Marine Ecology Progress Series,

155:269–301. http://dx.doi.org/10.3354/meps155269.

Hurlbut, C. J. 1991. The effects of larval abundance, settlement and juvenile mortality on the depth distribution of a colonial ascidian. Journal of Experimental 

Marine Biology and Ecology, 150:183–202. http://dx.doi.org/10.1016/0022

-0981(91)90067-7.

Johnson, S. L., and P. O. Yund. 2007. Variation in multiple paternity in natural 

populations of a free-spawning marine invertebrate. Molecular Ecology, 16: 

3253–3262. http://dx.doi.org/10.1111/j.1365-294X.2007.03366.x.

———. 2009. Effects of fertilization distance on male gain curves in a free-spawning 

marine invertebrate: A combined empirical and theoretical approach. Evolution, 63:3114–3123. http://dx.doi.org/10.1111/j.1558-5646.2009.00784.x.

Kupriyanova, E., and J. N. Havenhand. 2002. Variation in sperm swimming behaviour and its effect on fertilization success in the serpulid polychaete Galeolaria caespitosa. Invertebrate Reproduction and Development, 41:21–26. 

http://dx.doi.org/10.1080/07924259.2002.9652731.

Lamare, M. D. 1998. Origin and transport of larvae of the sea urchin Evechinus 

chloroticus (Echinodermata: Echinoidea) in a New Zealand fiord. Marine 

Ecology Progress Series, 174:107–121. http://dx.doi.org/10.3354/meps

174107.

Lamare, M. D., and M. F. Barker. 1999. In situ estimates of larval development 

and mortality in the New Zealand sea urchin Evechinus chloroticus (Echinodermata: Echinoidea). Marine Ecology Progress Series, 180:197–211. http://

dx.doi.org/10.3354/meps180197.

Lamare, M. D., and B. G. Stewart. 1998. Mass spawning by the sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) in a New Zealand fiord. Marine 

Biology, 132:135–140. http://dx.doi.org/10.1007/s002270050379.

Lasker, H. R. 2006. High fertilization success in a surface-brooding Caribbean gorgonian. Biological Bulletin, 210:10–17. http://dx.doi.org/10.2307/4134532.

Lasker, H. R., D. A. Brazeau, J. Calderon, M. A. Coffroth, R. Coma, and K. Kim. 

1996. In situ rates of fertilization among broadcast spawning gorgonian 

corals. Biological Bulletin, 190:45–55. http://dx.doi.org/10.2307/1542674.

Lasker H. R., C. Gutierrez-Rodriguez, K. Bala, A. Hannes, and J. P. Bilewitch. 2008. 

Male reproductive success during spawning events of the octocoral Pseudopterogorgia elisabethae. Marine Ecology Progress Series, 367:153–161. http://

dx.doi.org/10.3354/meps07614.

Lessios, H. A. 1984. Possible prezygotic reproductive isolation in sea urchins separated by the Isthmus of Panama. Evolution, 38:1144–1148. http://dx.doi.org

/10.2307/2408446.

———. 1988. Mass mortality of Diadema antillarum in the Caribbean: What have 

we learned? Annual Review of Ecology and Systematics, 19:371–393.

———. 2005. Diadema antillarum populations in Panama twenty years following 

mass mortality. Coral Reefs, 24:125–127. http://dx.doi.org/10.1007/s00338

-004-0443-5.

Lessios, H. A., D. R. Robertson, and J. D. Cubit. 1984. Spread of Diadema mass 

mortality through the Caribbean. Science, 226:335–337. http://dx.doi.org

/10.1126/science.226.4672.335.

Levitan, D. R. 1993. The importance of sperm limitation to the evolution of egg size 

in marine invertebrates. American Naturalist, 141:517–536. http://dx.doi.org

/10.1086/285489.
9 6 • smithsonian contributions to the marine sciences

———. 1996. Effects of gamete traits on fertilization in the sea and the evolution of sexual dimorphism. Nature, 382:153–155. http://dx.doi.org/10.1038

/382153a0.

———. 1998. Does Bateman’s Principle apply to broadcast-spawning organisms? 

Egg traits influence in situ fertilization rates among congeneric sea urchins.

Evolution, 52:1043–1056. http://dx.doi.org/10.2307/2411235.

———. 2000a. Sperm velocity and endurance trade off each other and influence 

fertilization in the sea urchin Lytechinus variegatus. Proceedings of the 

Royal Society of London: Biological Sciences, 267:531–534. http://dx.doi

.org/10.1098/rspb.2000.1032.

———. 2000b. Optimal egg size in marine invertebrates: Theory and phylogenetic analysis of the critical relationship between egg size and development 

time in echinoids. American Naturalist, 156:175–192. http://dx.doi.org/10

.1086/303376.

———. 2002a. Density-dependent selection on gamete traits in three congeneric 

sea urchins. Ecology, 83:464–479. http://dx.doi.org/10.1890/0012-9658

(2002)083[0464:DDSOGT]2.0.CO;2.

———. 2002b. The relationship between conspecific fertilization success and reproductive isolation among three congeneric sea urchins. Evolution, 56:1599–1609.

———. 2004. Density-dependent sexual selection in external fertilizers: Variances 

in male and female reproductive success along the continuum from sperm 

limitation to sexual conflict in the sea urchin Strongylocentrotus franciscanus.

American Naturalist, 164:298–309. http://dx.doi.org/10.1086/423150.

———. 2005. Sex specific spawning behavior and its consequences in an external fertilizer. American Naturalist, 165:682–694. http://dx.doi.org/10

.1086/429733.

———. 2008. Gamete traits influence the variance in reproductive success, the intensity of sexual selection, and the outcome of sexual conflict among congeneric sea urchins. Evolution, 62:1305–1316. http://dx.doi.org/10.1111/j

.1558-5646.2008.00378.x.

Levitan, D. R., and D. L. Ferrell. 2006. Selection on gamete recognition proteins depends on sex, density and genotype frequency. Science, 312:267–269. http://

dx.doi.org/10.1126/science.1122183.

Levitan, D. R., H. Fukami, J. Jara, D. Kline, T. M. McGovern, K. E. McGhee, C. A.

Swanson, and N. Knowlton. 2004. Mechanisms of reproductive isolation 

among sympatric broadcast-spawning corals of the Montastraea annularis

species complex. Evolution, 58:308–323.

Levitan, D. R., M. A. Sewell, and F.-S. Chia 1991. Kinetics of fertilization in the 

sea urchin Strongylocentrotus franciscanus: Interaction of gamete dilution, age, and contact time. Biological Bulletin, 181:371–378. http://dx.doi

.org/10.2307/1542357.

Levitan, D. R., and A. P. Stapper. 2010. Simultaneous positive and negative frequency dependent selection on sperm bindin, a gamete recognition protein in 

the sea urchin Strongylocentrotus purpuratus. Evolution, 64:785–797. http://

dx.doi.org/10.1111/j.1558-5646.2009.00850.x.

Levitan, D. R., C. P. Terhorst, and N. D. Fogarty. 2007. The risk of polyspermy 

in three congeneric sea urchins and its implications for gametic incompatibility and reproductive isolation. Evolution, 61:2007–2014. http://dx.doi

.org/10.1111/j.1558-5646.2007.00150.x.

Lewin, R. 1986. Supply-side ecology. Science, 234:25–27. http://dx.doi.org/10.1126/

science.234.4772.25.

Lillie, F. R. 1915. Studies of Fertilization. VII. Analysis of variations in the fertilization power of sperm suspensions of Arbacia. Biological Bulletin, 28:229–251. 

http://dx.doi.org/10.2307/1536390.

Lindquist, N., R. Bolser, and K. Laing. 1997. Timing of larval release by two Caribbean demosponges. Marine Ecology Progress Series, 155:309–313. http://

dx.doi.org/10.3354/meps155309.

Luttikhuizen, P. C., P. J. H. Honkoop, J. Drent and J. van der Meer. 2004. A general 

solution for optimal egg size during external fertilization, extended scope for 

intermediate optimal egg size and the introduction of Don Ottavio “tango.” 

Journal of Theoretical Biology, 231:333–343. http://dx.doi.org/10.1016/j

.jtbi.2004.06.028.

Mackie, J. A., M. J. Keough, and L. Christidis. 2006. Invasion patterns inferred from 

cytochrome oxidase I sequences in three bryozoans, Bugula neritina, Watersipora subtorquata, and Watersipora arcuata. Marine Biology, 149:285–295. 

http://dx.doi.org/10.1007/s00227-005-0196-x.

Mariani, S., T. Alcoverro, M. J. Uriz, and X. Turon. 2005. Early life histories in 

the bryozoan Schizobrachiella sanguinea: A case study. Marine Biology,

147:735–745. http://dx.doi.org/10.1007/s00227-005-1616-7.

Marshall, D. J., C. A. Styan, and M. J. Keough. 2002. Sperm environment affects 

offspring quality in broadcast spawning marine invertebrates. Ecology Letters, 5:173–176. http://dx.doi.org/10.1046/j.1461-0248.2002.00257.x.

Marshall, S. M., and T. A. Stephenson. 1933. The Breeding of Reef Animals, I. The 

Corals. Scientific Reports of the Great Barrier Reef Expedition, 3:219–245.

McCartney, M. A. 1997. Sex allocation and male fitness gain curves in a colonial, 

hermaphroditic marine invertebrate. Evolution, 51:127–140. http://dx.doi

.org/10.2307/2410966.

McEuen, F. S. 1988. Spawning behaviors of Northeast Pacific sea cucumbers (Holothuroidea, Echinodermata). Marine Biology, 98:565–585. http://dx.doi.org

/10.1007/BF00391548.

Miller, K. J., and C. N. Mundy. 2005. In situ fertilisation success in the scleractinian coral Goniastrea favulus. Coral Reefs, 24:313–317. http://dx.doi.org

/10.1007/s00338-005-0480-8.

Miller, M. W., K. L. Kramer, S. M. Williams, L. Johnston, and A. M. Szmant. 2009. 

Assessment of current rates of Diadema antillarum larval settlement. Coral 

Reefs, 28:511–515. http://dx.doi.org/10.1007/s00338-008-0458-4.

Miller, R. L. 1966. Chemotaxis during fertilization in the hydroid Campanularia. 

Journal of Experimental Zoology, 162:22–44. http://dx.doi.org/10.1002/jez

.1401620104.

Mortensen, T. 1938. Contributions to the study of the development and larval 

forms of echinoderms IV. Det Kongelige Danske Videnskabernes Selskabs 

Skrifter 9 Raekke, 7(3):1–59.

Oliver, J., and R. Babcock. 1992. Aspects of the fertilization ecology of broadcast 

spawning corals: Sperm dilution effects and in situ measurements of fertilization. Biological Bulletin, 183:409–417. http://dx.doi.org/10.2307/1542017.

Olson, R. R. 1983. Ascidian-Prochloron symbiosis: The role of larval photoadaptations in midday larval release and settlement. Biological Bulletin, 165:221–

240. http://dx.doi.org/10.2307/1541366.

———. 1985. The consequences of short distance larval dispersal in a sessile marine 

invertebrate. Ecology, 66:30–39. http://dx.doi.org/10.2307/1941304.

Olson, R. R., and R. McPherson. 1987. Potential vs. realized larval dispersal: Fish 

predation on larvae of the ascidian Lissoclinum patella (G http://dx.doi.org

/10.1016/0022-0981(87)90004-9.ottschaldt). Journal of Experimental Marine Biology and Ecology, 110:245–256.

Osman, R. W., and R. B. Whitlatch. 1995. The influence of resident adults on larval 

settlement: Experiments with four species of ascidians. Journal of Experimental Marine Biology and Ecology, 190:199–220. http://dx.doi.org/10.1016

/0022-0981(95)00036-Q.

Pearse, J. S., D. J. McClary, M. A. Sewell, W. C. Austin, A. Perezruzafa, and 

M. Byrne. 1988. Simultaneous spawning of six species of echinoderms in 

Barkley Sound, British Columbia. International Journal of Invertebrate Reproduction and Development, 14:279–288. http://dx.doi.org/10.1080/0168

8170.1988.10510385.

Pennington, J. T. 1985. The ecology of fertilization of echinoid eggs: The consequences of sperm dilution, adult aggregation and synchronous spawning. 

Biological Bulletin, 169:417–430. http://dx.doi.org/10.2307/1541492.

Pineda, J., F. Porri, V. Starczak, and J. Blythe. 2010. Causes of decoupling between 

larval supply and settlement and consequences for understanding recruitment 

and population connectivity. Journal of Experimental Marine Biology and 

Ecology, 392:9–21. http://dx.doi.org/10.1016/j.jembe.2010.04.008.

Podolsky, R. D. 2002. Fertilization ecology of egg coats: Physical versus chemical 

contributions to fertilization success of free-spawned eggs. Journal of Experimental Biology, 205:1657–1668.

———. 2004. Life history consequences of investment in free-spawned eggs and 

their accessory coats. American Naturalist, 163:735–753. http://dx.doi.org

/10.1086/382791.

Purchase, C. F., D. J. Hasselman and L. K. Weir. 2007. Relationship between fertilization success and the number of milt donors in rainbow smelt Osmerus 

mordax (Mitchell): Implications for population growth rates. Journal of Fish 

Biology, 70:934–946. http://dx.doi.org/10.1111/j.1095-8649.2007.01356.x.

Richmond, R. H., and C. L. Hunter. 1990. Reproduction and recruitment of corals: 

Comparisons among the Caribbean, the tropical Pacific, and the Red Sea. Marine 

Ecology Progress Series, 60:185–203. http://dx.doi.org/10.3354/meps060185.

Riffell, J. A., P. J. Krug and R. K. Zimmer. 2004. The ecological and evolutionary consequences of sperm chemoattraction. Proceedings of the National Academy 

of Sciences, 101:4501–4506. http://dx.doi.org/10.1073/pnas.0304594101.

Roughgarden, J., T. Pennington, and S. Alexander. 1994. Dynamics of the rocky 

intertidal zone with remarks on generalization in ecology. Philosophical 

Transactions of the Royal Society of London [B], 343:79–85. http://dx.doi

.org/10.1098/rstb.1994.0010.

Sammarco, P. W. 1980. Diadema and its relationships to coral spat mortality: 

Grazing, competition, and biological disturbance. Journal of Experimental 

Marine Biology and Ecology, 45:245–272. http://dx.doi.org/10.1016/0022

-0981(80)90061-1.
number 39 • 9 7

———. 1982. Echinoid grazing as a structuring force in coral communities: Whole 

reef manipulations. Journal of Experimental Marine Biology and Ecology,

61:31–55. http://dx.doi.org/10.1016/0022-0981(82)90020-X.

Sanchez, J. A., E. M. Alvarado, M. F. Gil, H. Charry, O. L. Arenas, L. H. Chasqui, 

and R. P. Garcia. 1999. Synchronous mass spawning of Montastraea annularis (Ellis & Solander) and Montastraea faveolata (Ellis & Solander) (Faviidae: Scleractinia) at Rosario Islands, Caribbean Coast of Colombia. Bulletin 

of Marine Science, 65:873–879.

Scheltema, R. S. 1988. Initial evidence for the transport of teleplanic larvae of benthic invertebrates across the East Pacific Barrier. Biological Bulletin, 174: 

145–152. http://dx.doi.org/10.2307/1541781.

Scoffin, T. P., C. W. Stearn, D. Boucher, P. Frydl, C. M. Hawkins, I. G. Hunter, and 

J. K. MacGeachy. 1980. Calcium carbonate budget of a fringing reef on the 

west coast of Barbados. Part II. Erosion, sediments and internal structure. 

Bulletin of Marine Science, 30:475–508.

Sewell, M. A., and D. R. Levitan. 1992. Fertilization success during a natural 

spawning of the dendrochirote sea cucumber Cucumaria miniata. Bulletin of 

Marine Science, 51:161–166.

Snelgrove, P. V. R., J. P. Grassle, J. F. Grassle, R. F. Petrecca, and H. G. Ma. 1999. In 

situ habitat selection by settling larvae of marine soft-sediment invertebrates.

Limnology and Oceanography, 44:1341–1347. http://dx.doi.org/10.4319/lo

.1999.44.5.1341.

Stearns, S. C. 1977. The evolution of life history traits: A critique of the theory and 

a review of the data. Annual Review of Ecology and Systematics, 8:145–171. 

http://dx.doi.org/10.1146/annurev.es.08.110177.001045.

Stoner, A. W., N. Mehta, and T. N. Lee. 1997. Recruitment of Strombus veligers 

to the Florida Keys reef tract: Relation to hydrographic events. Journal of 

Shellfish Research, 16:1–6.

Stoner, D. S. 1990. Recruitment of a tropical colonial ascidian: Relative importance of pre-settlement vs post-settlement processes. Ecology, 71:1682–1690. 

http://dx.doi.org/10.2307/1937577.

———. 1994. Larvae of a colonial ascidian use a non-contact mode of substratum selection on a coral reef. Marine Biology, 121:319–326. http://dx.doi

.org/10.1007/BF00346740.

Strathmann, R. R., E. S. Branscomb, and K. Vedder. 1981. Fatal errors in set as 

a cost of dispersal and the influence of intertidal flora on set of barnacles. 

Oecologia, 48:13–18. http://dx.doi.org/10.1007/BF00346982.

Swanson, W. J., and V. D. Vacquier. 2002. Reproductive protein evolution. Annual 

Review of Ecology and Systematics, 33:161–179. http://dx.doi.org/10.1146

/annurev.ecolsys.33.010802.150439.

Szmant, A. M. 1986. Reproductive ecology of Caribbean reef corals. Coral Reefs,

5:43–53. http://dx.doi.org/10.1007/BF00302170.

Thomas, F. I. M. 1994. Physical properties of gametes in three sea urchin species.

Journal of Experimental Biology, 194:263–284.

Thorson, G. 1946. Reproduction and larval development of Danish marine bottom 

invertebrates, with special reference to the planktonic larvae in the sound 

(Oresund). Meddelelser fra Kommision Danmarks Fiskeri og Havundersøkelser Serie: Plankton, 4:1–519.

Underwood, A. J., and P. G. Fairweather. 1989. Supply-side ecology and benthic 

marine assemblages. Trends in Ecology and Evolution, 4:17–20. http://dx.doi

.org/10.1016/0169-5347(89)90008-6.

Van Oppen, M. J. H., B. L. Willis, T. Van Rheede, and D. J. Miller. 2002. Spawning 

times, reproductive compatibilities and genetic structuring in the Acropora 

aspera group: Evidence for natural hybridization and semi-permeable species boundaries in corals. Molecular Ecology, 11:1363–1376. http://dx.doi

.org/10.1046/j.1365-294X.2002.01527.x.

Van Veghel, M. L. J. 1993. Multiple species spawning on Curacao reefs. Bulletin of 

Marine Science, 52:1017–1021.

Vermeij, M. J. A., A. O. Debrot, N. van der Hal, J. Bakker, and R. P. M. Bak. 2010. 

Increased recruitment rates indicate recovering populations of the sea urchin 

Diadema antillarum in Curaçao. Bulletin of Marine Science, 86:719–725.

Yonge, C. M. 1940. The biology of reef-building corals. Reports of the Great Barrier Reef Expedition, 1:353–389.

Yoshioka, P. M. 1982. Role of planktonic and benthic factors in the population dynamics of the bryozoan Membranipora membranacea. Ecology, 63:457–468. 

http://dx.doi.org/10.2307/1938963.

Young, C. M., and F.-S. Chia. 1984. Microhabitat-associated variability in survival 

and growth of subtidal solitary ascidians during the first 21 days after settlement. Marine Biology, 81:61–68. http://dx.doi.org/10.1007/BF00397626.

Yund, P. O. 1998. The effect of sperm competition on male gain curves in a colonial 

marine invertebrate. Ecology, 79:328–339. http://dx.doi.org/10.1890/0012

-9658(1998)079[0328:TEOSCO]2.0.CO;2.

Yund, P. O., S. L. Johnson, and L. E. Connolly. 2005. Multiple paternity and subsequent fusion/rejection interactions in a colonial ascidian. Integrative and 

Comparative Biology, 45:1101–1101.

Yund, P. O., and M. A. McCartney. 1994. Male reproductive success in sessile invertebrates: Competition for fertilizations. Ecology, 75:2151–2167. http://dx

.doi.org/10.2307/1940874.

Yund, P. O., and S. K. Meidel. 2003. Sea urchin spawning in benthic boundary layers: Are eggs fertilized before advecting away from females? Limnology and 

Oceanography, 48:795–801. http://dx.doi.org/10.4319/lo.2003.48.2.0795.

Zigler, K. S., M. A. McCartney, D. R. Levitan, and H. A. Lessios. 2005. Sea urchin 

bindin divergence predicts gamete compatibility. Evolution, 59:2399–2404.

Behavioral Ecology of Mobile Animals: 

Insights from In Situ Observations

David B. Eggleston, William F. Herrnkind, and Anson H. Hines

ABSTRACT. We draw on three primary examples from our collective work on mobile decapod 

crustaceans, fish, and humans, as well as the work by others on fish and invertebrates, to illustrate 

the beneficial influence of in situ observations on behavioral ecology, marine conservation, and education. Diver observations of mass migration and gregarious behavior in Caribbean spiny lobster 

(Panulirus argus) in the 1960s led to over 40 years of experimentation that identified (1) the environmental factors driving the mass migration of lobsters each fall, (2) queues of migrating lobsters 

that afforded them the benefits of reduced hydrodynamic drag and predation, (3) the body-odor 

attractant underlying gregarious behavior, and (4) the use of gregariousness as a type of “guidepost 

effect” that minimizes search time for shelter. In situ observation of spider crabs in kelp forests off 

central California showed complex resource partitioning along multiple niche dimensions in a guild 

of five species, driven by intense predation pressure by an array of fish and sea otters. Ultrasonic 

telemetry and innovative tagging studies, as well as diver-deployed experiments, revealed blue crab 

movement and behavior in murky estuarine waters of the Chesapeake Bay where direct visual observation is impossible. Over three decades, these studies showed mechanisms of dispersal and migration, foraging behavior in response to patchily distributed prey, and habitat selection for molting and 

minimization of intense cannibalism of juveniles by adults. We also highlight how in situ observations helped to refine behavioral ecological theory by testing whether humans display a relatively 

simple or sophisticated predatory response to varying densities of spiny lobster prey. Knowledge of 

human predatory behavior can identify how effective certain fishery management policies will be in 

sustaining the spiny lobster fishery. Improved conservation is also afforded by the knowledge about 

the novel responses of these mobile organisms to both the fishery disturbance and the nondisturbed 

habitats via lobster spill-in to marine protected areas (MPAs). The results also have value in improved diver education relating to reducing injury to sublegal lobsters. In situ observations have also 

contributed to our knowledge of differential reproductive strategies, species invasions, and range 

extensions, as well as novel behaviors. While no single research tool is or will be capable of addressing the entirety of these behavioral scales, it is clear that in situ observations have made, are making, 

and will continue to make profound contributions to the field of behavioral ecology.

INTRODUCTION

“Now I had become an amphibious being and could go along in the same way 

as the fish. I could hover, sit, turn, kneel or lie down. I could even have stood 

on my head. We could study the animals in their natural world as we swam like 

fishes amongst them. And then this slimy body glided with its long tentacles over 

the sea floor, obviously seeking to find a protective hole.” —Hans Hass, 1942

Hans Hass, a biologist and one of the pioneers of the development of scuba 

and its scientific use expressed the potential and discovery of direct observation in the description of his first experience using a rebreather (from the film 

Menschen unter Haien [Men among Sharks]).

David B. Eggleston, North Carolina State University, Department of Marine, Earth and Atmospheric Sciences, Raleigh, North Carolina 

27695-8208, USA. William F. Herrnkind,

Florida State University, Department of Biological 

Science, Tallahassee, Florida 32306, USA. Anson H. Hines, Smithsonian Environmental Research Center, P.O. Box 28, Edgewater, Maryland 

21037, USA. Correspondence: D. Eggleston, 

eggleston@ncsu.edu.

Manuscript received 25 January 2012; accepted 

5 March 2013.
100 • smithsonian contributions to the marine sciences

In situ behavioral observations of mobile benthic animals 

have helped to inform, refine, and test ecological theory, support conservation measures, and enhance education. Previous in 

situ observations of animal behavior in the marine realm have 

used direct observations including (1) submersibles, (2) remotely 

operated vehicles (ROVs), (3) time-lapse video recording from 

stationary platforms, (4) animal-borne video recordings, (5) hydroacoustic methods paired with scuba, and (6) scuba. Given 

that diver observations by snorkeling and scuba are limited primarily to 30 m depths, the use of manned research submersibles 

and unmanned ROVs has greatly extended the depth range and 

physical conditions under which scientists can study the natural history of marine organisms, particularly deep sea organisms 

and their behaviors (e.g., Cohen, 1977; Mackie and Miller, 1983; 

Hamner and Robison, 1992; Spanier et al., 1994; Gebruk et al., 

2000; Drazen et al., 2003; Uiblein et al., 2003). 

There are three major advantages to studying animal behavior in situ for natural history observations and subsequent 

experimentation: (1) mesocosms necessarily oversimplify the 

environment and may inhibit certain behaviors or produce behavioral artifacts; (2) natural conditions in situ can act as a control on experimental factors imposed on a particular community 

or system and can reveal unanticipated ecological synergisms; 

(3) field observations can reveal novel behaviors and ecological 

processes that would never be revealed in confined experimental conditions. For example, interactions of deep-sea organisms 

with their environment have been documented from videotapes 

taken from submersibles and ROVs, providing insight into the 

environmental variables that affect the distribution of these 

animals and their key habitats for spawning and feeding (Drazen et al., 2003; Uiblein et al., 2003). In situ diver observations 

have often been paired with hydroacoustic surveys capable of 

sampling in conditions beyond diver capabilities and over relatively large areas (MacLennan and Simmonds, 1992; Starr et al., 

1996; Taylor et al., 2006). Hydroacoustics, defined as measurement of active sound in water (sonar), is used to study mobile 

organisms, typically fish. Hydroacoustic assessments have traditionally employed either mobile surveys from boats to evaluate 

fish biomass and spatial distributions, or use of fixed locations 

that use stationary transducers to monitor fish passing an area. 

Hydroacoustics provide a method of noninvasive sampling of 

animal assemblages, collecting spatially continuous data in three 

dimensions on submeter to kilometer scales and rapidly assessing animal distribution, abundance, and movement over large 

spatial scales. For example, using hydroacoustic surveys off Little Cayman, British West Indies, Taylor et al. (2006) found that 

spawning aggregations of Nassau grouper (Epinephelus striatus) 

were three times larger in population size than diver estimates, 

remained near bottom along the reef edge during the day, formed 

a massive cone-shaped aggregation of fish near dusk that was 

punctuated by upward-swimming spawning rushes of four to 

eight individual fish, and moved as an aggregation just off the 

reef wall at night. These types of behavioral observations at night 

would not have been possible by diver surveys. 

In contrast, there are also research examples in which 

diver observations have proven critical to ground-truthing hydroacoustic surveys. In one example, a recent stock assessment 

for Nassau grouper in the Bahamas (Ehrhardt and Deleveaux, 

1999), acoustic sampling of possible grouper aggregations without visual ground truthing, suggested that “exploitation levels 

of Nassau grouper were still acceptable from a biological standpoint.” There was concern, however, that this acoustically based 

stock assessment, along with other assumptions, overestimated 

the population size of Nassau grouper. Subsequent hydroacoustic surveys of Nassau grouper populations in the Bahamas in 

1999–2001, coupled with ground truthing by scuba divers, 

found that both Nassau grouper and Bermuda chub (Kyphosus 

sectatrix) have nearly identical acoustic signatures, that many of 

the putative grouper spawning aggregations were actually aggregations of Bermuda chub, and that many of the grouper aggregations identified by diver observations in the mid-1980s (Colin,

1992) were extinct (Eggleston et al., 2003; Taylor et al., 2006). 

Thus, the sampling methods highlighted above, when coupled 

with diver observations as appropriate, provide a comprehensive 

suite of in situ research tools for studying behavior of mobile animals in the marine realm with important applications to fisheries 

management.

Ultrasonic biotelemetry, in which a sonic transmitter is attached to an animal and emits a unique frequency pulse that 

is detected with hydrophones, can provide detailed measures of 

location, behaviors, and environmental variables encountered by 

the organism (Wolcott and Hines, 1996). These data can be transmitted more or less continuously or stored by the tag for periods 

of time before transmission at intervals. Ultrasonic biotelemetry 

can thus keep up with moving organisms for long periods, at 

great speeds, and in low visibility or darkness, which cannot be 

achieved by direct observation. When paired with direct observations and experiments conducted by cameras, submersibles, and 

scuba, this is a powerful approach to determine in situ behavior.

WHY STUDY BEHAVIOR IN SITU?

There are three general areas of behavioral ecological theory 

where in situ observations in marine systems have been especially 

important: (1) optimization theory, (2) differential reproductive 

success, and (3) evolutionary stable strategies. The behavior of 

organisms in response to their environment is a central theme 

of ecology, since these traits are adaptive through natural selection to optimize ecological trade-offs, maximize efficiencies, 

and ultimately enhance fitness (Krebs and Davies, 1993; Begon 

et al., 2005; Cooper and Frederick, 2010; Webb et al., 2010). 

An inductive and deductive scientific approach, whereby behavioral observations lead to experimentation, often followed by 

more detailed observations of behavior and more refined experiments, has facilitated the rapid growth of the field of behavioral 

ecology (Herrnkind, 1974; Begon et al., 2005). Along with this 

progress, the urgency of understanding the evolutionary basis of 
number 39 • 101

behavioral ecology increases concomitant with the environmental changes in earth systems in which organisms exist (e.g., Parsons and Eggleston, 2006; Zeidberg and Robison, 2007; Albins 

and Hixon, 2008). 

The behavior of marine animals is especially interesting 

because of their phylogenetic and biological diversity, but also 

because many of their behavioral adaptations cannot be found 

in other environments (Herrnkind, 1974). For example, specially 

adapted animals not only tolerate but often thrive in deep-sea 

hydrothermal vent regions characterized by extremes in pressure 

and temperature, low oxygen, and the presence of toxic hydrogen sulfide and heavy metals. In most cases, this tolerance is due 

to a combination of physiological and behavioral adaptations 

that allow animals to avoid the extremes of their habitats and yet 

benefit from the chemoautotrophic production characteristic of 

these environments (McMullin et al., 2000). 

In addition to environments and behaviors characteristic 

of marine organisms and ecosystems, there are numerous examples of behavioral strategies that optimize ecological trade-offs 

or maximize efficiencies that can be compared and contrasted 

across marine, terrestrial, and aerial systems. These examples 

have helped to refine ecological theory and supported conservation measures. In many instances, these studies have benefited 

from direct, in situ observation by humans (Herrnkind, 1974; 

Begon et al., 2005). For example, in situ feeding observations 

by divers on 1,420 pelagic salps representing six species showed 

that feeding rates described from aquarium observations were 

much lower than in situ rates, therefore increasing former estimates of the trophic impact of salps (Madin, 1974). In situ observations provided important insights concerning the significance 

of salps as an important direct trophic link from nano–1-mmparticulate food to higher trophic levels, as well as the role of 

their fecal pellets in concentrating food and delivering it to the 

benthos (Madin, 1974). 

Direct observations by humans can also provide numerous 

distinct advantages over unmanned systems such as remotely 

operated vehicles, submersibles, gliders, and acoustic surveys 

(Taylor et al., 2006; Bellingham and Rajan, 2007). For example, 

humans are capable of rapid integration of and adjustment to 

changing circumstances under water, peripheral vision and use of 

multiple senses that are beyond the ability of unmanned systems, 

and adjusting swimming speed, buoyancy, and other behaviors 

in an interactive manner so as to maximize natural behaviors by 

the target organism(s) (Herrnkind, 1974). Moreover, unmanned 

systems can be prohibitively expensive (Starck, 1968; Herrnkind, 

1974). While much has changed in terms of underwater technological advances since the application of scuba to behavioral 

ecology in the 1960s and 1970s (Miller et al., 1971; Herrnkind, 

1974), much has remained the same in terms of the need for in 

situ observations by humans as a key component of research, 

outreach, and educational capabilities in marine systems.

In this paper, we draw on our collective expertise and experiences, as well as the scientific literature, to illustrate how in situ 

behavioral observations of mobile animals (including humans) 

made by scuba divers, underwater video, and biotelemetry has 

tested and refined our understanding of how animals optimize 

trade-offs and maximize efficiencies, and how such an understanding is contributing to the conservation of these species in 

a rapidly changing ocean system. We build on previous comprehensive reviews on this topic by Miller et al. (1971) and Herrnkind (1974), and reassess the contribution of in situ behavioral 

observations of mobile animals to testing and refining behavioral 

ecological theory, conservation, and education/outreach.

BEHAVIORAL ECOLOGICAL THEORY

Behavioral ecology is the study of the ecological and evolutionary basis for animal behavior, and the roles of behavior in 

enabling an animal to adapt to its environment and maximize 

its lifetime fitness or reproductive success (Krebs and Davies, 

1993). In addition to identifying novel behaviors and unanticipated ecological processes, there are three general areas of behavioral ecological theory where in situ observations in marine 

systems have been especially important: optimization theory, differential reproductive success, and evolutionary stable strategies. 

Optimization theory stipulates strategies that offer the highest 

return (e.g., caloric intake) to an animal given the various factors 

(e.g., prey availability or predatory abundance) and constraints 

(e.g., prey-handling time) facing the animal (Stephens and Krebs,

1986). Cost–benefit analyses and optimization models can help 

to identify environmental and biological conditions that drive 

behavioral decisions by mobile animals, such as when to mate or 

change habitats so as to maximize fitness (Stephens and Krebs, 

1986). For mobile animals that must make decisions about balancing conflicting demands associated with foraging and avoiding predators, simple optimality models predict that animals 

should respond to changes in mortality risk (u) and growth rate 

(g) by shifting habitats in a way that maximizes net benefits (McNamara and Houston, 1986). Minimizing the ratio of mortality 

risk to growth rate, also known as the minimize u/g rule, has 

been a useful construct for addressing ecological processes underlying ontogenetic habitat shifts in fish (Werner and Gilliam, 

1984; Dahlgren and Eggleston, 2000). 

As one example, field caging and tethering experiments conducted by scuba divers quantified habitat-specific growth rates 

and mortality risk, respectively, for three size classes of coral reef 

fish (E. striatus) during their tenure in off-reef nursery habitats 

(Dahlgren and Eggleston, 2000). These size classes bracketed the 

size at which this species undergoes an ontogenetic habitat shift 

from the interstices of macroalgal clumps (algal habitat) to areas 

outside, or adjacent to, macroalgae and other physically complex 

microhabitats (postalgal habitats; Eggleston, 1995). Results indicated that small fish trade off living in relatively safe algal habitat with achieving high growth rates in postalgal habitats—the 

value of u/g was significantly lower in algal habitats than in postalgal habitats for small fish, which typically reside in the algal 

habitat, and significantly lower in postalgal habitats for medium 
102 • smithsonian contributions to the marine sciences

and large fish that reside in postalgal habitats (Dahlgren and 

Eggleston, 2000). These results suggest that ontogenetic habitat 

shifts by juvenile E. striatus are consistent with the minimize u/g

rule, and highlight how behavioral responses to ecological processes, such as changing predation risk with body size, determine 

distribution patterns of mobile animals.

Ultimately, however, behavior is subject to natural selection 

just as any other trait, resulting in differential reproductive success. For example, animals that employ optimal behavioral strategies specific to their environment will generally leave greater 

numbers of offspring than their suboptimal conspecifics, and 

greater numbers of offspring generally lead to greater fitness 

(Krebs and Davies, 1993). Given that environments change over 

time, and at an ever-increasing rate due to anthropogenic factors,

an optimal behavior now may not be optimal in the future. In situ 

observations may provide great insight into evolved behavioral 

changes that come about because of environmental changes.

Behavioral patterns among interacting individuals can 

sometimes result in evolutionary stable strategies (ESS; Maynard 

Smith, 1982). For example, the more likely a rival male is to back 

down from a threat, the more value a male gets out of making 

the threat. The more likely, however, that a rival will attack if 

threatened, the less useful it is to threaten other males. ESS is 

considered to be the evolutionary end point selected for by these 

social interactions, and the fitness conveyed by a strategy is influenced by what other individuals are doing (Krebs and Davies, 

1993). Thus, animal behavior can be governed not only by optimality, but by the frequencies of strategies adopted by others. 

Behavioral evolution is therefore influenced by both the physical 

environment and interactions between other individuals. The latter line of research has particularly benefited from in situ observations, especially in observations of mating systems in fish. 

EXAMPLES OF IN SITU OBSERVATIONS, 

HYPOTHESES, AND KEY FINDINGS

Case Study: Mass Migration and Gregarious

Behavior in Caribbean Spiny Lobster

We begin our examples by continuing a line of observation 

and subsequent research that was first highlighted in Herrnkind’s (1974) review on this topic: a chance encounter by scientists using scuba with thousands of Caribbean spiny lobster 

(Panulirus argus) migrating in head-to-tail queues off the coast 

of Bimini, Bahamas (Figure 1; Herrnkind and Cummings, 1964; 

Herrnkind, 1969). The repeated observations of mass migrations, coupled with observations of gregarious den sharing by 

lobsters during the day and homing by lobsters back to specific 

dens after nighttime foraging (Herrnkind et al., 1975), hinted at 

a far more sophisticated and complex behavioral repertoire and 

lifestyle than previously considered for marine crustaceans.

These scuba observations of spiny lobster migratory behavior, first described in the scientific literature by Herrnkind 

and Cummings (1964), Herrnkind (1969), and Herrnkind et 

al. (1975), triggered an iterative process of laboratory experiments, field experiments, more field observations, and more refined experimentation that continues today. The initial migration 

research is reviewed by Herrnkind (1980, 1983) but described 

briefly here to demonstrate specific examples of the reciprocal 

interplay of scuba-mediated field insights with lab and semifield studies (see Herrnkind, 1980, 1983, 1985, and references 

therein for details). The first encounters by diving scientists with 

mass-migrating lobsters at Bimini in 1961 and 1963 were brief,

fortuitous, and involved no quantitative data recording. However, they revealed distinctive features: lobsters moved in daytime across atypical habitat (open sand), all migrants moved in 

single file (queues), most migrants were adult males and nongravid females, all observed queues moved in similar directional 

headings, and the mass migration event followed several days 

of autumnal squalls (late October). This latter coincidence was 

confirmed in the first planned field study in 1969 (and seasons 

thereafter), which tested the hypothesis that some component or 

combination of storm-caused environmental changes stimulated 

the mass migration. Since captive migrant lobsters were found 

to spontaneously queue around the periphery of outside circular pools, it was possible to set up replicated experiments under 

controlled conditions.

Based on field measures of storm-linked thermal and hydrodynamic changes, a series of indoor controlled pool experiments 

simulating storm levels showed that a sharp increase of current 

or turbulence induced day-long queuing, sometimes enhanced by 

combining a temperature decrease with shelter removal. While 

storm stimuli triggered mass movement, additional results under 

artificial fall photoperiod hinted at both a preliminary shift in internal state—probably hormonal—that increased susceptibility 

FIGURE 1. A queue of migrating spiny lobsters (Panulirus argus) 

crosses long stretches of shelterless sand substrate in daylight near 

Bimini, Bahamas. All queues orient southward parallel to the edge of 

the Great Bahama Bank following late fall bouts of stormy weather. 

Photo by W. Herrnkind.
number 39 • 103

to a migratory response, and a lingering poststimulation effect 

of gradual cessation of queuing hours or days after ambient conditions were restored. The underlying physiological mechanism 

remains to be fully investigated.

The striking and unique queuing formations begged functional explanation. Quantitative ethological studies revealed that 

queuing involved nearly continuous tactile (and probably chemotactile) contact by lobster followers using inner-antennular 

rami and anterior walking legs. Constraining any of these appendages induced more contact by the others. In this way, migrants are able to queue in complete darkness or high turbidity, 

as well as after severe appendage loss. Several hypotheses regarding how this queuing behavior may enhance lobster efficiency, 

survival, and, ultimately, fitness were then tested. Observations 

of lobsters walking in circular tanks in the laboratory provided 

weak evidence that queuing behavior enhanced directional orientation by lobsters. However, the most compelling evidence was 

for enhanced hydrodynamic efficiency. By placing lobsters into 

laboratory tow tanks, researchers determined that individuals 

in a queue benefit from reduced hydrodynamic drag via drafting in a manner similar to cyclists drafting (Bill and Herrnkind, 

1976). At migratory pace, nonleaders in a queue experience only 

about one-half the drag of solitary lobsters. Further tow tank 

data suggested that drag reduction was enhanced as the antennal 

angle was reduced (antennae brought closer together) as speed 

increased. This behavior was confirmed by time-lapse field photography under different walking speeds. Field observations of 

moving queues also revealed that the high-drag position of lead 

lobster spontaneously changed as queues joined or the lead individual briefly stopped to forage. Despite this strong behavioral 

evidence, no one has, as yet, tried to measure improved metabolic efficiency theorized to underlie functional drag reduction.

Mass migrants generally assembled in relatively large groups 

exceeding 20 individuals. Migrants rarely traveled or rested solitarily in the open (<2%; Herrnkind et al., 2001). Divers occasionally witnessed attacks by queen triggerfish (Balistes vetula) 

on isolated lobsters encountered over shelterless substrate that 

was characteristic of the migratory pathway. By contrast, threatened queues as long as ~50 migrants reassembled in a remarkable manner. The lead lobster pirouetted as the followers wound 

into a radial array, forming within minutes into a closely packed 

pod with all individuals facing outward or upward (Figure 2). 

We hypothesized that queues and the formations served as an 

antipredation strategy (Herrnkind et al., 2001).

Although divers witnessed too few natural predatory attacks on migrants to test the antipredation hypothesis, they took 

extensive data on group and queue numbers during migrations 

in 1969–1975. Notably, these data were prescient, taken well 

FIGURE 2. When threatened by predators (a descending diver in this case), a queue winds around the pirouetting lead lobster, quickly forming a stationary pod, all members directing their defensive antennae outward to 

confront attackers. Photo by W. Herrnkind.
104 • smithsonian contributions to the marine sciences

before socio-biological research emerged to focus on the evolution of cooperative behavior. Spiny lobster gregariousness serves 

as a useful model because their life cycle (six-month free-drifting 

larval period) and sometimes nomadic benthic nature obviate 

cooperation based on kinship or long-term, interindividual reciprocity (Herrnkind et al., 2001).

Lobster group-size frequencies under field conditions were 

compared to hypothetical optimal distributions for particular 

functions. For example, a dilution benefit (safety in numbers) 

predicts large, amorphous groups of migrants moving along 

close together whereas antipredatory vigilance predicts lines of 

relatively small numbers of individuals for rapid warning communication. Group numbers were evaluated for chance, crypticity, dilution, drag reduction, vigilance, and combined defense in 

behavioral categories of nonmigratory denning, migratory denning, movement from dens, movement in the open, and resting in 

the open (Herrnkind et al., 2001). The group distributions of lobsters differed statistically among categories and the distributions 

for each behavior supported two or more hypothetical functions. 

All migratory group types hypothetically benefit from antipredation. Strong cohesion among migrants is reflected by their migratory behavior in which lobsters initially leave crowded dens 

as small, loosely arranged groups, moving slowly, but thereafter 

join other groups as they are encountered, then move swiftly as 

queues. Queues predictably benefit from vigilance and drag reduction but, as they form pods to rest or to confront predators, 

also potentially benefit from both dilution and combined defense 

(Herrnkind et al., 2001).

The dilution and combined defense hypotheses were experimentally tested by pitting gray triggerfish (Balistes capriscus) against tethered lobsters in the field, as well as against 

free-moving lobsters in large, seminatural enclosures (~40 m2

) 

(Lavalli and Herrnkind, 2009). During field encounters, lobsters 

attached by swivel and cable ties to dive weights were alternately 

set out solitarily or in groups of five near reefs with 1–23 wild 

gray triggerfish. The lobsters defended by antennal points, whips, 

and lunges, rarely attempting tail-flip escape. After 90 minutes, 

~40% of solitary lobsters were killed or debilitated while none of 

the lobsters in the quintets were seriously wounded. Lobsters in 

a group were formidable defenders even with multiple attackers 

(Lavalli and Herrnkind, 2009).

The semifield encounters pitted 1, 3, 5, 10, and 20 lobsters 

against 1, 2, 5, and 10 triggerfish (Lavalli and Herrnkind, 2009). 

All the test triggerfish were initially observed to kill and devour a 

lobster and were not fed during the 24 hours before a trial. Captive lobsters confronted by triggerfish subsequently assembled into 

pods or phalanxes or queued around the pool periphery. Lobster 

group cohesion and assembly into a pod increased after a nearby 

lobster was bitten by an attacker. Lobster survival rate sharply 

improved as the number in the group increased. Solitary lobsters 

suffered ~70% mortality compared to ~80% survival among 

quintets. All debilitated lobsters were outside the pod, either having defected from the group or the group having moved away, isolating the attacked individual. However, five attacking triggerfish 

were no more effective than two attackers either in debilitating a 

lobster or in the time taken to do so. Competition or aggression 

among the triggerfish often interfered with the effectiveness of the 

attacks. When confronted by triggerfish during migration it is best 

for a lobster to stay amidst a large queue that quickly forms a 

pod, and for the attackers to be inexperienced. Simply expressing 

strongly cohesive behavior, especially during mass migration, provides antipredatory benefits to spiny lobsters approximating that 

achieved via kinship and reciprocal sociality in social mammals, 

birds, and insects (Lavalli and Herrnkind, 2009).

Scuba and the advent of manned undersea habitats (late 

1960s) contributed to understanding the mechanisms and benefits 

of spiny lobster gregariousness, particularly sharing of selected 

shelters—a hallmark of many spiny lobster species throughout 

benthic life. Until then, spiny lobsters were known to aggregate 

in dens and traps but it was not clear whether this was social 

attraction or merely attraction of many individuals to a common food source or sheltering structure. Tektite aquanauts/scientists in saturation mode, using visible coded tags and ultrasonic 

transmitters, discovered that lobsters homed over kilometers to 

specific dens for periods of weeks, often with the same den mates 

(Clifton et al., 1970; Herrnkind and McLean, 1971; Herrnkind 

et al., 1975). This raised questions of the fitness consequences of 

den quality, co-occupancy, and homing mechanisms.

Subsequent scuba research revealed that shelter was vital 

to survival of small, newly settled juvenile lobsters. Caribbean 

spiny lobsters were discovered to settle, reside, and feed within 

complex macroalgae attached to hard substrate (Marx and 

Herrnkind, 1985), with an eventual ontogenetic habitat shift 

to crevice dwelling. Field tethering experiments showed that juvenile lobsters suffer relatively high daily mortality in the absence of macroalgal shelter prior to crevice dwelling (Butler et 

al., 2006). A series of elegant field experiments (Eggleston et al., 

1990; Eggleston and Lipcius, 1992) using artificial dens (“casitas”) revealed that there is a trade-off between predation risk,

choosing a shelter scaled to your body size, and gregariousness. 

Under high predation risk, relatively small lobsters chose small 

shelters scaled to their body size in the absence of conspecifics, 

but chose to reside with larger conspecifics rather than shelters 

scaled to their body size when given a choice (Eggleston and Lipcius, 1992). Above a certain lobster size, the presence of conspecific coresidents also reduces the risk of predation (Mintz et al., 

1994; Butler et al., 1999).

Shelter choice and sharing by adult lobsters (Panulirus interruptus) was found by both lab and field studies to be facilitated by chemical odor attraction over meters to one or more 

conspecific individuals already in residence(Zimmer-Faust et al.,

1985). Conspecific odor of sufficient intensity also attracts juvenile Caribbean spiny lobsters as they become socially gregarious 

crevice dwellers, a response termed “guide effect” (Ratchford 

and Eggleston, 1998; Childress and Herrnkind, 2001). This 

odor-mediated attraction over distance reduces the time to locate 

a suitable den in a new foraging range as well as providing the 

added benefit of a codefender once there.
number 39 • 105

Recently, scuba-mediated field observations and follow-up 

lab experiments by Behringer (2003) showed that healthy juveniles avoid denning with conspecifics infected by a lethal virus, 

probably by chemo-sensing. Bouwma (2006) experimentally 

demonstrated rapid departure from a den, even by an individual 

lobster in daylight, cued by the body fluids of a recently killed 

conspecific. Based largely on insights from scuba observations in 

nature, research continues to reveal a complex and sophisticated 

behavioral, sensory, and ecological repertoire for spiny lobsters.

Conclusion

In the case study of the behavioral ecology of Caribbean 

spiny lobster, we have highlighted how in situ observations first 

identified mass migration and gregarious sheltering behavior in 

lobsters, and how a subsequent reciprocal interplay of scubamediated field insights with lab and semifield studies identified 

the mechanisms underlying these behaviors. The initiation of 

mass migrations of lobster queues in fall was driven by a combination of a shifting hormonal state of lobsters due to fall photoperiod and a sharp increase in current-speed characteristics of 

the first fall storms in the Caribbean. Queues of migrating lobsters were afforded the benefits of reduced hydrodynamic drag 

and predation. Lobsters exhibited a body odor attractant underlying their gregarious sheltering behavior, and this gregarious behavior served as a type of guidepost effect that minimized search 

time for shelter. 

Case Study: Behavior and Ecology of Crabs

How does one make observations of animal behavior when 

the animals cannot be seen? In this case study, we compare and 

contrast in situ observations of crabs in two distinctly challenging circumstances. In one, niche partitioning and its underlying 

mechanisms were analyzed for a guild of five species of spider 

crabs (Loxorhynchus crispatus, Pugettia producta, Pugettia

richii, Mimulus foliatus, Scyra acutifrons) in kelp forests off central California. While the water in this ecosystem is relatively 

clear, most of the crabs are small and extremely cryptic, requiring 

long hours of painstaking direct observations on scuba. In the 

other, the behavioral ecology of blue crabs (Callinectes sapidus) 

in soft-bottom communities was advanced in the turbid waters 

of Chesapeake Bay, where direct visual observation is impossible.

A Guild of Spider Crabs in Kelp Forests

Direct observations and collections on scuba allowed analysis of population dynamics and niche partitioning in a guild of 

spider crabs in giant kelp (Macrocystis pyrifera) forests of central 

California (Hines, 1982). All five species are highly cryptic and 

utilize dense cover of algal-invertebrate turf of the kelp forest,

often residing in crevices and interstices. All of the crabs exhibit 

different color morphs, color change (due to algal diet), and 

decorating behavior. Observations of these morphologies and 

behaviors generated the hypothesis that they are adaptive for 

concealment from predators (Palma and Steneck, 2002; Todd 

et al., 2006). Consistent with the hypothesis, the diversity of 

predators that take spider crabs as a major portion of their diets 

indicated that predation pressure is high and may limit overall 

population levels of the crabs. Predation by sea otters (Enhydra 

lutris) probably limits the density of P. producta, and fish predation, especially by sculpins and rockfish species (Sebastes), probably limits abundance of the other four species.

Diver counts and size-frequency measures of crabs in plots 

along a transect from the intertidal shoreline through the kelp 

forest out to a deep reef offshore showed that each species had 

zones of abundance. Pugettia richii was the most abundant species, with peaks in the inner and middle zone of the kelp forest. 

Mimulus foliatus was second most abundant, with peaks in the 

middle and outer zones of the kelp forest. Abundance of S. acutifrons had peak densities in the outer edge of the kelp. Fourth 

in abundance, P. producta had highest densities in the intertidal 

zone; juveniles recruit into the intertidal and shallow eelgrass 

zones and migrate out into the kelp forest as they grow. However, the other species did not have zones of recruitment separate 

from adult distribution. Loxorhynchus crispatus was present in 

low densities from the middle of the kelp forest to the deep reef. 

The greatest combined density of spider crabs (11 crabs/m2

) occurred in the middle of the kelp forest (Hines, 1982).

Body size at maturity of the five species varied an order 

of magnitude in carapace width from 1 cm for S. acutifrons to 

10 cm for L. crispatus. Mean size of mature females and mean 

body size of the entire population of all pairs of species except 

M. foliates and P. richii had ratios greater than Hutchinson’s 

(1959) predicted value of 1.28 for niche separation. Body size 

likely limits crabs’ use of crevice refuge in the microhabitat.

The cryptic morphology and behavior of the spider crabs 

required painstaking quantification of microhabitat use by substrate type. Mimulus foliatus had the largest microhabitat breadth 

and was found on most substrate types, with an important refuge 

in kelp holdfasts. Pugettia richii was found mainly on the alga 

Cystoseira and in coralline algal mats. Scyra acutifrons occurred 

mainly in interstices of algal-invertebrate turf, and L. crispatus

was found on top of the turf. Pugettia producta occurred on kelp 

plants and had the narrowest microhabitat niche breadth.

Stomach contents of diver-collected crabs also showed partitioning of food resources. Pugettia producta was a strict specialist grazing on giant kelp. Mimulus foliatus and P. richii also 

had narrow diets of mostly drift kelp. Scyra acutifrons had main 

food categories of detritus, sponge, and pieces of kelp trapped in 

the algal-invertebrate turf. Loxorhynchus crispatus was a dietary 

generalist on a broad range of invertebrates and kelp.

Niche separation in the guild is multidimensional, and similar 

use of one resource is generally complemented by dissimilar use 

in another resource. Niche analysis for three dimensions of microhabitat, food, and body size showed P. producta is an overall 

specialist, and L. crispatus is a generalist. Scyra acutifrons also has 

a distinct niche within the algal-invertebrate turf, but M. foliatus
106 • smithsonian contributions to the marine sciences

and P. richii exhibit extensive overlap in all of the variables measured. However, the degree to which a species is a specialist versus 

a generalist for a resource did not relate to the amount of niche 

overlap with the rest of the guild. Microhabitat resources appeared to be the most important for niche separation and may 

also be explained as adaptations for minimizing predation.

Blue Crabs in Chesapeake Bay

Blue crabs (Callinectes sapidus) are dominant benthic predators in estuaries of the U.S. East and Gulf coasts, and the ecology of juvenile and adult blue crabs has been reviewed recently 

by Hines (2007). Their distribution and abundance patterns vary 

as a function of their migratory life cycle using a diverse array 

of estuarine habitats. Newly settled blue crabs generally grow 

through a series of early juvenile instars (developmental stages 

punctuated by ecdysis) within seagrass and other settlement 

habitats of lower estuaries (Orth and van Montfrans, 1987; Pile 

et al., 1996; Pardieck et al., 1999). Upon attaining the fifth to 

seventh crab instar and ~20 mm carapace width (cw), juveniles 

typically disperse from their settlement site to exploit an array 

of habitats throughout the estuary (Pile et al., 1996; Etherington 

and Eggleston, 2003). However, dispersal may occur as early as 

the first crab instar shortly after settlement in some estuaries, 

such as in North Carolina (Reyns and Eggleston, 2004). Dispersed juveniles use a variety of microhabitats where they forage 

and grow for 6–18 months (depending on temperature and food 

availability) until they reach sexual maturity in the sixteenth to 

twentieth crab instar at ~110–180 mm cw (Van Engel, 1958; 

Tagatz, 1968). After mating, inseminated mature females cease 

molting and migrate back to the lower estuary, produce broods, 

and incubate eggs until larvae are released and transported out 

of the estuary onto the continental shelf. By contrast, mature 

males may continue to molt and grow for one to three additional 

instars (typical large size is 180–200 mm). Unlike females, mature males tend to remain dispersed in the upper estuary without 

migrating directionally along the salinity gradient (Van Engel, 

1958; Hines et al., 1990, 1995).

Blue crab movement varies with life stage and molt stage, 

and depends on habitat and geographic region, as well as on tidal 

and seasonal cycles (Gillanders et al., 2003), as seen from spatially or temporally disjunct distributions of life stages, as when 

immature females molt to maturity and mate in upper estuarine 

zones but ovigerous females later occur primarily near the mouth 

of estuaries (e.g., Van Engel, 1958). Movement between points 

(without knowing the route traveled) can be estimated directly 

by mark-recapture studies involving large numbers (thousands) 

of crabs marked with inexpensive external or internal tags (reviewed by Hines, 2007). External tags are readily visible to fishers 

and typically cause little harm to crabs, but they are lost during 

molting. As a result, external tags usually have been applied to 

large mature crabs that do not molt (females) or molt only infrequently (males). Internal tags that are retained during molting 

also have been used, but these may require expensive equipment 

for insertion (e.g., microwire tags; Davis et al., 2004a, 2004b) 

and detection (e.g., “pit tags”; Wolcott and Hines, 1996). Internal tags are often not seen by fishers, and also may cause significant mortality (e.g., dart tags; A. H. Hines, personal observation) 

or induce limb autotomy (e.g., elastomer injection; Davis et al., 

2004a, 2004b). However, some forms of internal tags (especially 

microwire or coded wire tags and elastomer injection) work well 

for juveniles as small as 10 mm cw (Davis et al., 2004a, 2004b).

External ultrasonic telemetry tags, which are expensive and 

usually applied to small numbers of crabs >60 mm cw, allow 

acquisition of detailed data on the path of movement and other 

selected aspects of behavior and physiological functions (Figure 

FIGURE 3. Biotelemetry tag attached to blue crab (Callinectes sapidus) eating a clam prey item. Photo by A. Hines.
number 39 • 107

3; Wolcott and Hines, 1989, 1990, 1996; Hines et al., 1995; 

Clark et al., 1999a, 1999b, 2000; Bell et al., 2003a, 2003b). Ultrasonic tags may also be used to transmit data on environmental variables (temperature, conductivity, depth, light) that crabs 

encounter, and they have been developed to signal physiological variables (muscle action potentials, posture, suture breaks of 

the exoskeleton) that are integral components of crab behaviors 

(locomotion, feeding, fighting, mating, molting) in relation to 

location and time (Wolcott, 1995; Wolcott and Hines, 1996). 

Electronic tags that record data about environmental variables 

on microchips and that can be downloaded to a computer when 

the tag is recaptured have been applied recently to blue crabs to 

deduce movement and behavior (Wolcott and Hines, 2004).

In subestuaries of the upper Chesapeake Bay, telemetry studies showed that juveniles (60–80 mm cw) move along shorelines 

within subestuaries, with a typical pattern of periods of meandering slowly (2 m h–1) in shallow (<1 m) water interspersed with 

rapid (>50 m h–1) directional movement to a new meandering 

area (Hines et al., 1995). Juveniles tend to move rather directly 

and rapidly across channels, and not meander in deeper water 

where they are most vulnerable to cannibalism by large crabs; 

however, small juveniles do not seem to move in a net direction 

along the axis of the subestuary as do larger prepubertal and 

adult crabs (Hines and Ruiz, 1995; Hines et al., 1995; Hines and 

Wolcott, unpublished data). Diver-deployed tethering and lab experiments indicated that the impacts of agonism is particularly 

acute for blue crabs in the upper Chesapeake Bay, where cannibalism by adults is the major (>90%) source of mortality of 

juveniles (20–70 mm cw) (Hines and Ruiz, 1995; Hines, 2007). 

Juveniles obtain an important partial refuge from cannibalism 

in shallow water (<50 cm deep), where foraging by adult crabs 

is infrequent and less effective (Dittel et al.,1995; Hines et al., 

1995), effectively restricting use of deeper water by juveniles. 

Biotelemetry and diver-deployed experiments in the Rhode 

River subestuary of the Chesapeake Bay were used to study the 

details of nonmigratory movements of adult and juvenile (>60 

mm cw) blue crabs (reviewed by Hines, 2007). These studies 

showed that intermolt crabs move at an average speed of about 

10 m h–1 during the warm season, but speed varied by month 

from a average high speed of about 15 m h–1 in July to a low average of about 5 m h–1 in May or late September, with no movement 

of males from late November to March. Speed also varied by size 

and life stage, with large males (>140 mm cw) moving faster 

(15 m h–1) than similar-sized females (8 m h–1) or large juveniles 

(100–120 mm cw; 5 m h–1). Movement of mature males decreased 

markedly at premolt stage about three days before ecdysis (Wolcott and Hines, 1990). In summer, adults meander while foraging on patches of infaunal bivalve (Macoma balthica) for periods 

of hours to days, and then suddenly depart the patch, moving 

rapidly in an oriented direction for 0.5–4 km along the estuary 

before stopping to meander and forage again (Wolcott and Hines, 

1989). Departure from the prey patch is triggered by increasing 

agonistic interactions among crabs as other crabs are attracted 

to the feeding site by chemical signals released as foraging crabs 

crush their prey (Clark et al., 1999a, 1999b, 2000). Predation 

rates diminish as agonistic threat displays increase (Clark et al., 

2000). Blue crab foraging can accelerate prey mortality in clam 

patches separated by moderate (7–10 m) distances by attracting 

other crabs, or impede predation by agonism among attracted 

crabs in nearby patches (<7 m) (Hines et al., 2009).

Caging experiments, benthic coring, and analyses of stomach contents showed that predation by demersal fishes and blue 

crabs regulate abundance and species composition of infaunal 

invertebrates in the central Chesapeake Bay (Hines et al., 1990). 

Predator exclusion cages installed and sampled by divers in late 

spring after recruitment of infaunal invertebrates but before summer activity of predators showed that infauna occurred at much 

higher densities within cages. Burrowing bivalves (Macoma 

balthica, Mya arenaria) comprised ~60% of stomach contents of 

blue crabs but not fishes. Diver-deployed and -sampled patches 

of dyed sediment showed that blue crab foraging and burrowing 

(bioturbation) reworked sediments to a depth of 10 cm, below 

which bivalve prey attained a depth refuge from predation.

Conclusion

In the case study of the behavioral ecology of crabs, we addressed the problem of how to determine resource use and movement in systems in which it is exceedingly difficult to make direct 

observations. Niche analysis of cryptic, often very small spider 

crabs required long hours of bottom time on scuba to quantify 

and collect crab population dynamics, depth zonation, habitat use, 

and diet. The crabs showed complex resource partitioning along 

multiple niche dimensions, driven by intense predation pressure 

by an array of fish and sea otters. Ultrasonic telemetry and innovative application of tagging studies as well as diver-deployed

experiments revealed blue crab movement and behavior in murky 

estuarine water. Over three decades, these studies showed mechanisms of dispersal and migration, foraging behavior in response 

to patchily distributed prey, and habitat selection for molting and 

to minimize intense cannibalism of adults on juveniles.

Case Study: Dynamic Behavior

of Fishermen and Their Prey

What is the predatory behavior of humans, and does it 

follow predictions from predator–prey theory? Fishermen are 

opportunistic and often use sophisticated equipment and upto-date information to respond to changes in distribution and 

abundance patterns of their quarry in a manner similar to natural predator–prey systems (Carpenter et al., 1994; Johnson and 

Carpenter, 1994; Post et al., 2002). Although recreational fishers 

often lack the economic incentives that can motivate commercial 

fishers to overexploit populations (Post et al., 2002), recreational 

fishers can produce strong direct and indirect effects in aquatic 

ecosystems (Magnuson, 1991; Kitchell, 1992; Kitchell and Carpenter, 1993; Post et al., 2002; Coleman et al., 2004; Eggleston 

et al., 2008). Recreational fishers have caused severe declines in 
108 • smithsonian contributions to the marine sciences

marine fish such as red drum, Sciaenops ocellatus (Vaughan and 

Carmichael, 2000), and intense reductions in local populations 

of abalone (Haliotis sp.) in central California (Haaker et al., 

1998) and Caribbean spiny lobster (P. argus) in the Florida Keys 

(Eggleston and Dahlgren, 2001; Eggleston et al., 2003, 2008; 

Eggleston and Parsons, 2008). To prevent overharvesting and associated ecological impacts by recreational fishers, as well as to 

successfully predict the outcome of fishery management actions 

such as catch limits or Marine Protected Areas (MPAs), fishery 

scientists and managers must understand the dynamic behavior 

of fishermen and their prey.

Interactions between fishermen, their prey, and management actions can be complex. The functional response, which is 

the relationship between the consumption rate of a predator and 

the density of its prey, provides a powerful theoretical framework to predict the outcome of fishery management actions on 

the dynamic relationship between humans and their prey (Hilborn and Walters, 1992; Carpenter et al., 1994; Johnson and 

Carpenter, 1994; Post et al., 2002; Eggleston et al., 2003, 2008). 

In this case study, a functional response framework was applied 

to sport divers harvesting Caribbean spiny lobster (P. argus) in 

the Florida Keys during a two-day, exclusively recreational fishing season that takes place in late July just prior to the opening 

of the fishing season for commercial fishers and after a threemonth closed period that allows lobsters to spawn (Figure 4). 

Recreational sport divers exploit the gregarious nature of lobsters by targeting dens with high densities of lobsters and coercing them into hand nets with “tickle sticks” (Eggleston et al., 

2003). The research approach in this case study used scuba diver 

surveys of lobster distribution and abundance patterns before 

and after the two-day fishing season, coupled with counts from 

recreational diver efforts at each sampling location, including 

MPAs where lobster harvest was prohibited. Research divers 

also quantified habitat damage (e.g., percent broken or overturned sponges and corals, percent anchor damage to corals, 

etc.; Figure 5) and the number of injured, sublegal lobsters from 

before and after the two-day fishery (Parsons and Eggleston,

2006). They also conducted “sneaky-diver” surveys aboard dive 

charter boats whereby diver behaviors were recorded via video 

and the number of contacts with the reef for a given activity 

(e.g., searching for lobsters, capturing lobsters, bagging lobsters) 

was recorded. In this case study, we answer four questions: (1) 

How do human predators and their prey interact? (2) How do 

sport divers impact their lobster prey? (3) How do Marine Protected Areas (MPAs) mediate (2)? (4) Can observations of diver 

behavior be used to reduce diver injury to lobsters and impacts 

to reefs, and enhance diver safety?

Recreational fishers are generally considered more complex 

in their motivations and behavior than commercial fishermen or 

the type of predators traditionally represented in predator–prey 

models (Carpenter et al., 1994; Johnson and Carpenter, 1994; 

Post et al., 2002). This case study indicates the opposite; exploitation rates of spiny lobster and fishing effort generally varied 

linearly with lobster density (type I functional response), such 

that catchability (i.e., proportion of lobsters extracted by divers per fishing effort), although extremely high (~80% in two 

days), was constant across lobster density in fished areas. There 

was no reduction of lobsters in MPAs during this time. The extraction rates of ~80% of legal-sized lobsters are some of the 

highest ever recorded for any recreational fishery in the world.

The management implications of the high extraction rates and 

simple predatory behavior of divers is that recreational landings 

can be used as a relatively reliable fishery-dependent index of 

lobster population size, and if there is a need to reduce the catch 

of lobsters, such as through catch limits, then there should be a 

proportionate reduction in lobster landings by sport divers due 

to their harvesting a constant proportion at a given lobster density (Eggleston et al., 2008).

Another unexpected finding was an apparent lobster “spillin” effect to certain reefs and MPAs from before to after the 

mini-season (Eggleston and Parsons, 2008; Eggleston et al., 

2008). Marine reserves have the potential to enhance fisheries 

productivity by increasing total spawning potential or by spillover, the migration of juveniles and adults from reserve to nonreserve areas (Sobel and Dahlgren, 2004 and references therein). 

Spill-over has been the focus of many studies and has been an 

important argument in promoting the benefits of marine reserves 

FIGURE 4. Sport divers with catch of P. argus during lobster fishing 

season. Photo by G. Plaia.
number 39 • 109

to gain public support (Sobel and Dahlgren, 2004). Few studies, however, have examined mechanisms for colonization or 

migrations into marine reserves (i.e., spill-in). This case study 

highlights how disturbance from an intense sport diver fishery 

can elevate the abundance of P. argus in nearby marine reserves, 

particularly in reserves containing relatively high densities of 

undisturbed lobsters, presumably through conspecific attraction 

where lobsters follow chemical cues to undisturbed sites in marine reserves. The mechanisms underlying this hypothesis are that 

lobsters disturbed by divers in fished areas would migrate from 

the shelters where they were disturbed (Herrnkind et al., 1975; 

Parsons and Eggleston, 2006) and follow queues of lobsters from 

undisturbed areas back to their shelters at dawn (Herrnkind et 

al., 1975) or use the attractive odors of conspecific lobsters as 

a volume-dependent guide effect (Childress and Herrnkind, 

1997; Ratchford and Eggleston, 1998; Nevitt et al., 2000), or 

both. Population redistribution following fishery disturbance 

has implications for marine reserve design and application. For 

example, risk-averse fishery management strategies might locate 

reserves adjacent to intensely fished areas to enhance spill-in of 

mobile species.

In addition to ~80% removal of legal-sized lobsters in just 

two days, in situ diver observations revealed that up to 27% of 

the remaining population of legal and sublegal lobsters may become visibly injured from interaction with sport divers (Parsons 

and Eggleston, 2005). Lobster injury can result from either an 

unsuccessful capture attempt or a successful capture and release 

of a sublegal lobster. These injuries are detrimental to lobsters 

by reducing their growth (Davis, 1981), causing direct mortality (Parsons and Eggleston, 2005), and increasing exposure to 

predation by emigration from daytime shelters (Parsons and 

Eggleston, 2006). Furthermore, the ability to attract other lobsters is eliminated when a lobster becomes injured (Parsons and 

Eggleston, 2005).

Conclusion

In this case study, we have highlighted how in situ observations helped to refine behavioral ecological theory by testing 

whether humans display a relatively simple or sophisticated 

predatory response to varying densities of spiny lobster prey, 

and the fishery management implications of such a predatory response; improve conservation by demonstrating a novel response 

of mobile organisms to fishery disturbance and undisturbed habitats via lobster spill-in to MPAs; and, improve the role of diver 

education in reducing injury to sublegal lobsters and impacts to 

coral reefs, and improving diver safety.

Case Studies: Reproduction

Diver observations have greatly increased our knowledge of 

the social and reproductive behavior of fish and invertebrates in 

their natural habitats, as well as testing ecological theory and 

informing conservation. Spawning behaviors of fish range from 

annual spawning aggregations of snapper and grouper at distinct locations along the reef tract in the Bahamas and Caribbean 

(Colin, 1992; Nemeth et al., 2006) to paired spawning within 

a male’s territory at sunset, as is the case with Caribbean eyed 

flounder, Bothus ocellatus (Konstantinou and Shen, 1995). For 

fish that form spawning aggregations, understanding the factors 

influencing the timing of migration to spawning sites, functional 

spawning migration area (i.e., the area from which fish migrate 

to an aggregation site), and the similarities and differences in 

residence time and movement patterns among males and females may provide predictable patterns that can be used in setting spatial or seasonal fishing closures to protect aggregations 

from overfishing (Nemeth, 2005). In the latter example of fish 

that spawn within a male’s territory, male B. ocellatus protect 

a harem of 2–6 females within their territory, with males and 

females displaying a courtship ritual that begins one hour before sunset with a male moving beneath a female who is resting 

on sandy bottom, followed by the pair slowly rising ~15–75 cm 

above bottom, followed by the release of gametes (Konstantinou 

and Shen, 1995).

The reproductive success of individuals in paired and 

grouped spawning has often been highest in the largest and most 

robust members of a species (Anderson, 1994; Wolcott et al., 

2005), however recent studies that have paired diver observations of mating behavior with the ability to genetically sample the 

involved individuals and their progeny have detected less mating 

selectivity than originally thought and highly complex sexual 

competition (Alonzo and Warner, 2000; Naud et al., 2004). For 

example, diver observations of spawning aggregations of giant 

cuttlefish, Sepia apama, found many more males than females, 

FIGURE 5. Incidents of habitat damage (e.g., broken corals and 

sponges, obvious anchor damage) per square meter from before and 

after the two-day mini-season for P. argus on patch coral heads in 

the lower Florida Keys during 2003–2005 (D. Eggleston, unpublished. data).
110 • smithsonian contributions to the marine sciences

with fierce competition for females; larger male cuttlefish tended 

to guard females but females chose both large and small males 

to mate with (Naud et al., 2004). Sneaker males were small and 

often colored like females and therefore able to access a guarded 

female cuttlefish. Females used sperm from paired, unpaired, and 

sneaker males, as well as from previous matings, to fertilize cuttlefish eggs (Naud et al., 2004). 

In terms of evolutionary stable strategies, Alonzo and Warner (2000) developed theoretical predictions of mating strategies 

in Mediterranean wrasse, Symphodus ocellatus, based on simultaneous occurrence of intersexual conflict and intrasexual competition, in this case the conflict between when females spawn 

their eggs on a substrate in the presence of nesting males and 

the sneaker males that would then fertilize these eggs. They then 

tested predictions with in situ diver observations in rocky bottom habitats off the coast of Calvi, Corsica, France (Alonzo and 

Warner, 2000). The in situ observations were consistent with a 

dynamic game in which females will not spawn unless in the 

presence of a male guarding a nest and with no sneaker males 

present. However, once a given nest has achieved a high reproductive success, females are more willing to spawn in the presence of sneaker males because of a decrease in the chances that 

a nest will be deserted by a male (Alonzo and Warner, 2000). 

Thus, a combination of computer simulation modeling and in 

situ diver observations and experimental manipulations were 

able to explain counterintuitive mating behavior in S. ocellatus, 

whereby females would deposit eggs in nests in the presence of 

sneaker males.

Conservation programs often focus on studying extinction risks encountered by small populations and determining 

minimum population sizes below which they cannot recover. 

In certain cases, per capita rates of population growth may become negative at low population density, leading to an “Allee 

effect,” or reproductive depensation (Courchamp et al., 1999). 

An example of how in situ observations tested for Allee effects 

in a marine invertebrate is the case of declining populations 

of queen conch, Strombus gigas, in the Bahamas. Strombus 

gigas is a large motile gastropod that supports one of the most 

important marine fisheries in the Caribbean region (Stoner, 

1997). The species has been overharvested throughout much 

of its geographic range, and diverse stock management regulations have been in place in Caribbean nations since the 1980s 

(Appeldoorn, 1994). Stoner and Ray-Culp (2000) conducted 

diver observations and surveys of adult density, reproductive 

behavior, and spawning in natural populations of S. gigas at 

two locations in the Exuma Cays, Bahamas, to test for Allee 

effects. Mating never occurred when density was <56 conch 

ha–1, and spawning never occurred at <48 conch ha–1, clearly 

demonstrating the operation of depensatory mechanisms. Reproductive behavior increased rapidly to asymptotes at densities near 200 conch ha–1 (Stoner and Ray-Culp, 2000). Heavily 

exploited populations of queen conch in the Caribbean have 

been slow to recover despite fishery closures, and this failure is 

likely due to spawning stock densities that are reduced to the 

point at which population growth is no longer possible (Stoner 

and Ray-Culp, 2000).

Conclusion

In these examples, we have highlight how in situ observation via scuba helped inform conservation and restoration of 

the reproductive capacity of marine species. For example, observations of fish during seasonal spawning aggregations helped 

establish spatial boundaries in MPAs or seasonal closures on 

fishing by quantifying the season of fish spawning, residence time 

by fish in certain spawning areas, and movement patterns within 

a given MPA. In situ observations of fish were also valuable in 

testing mating predictions from evolutionary stable strategies 

whereby wrasse fish displayed a type of counterintuitive game in 

which the selectivity of females for males of a certain size varied 

with the level of current reproductive success in a given nest. In 

situ observations also indicated that low population recovery of 

queen conch, despite fishery closures, was due to threshold densities below which conch did not mate.

Additional Examples: Species Invasions, 

Range Extensions, and Novel Behaviors

Range expansion and subsequent population establishment 

of species can have significant impacts on previously established food webs and predator–prey dynamics (Heatwole and 

Levins, 1972; Crawley, 1986; Hargeby et al., 1994). Changes 

in predator–prey dynamics, in turn, often impact population 

dynamics of both predator and prey species (Moorman et al., 

2009). The introduction and colonization of the Indo-Pacific 

lionfish, Pterois volitans, to Atlantic reef communities (Whitfield et al., 2002, 2007) resulted in predation on native fishes 

and reduced recruitment of those fish species to the reef by an 

average of 79% (Albins and Hixon, 2008). Similarly, the Humboldt squid, Dosidicus gigas, has extended its perennial range in 

the northeastern Pacific Ocean during a period of ocean-scale 

warming and concurrent declines in tuna and billfish populations, and may be responsible for the decline of the Pacific hake, 

Merluccius productus, due to predation (Zeidberg and Robison, 

2007). Stone crab, Menippe mercenaria, have apparently become 

established on subtidal oyster reefs in Pamlico Sound, North 

Carolina, at densities equivalent to those in other systems such 

as the Florida Panhandle, and their predatory impact on oysters 

can be high (Rindone and Eggleston, 2011). The common traits 

shared by these examples are the broad impact that relatively 

novel predators have had on their prey and ecosystems, and the 

use of in situ observations by divers to first identify these species 

in new geographic areas, observe their predatory behaviors, and 

subsequently sample these species for trophic analyses and collect them for laboratory predator–prey experiments.

Localized adaptive behaviors that might never have been 

imagined were easily documented by diver observations, underwater digital photography, and video. While octopus are well 
number 39 • 111

known for their ability to adapt their color and texture to their 

surroundings, another species that lives on bare sandy bottoms 

has developed the unique ability to mimic venomous animals as 

a defense. The mimic octopus, Thaumoctopus mimicus, which 

was recently described by divers for the first time, can mimic poisonous or distasteful animals (Norman et al., 2011). Thaumoctopus mimicus has a repertoire of at least five described mimic 

behaviors, three of which can be identified with local venomous 

flatfish, lionfish, and sea snakes. Other behaviors noted by divers 

were those resembling a stinging anemone and jellyfish. This type 

of mimicry is unique in that more than one behavior is exhibited 

by an individual octopus and a particular behavior appears to be 

selected not as a means of blending into the surroundings, but as 

the most appropriate active response to a specific threat (Norman et al., 2011).

The use of tools was originally regarded as a defining feature of humans and primates, yet tool-use behaviors have been 

subsequently found in a growing spectrum of mammals and 

birds (Hansell and Ruxton, 2008). Between 1999 and 2008, Finn 

et al. (2009) spent more than 500 diver hours (day and night) 

on subtidal soft-sediment substrates at depths of ~18 m off the 

coasts of Northern Sulawesi and Bali in Indonesia studying the 

behavior of more than 20 individuals of the veined octopus, Amphioctopus marginatus. They repeatedly observed soft-sedimentdwelling A. marginatus carrying around coconut shell halves 

and assembling them as a shelter when needed. While being carried, the shells offer no protection and placed a requirement on 

the carrier to use a novel and cumbersome form of locomotion, 

“stilt-walking” (Finn et al., 2009). While stilt-walking the octopus gains no protective benefits from the shell(s) it is carrying as 

the head and body are fully exposed to potential predators; the 

only benefit is the potential future deployment of the shell(s) as 

a surface shelter or buried encapsulating lair (Finn et al., 2009). 

Ultimately, the collection and use of objects by animals is likely 

to form a continuum stretching from insects to primates, with 

the definition of tools providing a perpetual opportunity for debate. However, the discovery of this octopus tiptoeing across the 

sea floor with its prized coconut shells suggests that even marine 

invertebrates engage in behaviors that we once thought the preserve of humans. 

CONCLUSIONS

Organisms’ behavior is inextricably linked to their fitness 

and knowledge of these behaviors is therefore paramount in understanding an organism’s ecology. Behaviors, their drivers, and 

subsequent consequences span the spatiotemporal continuum 

from individual foraging decisions on the order of seconds to 

annual migrations across ocean basins to multidecadal environmental oscillations. While no single research tool is or will be 

capable of addressing the entirety of these behavioral scales, it 

is clear that in situ observations have made, are making, and 

will continue to make profound contributions to the field of 

behavioral ecology, and, therefore, should remain a mainstay 

in ecological research programs. Scuba has been a key to making behavioral observations under water that contributed to 

understanding the natural history of species, testing hypotheses 

in situ, and ground truthing technologies such as ultrasonic telemetry and hydroacoustic surveys. Because marine systems are 

some of the most extensively alterable systems on earth, whether 

through rapidly changing food webs due to overfishing (Walsh et 

al., 2006; Jackson, 2008), eutrophication of coastal waters and 

resulting changes in water quality (Verity et al., 2006; Bricker 

et al., 2007), or global climate changes such as warming water 

temperatures and increasing acidification (Dixson et al., 2010; 

Logan, 2010), behavioral observations in the marine realm are 

increasing in their importance. 

ACKNOWLEDGMENTS

We thank Michael Lang for his leadership in organizing the 

Smithsonian Scientific Diving Symposium, and his patience in 

serving as coeditor of these proceedings. We also thank several 

anonymous referees for reviews of a previous draft of this paper, 

and the Smithsonian Institution for sponsoring the Scientific Diving Symposium and these proceedings. 

REFERENCES

Albins, M. A., and M. A. Hixon. 2008. Invasive Indo-Pacific lionfish Pterois volitans 

reduce recruitment of Atlantic coral-reef fishes. Marine Ecology Progress Series, 367:233–238. http://dx.doi.org/10.3354/meps07620.

Alonzo, S. H., and R. R. Warner. 2000. Dynamic games and field experiments examining intra- and intersexual conflict: explaining counterintuitive mating 

behavior in a Mediterranean wrasse, Symphodus ocellatus. Behavioral Ecology, 11:56–70. http://dx.doi.org/10.1093/beheco/11.1.56.

Anderson, M. B. 1994. Sexual selection. Princeton, N. J.: Princeton University Press.

Appeldoorn, R. S. 1994. Spatial variability in the morphology of queen conch and 

its implication for management regulations. In Queen conch biology, fisheries 

and management, ed. R. S. Appeldoor, and B. Rodriguez, pp. 145–158. Caracas: Fundación Científica Los Roques.

Begon, M., C. R. Townsend, and J. L. Harper. 2005. Ecology: From individuals to 

ecosystems. 4th ed. Oxford: Blackwell Publishing.

Behringer, D. C. 2003. The ecological ramifications of density and disease in the 

Caribbean spiny lobster Panulirus argus. Ph.D. diss., Norfolk, Va.: Old Dominion University.

Bell, G. W., D. B. Eggleston, and T. G. Wolcott. 2003a. Behavioral responses of 

free-ranging blue crabs to episodic hypoxia. I. Movement. Marine Ecology 

Progress Series, 259:215–225. http://dx.doi.org/10.3354/meps259215.

———. 2003b. Behavioral responses of free-ranging blue crabs to episodic hypoxia.

II. Feeding. Marine Ecology Progress Series, 259:227–235. http://dx.doi.org

/10.3354/meps259227.

Bellingham, J. G., and K. Rajan. 2007. Robotics in remote and hostile environments. Science, 318: 1098–1102. http://dx.doi.org/10.1126/science.1146230.

Bill, R., and W. F. Herrnkind. 1976. Drag reduction by formation movement in 

spiny lobster. Science, 193:1146–1148. http://dx.doi.org/10.1126/science.193

.4258.1146.

Bouwma, P. E. 2006. Aspects of antipredation in Panulirus argus and Panulirus 

guttatus: Behavior, morphology, and ontogeny. Ph.D. diss., Florida State University, Tallahassee.

Bricker, S., B. Longstaff, W. Dennison, A. Jones, K. Boicourt, C. Wicks, and J. Woerner. 2007. Effects of nutrient enrichment in the nation’s estuaries: A decade 

of change. NOAA Coastal Ocean Program Decision Analysis Series, No. 26. 
112 • smithsonian contributions to the marine sciences

Silver Spring, Md.: National Centers for Coastal Ocean Science. http://ccma

.nos.noaa.gov/publications/eutroupdate/.

Butler, M. J., A. B. MacDiarmid, and J. D. Booth. 1999. The cause and consequence of 

ontogenetic changes in social aggregation in New Zealand spiny lobsters. Marine Ecology Progress Series, 188:179–191. http://dx.doi.org/10.3354/meps

188179.

Butler, M. J., R. S. Steneck, and W. F. Herrnkind. 2006. Juvenile and adult ecology. In Lobsters: Biology, management, aquaculture and fisheries, ed.

B. Phillips, pp. 263–309. Oxford: Blackwell Scientific Press. http://dx.doi

.org/10.1002/9780470995969.ch8.

Carpenter, S. R., K. L. Cottingham, and C. A. Stow. 1994. Fitting predator–prey 

models to time series with observation errors. Ecology, 75:1254–1264.

Childress, M. J., and W. F. Herrnkind. 1997. Den sharing by juvenile Caribbean 

spiny lobsters (Panulirus argus) in nursery habitat: cooperation or coincidence? Marine and Freshwater Research, 48:751–758.

———. 2001. The guide effect influence on the gregariousness of juvenile Caribbean 

spiny lobsters. Animal Behavior, 62:465–472. http://dx.doi.org/10.1006/anbe

.2001.1760.

Clark, M. E., T. G. Wolcott, and A. H. Hines. 1999a. Foraging and agonistic 

activity co-occur in free-ranging blue crabs (Callinectes sapidus): Observations of animals by ultrasonic biotelemetry. Journal of Experimental Marine Biology and Ecology, 233:143–160. http://dx.doi.org/10.1016/S0022

-0981(98)00129-4.

———. 1999b. Intraspecific interference among foraging blue crabs Callinectes 

sapidus: Interference effects of predator density and prey patch distribution. Marine Ecology Progress Series, 178:69–78. http://dx.doi.org/10.3354

/meps178069.

Clark, M. E., T. G. Wolcott, D. L. Wolcott, and A. H. Hines. 2000. Foraging behavior of an estuarine predator, the blue crab Callinectes sapidus in a patchy 

environment. Ecography, 23:21–31. http://dx.doi.org/10.1111/j.1600-0587

.2000.tb00257.x.

Clifton, H. E., C. Mahnken, J. Van Derwalker, and R. Waller. 1970. Tektite I. Manin-the-sea project: Marine science program. Science, 168: 659–663. http://

dx.doi.org/10.1126/science.168.3932.659.

Cohen, D. M. 1977. Swimming performance of the gadoid fish Antimora rostrata at 

2400 m. Deep Sea Research, 24:275–277. http://dx.doi.org/10.1016/S0146

-6291(77)80006-4.

Coleman, D. C., D. A. Crossley, Jr., and P. F, Hendrix. 2004. Fundamentals of Soil 

Ecology, 2nd ed. Burlington, Mass.: Elsevier Academic Press.

Colin, P. L. 1992. Reproduction of the Nassau grouper, Epinephelus striatus (Pisces: 

Serranidae) and its relationship to environmental conditions. Environmental 

Biology of Fishes, 34:357–377.

Cooper, W. E., and W. G. Frederick. 2010. Predator lethality, optimal escape behavior, and autotomy. Behavioral Ecology, 21:91–96. http://dx.doi.org/10.1093

/beheco/arp151.

Courchamp, F., T. Clutton-Brock, and B. Grenfell. 1999. Inverse density dependence 

and the Allee effect. Trends in Ecology and Evolution, 14:405–410. http://

dx.doi.org/10.1016/S0169-5347(99)01683-3.

Crawley, M. J. 1986. The population biology of invaders. Philosophical Transactions of the Royal Society of London, B: 314:711–731. http://dx.doi

.org/10.1098/rstb.1986.0082.

Dahlgren, C. P., and D. B. Eggleston. 2000. Ecological processes underlying ontogenetic habitat shifts in a coral reef fish. Ecology, 8:2227–2240. http://dx.doi

.org/10.1890/0012-9658(2000)081[2227:EPUOHS]2.0.CO;2.

Davis, G. E. 1981. Effects of injuries on spiny lobster, Panulirus argus, and implications for fishery management. U.S. National Marine Fisheries Service Fishery 

Bulletin, 78:979–984.

Davis, J. L. D., A. C. Young-Williams, R. Aguilar, B. L. Carswell, M. R. Goodison, 

A. H. Hines, M. A. Kramer, Y. Zohar, and O. Zmora. 2004a. Differences between hatchery-raised and wild blue crabs (Callinectes sapidus): Implications 

for stock enhancement potential. Transactions of the American Fisheries Society, 133:1–14. http://dx.doi.org/10.1577/T03-004.

Davis, J. L. D., A. C. Young-Williams, A. H. Hines, and O. Zmora. 2004b. Fishery and population studies: Comparing two types of internal tags in juvenile blue crabs. Fisheries Research, 67:265–274. http://dx.doi.org/10.1016/j

.fishres.2003.11.005.

Dittel, A. I., A. H. Hines, G. M. Ruiz, and K. K. Ruffin. 1995. Effects of shallow 

water refuge on behavior and density-dependent mortality of juvenile blue 

crabs in Chesapeake Bay. Bulletin of Marine Science, 57:903–917.

Dixson, D. L., P. L. Munday, and G. P. Jones. 2010. Ocean acidification disrupts 

the innate ability of fish to detect predator olfactory cues. Ecology Letters,

13:68–75. http://dx.doi.org/10.1111/j.1461-0248.2009.01400.x.

Drazen, J. C., S. K. Goffredi, B. Schlining, and D. S. Stakes. 2003. Aggregations 

of deep-sea brooding fish and cephalopods on the Gorda escarpment: A reproductive hotspot. Biological Bulletin, 205:1–7. http://dx.doi.org/10.2307

/1543439.

Eggleston, D. B. 1995. Recruitment in Nassau Grouper, Epinephalus striatus: 

Post settlement abundance, microhabitat features, and ontogenetic habitat 

shifts. Marine Ecology Progress Series, 124:9–22. http://dx.doi.org/10.3354

/meps124009.

Eggleston, D. B., E. G. Johnson, G. T. Kellison, and D. A. Nadeau. 2003. Intense 

removal and non-saturating functional responses by recreational divers on 

spiny lobster Panulirus argus. Marine Ecology Progress Series, 257:197–203. 

http://dx.doi.org/10.3354/meps257197.

Eggleston, D. B., and R. N. Lipcius. 1992. Shelter selection by spiny lobster under 

variable predation risk, social conditions, and shelter size. Ecology, 73:992–

1011. http://dx.doi.org/10.2307/1940175.

Eggleston, D. B., R. N. Lipcius, L. Coba-Centina, and D. Miller. 1990. Shelter scaling regulates survival of juvenile spiny lobster, Panulirus argus. Marine Ecology Progress Series, 62:79–88. http://dx.doi.org/10.3354/meps062079.

Eggleston, D. B., and C. P. Dahlgren. 2001. Distribution and abundance of Caribbean spiny lobsters in the Key West National Wildlife Refuge: relationship to 

habitat features and impact of an intensive recreational fishery. Marine and 

Freshwater Research, 52:1567–1576.

Eggleston, D. B., and D. M. Parsons. 2008. Disturbance-induced spill-in of Caribbean spiny lobster to marine reserves. Marine Ecology Progress Series, 371: 

213–220. http://dx.doi.org/10.3354/meps07699.

Eggleston, D. B., D. M. Parsons, G. T. Kellison, G. R. Plaia, and E. G. Johnson. 

2008. Functional response of sport divers to lobsters with application to 

fisheries management. Ecological Applications, 18:258–272. http://dx.doi

.org/10.1890/06-1409.1.

Ehrhardt, N. M., and V. Deleveaux. 1999. Report on the 1999 Nassau grouper 

stock assessment in the Bahamas. Miami: University of Miami. 

Etherington, L. L., and D. B. Eggleston. 2003. Spatial dynamics of large-scale, multistage crab dispersal: Determinants and consequences for recruitment. Canadian Journal of Fisheries and Aquatic Sciences, 60:873–887. http://dx.doi

.org/10.1139/f03-072.

Finn, J. K., T. Tregenza, and M. D. Norman. 2009. Defensive tool use in a coconut carrying octopus. Current Biology, 19: R1069–R1070. http://dx.doi

.org/10.1016/j.cub.2009.10.052.

Gebruk, A. V., E. C. Southworth, H. Kennedy, and A. J. Southward. 2000. Food 

sources, behavior and distribution of hydrothermal vent shrimps at the MidAtlantic Ridge. Journal of the Marine Biological Association of the U.K., 

80:485–499. http://dx.doi.org/10.1017/S0025315400002186.

Gillanders, B. M., K. W. Abel, J. A. Brown, D. B. Eggleston, and P. F. Sheridan. 2003. 

Evidence for connectivity between juvenile and adult habitat for mobile marine fauna: Important component of nurseries. Marine Ecology Progress Series, 247:281–295. http://dx.doi.org/10.3354/meps247281.

Haaker, P. L., D. O. Parker, K. C. Barsky, and C. S. Y. Chun. 1998. Growth of red 

abalone, Haliotis rufescens (Swainson), at Johnsons Lee, Santa Rosa Island, 

California. Journal of Shellfish Research, 17:747–753.

Hamner, W. M., and B. H. Robison. 1992. In situ observations of giant appendicularians on Monterey Bay. Deep Sea Research, 39:1299–1313. http://dx.doi

.org/10.1016/0198-0149(92)90070-A.

Hansell, M., and G. D. Ruxton. 2008. Setting tool use within the context of animal 

construction behaviour. Trends in Ecology and Evolution, 23:73–78. http://

dx.doi.org/10.1016/j.tree.2007.10.006.

Hargeby, H., G. Andersson, I. Blindow, and S. Johansson. 1994. Trophic web 

structure in a shallow eutrophic lake during a dominance shift from phytoplankton to submerged macrophytes. Hydrobiologia, 279/280:83–90. http://

dx.doi.org/10.1007/BF00027843.

Heatwole, H., and R. Levins. 1972. Trophic structure stability and faunal 

change during recolonization. Ecology, 53:531–534. http://dx.doi.org/10

.2307/1934248.

Herrnkind, W. F. 1969. Queuing behavior of spiny lobsters. Science, 164:1425–

1427. http://dx.doi.org/10.1126/science.164.3886.1425.

———. 1974. In situ approach to marine behavioral research. In Experimental 

marine biology, ed. R. Mariscal, pp. 55–98. New York: Academic Press.

———. 1980. Movement patterns in palinurid lobsters. In The Biology and Management of Lobsters: Volume 1: Physiology and Behavior, ed. J. Cobb and 

B. Phillips, pp. 349–407. New York: Academic Press.

———. 1983. Movement patterns and orientation of Crustacea. In Biology of 

Crustacea: Volume 5: Behavior and Ecology of Crustacea, ed. F. Vernberg 

and W. Vernberg, pp. 41–105. New York: Academic Press. 
number 39 • 113

———. 1985. Evolution and mechanisms of mass single-file migration in spiny 

lobster: Synopsis. Contributions to Marine Science, 27:197–211.

Herrnkind, W. F., M. J. Childress, and K. L. Lavalli. 2001. Defense coordination and 

other benefits among exposed spiny lobsters: Inferences from mass migratory 

and mesocosm studies of group size and behavior. Marine and Freshwater 

Research, 52:1113–1124. http://dx.doi.org/10.1071/MF01044.

Herrnkind, W. F., and W. C. Cummings. 1964. Single file migrations of spiny lobster, 

Panulirus argus (Latreille). Bulletin of Marine Science of the Gulf and Caribbean, 14(1):123–125.

Herrnkind, W. F., and R. McLean. 1971. Field studies of orientation, homing, and 

mass emigration in the spiny lobster, Panulirus argus. Annals of the New 

York Academy of Sciences, 188:359–377. http://dx.doi.org/10.1111/j.1749-

6632.1971.tb13109.x.

Herrnkind, W. F., J. Vanderwalker, and L. Barr. 1975. Population dynamics, ecology and behavior of spiny lobster, Panulirus argus, of St. John, U.S. Virgin 

Islands: Habitation and pattern of movements. Results of the TEKTITE Program, Volume 2. Bulletin of the Natural History Museum of Los Angeles 

County, 20:31–45.

Hilborn, R., and C. J. Walters. 1992. Quantitative Fisheries Stock Assessment: 

Choice, Dynamics and Uncertainty. New York: Chapman and Hall.

Hines, A. H. 1982. Coexistence in a kelp forest: Size, population dynamics, and 

resource partitioning in a guild of spider crabs. Ecological Monographs, 52: 

179–198. http://dx.doi.org/10.2307/1942610.

———. 2007. Ecology of juvenile and adult blue crabs. In The Blue Crab Callinectes sapidus, ed. V. S. Kennedy and L. E. Cronin, pp. 565–654. College 

Park, Md.: Maryland Sea Grant College, Publication UM-SG-TS-2007-01.

Hines, A. H., A. M. Haddon, and L. A. Wiechert. 1990. Guild structure and foraging impact of blue crabs and epibenthic fish in a subestuary of Chesapeake 

Bay. Marine Ecology Progress Series, 67:105–126. http://dx.doi.org/10.3354/

meps067105.

Hines, A. H., W. C. Long, J. R. Terwin, and S. F. Thrush. 2009. Facilitation, interference, and scale: The spatial distribution of prey patches affects predation 

rates in an estuarine benthic community. Marine Ecology Progress Series,

385:127–135. http://dx.doi.org/10.3354/meps08055.

Hines, A. H., and G. M. Ruiz. 1995. Temporal variation in juvenile blue crab mortality: Nearshore shallows and cannibalism in Chesapeake Bay. Bulletin of 

Marine Science, 57:884–901.

Hines, A. H., T. G. Wolcott, E. González-Gurriarán, J. L. González-Gurriarán, and 

J. Friere. 1995. Movement patterns and migrations in crabs: Telemetry studies of juvenile and adult behavior in Callinectes sapidus and Maja squinado. 

Journal of the Marine Biological Association of the U.K., 75:27–42. http://

dx.doi.org/10.1017/S0025315400015174.

Hutchinson, G. E. 1959. Homage to Santa Rosalia, or why are there so many kinds 

of animals? American Naturalist, 93:45–159.

Jackson, J. B. C. 2008. Ecological extinction and evolution in the brave new ocean. 

Proceedings of the National Academy of Sciences, 105:11458–11465. http://

dx.doi.org/10.1073/pnas.0802812105.

Johnson, B. M., and S. R. Carpenter. 1994. Functional and numerical responses: a 

framework for fish-angler interactions? Ecological Applications, 4:808–821.

Kitchell, J. F., ed. 1992. Food web management: A case study of Lake Mendota. 

New York: Springer-Verlag.

Kitchell, J. F., and S. R. Carpenter. 1993. Variability in lake ecosystems: Complex responses by the apical predator. In Humans as components of ecosystems, ed. M. McDonnell and S. Pickett, pp. 111–124. New York: SpringerVerlag.

Konstantinou, H., and D. C. Shen. 1995. The social and reproductive behavior of 

the eyed flounder, Bothus ocellatus, with notes on the spawning of Bothus 

lunatus and Bothus ellipticus. Environmental Biology of Fishes, 44:311–324.

Krebs, J. R., and N. B. Davies. 1993. An introduction to behavioural ecology. Oxford: Wiley-Blackwell Publishing. 

Lavalli, K., and W. F. Herrnkind. 2009. Collective defense by spiny lobster (Panulirus argus Latrielle, 1804) against triggerfish (Balistes capriscus Gmelin, 

1788): Effects of number of attackers and defenders. New Zealand Journal 

of Marine and Freshwater Research, 43:15–28. http://dx.doi.org/10.1080

/00288330909509978.

Logan, C. A. 2010. A review of ocean acidification and America’s response. BioScience, 60:819–828. http://dx.doi.org/10.1525/bio.2010.60.10.8.

Mackie, G. O., and C. E. Miller. 1983. Use of Pisces IV submersible for zooplankton 

studies in coastal waters of British Columbia. Canadian Journal of Fisheries 

and Aquatic Sciences, 40:763–776. http://dx.doi.org/10.1139/f83-099.

MacLennan, D. N., and E. J. Simmonds. 1992. Fisheries acoustics. London: Chapman and Hall.

Madin, L. P. 1974. Field observations on the feeding behavior of salps (Tunicata: 

Thaliacea). Marine Biology, 25:143–147. http://dx.doi.org/10.1007/BF003

89262.

Magnuson, J. J. 1991. Fish and fisheries ecology. Ecological Applications, 1(1):13–26.

Marx, J. M., and W. F. Herrnkind. 1985. Macroalgae (Rhodophyta: Laurencia spp.) 

as habitat for young juvenile spiny lobsters, Panulirus argus. Bulletin of Marine Science, 36:423–431.

Maynard Smith, J. 1982. Evolution and the Theory of Games. Cambridge: Cambridge University Press.

McMullin, E. R., D. C. Berkquist, and C. R. Fisher. 2000. Metazoans in extreme environments: Adaptations of hydrothermal vent and hydrocarbon seep fauna. 

Gravitational and Space Biology Bulletin, 13:1–23.

McNamara, J. M., and A. I. Houston. 1986. The common currency for behavioral 

decisions. American Naturalist, 127:358–378.

Miller, J. W., J. VanDerwalder, and R. Waller, eds. 1971. Tektite I. Scientists-in-theSea. Washington, D.C.: U.S. Government Printing Office.

Mintz, J. D., R. N. Lipcius, D. B. Eggleston, and M. S. Seebo. 1994. Survival of juvenile Caribbean spiny lobster: Effects of shelter size, geographic location and 

conspecific abundance. Marine Ecology Progress Series, 112:255–266. http://

dx.doi.org/10.3354/meps112255.

Moorman, M. C., D. B. Eggleston, C. B. Anderson, A. Mansilla, and P. Szjener. 2009. 

The implications of North American beaver and trout invasion on native 

diadromous fish in the Cape Horne Biosphere Reserve, Chile. Transactions 

of the American Fisheries Society, 138:306–313. http://dx.doi.org/10.1577

/T08-081.1.

Naud, M.-J., R. T. Hanlon, K. C. Hall, P. W. Shaw, and J. N. Havenhand. 2004. 

Behavioral and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. Animal Behavior,

67:1043–1050. http://dx.doi.org/10.1016/j.anbehav.2003.10.005.

Nemeth, R. S. 2005. Recovery of a U.S. Virgin Islands red hind spawning aggregation following protection. Marine Ecology Progress Series, 286:81–97. http://

dx.doi.org/10.3354/meps286081.

Nemeth, R. S., E. Kadison, S. Herzlieb, J. Blondeau, and E. A. Whiteman. 2006. 

Status of a yellowfin (Mycteroperca venenosa) grouper spawning aggregation 

in the U.S. Virgin Islands with notes on other species. Proceedings of the Gulf 

and Caribbean Fisheries Institute, 57:541–558.

Nevitt, G., N. D. Pentcheff, K. J. Lohmann, and R. K. Zimmer. 2000. Den selection 

by the spiny lobster Panulirus argus: testing attraction to conspecific odors in 

the field. Marine Ecology Progress Series, 203:225–231.

Norman, M. D., J. Finn, and T. Tregenza. 2011. Dynamic mimicry in an IndoMalayan octopus. Proceedings of the Royal Society of London, B, 268:1755–

1758. http://dx.doi.org/10.1098/rspb.2001.1708.

Orth, R. J., and J. van Montfrans. 1987. Utilization of a seagrass meadow and tidal 

marsh creek by blue crabs Callinectes sapidus. I. Seasonal and annual variations in abundance with emphasis on post-settlement juveniles. Marine Ecology Progress Series, 41:283–294. http://dx.doi.org/10.3354/meps041283.

Palma, A., and R. S. Steneck. 2002. Does variable coloration in juvenile marine 

crabs reduce risk of visual predation? Ecology, 82:2961–2967. http://dx.doi

.org/10.1890/0012-9658(2001)082[2961:DVCIJM]2.0.CO;2.

Pardieck, R. A., R. J. Orth, R. J. Diaz, and R. N. Lipcius. 1999. Ontogenetic changes 

in habitat use by postlarvae and young juveniles of the blue crab. Marine Ecology Progress Series, 186:227–238. http://dx.doi.org/10.3354/meps186227.

Parsons, D. P., and D. B. Eggleston. 2005. Indirect effects of recreational fishing 

on spiny lobster behavior (Panulirus argus). Marine Ecology Progress Series, 

303:235–244. http://dx.doi.org/10.3354/meps303235.

———. 2006. Human disturbance, natural predators and unobserved mortality in 

a spiny lobster, Panulirus argus, fishery. Journal of Experimental Marine Biology and Ecology, 334:196–205.

Pile, A. J., R. N. Lipcius, J. van Montfrans, and R. J. Orth. 1996. Density-dependent 

settler–recruit–juvenile relationships in blue crabs. Ecological Monographs,

66:277–300. http://dx.doi.org/10.2307/2963519.

Post, E., N. C. Stenseth, R. O. Peterson, J. A. Vucetich, and A. M. Ellis. 2002. Phase 

dependence and population cycles in a large-mammal predator–prey system. 

Ecology, 83:2997–3002.

Ratchford, S. G., and D. B. Eggleston. 1998. Size- and scale-dependent chemical attraction contribute to an ontogenetic shift in sociality. Animal Behavior, 56: 

1027–1034. http://dx.doi.org/10.1006/anbe.1998.0869.

Reyns, N. B., and D. B. Eggleston. 2004. Environmentally controlled, densitydependent secondary dispersal in a local estuarine crab population. Oecologia, 140:280–288. http://dx.doi.org/10.1007/s00442-004-1581-8.

Rindone, R. R., and D. B. Eggleston. 2011. Predator–prey dynamics between recently established stone crabs (Menippe spp.) and oyster prey (Crassostrea 
114 • smithsonian contributions to the marine sciences

virginica). Journal of Experimental Marine Biology and Ecology, 407(2): 

216–225. http://dx.doi.org/10.1016/j.jembe.2011.06.018.

Sobel, J., and C. P. Dahlgren. 2004. Marine reserves: A guide to science, design and 

use. Washington, D.C.: Island Press.

Spanier, E., J. S. Cobb, and M. Clancy. 1994. Impacts of remotely operated vehicles (ROVs) on the behavior of marine animals: An example using American lobsters. Marine Ecology Progress Series,104:257–266. http://dx.doi

.org/10.3354/meps104257.

Starck, W. A. 1968. A list of fishes of Alligator Reef, Florida with comments on the 

nature of the Florida reef fish fauna. Undersea Biology, 1:4–40.

Starr, R. M., D. S. Fox, M. A. Hixon, B. N. Tissot, G. E. Johnson, and W. H. Barss. 

1996. Comparison of submersible-survey and hydroacoustic-survey estimates 

of fish density on a rocky bank. Fishery Bulletin U.S., 94:113–123.

Stephens, D. W., and J. R. Krebs. 1968. Foraging theory. Monographs in behavior 

and ecology. Princeton: Princeton University Press.

Stoner, A. W. 1997. The status of queen conch, Strombus gigas, research in the 

Caribbean. Marine Fisheries Research, 59:14–22.

Stoner, A. W., and M. Ray-Culp. 2000. Evidence for Allee effects in an over-harvested

marine gastropod: Density-dependent mating and egg production. Marine 

Ecology Progress Series, 202:297–302. http://dx.doi.org/10.3354/meps202297.

Tagatz, M. E. 1968. Biology of the blue crab, Callinectes sapidus Rathbun, in the St. 

John’s River, Florida. Fishery Bulletin, 67:17–33.

Taylor, J. C., D. B. Eggleston, and P. S. Rand. 2006. Nassau grouper (Epinephelus 

striatus) spawning aggregations: Hydroacoustic surveys and geostatistical 

analysis. In Emerging technologies in reef fisheries management, ed. J. C. Taylor, pp. 18–25. Seattle: NOAA Professional Paper NMFS 5.

Todd, P. A., R. A. Biers, R. J. Ladle, and F. Middleton. 2006. Phenotype-environment 

matching in the shore crab (Carcinus maenas). Marine Biology, 148:1357–

1367. http://dx.doi.org/10.1007/s00227-005-0159-2.

Uiblein, F., P. Lorance, and D. Latrouite. 2003. Behavior and habitat utilization of 

seven demersal fish species on the Bay of Biscay continental shelf, NE Atlantic. Marine Ecology Progress Series, 257:223–232. http://dx.doi.org/10.3354

/meps257223.

Van Engel, W. A. 1958. The blue crab and its fishery in Chesapeake Bay. Part 1. Reproduction, early development, growth, and migration. Commercial Fisheries 

Review, 20:6–17.

Verity, P. G., M. L. Alber, and S. B. Bricker. 2006. Development of hypoxia in wellmixed estuaries in the southeastern USA. Estuaries and Coasts, 29:665–673.

Walsh, M. R., S. B. Munch, S. Chibe, and D. O. Conover. 2006. Maladaptive changes 

in multiple traits caused by fishing: Impediments to population recovery. 

Ecology Letters, 9:142–148. http://dx.doi.org/10.1111/j.1461-0248.2005

.00858.x.

Webb, J. K., D. A. Pike, and R. Shine. 2010. Olfactory recognition of predators 

by nocturnal lizards: Safety outweighs thermal benefits. Behavioral Ecology,

21:72–77. http://dx.doi.org/10.1093/beheco/arp152.

Werner, E. E., and J. F. Gilliam. 1984. The ontogenetic niche and species interactions 

in size structured populations. Annual Review of Ecology and Systematics,

15:393–425.

Whitfield, P. E., T. Gardner, S. P. Vives, M. R. Gilligan, W. R. Courtenay, G. C. Ray, 

and J. A. Hare. 2002. Biological invasion of the Indo-Pacific lionfish Pterois 

volitans along the Atlantic coast of North America. Marine Ecology Progress 

Series, 235:289–297. http://dx.doi.org/10.3354/meps235289.

Whitfield, P. E., J. A. Hare, A. W. David, S. L. Harter, R. C. Muñoz, and C. M. Addison. 2007. Abundance estimates of the Indo-Pacific lionfish Pterois volitans/

miles complex in the Western North Atlantic. Biological Invasions, 9:53–64. 

http://dx.doi.org/10.1007/s10530-006-9005-9.

Wolcott, T. G. 1995. New options in physiological and behavioral ecology through 

multi-channel telemetry. Journal of Experimental Marine Biology and Ecology, 193:257–275. http://dx.doi.org/10.1016/0022-0981(95)00121-2.

Wolcott, T. G., and A. H. Hines. 1989. Ultrasonic biotelemetry of muscle activity 

from free-ranging marine animals: A new method for studying foraging by 

blue crabs (Callinectes sapidus). Biological Bulletin, 176:50–56. http://dx.doi

.org/10.2307/1541888.

———. 1990. Ultrasonic telemetry of small-scale movements and microhabitat selection by molting blue crabs. Bulletin of Marine Science, 46:83–94.

———. 1996. Advances in ultrasonic biotelemetry for animal movement and behavior: The blue crab case study. In Methods and techniques of underwater 

research, ed. M. A. Lang and C. C. Baldwin, pp. 229–236. Nahant, Mass.: 

American Academy of Underwater Sciences.

———. 2004. Migration of adult blue crabs to spawning grounds: Mechanisms and 

routes. In Chesapeake Bay fisheries research program symposium report 2003, 

ed. D. Orner, pp. 17–24. Annapolis, Md.: NOAA Chesapeake Bay Office.

Zeidberg, L. D., and B. H. Robison. 2007. Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Pacific. Proceedings of the 

National Academy of Sciences, 104:12948–12950. http://dx.doi.org/10.1073

/pnas.0702043104.

Zimmer-Faust, R. K., J. E. Tyre, and J. F. Case. 1985. Chemical attraction causing 

aggregation in the spiny lobster, Panulirus interruptus (Randall), and its probable ecological significance. Biological Bulletin, 169:106–118. http://dx.doi

.org/10.2307/1541391.
Kelp Forests in California

Michael S. Foster, Daniel C. Reed, Mark H. Carr, Paul K. Dayton, 

Daniel P. Malone, John S. Pearse, and Laura Rogers-Bennett

ABSTRACT. Kelp forests, with their complex structure and high diversity and productivity, are 

the most charismatic of nearshore, subtidal communities in temperate waters. Knowledge of their 

natural history and ecology, however, was meager until the 1950s when scuba gave investigators the 

freedom to work under water with relative ease. We highlight some of the knowledge gained using 

scuba in California kelp forests during the past 60 years. Underwater measurements have revealed 

that the net primary productivity of giant kelp (Macrocystis) and associated seaweeds is among the 

highest reported for any ecosystem. The producers are a suite of macroalgal canopy guilds that occur in patches and intercept light at various levels in the water column. The patches are dynamic, 

influenced within forests by biological interactions and among forests by disturbance. Invertebrates 

partition forest resources in a variety of ways, responding to variation in vegetation, predators, and 

competition. Grazing sea urchins and abalone have been of great interest relative to the dynamics of 

kelp forest ecosystems as the former can cause “deforestation” and the latter have severely declined 

due to overfishing and, more recently, disease. Recent research suggests that sea urchin population 

dynamics may differ among regions due to differences in disturbance and recruitment. From their 

beginning, scuba-enhanced studies of kelp forests pursued a variety of ecological questions including 

understanding human impacts related to degraded water quality, overfishing, and kelp harvesting. 

Concerns over human impacts have increased with further declines in many fished species as well 

as changes in ocean climate due to CO2 emissions, particularly changes in temperature, nutrients, 

frequency and intensity of ENSO, and pH. The present challenge is to understand the interactive 

effects of these stressors along with our fundamental understanding of how unperturbed kelp forest ecosystems are structured and function, and use the information to facilitate ecosystem-based 

management (EBM) of these important and productive coastal marine systems. The hope is that 

EBM, done in conjunction with the establishment of marine protected areas, will help sustain these 

remarkable underwater forests.

INTRODUCTION AND HISTORY

“The possibility of exploration by diving, and consequently of adding direct 

vision to direct collecting, ought to make of the eulittoral zone, in the near future, 

one of the best known parts of the underwater continental shelf.” —Drach, 1958

Giant kelp (Macrocystis) forests, dominated by float-bearing plants over 50 m long 

growing from the bottom and spreading thick canopies across the sea surface, provided 

food, materials, and no doubt intrigue for humans long before Darwin (1839) published 

the first insights into their ecology. Darwin’s observations and collections were necessarily made from the surface and, like trying to understand the ecology of terrestrial forests 

by observing tree canopies and trees pulled up from the ground, such study from the 

waterline could provide only a glimpse of the community. Progress required a suitable air 

supply and a warm, flexible diving suit to make observation and work under water into a 

Michael S. Foster, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, California 95039, USA. Daniel C. Reed,

Marine Science Institute, University of California, 

Santa Barbara, Santa Barbara, California 93106, 

USA. Mark H. Carr, University of California, 

Santa Cruz, Department of Ecology and Evolutionary Biology, Long Marine Laboratory, 100 

Shaffer Road, Santa Cruz, California 95060, 

USA. Paul K. Dayton, Mail Code 0227, Scripps 

Institution of Oceanography, La Jolla, California 92093, USA. Daniel P. Malone and John 

S. Pearse, University of California, Santa Cruz, 

Department of Ecology and Evolutionary Biology, Long Marine Laboratory, 100 Shaffer Road, 

Santa Cruz, California 95060, USA. Laura 

Rogers-Bennett, University of California, Davis, 

California Department of Fish and Game, Bodega 

Marine Laboratory, 2099 Westside Road, Bodega 

Bay, California 94923, USA. Correspondence:

M. Foster, foster@mlml.calstate.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
116 • smithsonian contributions to the marine sciences

practical pursuit. Primitive surface-supply diving equipment was 

used by Kitching et al. (1934) in their pioneering studies of kelp 

beds in the U.K. With the exception of Andrews (1945), however, who used “helmet diving” to collect giant kelp holdfasts 

for identification and enumeration of their fauna, surface supply 

was rarely used to study much larger giant kelp forests of the 

world, likely in part because hoses and lines readily tangle with 

kelp fronds.

The difficulties of working easily, efficiently, and safely 

under water were essentially eliminated by the development of 

scuba by Cousteau and Gagnan in 1943 (Dugan, 1965) and of 

the neoprene wet suit for divers by Bradner in 1951 (Rainey, 

1998). Drach was encouraged by Cousteau to train in the use 

of the new “scaphandre autonome” with the French Navy and 

to use the technology for ecological studies (Dugan, 1965). He 

was the first to publish a paper based on scuba observations in 

kelp communities, in this case Laminaria beds in Europe (Drach, 

1949). Drach (1958) later clearly recognized the positive impact 

this underwater tool would have on understanding the ecology 

of temperate reefs. Further studies using scuba to observe and 

describe kelp beds in Europe soon followed (e.g., Forster, 1954; 

Ernst, 1955; Kain, 1960). 

A few marine science graduate students in southern California began using scuba soon after the first Aqua-Lungs were 

imported from France in 1949. As in France, the availability and 

use of the equipment was facilitated by collaborations with the 

navy, in this case the U.S. Navy in San Diego. The beginnings 

of the use of scuba to study kelp forests were largely due to 

the curiosity and efforts of Conrad Limbaugh (Figure 1, left), a 

graduate student at Scripps Institution of Oceanography. He also 

developed training procedures, offered informal training courses, 

and began the first institutional marine science diving program 

at Scripps in 1953 (Dugan, 1965; Price, 2008). Limbaugh’s colleagues and students started a local dive store, a consulting firm 

specializing in underwater surveys, and the Underwater Instructor Certification Course supported by Los Angeles County, the 

first such program in the USA. Limbaugh’s pioneering work led 

to the rapid spread of scuba as a tool for basic and applied studies as well as recreation—a remarkable legacy. 

The use of this new technology in kelp forest ecology was 

initially concentrated along the southern California mainland, 

stimulated by concerns over the effects of harvesting giant kelp 

on sport fishing and of sewage discharges on the health and sustenance of kelp forests. Limbaugh (1955) was the first to investigate the effects of kelp harvesting, providing information on 

the habitat utilization and feeding habits of numerous kelp forest fishes and the distribution of common invertebrates. This research included comparing fish assemblages in harvested versus 

unharvested stands, the first field experiment in a kelp forest. 

Aleem (1956), a research fellow at Scripps in 1955, used scuba to 

provide the first quantitative description of kelp forest zonation 

and the standing crop of algae and invertebrates. The studies of 

Limbaugh and Aleem were followed by those of Limbaugh’s colleague Wheeler J. North (Figure 1, right). North’s investigations 

FIGURE 1. Conrad Limbaugh (left) and Wheeler J. North (right). Photos from Scripps Institution of Oceanograpy Archives, UC San Diego.
number 39 • 117

were focused both on kelp harvesting and sewage discharge effects, and done primarily from the perspective of the effects on 

Macrocystis itself (North, 1964; North and Hubbs, 1968). These 

early studies provided much of the basic descriptive and life history information about kelp forests, their associated organisms, 

and the phenomena that affect their abundance and distribution 

(summarized in North, 1971a) that continues to serve as a foundation and stimulus for new research. 

Perhaps more important than his studies, North established 

long-term research projects with the University of California Institute of Marine Resources in La Jolla, and later at the W. M. 

Keck Laboratory of Environmental Health Engineering at the 

California Institute of Technology. These long-term studies provided research funding support and research opportunities for 

numerous collaborators, many of whom went on to establish 

their own kelp forest research programs, thereby rapidly building this field of marine ecology. 

A search of “giant kelp forest ecology” on Google Scholar 

yields nearly 11,000 results, an indication of the success of these 

pioneer kelp forest ecologists and the daunting, perhaps futile 

task of producing a comprehensive review of the topic. Fortunately there have been a number of reviews of kelp forest ecology (Dayton, 1985a; Foster and Schiel, 1985; Schiel and Foster, 

1986) since North (1971a). The most recent reviews are by Graham et al. (2007, 2008). 

In this paper, rather than write another comprehensive review, we decided to write a brief synopsis of a few selected topics 

on the ecology of giant kelp forests that focus on our specific 

areas of expertise and interest, with each author taking the lead 

in the following themes: Introduction and History (MF), Patterns and Controls of Primary Production (DR), Disturbance and 

Patch Dynamics (PD), Resource Partitioning (JP), Kelp Forests, 

Sea Urchins, and Abalone (LRB), and Scuba-Based Management 

(MC and DM). We hope that this paper provides the reader with 

up-to-date and interesting perspectives on a few aspects of kelp 

forest ecology that have been shaped by the use of scuba.

PATTERNS AND CONTROLS 

OF PRIMARY PRODUCTION 

IN KELP FOREST ECOSYSTEMS

Net primary production (NPP) is the rate at which autotrophs transform carbon dioxide into organic matter per unit 

area of the Earth’s surface. It is perhaps the most defining attribute of an ecosystem because it influences virtually all ecological 

processes. When evaluated in this context giant kelp (Macrocystis 

pyrifera) forests have few rivals as their NPP ranks among the 

highest reported for any ecosystem in the world (Mann, 2000; 

Reed and Brzezinski, 2009). Had it not been for scuba, this important attribute of kelp forests may have gone undetected. 

Numerous methods have been used to estimate the standing 

biomass of giant kelp, and virtually all of them have involved the 

use of scuba (Table 1). The most direct method entails measuring 

the mass of all kelp in harvested plots (Wheeler and Druehl, 1986; 

Van Tussenbroek, 1989). The destructive nature of this method 

can limit the size and number of spatial replicates and constrains 

investigations of temporal dynamics as it eliminates the ability 

to sample the same plots repeatedly over time. These constraints 

have been reduced by diver estimates of plant or frond density 

coupled with simultaneous collections of representative plants or 

fronds that are returned to the laboratory and weighed and/or 

measured (Towle and Pearse, 1973; Gerard, 1976). North (1957) 

devised a stipe index for non-destructively estimating standing 

crop of Macrocystis based on the density of fronds >1 m tall 

(measured by divers) and a mean value for frond mass, which 

was adopted by McFarland and Prescott (1959). Rassweiler et 

al. (2008) modified this technique to include diver measurements 

of frond length (Figure 2). 

Many physical and biological factors interact to influence 

the biomass of giant kelp at any point in time (reviewed in Foster 

and Schiel, 1985; North, 1994; Graham et al., 2007), making 

it difficult to compare estimates from different studies. Regardless of the method used, however, it is unequivocally clear that 

the standing crop of giant kelp is substantially less than that of 

terrestrial forests despite it having equal or substantially higher 

NPP (Reed and Brzezinski, 2009). The relatively high production/biomass ratios (~6 to 7) and low levels of litter accumulation (~0.015 dry kg m–2) reported for Macrocystis within giant 

kelp forests (Gerard, 1976; Harrold and Reed, 1985; Reed et 

al., 2008) reflect high biomass turnover and little carbon storage 

because kelp detritus is either rapidly consumed or decomposed 

within the forests (Gerard, 1976; Harrold and Reed, 1985), 

or exported to adjacent beach and deep water habitats where 

it serves as an important carbon subsidy (Harrold et al., 1998; 

Dugan et al., 2003; Spalding et al., 2003).

The methods used to measure net photosynthesis fall into 

two general categories: physiological measurements and those 

based on growth. Each approach has its own strengths and weaknesses, which makes comparisons of NPP based on different 

methods problematic. In general, physiological measures of NPP 

are more likely than field measurements of growth to account 

for a greater fraction of the organic carbon fixed by photosynthesis. This likely explains in part the higher values of NPP reported for Macrocystis by Towle and Pearse (1973) and Jackson 

(1977) compared to those derived from measurements of growth 

(Table 1). Physiological-based measurements of NPP, however, 

are not without problems, as they often suffer from sampling 

artifacts (e.g., enclosures that alter gas and nutrient exchange), 

assumptions that are difficult to validate (e.g., estimating rates 

of carbon fixation from measurements of oxygen evolution), and 

poor replication that constrains the scale of spatial and temporal 

inference. This latter concern is particularly noteworthy given 

the high spatial heterogeneity and temporal variability that is 

characteristic of giant kelp forests. Jackson (1987) developed 

a physiological model that, in theory, could be used to predict 

Macrocystis NPP over a wide range of environmental conditions. 

Such models, however, have limited value in examining spatial 
118 • smithsonian contributions to the marine sciences

TABLE 1. Studies of net primary production in giant kelp forests. To facilitate comparisons, values of NPP were converted to kg dry 

mass m–2 y–1 using a wet/dry ratio of 10.31 and a carbon/dry ratio of 0.286, which were derived from monthly values at three sites 

averaged over 96 months (Rassweiler et al., 2008). NPP estimated in units of oxygen were converted to carbon using a photosynthetic 

quotient of 1 (following Rosenberg et al., 1995).

Duration NPP

Method Location of study (dry kg m–2 y–1) Reference

Giant kelp (Macrocystis pyrifera unless noted otherwise)

Product of blade standing crop and net carbon Monterey, CA Multiple days 8.68 Towle and 

assimilation as measured by in situ during 1 month Pearse, 1973 

incorporation of 14C by individual kelp blades 

during 3 h incubations

Difference between measured dissolved O2 San Diego, CA 1 day 12.12 Jackson, 1977 

concentration and the concentration predicted 

by temperature for mid-day in the middle of 

Pt. Loma kelp forest at 3–6 m depth

Simulation results from a model of whole plant 33°N NA 1.88 Jackson, 1987 

growth as a function of environmental (San Diego, CA) 

parameters that affect the flux of light

Standing crop of harvested plots coupled with Falkland Islands Spring & fall 2.80a Van Tussenbroek, 1993

rates of frond initiation and loss of 1 year

Product of the density of growing fronds and the Monterey, CA Monthly for 2.23 Gerard, 1976 

mean monthly increase in frond mass 21 months

Changes in standing crop based on allometric Santa Barbara, CA Monthly for 2.46b Rassweiler et al., 2008; 

measurements of fronds and plants in fixed plots 54 months; Reed et al., 2008 

combined with independent estimates of biomass data collection

loss from tagged plants and fronds is ongoing

Product of Leaf Area Index (LAI) from Macrocystis British Columbia Bimonthly for 4.33 Wheeler and

integrifolia harvested from Grappler kelp forest, 12 months Druehl, 1983 

and net photosynthetic rates measured in the 

laboratory

Giant kelp forest ecosystem

Dissolved O2

 concentrations in diurnal water Paradise Cove, CA 2 days 6.39c McFarland and 

samples collected in a kelp forest at discrete depths Prescott, 1959

Allometric measurements of changes in standing Santa Barbara, CA Monthly for 2.73d Miller et al., 2011 

crop combined with independent estimates of 17 months

biomass loss for giant kelp (O2 evolution in 

enclosed chambers for intact assemblages of 

understory algae; C13 incorporation for 

phytoplankton) 

a Average of spring and fall.

b Average of two sites (Mohawk and Arroyo Quemado).

c Average of two days.

d Average of three 12-month periods during 17 month study.
NUMBER 39 • 119

and temporal variability in NPP due to the lack of time series 

data for many of the input variables. 

The most useful studies for examining spatial and temporal 

patterns of NPP by Macrocystis and the environmental drivers 

that control them are those by Gerard (1976) and Reed et al. 

(2008), which were relatively long term (21 and 54 months, respectively). Both studies used fi eld measurements of growth to 

estimate NPP and reported remarkably similar values (2.23 and 

2.46 dry kg m–2 y–1, respectively) despite working in different 

locations and years (Table 1). These values underestimate NPP 

because they do not account for production lost as dissolved 

exudates, which can account for one- third of the production by 

Macrocystis on an annual basis (Miller et al., 2011). One of the 

most striking (though not surprising) observations reported by 

Gerard (1976) and Reed et al. (2008) was the strong correlation 

between NPP and standing biomass. 

The fi rst estimate of NPP for the entire kelp forest community was made by McFarland and Prescott (1959), who measured dissolved oxygen concentrations in diurnal water samples 

collected throughout the water column in the kelp forest at Paradise Cove in Santa Monica Bay. The short- term nature of this 

study coupled with uncertainties about currents during the measurement period cast doubt on the accuracy of these estimates 

(Jackson, 1987). The most comprehensive study of NPP by the 

entire kelp forest community was done by Miller et al. (2011), 

who simultaneously examined NPP by understory macroalgae 

(by measuring O2

 evolution from intact assemblages enclosed in 

benthic chambers), phytoplankton (using 13C- bicarbonate tracer 

incubations), and giant kelp (using the methods of Rassweiler et 

al., 2008) in areas with and without giant kelp. They found that 

the combined NPP by understory macroalgae and phytoplankton can be as high as that of giant kelp and serves to dampen 

interannual variability in kelp forest NPP caused by the loss of 

Macrocystis from wave disturbance. In the low- light environment beneath the surface canopy of giant kelp neither the architecture of the macroalgal understory nor the diversity of species 

within it appear to be important in determining the productivity of the forest understory (Miller et al., 2012). By virtue of its 

greater biomass, the productivity of the foliose component of the 

understory assemblage was three times higher than that of the 

turf component despite having a growth rate that was three times 

slower (Miller et al., 2009). 

DISTURBANCE AND PATCH DYNAMICS

All ecological communities are exposed to many types of 

perturbation varying in intensity and scales; the most common 

for kelp communities include prolonged periods of nutrient stress, 

storms, and grazing, usually by sea urchins. The greatest disruption to giant kelp forest communities typically occurs during El 

Niño, when large waves associated with severe winter storms 

combine with warm, nutrient- depressed surface waters caused 

by a deepening of the thermocline (Dayton and Tegner, 1989). 

The impacts of this combined set of conditions can be profound 

because they result in selective reduction of giant kelp in relation to understory species (Tegner et al., 1997). This is because 

the greater drag on Macrocystis makes it more prone to removal 

from large waves than smaller, lower- lying understory species 

(Dayton and Tegner, 1984). In addition, because the vast majority 

Length of longest surface frond

Number of fronds at 1m

1m 1m

Depth

Number

of fronds

at surface Subsurface fronds

Water column section

Canopy section Avg. Height

FIGURE 2. Measurements taken to estimate the mass of giant kelp fronds in the water column and surface canopy both for 

kelp plants that reach the surface and for subsurface kelp plants. See Rassweiler et al. (2008) for details.
120 • smithsonian contributions to the marine sciences

of Macrocystis’s biomass resides near the sea surface, it is much 

more vulnerable to the nutrient-depleted surface waters associated with El Niño conditions compared to understory species. 

The physiological stresses associated with El Niño are 

greater at the low-latitude limits of Macrocystis’s range, where 

nutrient limitation occurs more routinely. It is generally understood that the nutrient limitations associated with warm water 

have more severe effects than temperature (Dayton et al., 1999: 

fig. 1). For example, during the 1997–1998 El Niño nearly all 

giant kelp disappeared from the southern and central portions 

of its range in North America (i.e., Baja California, Mexico, and 

southern California), whereas only minor losses were observed 

in the northern portion of its range off central California (Edwards and Estes, 2006). Moreover, recovery from the El Niño 

generally took longer in the south, but varied substantially within 

regions due to a variety of factors including proximity to upwelling areas, competition with other algae, grazing, and propagule 

availability. Similar latitudinal patterns were observed in the 

Southern Hemisphere, where the northern limit of three species 

of brown algae shifted south toward higher latitudes following 

the El Niño event of 1982–1983 (Peters and Breeman, 1993). 

Such stresses may make kelps more susceptible to disease, and 

low-latitude kelps in northern New Zealand have succumbed to 

a disease that may have resulted from physiological stress (Cole 

and Babcock, 1996; Cole and Syms, 1999). 

Scuba diving observations, collections, and experiments have 

been central to understanding sea urchin–giant kelp interactions. 

Disturbance from sea urchin grazing occurs unpredictably in space 

and time and varies with the species of urchin, their abundance, 

and their nutritional condition. It leads to the creation of bare 

patches that range in size from several square meters to several 

square kilometers, which in some cases led to the complete loss of 

local populations of giant kelp and associated algae in southern 

California (Leighton et al., 1966; North and Pearse, 1970; Ebeling et al., 1985; Harrold and Reed, 1985; see the “Kelp Forests, 

Sea Urchins and Abalone” section in this paper). The deforestation of giant kelp forests from sea urchin grazing was ubiquitous 

in southern Chile in the early 1970s, patchy in other areas, and 

nonexistent in parts of Tierro del Fuego and Isla de los Estados in 

southern Argentina (Dayton, 1985b). 

It is difficult to generalize patchiness in kelp communities 

because the taxonomic patterns differ across regions. Nevertheless, underwater surveys have shown kelp communities are characterized by distinct canopy guilds, including floating canopies at 

or near the surface (Macrocystis pyrifera, Nereocystis luetkeana), 

stipitate canopies in which the fronds are supported off the substrata by stipes (Pterygophora californica, Eisenia arborea, Laminaria spp.), prostrate canopies in which the fronds move back and 

forth across the bottom (Laminaria farlowii, Dictyoneurum), and 

various associations of foliose, turf, and crustose algae (Figure 3). 

FIGURE 3. Sketch of a portion of the Pt. Loma kelp forest showing patches of algae with characteristic canopy guilds, including the floating canopy of giant kelp, Macrocystis pyrifera, the stipitate 

canopy of the understory kelps Pterygophora californica and Eisenia arborea, the prostrate canopy 

of the kelp Laminaria farlowii and the fucoid Cystoseira osmundacea, and patches of turf and nongeniculate (crustose) coralline algae. From Dayton et al. (1984).
number 39 • 121

Discrete monospecific patches of these different guilds can be very 

persistent and resist invasion for more than 10 years (Dayton et 

al., 1984). The dynamics of the patches relates to the postdisturbance succession. In this case, succession relates to the recruitment processes that tend to be inhibitory or neutral; usually the 

succession pathways follow relative dominance relationships that 

can be very site specific. 

Dominance patterns in giant kelp forests vary across environmental gradients, especially gradients in depth, available 

nutrients in the surface waters, and wave exposure (Dayton et 

al., 1984). However, the general processes are remarkably similar almost everywhere, such that questions have been asked and 

necessarily answered by diving observations and experiments. 

For example, dominance patterns and canopy interactions similar to those for California kelp communities have been reported 

for other types of kelp communities in Alaska (Dayton, 1975a), 

Washington State (Dayton, 1975b), Nova Scotia (Johnson and 

Mann, 1986), the northeast and northwest Atlantic (Kain, 1975; 

Witman, 1987), and Australia (Kennelly, 1989). The species defining the patches differ, but the biological and physical processes that maintain them tend to be general. Taller perennial 

canopy guilds tend to be dominant competitors for light (Reed 

and Foster, 1984; Santelices and Ojeda, 1984) but are much 

more susceptible to nutrient and wave stress (Jackson, 1977; 

Dayton and Tegner, 1984). Dominance hierarchies in the competition for light appear to be reversed in areas with low surface 

nutrients or with persistent wave stress (Dayton et al., 1984). 

During strong El Niño events, surface canopies lack sufficient 

nutrients to exert dominance; the cooler waters below the thermocline have more nutrients, thereby selecting for interactions 

among the understory species. In situations in which the surface 

waters are nutrient depleted, internal waves and other physical processes often result in nutrient infusion along the bottom 

in kelp habitats (Zimmerman and Kremer, 1984; Fram et al., 

2008). More highly wave-stressed habitats tend to be characterized by mixing and replete nutrients, but the wave stress tends to 

remove species with surface canopies such that with increasing 

wave stress, lower-level canopy guilds become dominant (Dayton, 1975a; Cowen et al., 1982; Schiel et al., 1995).

The different morphological adaptations of the canopy 

guilds appear to have been selected for different environmental 

situations in which exploitation of light is enhanced by higher 

canopies and superior stress tolerance of lower canopies. The adaptations of kelp forest algae appear to represent four distinct 

tactics: (1) ephemeral species with opportunistic life histories 

such as Desmarestia ligulata and filamentous algae in the order 

Ectocarpales; (2) surface canopy kelps such as Macrocystis and 

Nereocystis adapted to exploitative competition for light; (3) 

lower-level canopies such as stipitate kelps and foliose red algae 

adapted to lower light and/or physical stress from wave surge; 

and (4) algae such as corallines or those with chemical defenses 

that are adapted to resist grazing (Vadas, 1977). Within any particular site the relative patch dynamics are determined by biological relationships such as grazing resistance or competition, 

but the broad differences in patch dynamics among regions are 

determined by physical factors (Edwards, 2004).

RESOURCE PARTITIONING

Resource partitioning among similar, often closely related 

species is well known in the rocky intertidal where there are 

steep physical gradients related to wave exposure and tidal immersion (Stephenson and Stephenson, 1972). Different species of 

barnacles, for example, are found at different tidal heights and 

have different growth and reproductive modes reflecting differences in exposure to air, competition, and predation (Connell, 

1961; Hines, 1978). Moreover, the multitude of similar, closely 

related species found in the intertidal (e.g., snails, limpets, nudibranchs, isopods) are seen on close observation to be in specific 

microhabitats or exhibit different trophic or reproductive traits 

(Ricketts et al., 1985; Foster et al., 1988; see the “Disturbance 

and Patch Dynamics” section above). On the other hand, the subtidal habitat of kelp forests, always submerged and flushed with 

seawater, might be expected to be more homogeneous, and while 

the high diversity in kelp forests has long been known (Darwin, 

1839), that diversity might not be expected to partition into different uses of available resources. Such an expectation is quickly 

dispelled when kelp forests are entered using scuba diving. Subtidal zonation patterns reflecting different levels of surge and 

light are evident as one descends into deeper water (Limbaugh, 

1955; Aleem, 1956; McLean, 1962; Pequegnat, 1964; North, 

1971b; Foster and Schiel, 1985). Close observation reveals that 

similar species utilize different resources even within the same 

zones, illustrating as well as anywhere in the world the competitive exclusion principle and resultant resource partitioning (Hardin, 1960; Rosenzweig, 1991; McLoughlin et al., 2010). Here 

we present an example of resource partitioning among species 

of morphologically similar trochid gastropods that has been dissected out of the kelp forest in the Hopkins Marine Life Refuge 

(HMLR, now a portion of Lovers Point State Marine Reserve) in 

Monterey Bay off Pacific Grove, California. This kelp forest has 

been the site of ongoing research and teaching since 1971 (Pearse 

and Lowry, 1974; Pearse et al., this volume). 

Lowry et al. (1974) first documented habitat differentiation 

by six species of trochid snails—two of Chlorostoma and one of 

Promartynia (all formerly in the genus Tegula, commonly called 

turban snails), and three of Calliostoma (commonly called top 

snails)—on four contrasting species of kelp forest algae. They 

simply removed all the snails from different portions of the 

algae and found that while the top snails occurred mainly on 

the seasonal reproductive fronds of Cystoseira osmundacea, turban snails were found mainly on fronds of Macrocystis pyrifera. 

Moreover, the species were arranged along the length of the floating fronds, with some species being higher from the sea bottom 

than others, and the smaller individuals of all species being either 

near the sea bottom or on the two species of understory algae 

that were sampled. This preliminary study was followed-up in
122 • smithsonian contributions to the marine sciences

more detail by Riedman et al. (1981), who quantified the species 

of turban snails on both M. pyrifera and the sea bottom in both 

March and August. Most of the turban snails were on the sea 

bottom in March after the winter storms had thinned the canopy 

and knocked many snails off the kelp. However, in August Chlorostoma brunnea and Promartynia pulligo were mainly in the 

canopy of the well-developed kelp forest. Moreover, the species 

were concentrated in different portions of the kelp forest, with P. 

pulligo mainly in the outer, seaward side of the kelp forest and C. 

brunnea in the shoreward side extending into the lower intertidal, 

where it overlapped with the intertidal congener Chlorostoma 

funebralis (Figure 4). Chlorostoma montereyi was found mainly 

near or on the bottom in the middle of the kelp forest. 

In a beautiful series of observational monitoring and field 

experiments, Watanabe (1983, 1984a, 1984b) dissected out some 

of the factors responsible for this habitat partitioning among the 

turban snails. Larval recruitment appeared to be of major importance because adults showed little lateral movement and juveniles 

were found on the bottom in the same areas as the adults: C. brunnea recruits in the low intertidal/shallow subtidal on alga-covered

rocks, P. pulligo recruits in the outer portion of the kelp forest on 

shell rubble, and C. montereyi recruits in between. On the other 

hand, little evidence was found for interspecific competition for 

either food or space, with little difference seen between interspecific and intraspecific competition on growth and reproduction. 

Predation on adult snails, however, appeared to reflect the habitat partitioning, with benthic predators (e.g., sea stars, demersal 

fishes) driving poorly defended, light-bodied individuals of P. pulligo up onto the kelp and keeping heavy-shelled individuals of

C. brunnea in shallow water where surge and dense algal cover 

makes them more difficult to detect. Chlorostoma montereyi, 

with the most active escape response from predatory sea stars 

and a deep shell within which to retreat if caught, did the best on 

or near the bottom. By offering actively foraging individuals of 

the predatory sea star Pisaster giganteus (in situ on the kelp forest floor) choices of narcotized versus nonnarcotized individuals 

of P. pulligo, Harrold (1982) further demonstrated the effectiveness of the escape responses (running, twisting, tumbling) in these 

snails. On the other hand, it remained unclear what limits P. pulligo from occurring in shallow water. 

Harrold (1982) did the same experiments with Calliostoma 

ligatum, the top snail Lowry et al. (1974) found to occur mainly 

near or on the bottom. These snails display an especially lively 

escape response when they detect sea stars nearby, and upon 

contact in the field were seen to vigorously twist or even jump 

and tumble away. Moreover, they cover their shells with mucus, 

making it difficult for the sea star to grasp them, and at least in 

laboratory aquaria were seen to bite at the tube feet of pursuing 

sea stars. 

A second species of Calliostoma, C. canaliculata, was found 

by Lowry et al. (1974) to be mainly on the seasonal reproductive fronds of Cystoseira osmundacea in the summer, shifting to 

Macrocystis pyrifera in the fall after the reproductive fronds of 

C. osmundacea disintegrate. But it and the other species of snails 

also occur on the bottom, especially in the winter when the kelp is 

much reduced, where they all encounter sea star predators. Bryan 

et al. (1997) reported that not only does C. canaliculata have an 

escape response to sea stars, but if captured clamps down to the 

substrate and produces a noxious mucus that repels the sea star. 

The active compound, a cationic neurotoxin, has been isolated 

and characterized by Wolters et al. (2005). Studies by Schmitt 

(1982, 1987) on other species of closely related trochid snails in 

southern California kelp forests have revealed similar differences 

in responses to predators, with species that flee predators or are 

distasteful being found in different areas. 

Clearly, different species of kelp forest snails differ in their 

responses to predators in relation to where they mostly occur in 

kelp forests, and their responses appear to reflect natural selection in their main habitats. However, whether their antipredator 

responses as well as the differential recruitment patterns seen in 

turban snails in the HMLR led to or are a consequence of resource partitioning remains unresolved. 

FIGURE 4. Distribution of 3 species of Chlorostoma and Promartynia pulligo (both genera were within the genus Tegula) on fronds 

of Macrocystis pyrifera and on the bottom within the kelp forest of 

the Hopkins Marine Life Refuge from the upper intertidal to the 

seaward edge of the forest. At each station about 200 snails were collected from the bottom, and all snails collected at stations between 

depths 3 and 12 m were collected from single large kelp plants. From 

Riedman et al. (1981).
number 39 • 123

Physiological differences among these closely related snails 

also could reflect resource partitioning. Response to temperature, as evidenced by heat shock proteins (Tomanek and Somero, 

1999, 2002) and heart rate (Stenseng et al., 2005), for example, 

has been demonstrated to differ between the intertidal Chlorostoma funebralis and C. brunnea and C. montereyi in the adjacent 

kelp forest (Figure 4). However, little or no difference was found 

between the two species of kelp forest snails, even though they 

differ in their depth distributions. 

The example of resource partitioning in trochid snails can be 

repeated with other groups of related species. For example, Hines 

(1982) thoroughly documented resource partitioning among five 

species of spider crabs in the HMLR. These species varied in size, 

distribution, food, and mechanisms to avoid predation so that 

there was a multidimensional niche separation among them, and 

similar utilization of one resource was generally complemented 

by dissimilar utilization of another resource. This work has not 

been repeated elsewhere, nor has it been taken to greater depths 

to understand the mechanisms involved. However, Hultgren and 

Stachowicz (2008, 2009, 2010) have compared variation in color 

and extent of decoration as camouflage from predators in these 

and related crabs in northern California, extending Hines’s work 

on that aspect of their biology. 

Another suite of species that are conspicuous members of 

kelp forests in the HMLR are corals and corallimorpharians, 

and these vary in their distributions and life histories. The corals 

Balanophyllia elegans, Paracyathus stearnsii, and Astrangia lajollaensis generally occur on the tops, on the middle portions, and 

near the bases of vertical surfaces of rocks, respectively, while 

the corallimorpharian Corynactis californica occurs mainly on 

the tops and upper portions. Chadwick (1991) showed that this 

distributional pattern seen while diving reflects an interspecific 

dominance hierarchy demonstrated in the lab with C. californica

and influences the abundance and population structure of B. elegans by reducing reproductive output, increasing larval mortality, and altering recruitment patterns. Moreover, C. californica 

kills all three species of corals (Chadwick, 1987), in particular 

A. lajollaensis, which, like C. californica, grows by cloning, with 

clones of both species able to cover large areas (Fadlallah, 1982; 

Chadwick and Adams, 1991). Both A. lajollaensis and C. californica broadcast spawn eggs that produce pelagic larvae (Fadlallah, 1982; Holts and Beauchamp, 1993) whereas the other 

two coral species are solitary but differ in life span and mode 

of reproduction. Balanophyllia elegans is relatively short lived, 

broods embryos, and produces demersal, crawling larvae (Fadlallah and Pearse, 1982a; Fadlallah, 1983), while P. stearnsii is 

long lived, broadcasts eggs, and produces pelagic larvae (Fadlallah and Pearse, 1982b). These differences in reproductive modes 

not only affect patterns of recruitment (high in B. elegans, low 

in P. stearnsii), but also influence the genetic structure of the 

populations over their range on the west coast (Beauchamp and 

Powers, 1996; Hellberg, 1996). 

These three examples illustrate quite different forms of 

resource partitioning among similar taxa within a kelp forest. 

With the trochid snails and spider crabs, the issue appears to be 

mainly predators and dealing with them in different portions of 

the kelp forest with different defensive tactics, while with the 

corals and corallimorpharians direct interspecific competition is 

more important and is dealt with both spatially and temporally. 

Although these interactions are general, and can be looked at in 

all habitats, terrestrial or marine, they differ in specifics depending on the particular taxa involved. Testing and understanding 

the mechanisms of resource partitioning in kelp forests has been 

enabled by the use of scuba, allowing for both the evaluation of 

the robustness of ecological theory and the teasing apart of how 

similar species live together in this important coastal ecosystem. 

KELP FORESTS, SEA URCHINS, 

AND ABALONE

Sea urchin grazing is well known to impact algal communities (Lawrence, 1975; Harrold and Pearse, 1987), knowledge 

gained primarily through observations, quantitative sampling, 

and experiments done with scuba. In some regions, two alternate 

stable states have been reported: lush kelp forests with high species diversity, and deforested areas, which have been described 

as depauperate barrens dominated by sea urchins and crustose 

coralline algae (Leighton et al., 1966; Steneck et al., 2002). While 

this description highlights the extremes, many locations fall along 

a continuum (Graham, 2004). In California, kelp forests exist 

that exhibit a range of community compositions, with large-scale

deforestation being characteristic of less than 10% of forests described (Foster and Schiel, 1988). The composition of individual 

forests varies, in part due to changes in sea urchin feeding behavior from passive capture of drift algae to active grazing in “fronts” 

that remove giant kelp, subcanopy, and turf algae alike (Dean et 

al., 1984). Severe storms appear to be important triggers for this 

behavioral switch as they decrease the availability of drift algae 

(Ebeling et al., 1985; Harrold and Reed, 1985). 

While human fishing has dramatically reduced large predators in giant kelp forests in southern California (Dayton et al., 

1998), there are conflicting views concerning the importance 

of fishing in determining the state (forested or barren) of rocky 

reef communities in this region (Jackson et al., 2001; Foster and 

Schiel, 2010). In addition to fishing, disease and physical and 

chemical factors such as temperature, nutrients, sedimentation, 

and large waves are also known to control algae and the herbivores that graze on them (Pearse et al., 1970; Cowen et al., 1982; 

Dayton et al., 1999; Behrens and Lafferty, 2004). It is becoming 

increasingly clear that all such factors acting alone or in combination contribute to kelp deforestation and the formation of sea 

urchin barrens. 

As Polis and Strong (1996) proposed for terrestrial systems, 

the complex food webs of California kelp forests may buffer the 

community from trophic cascades that result in deforestation. Byrnes et al. (2006) argue based on kelp forest monitoring data from 

southern California that kelp abundance is related to predator 
124 • smithsonian contributions to the marine sciences

diversity, not predator density. Strong trophic cascades, however, 

have been described in Alaska where food webs are simpler (Estes 

and Palmisano, 1974). Elsewhere in the world, local environmental factors such as wave action and sedimentation appear to impact kelp forest trophic cascades (Shears et al., 2008). 

There is little evidence for kelp deforestation in northern 

California (from San Francisco north to the Oregon border). 

Canopy-producing kelps in the region are predominantly bull 

kelp, Nereocystis luetkeana, one of the fastest growing and most 

productive annual kelps in the world. This region has relatively 

high nutrients, and intense wave action that can cause sea urchin mortality (Ebeling et al., 1985) and impede feeding (Lissner, 

1983) for much of the year (Foster and Schiel, 1985). Drift algal 

abundance is highly seasonal with a peak in the fall when the 

first winter storms rip out summer’s growth, providing a brief 

pulse of drift algae (Rogers-Bennett, 1994). In addition, sea urchin recruitment in the area appears to be lower and more sporadic than in southern California (Ebert et al., 1994), suggesting 

sea urchin recruitment may not be as successful in the north. 

To examine the potential effects of fishing red sea urchins on 

kelp deforestation in northern California, one study compared 

kelps and subtidal algae inside and outside two areas closed to 

sea urchin fishing for 20 years (Figure 5). There was no evidence 

for deforestation inside the closures despite more than double the 

density of red sea urchins compared to fished areas outside. Aerial 

surveys from multiple years showed interannual variability in surface canopy cover, but no differences in surface canopies inside 

and outside the sea urchin closures. Furthermore, subtidal surveys 

inside and outside the closed areas showed no differences in canopy, subcanopy, turf, or crustose coralline algae cover (RogersBennett et al., 2011). This study suggests that areas where sea 

urchin fishing is prohibited will not become overpopulated with 

sea urchins and deforested at these spatial scales within a twentyyear time period. Behrens and Lafferty (2004) found that rocky 

reefs inside one reserve in southern California were more likely 

to support kelp compared to fished sites, and the difference was 

attributed to fishing for sea urchin predators such as lobster (Lafferty, 2004). This differs from northern California where the reserve protected sea urchins from the sea urchin fishery. 

Sea urchins directly and indirectly modulate shelter and 

food resources within kelp forests and can be regionally important ecosystem engineers (Rogers-Bennett, personal observation). 

Through their role as dominant grazers, sea urchins act to structure surrounding assemblages of algae and sessile invertebrates. 

Urchin grazing of giant kelp holdfasts can weaken structural integrity and lead to increased mortality during storms, while even 

slight damage to stipes can result in substantial losses of biomass 

even during relatively calm conditions (Tegner et al., 1995; Duggins et al., 2001). Sea urchins can also modify rocky substrates 

by forming home scars, which they maintain free of algae and 

invertebrates (Rogers-Bennett, 1994). 

The canopies of spines of individual and groups of sea urchin 

species provide important biogenic structures in kelp communities 

in many parts of the world (Tegner and Dayton, 1977; Kojima, 

1981; Mayfield and Branch, 2000; Townsend and Bologna, 2007). 

In California, red sea urchins provide refuge for both juvenile 

FIGURE 5. Divers surveying red sea urchins along a subtidal transect in northern California (left; photo by S. Fitzgerald) and red sea urchin 

spine canopy with juvenile sea urchins beneath (right; photo by L. Rogers-Bennett).
number 39 • 125

conspecifics (Figure 5; Tegner and Dayton, 1977; Rogers-Bennett

et al.,1995) and a suite of other organisms such as juvenile fishes, 

crabs, and snails (Rogers-Bennett and Pearse, 2001). Juvenile abalone have been shown to utilize sea urchin spine canopies in California (Rogers-Bennett and Pearse, 2001), Canada (Tomascik and 

Holmes, 2003) and South Africa (Mayfield and Branch, 2000). 

Animals that take shelter under the spine canopy garner protection from wave action and predators, but do not appear to benefit 

from additional food (Nishizaki and Ackerman, 2004). In the laboratory, the number of juvenile sea urchins moving toward spine 

canopy shelter increased with increasing water flow and predators 

(Nishizaki and Ackerman, 2001). Similar behavior observed in the 

presence of predators was attributed to the release of a chemical 

cue by adults that triggered juveniles to seek shelter. Adults did 

not respond to the cue presumably because they have a size refuge 

from predation (Nishizaki and Ackerman, 2005).

Much like that by sea urchins, grazing by abalone alters 

the structure of kelp forest communities by maintaining patches 

dominated by crustose coralline algae (Douros, 1985; Miner 

et al., 2007). The formation of such patches provides chemical cues critical for successful settlement and metamorphosis of 

their larvae (Morse et al., 1979). This in turn maintains coralline 

algal patches over time. Sedimentation (Onitsuka et al., 2008) 

and conditions that lead to overgrowth by fleshy algae hinder 

settlement of abalone larvae, ultimately leading to the demise 

of coralline patches. In one long-term study of intertidal black 

abalone, Haliotis cracherodii, in California, sites with few black 

abalone had recruitment failure following population devastation from a virulent disease, which led to a dramatically altered 

community structure (Miner et al., 2007). Sites without abalone 

had less crustose coralline algae and more fleshy algae and sessile 

invertebrates such as tube worms, sponges, and tunicates, which 

further hinder abalone recruitment (Miner et al., 2007). With 

this negative feedback further preventing abalone recovery, these 

changes in community structure may be long term.

As described above, interactions among kelp, sea urchins, 

and abalone can have profound effects on the structure and dynamics of giant and bull kelp forest communities. Moreover, there 

is a growing awareness of the role oceanographic processes play 

in driving kelp dynamics (Dayton and Tegner, 1984; Tegner and 

Dayton, 1987; see “Patterns and Controls of Primary Production 

in Kelp Forest Ecosystems” and “Disturbance and Patch Dynamics” sections in this paper), sea urchin recruitment (Watanabe and 

Harrold, 1991; Ebert et al., 1994), and abalone growth (Haaker et 

al., 1998) and reproduction (Vilchis et al., 2005; Rogers-Bennett

et al., 2010). All of these species are (or have been) fished for 

recreational and commercial use in California. Overfishing can 

have widespread detrimental impacts on biodiversity (Coleman 

and Williams, 2002). Consequently, a management approach for 

kelp forests based on the ecosystem rather than on individual 

component species will likely be most successful in conserving 

the diversity and ecological function of these prominent and important coastal ecosystems and their services. The establishment 

of a network of marine protected areas in California is one tool 

managers can use to implement ecosystem-based management 

(see “Scuba-Based Management” section in this paper).

Ocean warming has the potential to have major impacts 

on kelp forest communities in California (Schiel et al., 2004). 

Extensive work has shown that low nutrients associated with 

warm water conditions lead to reductions in the extent of giant 

kelp canopies (Tegner and Dayton, 1987; Edwards, 2004). Warm 

water is also associated with increases in sea urchin recruitment, 

perhaps due to increases in planktonic food for larvae or higher 

larval settlement enhanced by reductions in offshore advective 

currents (Ebert et al., 1994). When prolonged, such conditions 

lead to greater competition for food among adult sea urchins, 

reducing gonad development and subsequent larval production. 

When food is in short supply, sea urchins may switch from passively feeding on drift algae to more destructive, active grazing, 

which in turn further reduces the availability of their food resources. Not surprisingly, commercial landings of the red sea 

urchins in southern California are negatively associated with El 

Niño (Foster and Schiel, 2010) as the warm, nutrient-poor water 

coupled with large waves leads to drastic reductions in kelp and 

subsequent decreases in sea urchin gonad production, thereby 

reducing the quality of fishery gonad product. 

During periods of warm ocean conditions, abalone have 

decreased growth (Haaker et al., 1998), decreased reproduction 

(Vilchis et al., 2005), and enhanced mortality due to starvation 

or disease events (Rogers-Bennett et al., 2010). Warm water 

along with bacterial infection is needed to trigger the expression 

of the lethal disease Withering Syndrome (Moore et al., 2000). 

One species of abalone protected in California, the flat abalone, 

H. walallensis, has shifted its range north into Oregon, perhaps 

as a consequence of ocean warming, making it vulnerable to a 

small commercial fishery (Rogers-Bennett, 2007). At the same 

time, warm water events may enhance the recruitment of abalone predators such as sheephead (Cowen, 1985) and spiny lobsters in southern California, further evidence of the need for an 

ecosystem perspective. 

The collective evidence to date suggests that fishing, ocean 

warming, andnutrient reduction may act synergistically to negatively impact giant kelp forest communities (Harley and RogersBennett, 2004; Ling et al., 2009). As ocean warming increases, 

sustainable management of species within kelp forest communities will be critical and complex. A greater understanding of the 

direct and interactive effects of physical and biological processes 

that drive population dynamics of key species in California’s kelp 

forests will be needed to successfully implement ecosystem management and sustain kelp forest communities; this understanding will demand the observational and experimental research on 

kelp forest systems enabled by scuba.

SCUBA-BASED MANAGEMENT

When Aqua-Lungs arrived in California, they were almost 

immediately used to investigate concerns raised by the public, 
126 • smithsonian contributions to the marine sciences

fishers, and resource managers about human impacts on kelp 

forest ecosystems. These concerns reflected the great diversity of 

resources and services that kelp forests provide society, their economic and recreational values, and the growing intensity of uses. 

Most recently, ecosystem-based approaches to management have 

fueled appreciation for a more holistic understanding of these 

forests and assessment of the cumulative impacts of humans. 

The many contributions of science to fundamental advances in 

conservation and management of kelp forests in California and 

elsewhere would simply not have happened without scuba. 

In its present form, ecosystem-based management (EBM) 

represents a movement away from single species and toward 

comprehensive consideration of the structural and functional 

attributes of ecosystems, how these attributes contribute to 

ecosystem resiliency and the production and sustainable use of 

resources, and how ecosystems respond to both environmental 

perturbations (e.g., climate variation) and human interventions 

(e.g., fishing and pollution). Ecosystem-based management employs and evaluates new approaches and tools to best manage 

human impacts. In this section, we provide brief examples to illustrate the contribution of scuba-based research in kelp forest 

ecosystems to various aspects of EBM.

Scuba-based research has been essential as it provides quantitative descriptions of kelp forest ecosystems that are the basis 

of numeric and conceptual models of these ecosystems (e.g., Foster and Schiel, 1985; Graham et al., 2008; Byrnes et al., 2011). 

Particularly important is understanding the relationships between the abiotic and biotic components. One example of this 

approach is the design of mitigation for human-caused losses of 

forests. When the discharge of cooling waters from a power plant 

in southern California led to kelp forest losses, it was decided 

to mitigate that impact by creating a comparable forest and its 

associated recreational and commercial fisheries on a man-made 

reef placed nearby (Ambrose, 1994). To determine the most appropriate physical structure for the reef, wide-ranging regional 

surveys (Ambrose and Swarbrick, 1989) and experimental modules that varied reef size and substrate type, size, and complexity were conducted by divers to quantify how the structure of 

the kelp forest community responded to variation in these reef 

features (Reed et al., 2006). Based on the responses (California 

Coastal Commission, 2008), a large man-made rocky reef was 

constructed that, as revealed by continuing surveys, appears to 

support a kelp forest with the biotic attributes of natural forests in the region (Reed et al., 2012). In this example, surveys 

to determine species–habitat relationships were used to inform 

a mitigation program, but these relationships are also useful for 

identifying “essential fish habitat,” habitat like kelp forests that, 

if protected, helps ensure sustainable populations of temperate 

reef fishes and invertebrates. 

Some species have particularly influential functions in ecosystems, and identifying these species and their functions and 

understanding the consequences of their loss are critical requirements for EBM. Canopy-forming kelps are a clear example; 

changes in their abundance affect, directly or indirectly, the 

species composition, abundance, and diversity of other algae, invertebrates, and fishes associated with kelp forests (e.g., Reed and 

Foster, 1984; Graham, 2004). Their influence is also manifested 

at the highest trophic levels (e.g., fishes, birds, marine mammals, 

human use) by extending habitat structure and fueling phenomenally productive detritus- and grazer-based trophic pathways 

(e.g., Duggins et al., 1989; Salomon et al., 2008) that support 

the production of valuable fished species such as abalone, sea 

urchins, and, indirectly, spiny lobster. As habitat structure, kelps 

and other algae provide refuge from predation for adult and 

young fishes (reviews by Carr and Syms, 2006; Steele and Anderson, 2006), and habitat for predatory fishes to hide in, allowing a greater occupation of the water column of the reef. Early 

studies (e.g., North and Hubbs, 1968) used scuba to experimentally evaluate the effects of harvesting giant kelp canopies (for 

chemicals and food) on adult fish and giant kelp populations, 

and the results were used to inform harvest management. Recent 

studies are producing recommendations for harvest practices 

that would minimize impact on the canopy function of nursery 

for young fishes (M. W. Beck, The Nature Conservancy, personal 

communication).

Ecosystem-based management of kelp forest systems is also

concerned with understanding and predicting how they respond 

to climate variation, information that can be used to adjust 

management scenarios to accommodate that variation. Studies 

using scuba have characterized the response of kelp forests to 

climatic variation and how these responses vary geographically 

and over time for both shorter- (e.g., El Niño/La Niña) as well 

as longer-term (e.g., Pacific Decadal Oscillations [PDO]) changes 

in oceanographic conditions. For example, long-term monitoring of recruitment dynamics of kelp forest fishes using visual

surveys or larval collectors (e.g., light traps, SMURFs [Standard 

Monitoring Units for the Recruitment of Temperate Reef Fishes]), 

has been coupled with oceanographic observations and indices 

(e.g., upwelling indices) to identify conditions that drive temporal and spatial variation in the replenishment of fish populations 

(e.g., Findlay and Allen, 2002; Carr and Syms, 2006; Caselle et 

al., 2010a, 2010b). Such knowledge is critical to predictions of 

year-class strength of fisheries and longer-term changes in the productivity of fishery stocks. Large-scale, long-term surveys of kelp

forests have characterized the marked response of kelp forest ecosystems to episodic storm events, including those associated with 

El Niño and La Niña events (Dayton and Tegner, 1984; Ebeling et 

al., 1985; Dayton et al., 1992, 1999; Reed et al., 2000), and how 

the scales of response and recovery vary geographically (Edwards, 

2004). Such surveys have also identified how fish assemblages 

in kelp forests change in response to longer-term oscillations in

oceanographic conditions such as the PDO (Holbrook et al., 

1997). By explaining variation in population abundance and productivity of entire kelp forest ecosystems, fisheries managers can 

modify fishing mortality accordingly. These studies also provide 

insight into how kelp forests and associated fisheries production 

may respond to impending changes in ocean climate (Carr et al., 

2011), as do studies that have capitalized on artificially altered 
number 39 • 127

environmental conditions such as warm water discharged into 

kelp forests by coastal power plants (Schiel et al., 2004).

Key to the success of EBM and the sustainable use of kelp 

forest resources is the development of management strategies 

that facilitate ecosystem integrity, productivity, and resilience. 

One strategy of growing attraction is networks of marine protected areas (MPAs), including marine reserves, designed to protect structural and functional attributes of whole ecosystems. In 

addition to their conservation potential, ecosystems inside MPA 

networks provide reference conditions which, when compared 

with carefully selected, similar ecosystems subjected to human 

uses (Hamilton et al., 2010), can better identify the ecosystemwide consequences of those activities. For example, coupled with 

oceanographic observations, monitoring MPA networks with 

scuba can distinguish responses of ecosystems to fishing from 

responses to climatic variation (Carr et al., 2011), a problem that 

has vexed fisheries management from its inception. One common goal of MPA networks is to preserve biodiversity within 

and among ecosystems, and knowledge of the geographic variation of kelp forest community structure is critical to ensure that 

the distribution of MPAs encompasses that variation. Large-scale 

surveys of kelp forest ecosystems with scuba were used to inform the design of MPA networks developed along the coast of 

California. These surveys were critical to identifying geographic 

patterns of ecosystem structure and were used to define “bioregions” with distinct community composition (California MLPA, 

2009). Marine protected area networks were then designed to 

ensure protection of replicate areas of key habitat in each “bioregion,” thereby ensuring protection of the diversity of community 

or ecosystem types across the network. 

Scuba studies along the California coast (Figure 6) have 

played a critical role in informing the size and spacing of MPAs, 

and fisheries management in general by facilitating observational 

and telemetric studies of fish movement. Scuba greatly enhances 

the deployment and maintenance of telemetry equipment, and 

the collection, return, and supplemental observation of tagged 

fishes. The data allow scientists to determine the home range 

sizes of important fish species targeted by fishing, which are 

used as a guideline to determine the minimum size of individual 

MPAs. Likewise, quantitative relationships between species diversity and habitat area generated from surveys with scuba are 

used to determine the MPA size necessary to include substantial 

portions of the biodiversity present in a given region (California 

MLPA, 2009). 

Functioning MPA networks require population connectivity through larval dispersal of the species they protect, so 

spacing MPAs at distances within the range of larval dispersal 

enhances replenishment between adjacent MPAs and to habitats between MPAs to help replenish fished populations. Collection of recently settled fish larvae with hand nets (e.g., BINCKE 

[Benthic Ichthyo-fauna Net for Coral/Kelp Environments] nets; 

Anderson and Carr, 1998) and larval collectors (e.g., SMURFs; 

Ammann, 2004) facilitates estimates of larval durations derived 

from counting daily increment formation in otoliths (ear bones 

of fishes). These larval duration estimates have been used in conjunction with ocean circulation models to estimate dispersal distances to inform the spacing of MPAs in a network. 

Diving surveys play a critical role in monitoring MPAs and 

evaluating how effective they are in protecting kelp forest ecosystems (Figure 6), and have been used to identify population 

and ecosystem responses to MPAs in California (e.g., Hamilton 

et al., 2010) and elsewhere (e.g., Ling et al., 2009). However, it 

is all too often lost on management agencies and policy makers 

that these MPA monitoring programs produce information of far 

wider-ranging application. Comparison of changes in abundance 

of species inside and outside MPAs has allowed the discovery of 

important species interactions, functional roles of species, and 

species’ responses to fishing effects (Babcock et al., 1999; Shears 

and Babcock, 2002, 2003; Barrett et al., 2009). As such, monitoring studies for MPA evaluation simultaneously provide the 

FIGURE 6. Map of marine protected areas (MPAs) on the coast 

of central California between Monterey Bay and Point Conception. Monitoring sites surveyed to evaluate responses of kelp forest–

associated species are indicated inside (red diamonds) and outside

(green diamonds) of individual MPAs.
128 • smithsonian contributions to the marine sciences

information necessary to identify the ecosystem-wide effects of 

fishing, a fundamental objective of EBM as mentioned above. 

Moreover, recent studies have demonstrated how scuba surveys can produce more precise and comprehensive descriptions 

of fish assemblages than fishery-based sampling methods alone 

(hook and line, traps, etc.), thereby better identifying the local 

changes in fish assemblages in response to fishing (Starr et al., 

2010). Scuba surveys in and out of MPAs can also produce better estimates of the trends in fishery stocks associated with kelp 

forests than can be gleaned from fishery-dependent data alone,

which are often confounded by serial depletion (i.e., by serially 

sampling populations in previously unfished locations, no evidence of overharvesting is detected; Schroeter et al., 2001). The 

insights gained from such an approach have been clearly shown 

by Ling et al. (2009), who unraveled complex relationships between ocean warming, sea urchin dispersal and abundance, kelp 

forest dynamics, abalone abundance, and lobster fishing. This 

ecosystem-based study led to the recognition of the important 

function of large lobsters in Tasmanian kelp forest ecosystems 

altered by climate change. 

CONCLUSIONS

The use of scuba as a research tool in the USA has its holdfast in the giant kelp forests of California. The above discussions 

cover only a few of the past and present uses of scuba but clearly 

show it has been and will continue to be an indispensable tool 

for scientists, conservationists, and resource managers. In addition to scuba and the accessory research tools and techniques for 

use with it, there have been significant advances in and deployment of satellite and in situ systems that can record a variety of 

relevant oceanographic phenomena (and often require scuba diving for placement and maintenance). The implementation and integration of these ocean-observing systems, MPA networks, and 

long-term monitoring studies provides unprecedented opportunities (Carr et al., 2010). Never before have such valuable tools 

been available to explore kelp forest ecosystems. The knowledge 

gained from their exploration informs conservation efforts, ensuring that humans continue to benefit from these fascinating 

and valuable ecosystems but do not impair their integrity, biodiversity, productivity, and resilience. Moreover, scuba allows 

scientists to observe obscure biological phenomena and interactions among species in a formerly inaccessible world, reviving 

the ability for people to follow their curiosity into understanding both intricate details and a grander perspective on how our 

world functions as a whole.

ACKNOWLEDGMENTS

Mark Carr and Daniel Malone’s support was provided by 

the Partnership for Interdisciplinary Studies of Coastal Oceans 

(PISCO), which is supported by the Gordon and Betty Moore 

Foundation and the David and Lucile Packard Foundation. This 

is PISCO contribution number 380. Daniel Reed’s support was 

provided by the National Science Foundation’s Long-Term Ecological Research Program. LRB: This is a contribution of the University of California, Davis Bodega Marine Laboratory.

We dedicate this paper to the memory of Michael Neushul, 

Jr. (1933–1993). His enthusiasm for science was contagious, his 

generosity enormous, and his insights into kelp forest biology 

based on innovative research using scuba truly inspirational. 

REFERENCES

Aleem, A. A. 1956. Quantitative underwater study of benthic communities inhabiting kelp beds off California. Science, 123:183. http://dx.doi.org/10.1126

/science.123.3188.183.

Ambrose, R. F. 1994. Mitigating the effects of a coastal power plant on a kelp forest community: Rationale and requirements for an artificial reef. Bulletin of 

Marine Science, 55:694–708.

Ambrose, R. F., and S. L. Swarbrick. 1989. Comparison of fish assemblages on 

artificial and natural reefs off the coast of southern California. Bulletin of 

Marine Science, 44:718–733.

Ammann, A. J. 2004. SMURFs: Standard monitoring units for the recruitment of 

temperate reef fishes. Journal of Experimental Marine Biology and Ecology,

299:135–154. http://dx.doi.org/10.1016/j.jembe.2003.08.014.

Anderson, T. W., and M. H. Carr. 1998. BINCKE: A highly efficient net for collecting reef-associated fishes. Environmental Biology of Fishes, 51:111–115. 

http://dx.doi.org/10.1023/A:1007355408723.

Andrews, H. L. 1945. The kelp beds of the Monterey region. Ecology, 26:24–37. 

http://dx.doi.org/10.2307/1931912.

Babcock, R. C., S. Kelly, N. T. Shears, J. W. Walker, and T. J. Willis. 1999. Changes in 

community structure in temperate marine reserves. Marine Ecology Progress 

Series, 189:125–134. http://dx.doi.org/10.3354/meps189125.

Barrett, N. S., C. D. Buxton, and G. J. Edgar. 2009. Changes in invertebrate and 

macroalgal populations in Tasmanian marine reserves in the decade following 

protection. Journal of Experimental Marine Biology and Ecology, 370:104–

119. http://dx.doi.org/10.1016/j.jembe.2008.12.005.

Beauchamp, K. A., and D. A. Powers. 1996. Sequence variation of the first internal 

spacer (IT-1) of ribosomal DNA in ahermatypic corals from California. Molecular Marine Biology Biotechnology, 5:357–362.

Behrens, M. D., and K. D. Lafferty. 2004. Effects of marine reserves and urchin disease on southern Californian rocky reef communities. Marine Ecology Progress Series, 279:129–139. http://dx.doi.org/10.3354/meps279129.

Bryan, P. J., J. B. McClintock, and M. Hamann. 1997. Behavioral and chemical 

defenses of marine prosobranch gastropod Calliostoma canaliculatum in 

response to sympatric seastars. Journal of Chemical Ecology, 23:645–658. 

http://dx.doi.org/10.1023/B:JOEC.0000006401.97339.b9.

Byrnes, J. E., D. C. Reed, B. J. Cardinale, K. C. Cavanaugh, S. J. Holbrook, R. J. 

Schmitt. 2011. Climate-driven increases in storm frequency simplify kelp forest food webs. Global Change Biology, 17(8):2513–2524. http://dx.doi.org

/10.1111/j.1365-2486.2011.02409.x.

Byrnes, J. E., J. J. Stachowicz, K. M. Hultgren, A. R. Hughes, S. V. Olyarnik, and 

C. S. Thornber. 2006. Predator diversity strengthens trophic cascades in kelp 

forests by modifying herbivore behavior. Ecology Letters, 9:61–71.

California Coastal Commission. 2008. SONGS mitigation reef permit E-07-010 

adopted findings and conditions—Feb 06 2008. http://marinemitigation.msi.

ucsb.edu/documents/artificial_reef/index.html.

California MLPA Master Plan Science Advisory Team. 2009. Draft methods used 

to evaluate marine protected area proposals in the MLPA South Coast study 

region. http://www.dfg.ca.gov/mlpa/pdfs/agenda_102009b1.pdf.

Carr, M. H., and C. Syms. 2006. Recruitment. In The ecology of marine fishes: 

California and adjacent waters, ed. L. G. Allen, D. J. Pondella II, and M. H. 

Horn, pp. 411–427. Berkeley: University of California Press.

Carr, M. H., C. B. Woodson, O. M. Cheriton, D. Malone, M. A. McManus, and 

P. T. Raimondi. 2011. Knowledge through partnerships: Integrating marine 

protected area monitoring and ocean observing systems. Frontiers in Ecology

and the Environment, 9:342–350. http://dx.doi.org/10.1890/090096.
number 39 • 129

Caselle, J. E., M. H. Carr, D. P. Malone, J. R. Wilson, and D. E. Wendt. 2010b. Can 

we predict interannual and regional variation in delivery of pelagic juveniles 

to nearshore populations of rockfishes (genus Sebastes) using simple proxies 

of ocean conditions? CalCOFI Report, 51:91–205.

Caselle, J. E., B. P. Kinlan, and R. R. Warner. 2010a. Temporal and spatial scales of 

influence on nearshore fish settlement in the southern California bight. Bulletin of Marine Science, 86:355–385.

Chadwick, N. E. 1987. Interspecific aggressive behavior of the corallimorpharian 

Corynactis californica (Cnidaria: Anthozoa): Effects on sympatric corals 

and sea anemones. Biological Bulletin, 173:110–125. http://dx.doi.org/10

.2307/1541866.

———. 1991. Spatial distribution and the effects of competition on some temperate Scleractinia and Corallimorpharia. Marine Ecology Progress Series, 70: 

39–48. http://dx.doi.org/10.3354/meps070039.

Chadwick, N. E., and C. Adams. 1991. Locomotion, asexual reproduction, and killing of corals by the corallimorpharian Corynactis californica. Hydrobiologia,

216/217:263–269. http://dx.doi.org/10.1007/BF00026473.

Cole, R. G., and R. C. Babcock. 1996. Mass mortality of a dominant kelp (Laminariales) at Goat Island, north-eastern New Zealand. Marine and Freshwater 

Research, 47:907–911. http://dx.doi.org/10.1071/MF9960907.

Cole, R. G., and C. Syms. 1999. Using spatial pattern analysis to distinguish causes 

of mortality: An example from kelp in northeastern New Zealand. Journal of 

Ecology, 87:963–972. http://dx.doi.org/10.1046/j.1365-2745.1999.00418.x.

Coleman, F. C., and S. L. Williams. 2002. Overexploiting marine ecosystem engineers: Potential consequences for biodiversity. Trends in Ecology and Evolution, 17:40–44. http://dx.doi.org/10.1016/S0169-5347(01)02330-8.

Connell, J. H. 1961. The influence of interspecific competition and other factors on 

the distribution of the barnacle Chthamalus stellatus. Ecology, 42:710–723. 

http://dx.doi.org/10.2307/1933500.

Cowen, R. K. 1985. Large scale pattern of recruitment by the labrid, Semicossyphus 

pulcher: Causes and implications. Journal of Marine Research, 43:719–742. 

http://dx.doi.org/10.1357/002224085788440376.

Cowen, R. K., C. R. Agegian, and M. S. Foster. 1982. The maintenance of community structure in a central California giant kelp forest. Journal of Experimental 

Marine Biology and Ecology, 64:189–201. http://dx.doi.org/10.1016/0022

-0981(82)90152-6.

Darwin, C. 1839. The Voyage of the Beagle. New York: Harvard Classics.

Dayton, P. K. 1975a. Experimental studies of algal–canopy interactions in a sea 

otter dominated kelp community at Amchitka Island, Alaska. Fishery Bulletin, United States, 73:230–237.

———. 1975b. Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecological Monographs, 45:137–159. http://dx.doi.org

/10.2307/1942404.

———. 1985a. Ecology of kelp communities. Annual Review of Ecology and Systematics, 16:215–245. http://dx.doi.org/10.1146/annurev.es.16.110185.001243.

———. 1985b. The structure and regulation of some South American kelp communities. Ecological Monographs, 55:447–468. http://dx.doi.org/10.2307

/2937131.

Dayton, P. K., V. Currie, T. Gerrodete, B. D. Keller, R. Rosenthal, and D. Van Tresca. 

1984. Patch dynamics and stability of some California kelp communities. 

Ecological Monographs, 54:253–289. http://dx.doi.org/10.2307/1942498.

Dayton, P. K., and M. J. Tegner. 1984. Catastrophic storms, El Niño, and patch stability in a southern California kelp community. Science, 224:283–285. http://

dx.doi.org/10.1126/science.224.4646.283.

———. 1989. Bottoms beneath troubled water, benthic impacts of the 1982–1984 

El Niño in the temperate zone. In Global Ecological Consequences of the 

1982–1983 El Niño-Southern Oscillation, ed. P.W. Glynn, pp. 433–472. Elsevier Oceanography Series 52. Amsterdam: Elsevier Science.

Dayton, P. K., M. J. Tegner, P. B. Edwards, and K. L. Riser. 1998. Sliding baselines, 

ghosts and reduced expectations in kelp forest communities. Ecological Applications, 8:309–322. http://dx.doi.org/10.1890/1051-0761(1998)008[0309

:SBGARE]2.0.CO;2.

———. 1999. Temporal and spatial scales of kelp demography: The role of 

oceanographic climate. Ecological Monographs, 69:219–250. http://dx.doi

.org/10.1890/0012-9615(1999)069[0219:TASSOK]2.0.CO;2.

Dayton, P. K, M. J. Tegner, P. E. Parnell, and P. B. Edwards. 1992. Temporal and 

spatial patterns of disturbance and recovery in a kelp forest community. Ecological Monographs, 62:421–445. http://dx.doi.org/10.2307/2937118.

Dean, T. A., S. C. Schroeter, and J. D. Dixon. 1984. Effects of grazing by two species of sea urchins (Strongylocentrotus franciscanus and Lytechinus anamensis) on recruitment and survival of two species of kelp (Macrocystis pyrifera

and Pterygophora californica). Marine Biology, 78:301–313. http://dx.doi

.org/10.1007/BF00393016.

Douros, W. J. 1985. Density, growth reproduction and recruitment in an intertidal 

abalone: Effects of intraspecific competition and prehistoric predation. Master’s thesis, University of California at Santa Barbara, Santa Barbara.

Drach, P. 1949. Premières recherches en scaphandre autonome sur les formations 

de laminaires en zone littorale profonde. Comptes Rendus Sommaire des Sciences. Societe de Biogeographie, Paris, 26(227):46–49.

———. 1958. Perspectives in the study of benthic fauna of the continental shelf. In 

Perspectives in marine biology, ed. A. A. Buzzati-Traverso, pp. 33–46. Berkeley: University of California Press. 

Dugan, J. 1965. Man under the sea. New York: Collier Books.

Dugan, J. E., D. M. Hubbard, M. D. McCrary, and M. O. Pierson. 2003. The response 

of macrofauna communities and shorebirds to macrophyte wrack subsidies 

on exposed sandy beaches of southern California. Estuarine Coastal Shelf 

Science, 58S:25–40. http://dx.doi.org/10.1016/S0272-7714(03)00045-3.

Duggins, D., J. E. Eckman, C. E. Siddon, and T. Klinger. 2001. Interactive roles of 

mesograzers and current flow in survival of kelps. Marine Ecology Progress 

Series, 223:143–155. http://dx.doi.org/10.3354/meps223143.

Duggins, D. O., C. A. Simenstad, and J. A. Estes. 1989. Magnification of secondary 

kelp detritus in coastal marine ecosystems. Science, 245:170–173. http://dx

.doi.org/10.1126/science.245.4914.170.

Ebeling, A. W., D. R. Laur, and R. J. Rowley. 1985. Severe storm disturbances and 

the reversal of community structure in a southern California kelp forest. Marine Biology, 84:287–294. http://dx.doi.org/10.1007/BF00392498.

Ebert, T. A., S. C. Schroeter, J. D. Dixon, and P. Kalvass. 1994. Settlement patterns of 

red and purple sea urchins (Strongylocentrotus franciscanus and S. purpuratus) in California, USA. Marine Ecological Progress Series, 111:41–52. http://

dx.doi.org/10.3354/meps111041.

Edwards, M. S. 2004. Estimating scale-dependency in disturbance impacts: El Niños and giant kelp forests in the northeast Pacific. Oecologia, 138:436–447. 

http://dx.doi.org/10.1007/s00442-003-1452-8.

Edwards, M. S., and J. A. Estes. 2006. Catastrophe, recovery and range limitation 

in NE Pacific kelp forests: A large-scale perspective. Marine Ecology Progress 

Series, 320:79–87. http://dx.doi.org/10.3354/meps320079.

Ernst, J. 1955. Sur la vegetation sous-marine de la Mauche d’après des observations 

en scaphandre autonome. Comptes Rendus Académie des Sciences, Paris,

241:1066–1068.

Estes, J. A., and J. F. Palmisano. 1974. Sea otters: Their role in structuring nearshore 

communities. Science, 185:1058–1060. http://dx.doi.org/10.1126/science.185

.4156.1058.

Fadlallah, Y. H. 1982. Reproductive ecology of the coral Astrangia lajollaensis: 

Sexual and asexual patterns in a kelp forest habitat. Oecologia, 55:379–388. 

http://dx.doi.org/10.1007/BF00376926.

———. 1983. Population dynamics and life history of a solitary coral, Balanophyllia elegans, from central California. Oecologia, 58:200–207. http://dx.doi

.org/10.1007/BF00399217.

Fadlallah, Y. H., and J. S. Pearse. 1982a. Sexual reproduction in solitary corals: 

Overlapping oogenic and brooding cycles, and benthic planulas in Balanophyllia elegans. Marine Biology, 71:223–231. http://dx.doi.org/10.1007/BF

00397039.

———. 1982b. Sexual reproduction in solitary corals: Synchronous gametogenesis 

and broadcast spawning in Paracyathus stearnsii. Marine Biology 71:233–

239. http://dx.doi.org/10.1007/BF00397040.

Findlay, A. M., and L. G. Allen. 2002. Settlement patterns of a temperate reef fish, 

the kelp bass (Paralabrax clathratus), at Santa Catalina Island, CA. Marine

Ecology Progress Series, 238:237–248. http://dx.doi.org/10.3354/meps

238237.

Forster, G. R. 1954. Preliminary note on a survey of Stoke Point rocks with 

self-contained diving apparatus. Journal of the Marine Biological Association of theUnited Kingdom, 33:341–344. http://dx.doi.org/10.1017/S00

25315400008389.

Foster, M. S., A. P. DeVogelaere, C. Harrold, J. S. Pearse, and A. B. Thum. 1988. 

Causes of spatial and temporal patterns in rocky intertidal communities of 

central and northern California. Memoirs of the California Academy of Sciences, 9:1–45. 

Foster, M. S., and D. R. Schiel. 1985. The ecology of giant kelp forests in California: 

A community profile. Biological Report 85 (7.2). Washington, D.C.: U.S. Fish 

and Wildlife Service. 

———.1988. Kelp communities and sea otters: Keystone species or just another brick in the wall? In The community ecology of sea otters, ed. G. R. 
130 • smithsonian contributions to the marine sciences

VanBlaricom and J. A. Estes, pp. 92–115. Berlin: Springer-Verlag. http://dx

.doi.org/10.1007/978-3-642-72845-7.

———. 2010. Loss of predators and the collapse of southern California kelp forests: Alternatives, explanations and generalizations. Journal of Experimental 

Marine Biology and Ecology, 393:59–70. http://dx.doi.org/10.1016/j.jembe

.2010.07.002.

Fram, J. P., H. L. Stewart, M. Brezinski, B. Gaylord, D. C. Reed, S. L. Williams, 

and S. MacIntyre. 2008. Physical pathways and utilizations of nitrate supply 

to the giant kelp, Macrocystis pyrifera. Limnology and Oceanography, 53: 

1589–1603. http://dx.doi.org/10.4319/lo.2008.53.4.1589.

Gerard, V. A. 1976. Some aspects of material dynamics and energy flow in a kelp 

forest in Monterey Bay, California. Ph.D. diss., University of California at 

Santa Cruz, Santa Cruz.

Graham, M. H. 2004. Effects of local deforestation of the diversity and structure 

of southern California giant kelp forest food webs. Ecosystems, 7:341–357. 

http://dx.doi.org/10.1007/s10021-003-0245-6.

Graham, M. H., B. Halpern, and M. Carr. 2008. Diversity and dynamics of Californian Subtidal kelp forests. In Food webs and the dynamics of marine 

benthic ecosystems, ed. T. R. McClanahan and G. R. Branch, pp. 103–134. 

Oxford: Oxford University Press. http://dx.doi.org/10.1093/acprof:oso

/9780195319958.003.0005.

Graham, M. H., J. A. Vásquez, and A. H. Buschmann. 2007. Global ecology of 

the giant kelp Macrocystis: From ecotypes to ecosystems. Oceanography and 

Marine Biology: An Annual Review, 45:39–88.

Haaker, P. L., D. O. Parker, K. C. Barsky, and C. S. Y. Chun. 1998. Growth of red 

abalone, Haliotis rufescens (Swainson), at Johnson’s Lee, Santa Rosa Island, 

California. Journal of Shellfish Research, 17:747–753.

Hamilton, S. L., J. E. Caselle, D. Malone, and M. H. Carr. 2010. Incorporating biogeography into evaluations of the Channel Islands marine reserve network. 

Proceedings of the National Academy of Sciences, http://dx.doi.org/10.1073/

pnas.0908091107.

Hardin, G. 1960. The competitive exclusion principle. Science, 131:1292–1297. 

http://dx.doi.org/10.1126/science.131.3409.1292.

Harley, C. D. G., and L. Rogers-Bennett. 2004. The potential synergistic effects 

of climate change and fishing pressure on exploited invertebrates on rocky 

intertidal shores. CalCOFI Reports, 45:98–110.

Harrold, C. 1982. Escape responses and prey availability in a kelp forest predator–

prey system. The American Naturalist, 119:132–135. http://dx.doi.org/10

.1086/283898.

Harrold, C., K. Light, and S. Lisin. 1998. Organic enrichment of submarine-canyon 

and continental-shelf benthic communities by macroalgal drift imported from 

nearshore kelp forests. Limnology and Oceanography, 43:669–678. http://

dx.doi.org/10.4319/lo.1998.43.4.0669.

Harrold, C., and J. S. Pearse. 1987. The ecological role of echinoderms in kelp forests. Echinoderm Studies, 2:137–234.

Harrold, C., and D. C. Reed. 1985. Food availability, sea urchin grazing, and 

kelp forest community structure. Ecology, 66:1160–1169. http://dx.doi.org

/10.2307/1939168.

Hellberg, M. E. 1996. Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution, 50:1167–

1175. http://dx.doi.org/10.2307/2410657.

Hines, A. H. 1978. Reproduction in three species of intertidal barnacles from 

central California. Biological Bulletin, 154:262–281. http://dx.doi.org/10

.2307/1541126.

———. 1982. Coexistence in a kelp forest: Size, population dynamics, and resource 

partitioning in a guild of spider crabs (Brachyura, Majidae). Ecological 

Monographs, 52:179–198. http://dx.doi.org/10.2307/1942610.

Holbrook, S. J., R. J. Schmitt, and J. S. Stephens. 1997. Changes in an assemblage 

of temperate reef fishes associated with a climate shift. Ecological Applications, 7:1299–1310. http://dx.doi.org/10.1890/1051-0761(1997)007[1299

:CIAAOT]2.0.CO;2.

Holts, L. J., and K. A. Beauchamp. 1993. Sexual reproduction in the corallimorpharian sea anemone Corynactis californica in a central California 

kelp forest. Marine Biology, 116:129–136. http://dx.doi.org/10.1007/BF

00350740.

Hultgren, K. M., and J. J. Stachowicz. 2008. Alternative camouflage strategies mediate predation risk among closely related co-occurring kelp crabs. Oecologia,

155:519–528. http://dx.doi.org/10.1007/s00442-007-0926-5.

———. 2009. Evolution of decoration in majid crabs: A comparative phylogenetic 

analysis of the role of body size and alternative defensive strategies. The 

American Naturalist, 173:566–578. http://dx.doi.org/10.1086/597797.

———. 2010. Size-related habitat shifts facilitated by positive preference induction in a marine kelp crab. Behavioral Ecology, 21:329–336. http://dx.doi

.org/10.1093/beheco/arp192.

Jackson, G. A. 1977. Nutrients and production of giant kelp, Macrocystis pyrifera, 

off southern California. Limnology and Oceanography, 22:979–995. http://

dx.doi.org/10.4319/lo.1977.22.6.0979.

———. 1987. Modeling the growth and harvest yield of the giant kelp Macrocystis pyrifera. Marine Biology, 95:611–624. http://dx.doi.org/10.1007/BF

00393105.

Jackson, J. B. C., M. X. Kirby, W. H. Berger, K. A. Bjorndal, L. W. Botsford, B. J. 

Bourque, R. H. Bradbury, R. Cooke, J. Erlandson, J. A. Estes, T. P. Hughes,

S. Kidwell, C. B. Lange, H. S. Lenihan,J. M. Pandolfi, C. H. Peterson, R. S. Steneck, M. J. Tegner, and R. R. Warner. 2001. Historical overfishing and the recent 

collapse of coastal ecosystems. Science, 293:629–637. http://dx.doi.org/10

.1126/science.1059199.

Johnson, C. R., and K. H. Mann. 1986. The importance of plant defense abilities to 

the structure of subtidal seaweed communities: The kelp Laminaria longicruris de la Pylaie survives grazing by the snail Lacuna vincta (Montagu) at high 

populations densities. Journal of Experimental Marine Biology and Ecology,

97:231–267. http://dx.doi.org/10.1016/0022-0981(86)90244-3.

Kain, J. M. 1960. Direct observations on some Manx sublittoral algae. Journal 

of the Marine Biological Association of the United Kingdom, 39:609–630. 

http://dx.doi.org/10.1017/S0025315400013588.

———. 1975. Algal recolonization of some cleared subtidal areas. Journal of Ecology, 63:739–765. http://dx.doi.org/10.2307/2258599.

Kennelly, S. J. 1989. Effects of kelp canopies on understory species due to shade 

and scour. Marine Ecology Progress Series, 50:215–224. http://dx.doi.org/10

.3354/meps050215.

Kitching, J. A., T. T. Macan, and H. C. Gilson. 1934. Studies in sublittoral ecology. 

I. A submarine bully in Wembury Bay, South Devon. Journal of the Marine

Biological Association of the United Kingdom, 19:677–705. http://dx.doi.org

/10.1017/S0025315400046713.

Kojima, H. 1981. Mortality of young Japanese black abalone Haliotis discus after transplantation. Bulletin of the Japanese Society of Scientific Fisheries,

47:151–159. http://dx.doi.org/10.2331/suisan.47.151.

Lafferty, K. D. 2004. Fishing for lobsters indirectly increases epidemics in sea urchins. 

Ecological Applications, 14:1566–1573. http://dx.doi.org/10.1890/03-5088.

Lawrence, J. M. 1975. On the relationships between marine plants and sea urchins. 

Oceanography and Marine Biology: An Annual Review, 13:213–286.

Leighton, D. J., L. G. Jones, and W. J. North. 1966. Ecological relationships between 

giant kelp and sea urchins in southern California. Proceedings of the International Seaweed Symposium, 5:141–153.

Limbaugh, C. 1955. Fish life in the kelp beds and the effects of kelp harvesting. La 

Jolla, Calif.: University of California, Institute of Marine Resources.

Ling, S. D., C. R. Johnson, S. D. Frusher, and K. R. Ridgway. 2009. Overfishing 

reduces resilience of kelp beds to climate-driven catastrophic phase shift.

Proceedings of the National Academy of Sciences 106:22341–22345. http://

dx.doi.org/10.1073/pnas.0907529106.

Lissner, A. L. 1983. Relationship of water motion to the shallow water distribution 

and morphology of two species of sea urchins. Journal of Marine Research,

41:691–709. http://dx.doi.org/10.1357/002224083788520432.

Lowry, L. F., A. J. McElroy, and J. S. Pearse. 1974. The distribution of six species of 

gastropod molluscs in a California kelp forest. Biological Bulletin, 147:386–

396. http://dx.doi.org/10.2307/1540456.

Mann, K. H. 2000. Ecology of coastal waters. Maiden, Mass.: Blackwell.

Mayfield, S., and G. M. Branch. 2000. Interrelations among rock lobsters, sea urchins, and juvenile abalone: Implications for community management. Canadian Journal of Fisheries and Aquatic Sciences, 57:2175–2185. http://dx.doi

.org/10.1139/f00-198.

McFarland, W. N., and J. Prescott. 1959. Standing crop, chlorophyll content and in 

situ metabolism of a giant kelp community in southern California. Publication of the Institute of Marine Science University Texas, 6:109–132.

McLean, J. H. 1962. Sublittoral ecology of kelp beds of the open coast area near 

Carmel, California. Biological Bulletin, 122:95–114. http://dx.doi.org/10

.2307/1539325.

McLoughlin, P. D., D. W. Morris, D. Fortin, E. Vander Wal, and A. L. Contasti. 2010. 

Considering ecological dynamics in resource selection functions. Journal of Animal Ecology, 79:4–12. http://dx.doi.org/10.1111/j.1365-2656.2009.01613.x.

Miller, R. J., S. Harrer, and D. C. Reed. 2012. Addition of species abundance and 

performance predicts community primary production of macroalgae. Oecologia, 168(3):797–806.
number 39 • 131

Miller, R. J., D. C. Reed, and M. A. Brzezinski. 2009. Community structure and 

productivity of subtidal turf and foliose algal assemblages. Marine Ecology 

Progress Series, 388:1–11. http://dx.doi.org/10.3354/meps08131.

———. 2011. Partitioning of primary production among giant kelp (Macrocystis pyrifera), understory macroalgae and phytoplankton on a temperate reef. 

Limnology and Oceanography, 56:119–132. http://dx.doi.org/10.4319/lo

.2011.56.1.0119.

Miner, C. M., J. M. Alstatt, P. T. Raimondi, and T. E. Minchinton. 2007. Recruitment failure and shifts in community structure following mass mortality 

limit recovery prospects of black abalone. Marine Ecology Progress Series,

327:107–117. http://dx.doi.org/10.3354/meps327107.

Moore, J. D., T. T. Robbins, and C. S. Friedman. 2000. Withering syndrome in farmed 

red abalone Haliotis rufescens: Thermal induction and association with a gastrointestinal rickettsiales-like prokaryote. Journal of Aquatic Animal Health,

12:26–34. http://dx.doi.org/10.1577/1548-8667(2000)012<0026:WSIFRA

>2.0.CO;2.

Morse, D. E., N. Hooker, H. Duncan, and L. Jensen. 1979. Aminobutyric acid, a 

neurotransmitter, induces planktonic abalone larvae to settle and begin metamorphosis. Science, 204:407–410. http://dx.doi.org/10.1126/science.204

.4391.407.

Nishizaki, M. T., and J. D. Ackerman. 2001. Gimme shelter: Factors influencing 

juvenile sheltering in Strongylocentrotus franciscanus. In Echinoderms 2000, 

ed. M. Barker, pp. 515–520. Lisse, Netherlands: Swets and Zeitlinger.

———. 2004. Juvenile–adult associations in sea urchins Strongylocentrotus franciscanus and S. droebachiensis: Is nutrition involved? Marine Ecology Progress 

Series, 268: 93–103. http://dx.doi.org/10.3354/meps268093.

———. 2005. A secondary chemical cue facilitates juvenile–adult postsettlement 

associations in red sea urchins. Limnology and Oceanography, 50:354–362. 

http://dx.doi.org/10.4319/lo.2005.50.1.0354.

North, W. J. 1957. Experimental ecology. In Kelp investigation program: Annual 

Report, ed. W. J. North, pp.11–24. IMR Ref 57-4. La Jolla, Calif.: University 

of California Institute of Marine Resources.

———. 1964. An investigation of the effects of discharged wastes on kelp. State 

Water Quality Control Board Publication No. 26. Sacramento, Calif.: The 

Resources Agency of California, State Water Quality Control Board.

———, ed. 1971a. The biology of giant kelp beds (Macrocystis) in California. Nova 

Hedwegia, 32:1–600.

———. 1971b. Introduction and background. In The biology of giant kelp beds 

(Macrocystis) in California, ed. W. J. North, pp. 1–97. Nova Hedwegia, 32.

———. 1994. Review of Macrocystis biology. In Biology of economic algae, ed. 

I. Akatsuka, pp. 447–527. The Hague: SPB Academic Publishing.

North, W. J., and C. L. Hubbs, eds. 1968. Utilization of kelp-bed resources in southern California. Fish Bulletin No. 139. Sacramento, Calif.: The Resources 

Agency, California Department of Fish and Game.

North, W. J., and J. S. Pearse. 1970. Sea urchin population explosion in southern California coastal waters. Science, 167:209. http://dx.doi.org/10.1126

/science.167.3915.209-a.

Onitsuka, T., T. Kawamura, S. Ohashi, S. Iwanaga, T. Horii, and Y. Watanabe. 2008. 

Effects of sediments on larval settlement of abalone Haliotis diversicolor. 

Journal of Experimental Marine Biology and Ecology, 365:53–58. http://

dx.doi.org/10.1016/j.jembe.2008.07.042.

Pearse, J. S., M. E. Clark, D. L. Leighton, C. T. Mitchell, and W. J. North. 1970. 

Marine waste disposal and sea urchin ecology. In Kelp habitat improvement 

project: Annual Report 1 July, 1969–30 June, 1970, ed. W. J. North, pp. 1–93. 

Pasadena, Calif.: W. M. Keck Laboratory, California Institute of Technology.

Pearse, J. S., and L. F. Lowry, eds. 1974. An annotated species list of the benthic 

algae and invertebrates in the kelp forest community at Point Cabrillo, Pacific 

Grove, California. Technical Report 1. Santa Cruz, Calif.: Coastal Marine 

Laboratory, University of California at Santa Cruz.

Pequegnat, W. E. 1964. The epifauna of a California siltstone reef. Ecology, 

45:272–283. http://dx.doi.org/10.2307/1933840.

Peters, A. F., and A. M. Breeman. 1993. Temperature tolerances and latitudinal 

range of brown algae from temperate Pacific South America. Marine Biology, 

115:143–150. http://dx.doi.org/10.1007/BF00349396.

Polis, G. A., and D. R. Strong. 1996. Food web complexity and community dynamics. American Naturalist, 147:813–846. http://dx.doi.org/10.1086/285880.

Price, M. L. 2008. A biography of Conrad Limbaugh. Histories on SIO. UC San 

Diego. http://libraries.ucsd.edu/locations/sio/scripps-archives/history.html.

Rainey, C. 1998. Wet suit pursuit: Hugh Bradner’s development of the first wet 

suit. Histories on SIO. UC San Diego. http://libraries.ucsd.edu/locations/sio

/scripps-archives/history.html.

Rassweiler, A., K. K. Arkema, D. C. Reed, M. A. Brzezinski, and R. C. Zimmerman. 

2008. Net primary production, growth and standing crop of Macrocystis pyrifera in southern California. Ecology, 89:2068. http://dx.doi.org/10.1890/07

-1109.1.

Reed, D. C., and M. A. Brzezinski. 2009. Kelp forests. In The management of natural coastal carbon sinks, ed. D. Laffoley and G. Grimsditch, pp. 30–37. Gland,

Switzerland: International Union for Conservation of Nature.

Reed, D. C., and M. S. Foster. 1984. The effects of canopy shading on algal recruitment and growth in a giant kelp forest. Ecology, 65:937–948. http://dx.doi

.org/10.2307/1938066.

Reed, D. C., P. T. Raimondi, M. H. Carr, and L. Goldwasser. 2000. The role of dispersal and disturbance in determining spatial heterogeneity in sedentary kelpforest organisms. Ecology, 81:2011–2026. http://dx.doi.org/10.1890/0012

-9658(2000)081[2011:TRODAD]2.0.CO;2.

Reed, D. C., A. Rassweiler, and K. K. Arkema. 2008. Biomass rather than growth 

determines net primary production by giant kelp. Ecology, 89:2493–2505. 

http://dx.doi.org/10.1890/07-1106.1.

Reed, D. C., S. C. Schroeter, D. Huang, T. W. Anderson, and R. F. Ambrose. 2006. 

Quantitative assessment of different artificial reef designs in mitigating losses 

to kelp forest fishes. Bulletin of Marine Science, 78:133–150.

Reed, D. C., S. C. Schroeter, and M. Page. 2012. SONGS mitigation program: 2011 

annual report of the status of condition C – kelp reef mitigation. http://marine 

mitigation.msi.ucsb.edu/documents/artificial_reef/annual_monitoring_reports

/2011_annualreport-SONGS_kelp_reef_mitigation.pdf 

Ricketts, E. F., J. Calvin, J. W. Hedgpeth, and D. W. Phillips. 1985. Between Pacific 

tides. 5th ed. Palo Alto, Calif.: Stanford University Press. 

Riedman, M. L., A. H. Hines, and J. S. Pearse. 1981. Spatial segregation of four 

species of turban snails (Gastropoda: Tegula) in central California. Veliger,

24:97–102.

Rogers-Bennett, L. 1994. Spatial patterns in the life history characteristics of red sea 

urchins, Strongylocentrotus franciscanus: Implications for recruitment and 

the California fishery. Ph.D. diss., University of California at Davis, Davis.

———. 2007. Is climate change contributing to range reductions and localized extinctions in northern, (Haliotis kamtschatkana), and flat, (Haliotis walallensis), abalones? Bulletin of Marine Science, 81:283–296.

Rogers-Bennett, L., B. L. Allen, and D. P. Rothaus. 2011. Status and habitat associations of the threatened northern abalone: importance of kelp and coralline algae. Aquatic Conservation: Marine and Freshwater Ecosystems, 21(6): 

573–581.

Rogers-Bennett, L., W. A. Bennett, H. C. Fastenau, and C. M. Dewees. 1995. Spatial variation in red sea urchin reproduction and morphology: Implications 

for harvest refugia. Ecological Applications, 5:1171–1180. http://dx.doi.org

/10.2307/2269364.

Rogers-Bennett, L., R. F. Dondanville, J. D. Moore, and L. I. Vilchis. 2010. Response 

of red abalone reproduction to warm water, starvation and disease stressors: 

Implications of ocean warming. Journal of Shellfish Research, 29(3):599–611. 

http://dx.doi.org/10.2983/035.029.0308.

Rogers-Bennett, L., and J. S. Pearse. 2001. Indirect benefits of marine protected 

areas for juvenile abalone. Conservation Biology, 15:642–647. http://dx.doi

.org/10.1046/j.1523-1739.2001.015003642.x.

Rosenberg, G., D. S. Littler, M. M. Littler, and E. C. Oliveira. 1995. Primary production and photosynthetic quotients of seaweeds from Sao-Paulo State, Brazil. 

Botanica Marina, 38:369–377. http://dx.doi.org/10.1515/botm.1995.38.1-6

.369.

Rosenzweig, M. L. 1991. Habitat selection and population interactions: The 

search for mechanism. The American Naturalist, 137:S5–S28. http://dx.doi

.org/10.1086/285137.

Salomon, A. K., N. T. Shears, T. Langlois, and R. C. Babcock. 2008. Cascading effects of fishing can alter carbon flow through a temperate coastal ecosystem.

Ecological Applications, 18:1874–1887. http://dx.doi.org/10.1890/07

-1777.1.

Santelices, B., and F. P. Ojeda. 1984. Effects of canopy removal on the understory 

algal community structure of coastal forests of Macrocystis pyrifera from 

southern South America. Marine Ecology Progress Series, 14:165–173. http://

dx.doi.org/10.3354/meps014165.

Schiel, D. R., N. L. Andrew, and M. S. Foster. 1995. The structure of subtidal algal 

and invertebrate assemblages at the Chatham Islands, New Zealand. Marine 

Biology, 123:355–367. http://dx.doi.org/10.1007/BF00353627.

Schiel, D. R., and M. S. Foster. 1986. The structure of subtidal algal stands in temperate waters. Oceanography and Marine Biology: An Annual Review, 24: 

265–307. 
132 • smithsonian contributions to the marine sciences

Schiel, D. R., J. R. Steinbeck, and M. S. Foster. 2004. Ten years of induced ocean 

warming causes comprehensive changes in marine benthic communities. 

Ecology, 85:1833–1839. http://dx.doi.org/10.1890/03-3107.

Schmitt, R. J. 1982. Consequences of dissimilar defenses against predation in a subtidal marine community. Ecology, 63:1588–1601. http://dx.doi.org/10.2307

/1938882.

———. 1987. Indirect interactions between prey: Apparent competition, predator 

aggregation, and habitat segregation. Ecology, 68:1887–1897. http://dx.doi

.org/10.2307/1939880

Schroeter, S. C., D. C. Reed, D. J. Kushner, J. A. Estes, and D. S. Ono. 2001. The use 

of marine reserves in evaluating the dive fishery for the warty sea cucumber 

(Parastichopus parvimensis) in California, U.S.A. Canadian Journal of Fisheries and Aquatic Science, 58:1773–1781. http://dx.doi.org/10.1139/f01-127.

Shears, N. T., and R. C. Babcock. 2002. Marine reserves demonstrate top-down 

control of community structure on temperate reefs. Oecologia, 132:131–142. 

http://dx.doi.org/10.1007/s00442-002-0920-x.

———. 2003. Continuing trophic cascade effects after 25 years of no take marine 

reserve protection. Marine Ecology Progress Series, 246:1–16. http://dx.doi

.org/10.3354/meps246001.

Shears, N. T., R. C. Babcock, and A. K. Salomon. 2008. Context-dependent effects

of fishing: Variation in kelp forest trophic cascades across environmental gradients. Ecological Applications, 18:1860–1873. http://dx.doi.org/10.1890/07

-1776.1.

Spalding, H., M. S. Foster, and J. N. Heine. 2003. Composition, distribution, and 

abundance of deep water (>30 m) macroalgae in central California. Journal of 

Phycology, 39:273–284. http://dx.doi.org/10.1046/j.1529-8817.2003.02010.x.

Starr, R. M., M. H. Carr, D. Malone, A. Greenley, and S. McMillan. 2010. Complementary sampling methods to inform ecosystem-based management of nearshore fisheries. Marine and Coastal Fisheries: Dynamics, Management, and

Ecosystem Science, 2:159–179. http://dx.doi.org/10.1577/C08-056.1.

Steele, M. A., and T. W. Anderson. 2006. Predation. In The ecology of marine fishes: 

California and adjacent waters, ed. L. G. Allen, M. H. Horn, and D. J. Pondella II, pp. 428–448. Berkeley: University of California Press.

Steneck, R. S., M. H. Graham, B. J. Bourque, D. Corbett, J. M. Erlandson, J. A. 

Estes, and M. J. Tegner. 2002. Kelp forest ecosystems: Biodiversity, stability, resilience and future. Environmental Conservation, 29:436–459. http://dx

.doi.org/10.1017/S0376892902000322.

Stenseng, E., C. E. Braby, and G. N. Somero. 2005. Evolutionary and acclimationinduced variation in the thermal limits of heart function in congeneric marine 

snails (genus Tegula): Implications for vertical zonation. Biological Bulletin,

208:138–144. http://dx.doi.org/10.2307/3593122.

Stephenson, T. A., and A. Stephenson. 1972. Life between tidemarks on rocky 

shores. San Francisco: W. H. Freeman and Company.

Tegner, M. J., and P. K. Dayton. 1977. Sea urchin recruitment patterns and implications of commercial fishing. Science, 196:324–326. http://dx.doi.org/10

.1126/science.847476.

———. 1987. El Niño effects on southern California kelp forest communities. 

Advances in Ecological Research, 17:243–279. http://dx.doi.org/10.1016

/S0065-2504(08)60247-0.

Tegner, M. J., P. K. Dayton, P. B. Edwards, and K. L. Riser. 1995. Sea urchin cavitation of giant kelp (Macrocystis pyrifera C. Agardh) holdfasts and its effects 

on kelp mortality across a large California forest. Journal of Experimental 

Marine Biology and Ecology, 191:83–99. http://dx.doi.org/10.1016/0022

-0981(95)00053-T.

———. 1997. Large-scale, low-frequency oceanographic effects on kelp forest succession: A tale of two cohorts. Marine Ecology Progress Series, 146:117–134. 

http://dx.doi.org/10.3354/meps146117.

Tomanek, L., and G. N. Somero. 1999. Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) 

from different thermal habitats: Implications for limits of thermotolerance 

and biogeography. Journal of Experimental Biology, 202:2925–2936.

———. 2002. Interspecific- and acclimation-induced variation in levels of heatshock proteins 70 (HSP70) and 90 (HSP90) and heat-shock transcription 

factor-1 (HSF1) in congeneric marine snails (genus Tegula): Implications for 

regulation of HSP gene expression. Journal of Experimental Biology, 205: 

677–685. 

Tomascik, T., and H. Holmes. 2003. Distribution and abundance of Haliotis kamtschatkana in relation to habitat, competitors and predators in the Broken Group Islands, Pacific Rim National Park Reserve of Canada. Journal of 

Shellfish Research, 22:831–838.

Towle, D. W., and J. S. Pearse. 1973. Production of the giant kelp Macrocystis, estimated by the in situ incorporation of 14C in polyethylene bags. Limnology and 

Oceanography, 18:155–159. http://dx.doi.org/10.4319/lo.1973.18.1.0155.

Townsend, T., and P. Bologna. 2007. Use of Diadema antillarum spines by juvenile 

fish and mysid shrimp. Gulf and Caribbean Research, 19:55–58.

Vadas, R. L. 1977. Preferential feeding: An optimization strategy in sea urchins. 

Ecological Monographs, 47:337–371. http://dx.doi.org/10.2307/1942173.

Van Tussenbroek, B. I. 1989. Seasonal growth and composition of fronds of Macrocystis pyrifera in the Falkland Islands. Marine Biology, 100:419–430. http://

dx.doi.org/10.1007/BF00391158.

Vilchis, L. I., M. J. Tegner, J. D. Moore, C. S. Friedman, K. L. Riser, T. T. Robbins, 

and P. K. Dayton. 2005. Ocean warming effects on growth, reproduction, 

and survivorship of Southern California abalone. Ecological Applications,

15:469–480. http://dx.doi.org/10.1890/03-5326.

Watanabe, J. M. 1983. Anti-predator defenses of three kelp forest gastropods: Contrasting adaptations of closely-related prey species. Journal of Experimental 

Marine Biology and Ecology, 71:257–270. http://dx.doi.org/10.1016/0022

-0981(83)90119-3.

———. 1984a. The influence of recruitment, competition, and benthic predation 

on spatial distributions of three species of kelp forest gastropods (Trochidae: 

Tegula). Ecology, 65:920–936. http://dx.doi.org/10.2307/1938065.

———. 1984b. Food preference, food quality and diets of three herbivorous gastropods (Trochidae: Tegula) in a temperate kelp forest habitat. Oecologia,

62:47–52. http://dx.doi.org/10.1007/BF00377371.

Watanabe, J. M., and C. Harrold. 1991. Destructive grazing by sea urchins Strongylocentrotus spp. in a central California USA kelp forest: Potential roles of 

recruitment, depth, and predation. Marine Ecology Progress Series, 71:125–

141. http://dx.doi.org/10.3354/meps071125.

Wheeler, W. N., and L. D. Druehl. 1986. Seasonal growth and productivity of Macrocystis integrefolia in British Columbia, Canada. Marine Biology, 90:181–

186. http://dx.doi.org/10.1007/BF00569125.

Witman, J. D. 1987. Subtidal coexistence: Storms, grazing, mutualism, and the 

zonation of kelps and mussels. Ecological Monographs, 57:167–187. http://

dx.doi.org/10.2307/1942623.

Wolters, A. M., D. A. Jayawickrama, and J. V. Sweedler. 2005. Comparative analysis of a neurotoxin from Calliostoma canaliculatum by on-line capillary 

isotachophoresis/1

H NMR and diffusion 1H NMR. Journal of Natural Products, 68:162–167. http://dx.doi.org/10.1021/np030302p.

Zimmerman, R. C., and J. N. Kremer. 1984. Episodic nutrient supply to a kelp forest ecosystem in Southern California. Journal of Marine Research, 42:591–

604. http://dx.doi.org/10.1357/002224084788506031.
Kelpbeds As Classrooms: 

Perspectives and Lessons Learned

John S. Pearse, Mark H. Carr, Charles H. Baxter, James M. 

Watanabe, Michael S. Foster, Diana L. Steller, James A. Coyer, 

Brenda Konar, David O. Duggins, and Paul K. Dayton

ABSTRACT. Field courses using scuba allow university students to experience kelp forests and 

other shallow, subtidal ecosystems. They are unusually effective for instilling essential scientific values: an appreciation of natural history and an enhanced ability to ask meaningful questions and 

think holistically. After teaching such courses at six institutions over the past 40 years, we discovered 

common aspects in how our students developed; how the courses were taught; issues of logistics 

and safety; and the regulatory obstacles we had to overcome. We highlight the opportunities and 

the need for getting more students into observing natural history through such field courses, thereby 

enabling them to better grasp and address the looming crises of the world’s ecosystems that support 

the human population.

INTRODUCTION

Natural history—the description and study of organisms and natural objects, generally using observational approaches—has been the bedrock of science since Aristotle. Although the discipline was largely ignored during the medieval period, it was resurrected 

during the Renaissance in Europe (Rudwick, 2005; Holmes, 2008), which in turn led 

to Darwin’s biological revolution in the mid-nineteenth century. Subsequent technological and laboratory successes and experimentation in science steadily eroded the prominence of natural history and observational science in much of the twentieth century, 

even though understanding the natural history of systems has remained the cornerstone 

of ecological work (Bartholomew, 1986). Now, in the first decade of the twenty-first 

century, it is clear that an understanding of natural history is essential for understanding 

and responding to the multiple anthropogenic environmental crises that are appearing all 

around us (Dayton and Sala, 2001; Sagarin, 2008).

Instilling an appreciation of natural history and the accompanying sense of wonder 

of the natural world in the next generation of students and teachers is challenging. Science 

is not simply a collection of facts, but a search for mechanistic understanding of patterns. 

However, the development of subdisciplines in science has led to a decline in the thrill of 

observing and learning from natural objects and processes—the essential nature of science that is both tentative and creative (Bickmore et al., 2009). For ecology, these losses 

and difficulties are associated with a society that has become increasingly urbanized, with 

individuals spending less time in nature (Pergams and Zaradic, 2008). Unfortunately, in 

John S. Pearse and Mark H. Carr, Department of 

Ecology and Evolutionary Biology, Long Marine 

Laboratory, University of California, Santa Cruz, 

100 Shaffer Road, Santa Cruz, California 95060, 

USA. Charles H. Baxter and James M. Watanabe, Hopkins Marine Station, Stanford University, 120 Ocean View Blvd., Pacific Grove, California 93950, USA. Michael S. Foster and Diana L. 

Steller, Moss Landing Marine Laboratories, 8272 

Moss Landing Road, Moss Landing, California 

95039, USA. James A. Coyer, Shoals Marine 

Laboratory, 400 Little Harbor Road, Portsmouth, 

New Hampshire 03801, USA. Brenda Konar,

School of Fisheries and Ocean Science, University 

of Alaska Fairbanks, Fairbanks, Alaska 99775, 

USA. David O. Duggins, University of Washington, Friday Harbor Laboratories, Friday Harbor, Washington 98250, USA. Paul K. Dayton,

Scripps Institution of Oceanography, University 

of California, San Diego, 9500 Gilman Drive, La 

Jolla, California 92093, USA. Correspondence:

J. Pearse, pearse@biology.ucsc.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
134 • smithsonian contributions to the marine sciences

many institutions students are no longer trained in the fundamentals of natural history, which underpin a more holistic view 

of nature, so it is difficult to find people able to mentor subsequent generations of students about the natural world.

Much current teaching of biology is based on theoretical constructs of mathematical theory and model systems. The 

ability to translate these perspectives to the real world, with its 

complexity and inherent variability, let alone validate model predictions, requires embedded field experience in order to develop 

functional cognitive pattern recognition. Experience in the field, 

or natural settings and environments, effectively juxtaposes academic constructs with the realities of the natural world that we 

hope to better understand, protect, and, in some cases, restore. 

Yet from our experience, and those of our colleagues, neglecting 

field courses is not only an impediment to teaching how ecosystems function, but also imposes severe restrictions on the potential to recruit and excite young scientists. We need to develop 

the cognitive abilities in students to intuitively visualize patterns 

in nature, which in turn open new directions to explore. It is 

through many hours of observing species, community patterns, 

and their natural settings that our minds can develop the skill 

to address and understand complex interactions between species 

and their environments.

Observing nature and creating stories that can be continuously refined and clarified with subsequent observations is the 

heart of science (Grobstein, 2005). The process is intrinsic in 

children as they become cognizant of their world, but all too 

often vanishes as people age. An appreciation of natural history 

fans the flame of curiosity throughout a person’s life, benefiting 

him or herself but also society in general by providing context 

for a coherent, rational, and nature-based world view. Indeed, 

research has shown that there is a positive correlation between 

experience with nature and support for legislation on environmental issues (Zaradic et al., 2009).

A lifelong appreciation of natural history can be developed 

and promoted in students through field courses in which they 

conduct structured and meaningful observations of their world. 

Among such courses is one simply called Field Quarter, which 

has been taught for many years at the University of California, 

Santa Cruz (UCSC; Norris, 2010). Such courses, however, because they are difficult and expensive to conduct and are sometimes viewed as extraneous by other academics, appear to have 

been increasingly eliminated from college curricula. Despite such 

barriers, there are strong arguments for supporting natural history at the university level (Dayton, 2003), both in the curriculum and in the enterprises of research. 

The authors of the present paper have successfully taught 

such field-oriented, natural history–based courses in a variety of 

habitats, including subtidal temperate kelp forests. Accordingly, 

our paper summarizes our field courses in kelp forest ecology: 

how they were developed over the past 40 years, their strengths 

and problems, how they advanced our knowledge of subtidal 

(kelp forest) ecology, and what they offer to students and education. Most importantly, we explore how scuba has facilitated 

these advances and the opportunities for and ability of researchers and students to personally experience one of the most productive and species-rich ecosystems on Earth.

A BRIEF HISTORY

In his pioneering work in kelp forest ecology, Wheeler J. 

North (Foster et al., this volume) employed undergraduates from 

the California Institute of Technology to assist in his summer 

research. Although students were not part of a formal course, 

they were taught to use scuba and conducted directed underwater research in kelp forests, providing North with information that was otherwise nearly unattainable. At the same time, 

in the 1960s, faculty at Stanford University’s Hopkins Marine 

Station (HMS) developed a very successful one-quarter “Spring 

Class” that involved directed student research in the rocky intertidal, both providing students with rich field experiences and 

generating basic information of that marine habitat (Abbott et 

al., 1968).A diversity of scuba-based field courses eventually radiated along the U.S. west coast and into New England (Table 

1). Most of us were inspired by these approaches that engaged 

students in the field while generating data.

Complementary field courses at UCSC involving scuba are 

now alternately taught in other locations (e.g., Gulf of California, Moorea, Corsica). Foster likewise alternated his kelp forest ecology class in later years with a similar field course taught 

in rhodolith beds in the Gulf of California, which is also now 

taught by Steller and various Moss Landing Marine Laboratories 

(MLML) faculty (Foster et al., 2007). 

Although there are other courses at other institutions that 

introduce students to the subtidal environment using scuba, especially in tropical settings, this essay describes courses taught in 

temperate, subtidal environments by the contributing authors. By 

combining our collective experiences and perspectives gleaned 

from teaching similar courses at different institutions and with 

different sets of species, we provide an overview of the value and 

challenges of such courses for bringing natural history perspectives to students.

GENERAL COURSE STRUCTURE 

AND APPROACHES

The students in our courses are generally upper-division undergraduates (e.g., University of California Santa Cruz [UCSC], 

Hopkins Marine Station [HMS], Shoals Marine Laboratory 

[SML], Friday Harbor Laboratories [FHL], University of Alaska 

Fairbanks [UAF]) and beginning graduate students (e.g., Moss 

Landing Marine Laboratories [MLML], UCSC, and UAF). Their 

backgrounds vary, but many students, and more so in recent 

times, have had little exposure to organismal biology or doing 

any kind of science, except for those at MLML. Despite this inexperience, we encourage highly motivated students, even those 
number 39 • 135

who have little or no background in biology or even in science, to 

enroll in these courses. Even though they lack the background of 

some students, most students currently enrolling in our courses 

are highly motivated, this being almost a requirement because 

the courses tend to be physically and mentally demanding. Our 

collective experiences highlight many examples of students with 

little background in science being among the best students, 

with some of them changing fields to pursue degrees in biology/

science. 

Regardless of institutional affiliation and field locations, our 

courses are similar in that they place an initial emphasis on (1) 

familiarity with the local flora and fauna, (2) concepts of scientific 

research in general (observing, recording, generating hypotheses, 

experimenting, analyzing, and interpreting), (3) fundamental ecology and natural history, and (4) practices for safely conducting research under water. The natural history of the species in the kelp 

forest was the main objective of Pearse’s first few classes; students 

were assigned different groups of organisms to learn about and 

document in order to develop a good annotated list of the species 

in the Hopkins Marine Life Refuge (Pearse and Lowry, 1974). 

An annotated list was used for many years as a central teaching 

tool in the UCSC course, and updated web versions are now used 

by the classes at both UCSC (http://bio.classes.ucsc.edu/biol161/) 

and HMS (http://seanet.stanford.edu/). 

Similarly, the first few years of the course at SML had students conducting replicated underwater transects to gauge spatial and temporal patterns of abundance of species present, and 

that database has been used in subsequent years. At MLML, a 

collection of photos of common organisms has been assembled 

and annotated to help students get to know what they are observing under water. Moreover, a select set of original papers is 

provided to show students what has been done (e.g., Foster and 

Schiel, 1985). All of these teaching aids and references are now 

made available to students at course web sites.

The diving conducted in the summer course now taught by 

Watanabe at HMS is augmented by lectures covering organismal, 

population, and community ecology. Concepts of physiology, 

biomechanics, population regulation, competition, predation, 

and disturbance are made tangible and relevant by what the 

students see while diving. Instruction on sampling methods and 

basic statistics are integrated with data collected for a growing set of time series that document the abundance of sea stars, 

abalones, and an invasive bryozoan. These data are invaluable 

for demonstrating the year-to-year variation seen in kelp forests 

TABLE 1. Chronology of the radiation of scuba-based kelp forest courses in the United States.

Course titles Institution When offered Instructors

Special Projects; Biology for Divers; Stanford University, Hopkins 1971 to present John Pearse, Charles Baxter, Steve

Subtidal Communities; Ecology Marine Station (HMS) Webster, James Watanabe, David

and Conservation of Kelp Forest Schiel, Michael Foster 

Communities

Neritic Ecology; Kelp Forest Ecology University of California, 1972 to present John Pearse, Baldo Marinovic, 

Santa Cruz (UCSC) Giacomo Bernardi, Peter Raimondi, 

Mark Carr

Advanced Methods in Underwater University of Southern California, 1970s Robert R. Given and Andrew A. 

Research Wrigley Marine Science (no longer taught) Pilmanis

Center on Catalina Island

Subtidal Ecology California State universities, 1978 to present Michael Foster, Michael Graham, 

Moss Landing Marine Diana Steller, Scott Hamilton 

Laboratories (MLML)

Underwater Research Cornell University/University of Late 1970s Larry Harris, James Coyer, Jon Witman, 

New Hampshire, Shoals Marine to present Phil Levin, Jon Grabowski, Deb 

Laboratory (SML) Robertson, Elizabeth Siddon

Kelp Forest Ecology; Field Studies University of Alaska Fairbanks 2000 to present Brenda Konar

in Subtidal Ecology (UAF)

Research Apprenticeship Program; University of Washington, Friday 2009 to 2010 David Duggins, Kevin Britton-Simmons, 

Scientific Diving Harbor Laboratories (FHL) (Research Pema Kitaeff

 Apprenticeship

Program); 2010 

to present 

(Scientific Diving)
136 • smithsonian contributions to the marine sciences

(Figure 1). The course ends with an emphasis on conservation 

issues, which is particularly appropriate at HMS, the site of one 

of the oldest marine protected areas in the country. 

A major portion of the courses taught at UCSC, MLML, 

UAF, and FHL is devoted to directed projects involving sampling 

and experiments that are pursued by individual or small groups 

of students and culminate in both written and oral reports. Some 

students from these courses present their reports in talks and 

posters at local and national scientific meetings. At UCSC, with 

a quarter-long course, and at MLML and UAF, with semesterlong courses, students are responsible for project development: 

they find and digest original papers relevant for their proposed 

research, identify questions and goals, and design sampling and 

analysis protocols. Experiments are encouraged where appropriate and feasible. While the much shorter duration summer course 

at UAF also has projects and reports, the summer courses at SML 

and FHL preclude detailed projects. Instead, SML students individually collect preliminary results, which are then integrated 

into a formal research proposal that forms an essential component of the course. Project proposals are developed after initial 

exploratory dives, which are critical for getting students to ask 

questions based on their own field observations combined with 

guidance from relevant literature. Using exploratory dives, SML 

students compile a list of 20 questions that are of personal interest. The five best questions are presented before the entire class, 

with the resulting discussion invariably helping to formulate one 

of the questions into the student’s project proposal. The proposal 

format allows students to creatively extrapolate project design 

beyond the course’s two-week limitation. Friday Harbor Laboratories has an apprenticeship model for student project activities 

that groups a small number of undergraduate researchers with 

an active research project, and relies less on a classic lecture–lab 

format than on a mentor–apprentice structure based on a specific 

research question. 

Projects as a pedagogical tool give students first-hand exposure to actively engaging in creative science and developing 

questions through direct observations. This teaches them to develop a hypothesis and then design and carry out manipulations, 

experiments, data analyses, and further observations to test that 

hypothesis. It is important, of course, for the students to realize that answers are rarely definitive in science, especially those 

obtained during courses only 2–15 weeks in duration. In shortterm student projects, there is always some concern about data 

quality, so alert instructors and teaching assistants are essential 

for helping to provide quality control. 

Some student projects from our classes have been published 

nearly as completed in the class (e.g., Lowry and Pearse, 1973; 

Towle and Pearse, 1973; Lowry et al., 1974; Aris et al., 1982; 

Foster et al., 2007); others have led to senior theses at UCSC and 

published master’s theses at MLML and UAF (Reed and Foster, 

1984; Singer, 1985; Hoelzer, 1988; Hymanson et al., 1990; Carr, 

1991; Konar and Foster, 1992; Konar, 1993; Leonard, 1994; Edwards, 1998; Clark et al., 2004, Brewer and Konar, 2005; Chenelot and Konar, 2007; Hamilton and Konar, 2007; Daly and 

Konar, 2008, 2010). Some have contributed useful data to other 

papers (e.g., Hines and Pearse, 1982; Harrold and Pearse, 1987; 

Pearse and Hines, 1987; Watanabe and Harrold, 1991; Figure 

2). At FHL, the 2009 Subtidal Ecology Apprenticeship class generated much of the preliminary data used for a successful NSF 

proposal on the fate of kelp detritus. Other student projects in 

our courses have facilitated successful NSF Graduate Research 

Fellowships. Additionally, the SML course led to production of 

FIGURE 1. Abundance of giant kelp Macrocystis pyrifera collected 

yearly (usually in early July) by J. Watanabe’s kelp forest ecology 

summer course at Hopkins Marine Station. Populations are sampled 

at two sites in southern Monterey Bay, California: Hopkins Marine Station within a fully protected state marine reserve (36°37′N, 

121°54′W), and Otter Point within a state marine conservation 

area that allows recreational fishing and kelp harvesting (36°38′N, 

121°55′W). Data are from either 10 m2

 circular plots or 10×2 m

transects placed randomly within each site; values have all been standardized to number (No.) per 10 m2

. Sample sizes range from 20 to 

>50 for each year. Plants <1 m tall are sporelings, those >1 m tall but 

with 4 or fewer fronds are juveniles, and all other plants are considered adults (J. Watanabe, unpublished data).
number 39 • 137

The Underwater Catalog (Coyer et al., 2011), a techniques guide 

for subtidal research that is now used in many classes.

Regardless of which career path students follow after completing our classes, it is our conviction that they are enriched by 

experiencing field courses such as those mentioned here on kelp 

forest ecology, and society in general benefits by having these 

graduates dispersed throughout academics, business, politics, 

and indeed all walks of life.

THE DISTINCTIVE NATURE OF 

KELP FOREST ECOLOGY COURSES

Although similar to many other field courses that include 

a focused, independent research module, our courses in kelp 

forest and subtidal ecology feature distinctive aspects with the 

potential to make them more effective in giving students a full 

appreciation of natural history and ecological research. To begin 

with, scuba diving is a challenging and exciting endeavor for 

students. By having a course using scuba as a tool for conducting research, we have a magnet for recruiting motivated students 

yearning for something different. This is particularly true in areas 

such as Alaska, where the diving is taken to an even more challenging level, requiring drysuits and other tools for cold water. To 

students arriving from noncoastal states, the nearshore subtidal 

environment is literally another world, but even students raised 

in view of (and in some cases on and in) the oceans find the 

subtidal world to be very engaging. To both sets of students, indepth exploration of life history characteristics and/or different 

forms of organisms can present a whole new world of discovery, setting the stage for fresh perspectives. To use a contemporary example, the experience is quite similar to the effect of the 

uniqueness and beauty of Pandora in the movie Avatar, which

captured the imagination of a large and diverse audience. Discussions in our classes of the magnitude and implications of the differences between marine and terrestrial ecosystems with regards 

to evolutionary and ecological processes as well as approaches 

for conservation and management (e.g., Carr et al., 2003; Shurin 

et al., 2006) reinforce and build upon student impressions from 

their experiences in the field. For any of us, whether a beginning 

student or experienced marine researcher, focusing on a small 

copepod while we are suspended in a visually infinite body of 

water is a moving and profound experience. Peering at the world 

through the confines of a facemask while swimming close to the 

bottom brings a focus not experienced on land, where it is easy 

to be distracted in many different directions. 

There is no substitute for seeing organisms up close and personal in their habitat, rather than in drawings, photos, videos, 

or movies. Observing organisms in their habitat is three dimensional, whereas the other depictions are two dimensional. In the 

Monterey area, for example, sea urchins and abalones are tucked 

away in crevices, holding and munching on pieces of kelp, while 

broken shells litter the bottom in evidence of sea otter predation on those same urchin and abalone species. Kelp crabs and 

snails move about and graze on the kelp, and their predators, 

rock fishes and sea stars, are conspicuous on the bottom. There 

are also all of those strange, sessile, suspension feeders, some 

overgrowing others, suggesting severe competition for space. The 

total picture cannot be perceived by looking at two dimensional 

representations such as photos or videos. Only by literally being 

there and experiencing three-dimensional space can the entirety 

of the interactions be appreciated, which then leads to the creative endeavor of posing questions, hypotheses, experiments, 

and generalizations. Even statistics become palatable to students 

when framed with kelp-forest denizens and the opportunity to 

design a small study that includes collecting their own data.

Moreover, kelp forests and similar nearshore communities 

are extremely dynamic. Kelps grow rapidly, but then entire beds 

can be removed almost overnight by storms. Evidence of change 

and turnover are often conspicuous from one dive to the next. 

In addition, dramatic changes can also take place over the years, 

FIGURE 2. Densities of five species of asteroids in the Hopkins 

Marine Life Refuge, Pacific Grove, California. Densities were determined by counting all individuals within 10–21 circular plots, each 

10 m2

, located at random in a 1600 m2 study area. The data for the 

fall of 1973, 1975, and 1977 were taken by students who were in the 

kelp forest ecology class of the University of California, Santa Cruz; 

much of the other data were taken by students who followed the 

class with independent study or by assisting the researchers. From 

Pearse and Hines (1987).
138 • smithsonian contributions to the marine sciences

and time-series datasets to which each new cohort of students

contributes connect the relatively brief contact each student has 

with a longer-term temporal component of the kelp forest. For 

example, at SML the nearshore community has changed from 

lush kelp forests to sea urchin barrens to meadows of an invasive 

green alga (Codium fragile) then back to lush kelp forests and 

now (2013) to extensive beds of an invasive red alga (Heterosiphonia japonica) within the past 33 years. Invasive species are 

common in the Gulf of Maine and synergistic interactions between two invasive species, Codium fragile and the invasive bryozoan Membranipora membranacea, shaped the entire community. 

In the Monterey Bay area, we have seen the kelp forest recover 

after being almost stripped from the bottom by storms or sea 

urchin grazing. In Kachemak Bay, Alaska, canopy-forming kelps

have alternated between Nereocystis luetkeana and Eualaria fistulosa over the last 30+ years for as yet unknown reasons. Also in 

Kachemak Bay, the small gastropod Lacuna vincta can overgraze 

kelp beds, leaving the same destruction as sea urchins elsewhere. 

Consequently, kelp forest systems, regardless of the species of 

kelp or dominant grazer, are excellent for introducing students to 

the concept of resiliency, thereby broadening their appreciation 

of ecosystems beyond the more familiar experience of seasonal 

changes on land and how humans contribute to changes. 

Being completely immersed in kelp beds makes students realize that nature is everywhere, all around them, whether under 

water or on land. It is not just somewhere else, as seen in those 

spectacular videos with the never-ending string of superbly 

filmed but sanitized, digitized, razor-edited, or once-in-a-lifetime 

shots complete with background music. Students can experience 

the reality themselves in the gritty, cold, murk under water, and 

realize that nature is all around them as they rekindle their innate 

childhood curiosity. 

Finally and importantly, most underwater experiences are 

for the most part intensely private, without conversation or interactions with others, and without distractions such as iPods, 

cell phones, text messaging, or internet access (Carr, 2010). On 

the other hand, scuba requires frequent attention to the equipment that allows one to survive the experience, underscoring 

how well-trained and experienced divers can benefit most from 

these experiences. Nonetheless, the wonder and solitude ignite 

the process of thinking, of questioning, and of finding potential 

answers. Only afterward can the students share their experiences 

with others in the class. And they often do so with excitement, 

enthusiasm, and considerable reflection. 

CHALLENGES

Safety

Most of us have been involved with the development of our 

institutional diving programs, both through our own research programs and by serving on our institutions’ Diving Control Boards. 

Working with our institutions’ Diving Safety Officers and Risk 

Management Departments, our courses have developed diving 

safety prerequisites over time that now include diver certification, 

a complete medical examination, certifications in CPR/First Aid/

Emergency Oxygen Administration, standardized swim and scuba 

practical exams, and possession of appropriate equipment. We are 

fortunate in having active diving safety programs on our respective campuses that can certify the students, at least as Divers-inTraining, before they take our courses, although many students 

obtain certification from other sources. In some cases, scientific 

diving certification through the American Academy of Underwater 

Sciences (AAUS) guidelines is also necessary, although students who 

successfully complete the “Underwater Research” course at SML 

receive a letter of reciprocity and AAUS Scientific Diver status (as 

long as annual requirements are met). At Friday Harbor, students 

are required to have logged at least 20 open-water dives and, as at 

many institutions, take a short rescue diving course or refresher 

diving course during the first week of their “Subtidal Ecology” 

course. Furthermore, many programs provide mixed gas (enriched 

air nitrox) and nitrox certification with additional training. 

A key element of our teaching is to do whatever is necessary to safely get students under water so they can begin the 

process of discovery. This means that we closely watch hesitant 

(but otherwise enthusiastic) divers and many times accompany 

them on their initial dives. Our primary goals are safety and “getinto-the-water”—goals that are by no means mutually exclusive.

Diving is usually restricted to depths less than 15 m, always done in buddy pairs, and always under supervision of 

dive-experienced faculty and teaching assistants (who serve as 

the lead diver and divemaster). Diving occurs from shore (with 

a standby boat with additional tanks for emergencies), small 

boats (inflatable or hard shell), or a dive float (anchored floating 

platforms with a standby boat) (Figure 3). Dive locations are 

usually in protected areas with easy access and relatively calm 

conditions. In nearly 40 years of teaching our courses, involving 

nearly one thousand students and tens of thousands of dives, 

very few dive incidents have occurred. The rare accidents (e.g., 

decompression sickness) occurred while diving within the standard no-decompression limits and were successfully treated in 

nearby recompression chambers. Other minor incidents include 

the predictable ear (external and middle) and respiratory (upper 

and lower) infections. The experience the students gain from diving safely with a group of experienced subtidal instructors and 

teaching assistants no doubt contributes to their development 

into safe, confident, and independent underwater researchers.

Logistics

Kelp forest ecology courses are not much different from 

other field courses that demand logistical preparation beyond 

the lectures and organized laboratory sessions. Students need 

to have operable and certified diving equipment available, have 

transportation to diving field sites, and be able to clean and service their gear after diving. We generally have students take the 

course at the field site (a marine station), or they are transported 
number 39 • 139

in university vehicles or drive on their own to the field sites. 

The latter raises the specter of liability, which needs to be addressed institutionally. We expect the students to provide their 

own equipment in good working condition (usually with annual 

safety inspections), although tanks, weights, and/or air fills are 

often provided. Small boats (Boston Whalers, inflatables, skiffs) 

are used for conveying students and equipment to and from the 

dive sites, as well as for safety. At most institutions, instruction 

on small boat safety and operation are part of the course. Most 

marine laboratories now have dive lockers or equivalent infrastructure that provide students with dressing rooms, after-dive 

showers, and areas for cleaning gear and logging dives. 

Field courses at remote sites such as those offered by UCSC 

and MLML in Baja California (Figure 4), Moorea, and Corsica, 

and by UAF at the Kasitsna Bay Laboratory present additional 

logistical challenges, but these are more than compensated for 

by the total immersion and lack of distraction for one to several 

weeks of almost continuous discussion of projects and observations. Not all of these remote-site courses, of course, focus on 

kelp forest ecology, but rather on a broader context of shallow 

subtidal ecology. Such courses can introduce the students to very 

unfamiliar natural environments, opening eyes and minds to new 

organisms and ecologies for comparison with kelp forests near 

their home institutions.

Regulations for Collecting and Field Experiments

State and federal regulations governing coastal ocean 

activities and impacts have increased dramatically over the 

past 40 years, even for scientific research and education. 

FIGURE 3. Students in their “classrooms.” Top: Stanford University’s Ecology and Conservation of Kelp Forest Communities class at Hopkins 

Marine Station preparing for a surf entry at Monastery Beach, Carmel Bay (left), and returning in small boats from a dive in the kelp classroom 

behind them (right) (photos by James M. Watanabe). Bottom: Shoals Marine Laboratory’s Underwater Research class on their tethered dive 

float off Appledore Island in the Gulf of Maine (photo by Amy E. Broman).
140 • smithsonian contributions to the marine sciences

Nongovernmental groups have surged in their activity aimed at 

increasing public awareness and pushing for additional regulations for environmental protection, resulting in remarkable regional improvements of our ocean environment (e.g., Palumbi 

and Sotka, 2010). Although we welcome strong regulation of 

human activities in the ocean along our coasts, as well as on 

land, and recognize the benefits of protecting the environment 

for present and future generations, regulation can hamper and 

constrain our ability to carry out scientific studies and collections. In some cases, the regulatory demands are more than a 

mere nuisance; they seriously discourage or prevent scientific 

monitoring, collecting, and experimental manipulations to the 

extent that areas or species are effectively off limits for science. 

Restrictions on working with vertebrates (fishes) can be particularly constraining. Regulation needs to be given careful consideration in teaching field courses such as kelp forest ecology, where 

reasonable and prudent collecting and experimental manipulations are needed to adequately educate future scientists as well as 

keep a finger on the pulse of community changes in local habitats. It would be particularly good if the regulators themselves 

better understood science by taking our courses. 

Another type of regulation with potential negative impacts 

on the conduct of our field courses pertains to diver safety and 

associated liability issues. When the courses discussed in this 

essay were initiated, there were very few regulations; students 

received diver certification from a commercial dive shop and provided evidence of passing a standard medical exam. As student 

numbers increased, concerns about liability also increased, inevitably leading to more and more regulations requiring the need 

for (and expense of) dive programs and diving safety officers 

to run the programs at a home institution. In some cases, diver 

certification courses are also offered. Fortunately, the guidelines 

currently developed by AAUS strike a reasonable balance between the sometimes conflicting demands of academics and risk 

management (essential training and exams) so that students are 

not precluded from obtaining first-hand experience of diving and 

working within kelp forest ecosystems. We believe it is crucial for 

this balance to continue and that easy access for training scientific divers is imperative to making subtidal scientific discoveries. 

Our continued involvement as diving researchers and instructors 

on the Diving Control Boards of our institutional dive programs 

greatly assists in maintaining diving access for these introductory 

courses. 

It is important to realize that excessive regulation can and 

has destroyed research programs. For example, scientific diving 

is so restricted in parts of the European Union that it would be 

virtually impossible to offer any of our courses, as regulations 

regarding standby divers, training, diving medical certifications, 

FIGURE 4. Moss Landing Marine Laboratory’s Subtidal Ecology class at a remote dive site on the shore of the Gulf of California, 

Baja California, Mexico. (Photo by Michael S. Foster.)
number 39 • 141

and required equipment (among other items) combine to make 

scientific diving as a course prohibitively expensive. It is no surprise, therefore, that although pioneered in Europe (e.g., Kitching, 1941), the amount of shallow subtidal scientific research 

now conducted in Europe pales in comparison to what is done in 

the US. While we all recognize the need for diving regulations, we 

stress that they need to be reasonable, as reflected in the current 

level of AAUS regulations and program certifications. 

FUTURE CHALLENGES 

AND RECOMMENDATIONS

There are continual challenges to both justify and offer field 

courses such as ours in kelp forest ecology. At the same time, 

the need to develop an awareness and appreciation of natural 

history in the next generation of students is greater than ever. As 

our human population grows and is matched in the levels of consumption and exploitation of our environmental resources, more 

and more of the Earth systems that support us will deteriorate, 

even the vast and seemingly indestructible oceans (Jackson et al., 

2001; Worm et al., 2006; Danson, 2011). 

The need for more strategic regulation in the use and harvesting of marine resources based on ecosystem-based management (EBM) is becoming increasingly evident (Ruckelshaus et 

al., 2008; McLeod and Leslie, 2009; Foster et al., this volume). 

Major components of EBM are marine protected areas (MPAs), 

which can be monitored to evaluate the effectiveness of regulating human activities. Such monitoring, and the interpretation of 

the information collected, demands well-trained personnel. Not 

only will kelp forest ecology courses help provide such people, 

but the courses themselves can assist with required monitoring within and outside MPAs. Friday Harbor Laboratories and 

Hopkins Marine Station, for example, are located within MPAs 

where no fishing or take of marine life is allowed except for scientific research. The MPA at HMS is bounded on both sides by 

state marine conservation areas that allow recreational fishing 

and the harvesting of kelp biomass to feed cultured abalones. 

Students taking kelp forest ecology classes taught at HMS by 

UCSC and HMS faculty can monitor fish and kelp populations 

both inside and outside of the state marine reserve to evaluate 

the impact of recreational fishing and kelp harvesting (see Figure 

1), a win–win scenario for the courses and the regulatory agencies. In addition, UAF’s “Subtidal Ecology” course collects data 

that are loaded into the Ocean Biogeographic Information System (OBIS; http://www.iobis.org/) database, which is publically 

accessible and allows any user to search distribution of marine 

species from all of the world’s oceans.

The oceans increasingly are considered the last places on 

this planet with the ample resources needed to support our growing human population. These resources are not just seafood, but 

also minerals, energy, and even potable water. Students in field 

courses such as the kelp forest ecology courses noted here should 

become better-informed citizens, regardless of whether they 

pursue a career in science. Accordingly, they will form a pool 

of educated citizens to serve not only as scientists working in 

laboratories around the world, but also as policy makers, business leaders, and voters who become involved in issues related to 

our interactions with the natural world. With a better appreciation of all that natural history teaches about complex ecosystems 

(obtained by participation in field courses), they just might find a 

way to attain a more balanced approach to human ecology and 

a steady-state, sustainable future.

CONCLUSIONS

Kelp forest and subtidal ecology courses in which students 

use scuba and are literally immersed in an ecosystem have been 

offered successfully and continuously for over 40 years. Students 

emerge with an appreciation of natural history, the mother lode 

of science as a way of knowing about the world. There is a strong 

rationale for teaching university-level field courses: students with 

such a broadened world view are far better equipped with the 

critical skills they need, now and in the future, to deal with the 

multiple crises faced by human populations and the ecosystems 

that support them.

ACKNOWLEDGMENTS

We thank Michael A. Lang, Roberta L. Marinelli, Susan J. 

Roberts, and Phillip R. Taylor for welcoming this manuscript into 

“The Revolution of Science through Scuba” symposium proceedings volume. We are indebted to our colleagues and the administrators of our institutions for supporting our subtidal ecology 

classes through the years. Most of all, we are pleased with the 

enthusiastic participation of hundreds—indeed thousands—of 

students who have made teaching our courses so rewarding.

We dedicate this paper to Wheeler J. North, who welcomed 

undergraduates into his pioneering research program in kelp forest ecology early on, and who was a mentor and model of a gracious human being to all who knew him.

REFERENCES

Abbott, D. P., D. Epel, J. H. Phillips, I. A. Abbott, and R. Stohler, eds. 1968. The 

biology of Acmaea. Veliger, 11(Suppl.): 1–112. 

Aris, J. P., A. D. Eisemann, and L. Moulton. 1982. The occurrence of Pugettia richii

(Crustacea: Decapoda) on Cystoseira osmundacea follows a diel pattern. Bulletin of Marine Science, 32:243–249.

Bartholomew, G. A. 1986. The role of natural history in contemporary biology. 

BioScience, 36:324–329. http://dx.doi.org/10.2307/1310237.

Bickmore, B. R., K. R. Thompson, D. A. Grandy, and T. Tomlin. 2009. Science as 

storytelling for teaching the nature of science and the science–religion interface. Journal of Geoscience Education, 57:178–190. http://dx.doi.org/10

.5408/1.3544263.

Brewer, R., and B. Konar. 2005. Chemosensory responses and foraging behavior of 

the seastar Pycnopodia helianthoides. Marine Biology, 147:789–795. http://

dx.doi.org/10.1007/s00227-005-1608-7.
142 • smithsonian contributions to the marine sciences

Carr, M. H. 1991. Habitat selection and recruitment of an assemblage of temperate zone reef fishes. Journal of Experimental Marine Biology and Ecology,

146:113–137. http://dx.doi.org/10.1016/0022-0981(91)90257-W.

Carr, M. H., J. E. Neigel, J. A. Estes, S. J. Andelman, R. R. Warner, and J. L. Largier. 

2003. Comparing marine and terrestrial ecosystems: Implications for the design of coastal marine reserves. Ecological Applications, 13:S90–S107. http://

dx.doi.org/10.1890/1051-0761(2003)013[0090:CMATEI]2.0.CO;2.

Carr, N. 2010. The shallows: What the Internet is doing to our brains. New York: 

W. W. Norton & Company. 

Chenelot, H., and B. Konar. 2007. Lacuna vincta herbivory on juvenile and adult 

Nereocystis luetkeana. Hydrobiologia, 583:107–118. http://dx.doi.org/10

.1007/s10750-006-0484-6.

Clark, R. P., M. S. Edwards, and M. S. Foster. 2004. Effects of shade from multiple 

kelp canopies on an understory algal assemblage. Marine Ecology Progress 

Series, 267:107–119. http://dx.doi.org/10.3354/meps267107.

Coyer, J., D. Steller, and J. Witman. 2011. The underwater catalog: A guide to methods in underwater research. 3rd ed. Ithaca, N.Y.: Shoals Marine Laboratory.

Daly, B., and B. Konar. 2008. Effects of macroalgal structural complexity on nearshore larval and post-larval crab composition. Marine Biology, 153: 1055–

1064.

———. 2010. Temporal trends in nearshore juvenile and adult crab populations in 

different habitats. Crustaceana, 83:659–669.

Danson, T. 2011. Oceana: Our endangered oceans and what we can do to save 

them. New York: Rodale. 

Dayton, P. K. 2003. The importance of the natural sciences to conservation. The 

American Naturalist, 162:1–13. http://dx.doi.org/10.1086/376572.

Dayton, P. K., and E. Sala. 2001. Natural history: The sense of wonder, creativity 

and progress in ecology. Scientia Marina, 65(Suppl. 2):199–206. 

Edwards, M. S. 1998. Effects of long-term kelp canopy exclusion on the abundance 

of the annual alga Desmarestia ligulata (Light F). Journal of Experimental Marine Biology and Ecology, 228:309–326. http://dx.doi.org/10.1016

/S0022-0981(98)00046-X.

Foster, M. S., L. M. McConnico, L. Lundsten, T. Wadsworth, T. Kimball, L. B. 

Brooks, M. Medina-Lopez, R. Riosmena-Rodríguez, G. Hernandez-Carmona,

R. Vasquez-Elisando, S. Johnson, and D. L. Steller. 2007. The diversity and 

natural history of a Lithothamnion muelleri–Sargassum horridum community in the Gulf of California. Ciencias Marinas, 33:367–384.

Foster, M. S., D. C. Reed, P. K. Dayton, M. H. Carr, D. P. Malone, J. S. Pearse, and 

L. Rogers-Bennett. 2012. Kelp forests in California. In Research and Discoveries: The Revolution of Science through Scuba, ed. M. A. Lang, R. L. Marinelli, S. J. Roberts, and P. R. Taylor, pp. 115–132. Smithsonian Contributions 

to the Marine Sciences, No. 39, Washington, D.C.: Smithsonian Institution 

Scholarly Press.

Foster, M. S., and D. R. Schiel. 1985. The ecology of giant kelp forests in California: 

A community profile. Biological Report 85 (7.2). Washington, D. C.: U.S. Fish 

and Wildlife Service.

Grobstein, P. 2005. Revisiting science in culture: Science as story telling and story 

revising. Journal of Research Practice, 1(1): Article M1.

Hamilton, J., and B. Konar. 2007. The influence of kelp variability and substrate 

complexity on northern nearshore fish abundance. Fishery Bulletin, 105:189–

196.

Harrold, C., and J. S. Pearse. 1987. The ecological role of echinoderms in kelp 

forests. In Echinoderm Studies 2, ed. M. Jangoux and J. M. Lawrence, pp.

137–233. Rotterdam: A. A. Balkema.

Hines, A. H., and J. S. Pearse. 1982. Abalones, shells, and sea otters: Dynamics of 

prey population in central California. Ecology, 63:1547–1560. http://dx.doi

.org/10.2307/1938879.

Hoelzer, G. A. 1988. Juvenile movement patterns in a territorial scorpaenid fish 

before and during settlement. Marine Ecology Progress Series, 45:193–195. 

http://dx.doi.org/10.3354/meps045193.

Holmes, R. 2008. The age of wonder. New York: Vintage Books.

Hymanson, Z. P., D. C. Reed, M. S. Foster, and J. W. Carter. 1990. The validity of 

using morphological characteristics as predictors of age in the kelp Pterygophora californica Laminariales Phaeophyta. Marine Ecology Progress Series, 59:295–304. http://dx.doi.org/10.3354/meps059295.

Jackson, J. B. C., M. X. Kirby, W. H. Berger, K. A. Bjorndal, L. W. Botsford, B. J. 

Bourque, R. H. Bradbury, R. Cooke, J. Erlandson, J. A. Estes, T. P. Hughes, 

S. Kidwell, C. B. Lange, H. S. Lenihan, J. M. Pandolfi, C. H. Peterson, R. S. 

Steneck, M. J. Tegner, and R. R. Warner. 2001. Historical overfishing and the 

recent collapse of coastal ecosystems. Science, 293:629–637. http://dx.doi.org

/10.1126/science.1059199.

Kitching, J. A. 1941. Studies in sublittoral ecology. III. Laminaria forest of the west 

coast of Scotland; a study of zonation in relation to wave action and illumination. Biological Bulletin, 80:324–337. http://dx.doi.org/10.2307/1537719.

Konar, B. 1993. Demography and morphology of the geniculate coralline, Bossiella 

californica ssp. schmittii (Corallinales, Rhodophyta) in a central California kelp 

forest. Phycologia, 32:284–291. http://dx.doi.org/10.2216/i0031-8884-32-4

-284.1.

Konar, B., and M. S. Foster. 1992. Distribution and recruitment of subtidal geniculate coralline algae. Journal of Phycology, 28:273–280. http://dx.doi.org

/10.1111/j.0022-3646.1992.00273.x.

Leonard, G. H. 1994. Effect of the bat star Asterina miniata (Brandt) on recruitment of the giant kelp Macrocystis pyrifera C. Agardh. Journal of Experimental Marine Biology and Ecology, 179:81–98. http://dx.doi.org/10.1016/0022

-0981(94)90018-3.

Lowry, L. F., A. J. McElroy, and J. S. Pearse. 1974. The distribution of six species of 

gastropod molluscs in a California kelp forest. Biological Bulletin, 147:386–

396. http://dx.doi.org/10.2307/1540456.

Lowry, L. F., and J. S. Pearse. 1973. Abalones and sea urchins in an area inhabited by sea otters. Marine Biology, 23:213–219. http://dx.doi.org/10.1007/BF

00389487.

Macleod, K. L., and H. M. Leslie, eds. 2009. Ecosystem-based management for the 

oceans. Washington, D.C.: Island Press. 

Norris, K. S. 2010. Mountain time. Oakland: University of California Natural Reserve System.

Palumbi, S. R., and C. Sotka. 2010. The death and life of Monterey Bay: A story of 

revival. Washington, D.C.: Island Press. 

Pearse, J. S., and A. H. Hines. 1987. Long-term population dynamics of sea urchins 

in a central California kelp forest: Rare recruitment and rapid decline. Marine Ecology Progress Series, 39:275–283. http://dx.doi.org/10.3354/meps

039275.

Pearse, J. S., and L. F. Lowry, eds. 1974. An annotated species list of the benthic 

algae and invertebrates in the kelp forest community at Point Cabrillo, Pacific 

Grove, California. Technical Report Number 1. Santa Cruz, Calif.: Coastal 

Marine Laboratory, University of California, Santa Cruz. 

Pergams, O. R. W., and P. A. Zaradic. 2008. Evidence for a fundamental and pervasive shift away from nature-based recreation. Proceedings of the National 

Academy of Sciences, 105:2295–2300. 

Reed, D. C., and M. S. Foster. 1984. The effects of canopy shading on algal recruitment and growth in a giant kelp forest. Ecology, 65:937–948. http://dx.doi

.org/10.2307/1938066.

Ruckelshaus, M., T. Klinger, N. Knowlton, and D. P. DeMaster. 2008. Marine 

ecosystem-based management in practice: Scientific and governance challenges. BioScience, 58:53–63. http://dx.doi.org/10.1641/B580110.

Rudwick, M. J. S. 2005. Bursting the limits of time. Chicago: The University of 

Chicago Press.

Sagarin, R. D. 2008. Return to natural history. Science, 320:180. http://dx.doi.org

/10.1126/science.1155994.

Shurin, J. B., D. S. Gruner, and H. Hillebrand. 2006. All wet or dried up? Real differences between aquatic and terrestrial food webs. Proceedings of the Royal 

Society, 273:1–9. http://dx.doi.org/10.1098/rspb.2005.3377.

Singer, M. M. 1985. Food habits of juvenile rockfishes (Sebastes) in a central California kelp forest. Fishery Bulletin, 83:531–541. 

Towle, D. W., and J. S. Pearse. 1973. Production of the giant kelp Macrocystis, estimated by the in situ incorporation of 14C in polyethylene bags. Limnology and 

Oceanography, 18:155–159. http://dx.doi.org/10.4319/lo.1973.18.1.0155.

Watanabe, J. M., and C. Harrold. 1991. Destructive grazing by sea urchins Strongylocentrotus spp. in a central California kelp forest: Potential roles of recruitment, depth, and predation. Marine Ecology Progress Series, 71:125–141. 

http://dx.doi.org/10.3354/meps071125.

Worm, B., E. B. Barbier, N. Beaumont, J. E. Duffy, C. Folke, B. S. Halpern, J. B. 

C. Jackson, H. K. Lotze, F. Micheli, S. R. Palumbi, E. Sala, K. A. Selkoe, J. J. 

Stachowicz, and R. Watson. 2006. Impacts of biodiversity loss on ocean 

ecosystem services. Science, 314:787–790. http://dx.doi.org/10.1126/science

.1132294.

Zaradic, P. A., O. R. W. Pergams, and P. Kareiva. 2009. The impact of nature experience on willingness to support conservation. PLoS ONE, 4(10):e7367. http://

dx.doi.org/10.1371/journal.pone.0007367.
Rhodoliths and Rhodolith Beds

Michael S. Foster, Gilberto M. Amado Filho, Nicholas A. Kamenos, 

Rafael Riosmena-Rodríguez, and Diana L. Steller

ABSTRACT. Rhodolith (maërl) beds, communities dominated by free living coralline algae, are 

a common feature of subtidal environments worldwide. Well preserved as fossils, they have long 

been recognized as important carbonate producers and paleoenvironmental indicators. Coralline 

algae produce growth bands with a morphology and chemistry that record environmental variation. Rhodoliths are hard but often fragile, and growth rates are only on the order of mm/yr. The 

hard, complex structure of living beds provides habitats for numerous associated species not found 

on otherwise entirely sedimentary bottoms. Beds are degraded locally by dredging and other anthropogenic disturbances, and recovery is slow. They will likely suffer severe impacts worldwide 

from the increasing acidity of the ocean. Investigations of rhodolith beds with scuba have enabled 

precise stratified sampling that has shown the importance of individual rhodoliths as hot spots of 

diversity. Observations, collections, and experiments by divers have revolutionized taxonomic studies by allowing comprehensive, detailed collection and by showing the large effects of the environment on rhodolith morphology. Facilitated by in situ collection and calibrations, corallines are now 

contributing to paleoclimatic reconstructions over a broad range of temporal and spatial scales. 

Beds are particularly abundant in the mesophotic zone of the Brazilian shelf where technical diving 

has revealed new associations and species. This paper reviews selected past and present research on 

rhodoliths and rhodolith beds that has been greatly facilitated by the use of scuba. 

INTRODUCTION

Relative to other abundant nearshore communities like kelp forests and coral reefs, 

rhodolith or maërl beds have been little investigated by marine ecologists. Even in clear, 

shallow water, their lack of vertical structure in the water column makes them difficult 

to distinguish from entirely soft bottoms. Observed and sampled from the bottom with 

scuba, however, these purple and pink fields are complex communities formed by aggregations of unattached, nongeniculate (lacking uncalcified joints) coralline algae with 

individual thalli ranging in size on the order of one to tens of cm and in shape from highly 

branched twigs and fans to spheres. Live individuals may be stacked a few cm deep, 

often grading below into dead fragments mixed with carbonate and terrigenous sediment 

(Figure 1). They provide hard habitat for numerous other marine algae that live on their 

surfaces, and for invertebrates living on and in the rhodoliths and surrounding sediments 

(see the “Rhodolith Systems: Communities and Conservation” section in this paper). 

There are few descriptive or experimental data to characterize the environmental 

conditions that lead to rhodolith bed formation and persistence. It does appear that beds 

are generally found on fairly level bottoms where light is sufficient for growth and water 

motion and bioturbation are sufficient to prevent burial and anoxia from sedimentation and to move the rhodoliths. High water motion, however, can inhibit bed formation by transporting individuals out of otherwise suitable habitat or causing mechanical 

Michael S. Foster, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, California 95039, USA. Gilberto M.

Amado Filho, Instituto de Pesquisas, Jardim 

Botânico do Rio Janeiro, Rua Pacheco Leão 

915, 22460-30, Rio de Janeiro, Brazil. Nicholas A. Kamenos, School of Geographical and 

Earth Sciences, Gregory Building, University of 

Glasgow, Glasgow, G12 8QQ, Scotland. Rafael 

Riosmena-Rodríguez, Programa de Investigacíon 

en Botaníca Marina, Departamento de Biologia 

Marina, Universidad Autónoma de Baja California Sur, Apartado postal 19-B, La Paz, B.C.S. 

23080, Mexico. Diana L. Steller, Moss Landing 

Marine Laboratories, 8272 Moss Landing Road, 

Moss Landing, California 95039, USA. Correspondence: Michael S. Foster, foster@mlml

.calstate.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
144 • smithsonian contributions to the marine sciences

destruction (reviewed in Foster, 2001). These conditions can result in free-living individuals of other organisms such as corals 

and bryozoans co-occurring with rhodoliths (e.g., James et al., 

2006). Once thought to be primarily subtropical, they are now 

known to occur from tropical to polar waters and from the low 

intertidal zone to 150 m deep (Bosence, 1983; Foster, 2001).

Our understanding of rhodoliths and rhodolith beds has 

grown from a synergy between geologists and biologists. Geologists were the first to become interested in rhodoliths, albeit dead 

ones, because these corallines are well preserved in the fossil record. At least since Darwin’s (1844) observations of rhodoliths 

(“nullipores”) in calcareous strata in the Cape Verde Archipelago, rhodolith deposits have been used to interpret geological 

change and paleoenvironments (e.g., Bassi et al., 2009). Early 

ecological work on live beds was pursued in the intertidal zone, 

or subtidally with dredges or grabs, and was focused on species 

composition and natural history (e.g., Weber-van Bosse and Foslie, 1904). In contrast to attached organisms on hard bottoms, 

dredging in rhodolith beds can provide good samples of the 

FIGURE 1. Rhodolith beds around Isla El Requéson, Baja California Sur, Mexico. 

Aerial shot: Dense aggregations of rhodoliths appear as dark ribbons and occur to 

a depth of 12 m. The island is 100 m across at widest point. The wide gray diagonal 

bar in lower right is the airplane wing strut (photo by M. S. Foster). In situ photo: 

spherical Lithophyllum margaritae rhodoliths at a depth of 6 m; diameters are 

4–5 cm (photo by D. L. Steller). Core cylinder photo: Core taken through the bed

at depth of 6 m. Note stratification, with living plants at the surface grading into 

dead fragments and fine sediment below; diameter = 9 cm (photo by D. L. Steller).
number 39 • 145

organisms present. This method is still being used to locate beds 

and their boundaries (e.g., Foster et al., 1997), especially over 

large areas where scuba is inefficient and acoustical mapping 

equipment (e.g., Ehrhold et al., 2006) is not available. Dredging can be effective for species information and mapping, but 

as in other shallow-water habitats, observation of microhabitat 

distribution and use, studies of processes, and field experimental 

manipulations require scuba. 

One of the first and the most comprehensive in situ studies 

on rhodolith systems was by Bosence (1976), a geologist interested in using characteristics of living rhodoliths and rhodolith 

beds to better interpret fossil deposits. Bosence (1976) carefully 

mapped rhodolith distribution in a bay in Ireland, and examined the relationships between the environment (especially water 

motion) and rhodolith species distribution and morphology. He 

wrote the first review of rhodolith ecology (Bosence, 1983), highlighting the advantages of scuba as a research tool and providing 

a foundation and stimulus for future studies that now include 

the full spectrum of ecological topics and approaches, including past and present climate change. Rhodoliths are particularly 

useful for the latter as they are widely distributed, grow slowly 

(~mm/yr) and, like temperate trees and hermatypic corals, leave 

a record of their growth as bands within the thallus (see the 

“Rhodoliths as Environmental Recorders” section in this paper). 

Sadly, reduced growth and dissolution caused by future changes 

in ocean pH and temperature may result in the absence of bands 

and the decline of rhodolith beds. 

A thorough review of rhodoliths and rhodolith bed ecology 

is beyond the scope of this paper. Instead, each author discusses 

a current topic in his or her area of interest and expertise: Introduction (MSF), Diving to the Edge of Rhodolith Taxonomy and 

Evolution (RRR), Rhodolith Communities and Conservation 

(DLS), Deep Beds in Brazil (GAF), and Rhodoliths as Environmental Recorders (NAK). Investigations of these topics have all 

been greatly facilitated by the use of scuba. We hope the reader 

will find the discussions interesting and informative, stimulating 

further interest in and study and conservation of these tumble 

weeds of the sea. 

DIVING TO THE EDGE OF RHODOLITH 

SYSTEMATICS AND EVOLUTION

Seaweed distribution and the factors that affect it are key 

scientific questions; Setchell (1893) clearly understood the importance of temperature limits to the geographic distribution of 

kelp species and the importance of distribution to systematics. 

The utility of such information, however, depends on the validity 

of the species identification and how well collections represent 

the geographic and depth distributions of species in nature. These 

problems have been particularly difficult to overcome in coralline red algae (Corallinales, Rhodophyta), and especially with the 

nongeniculate species that occur as rhodoliths. The characteristics 

used to classify rhodoliths in the early 1700s could not segregate 

them from corals or stones (Woelkerling, 1988) and names such 

as Lithophyllum are still in use for both algae and corals (Veron, 

1995). After recognizing rhodoliths as calcified, photosynthetic 

organisms, most investigators thought that species of Lithophyllum were characteristic of warm waters and Lithothamnium of 

cold waters (Foslie, 1900). Such relationships were based on sampling and observations from the intertidal zone or on specimens 

dredged from the shallow subtidal. Distributional knowledge was 

further compromised by the numerous species that were described 

based largely on external morphology. For example, investigators 

like Mikael Foslie described 485 species and varieties (Woelkerling et al., 2005) based primarily on external morphology, at least 

half of which were rhodolith-forming species.

As a consequence of developments in underwater technology including scuba, other diving methods, and better remote 

sampling devices, it soon became clear that coralline red algae 

were abundant, widespread, and often a key component of the 

ocean floor at depths to nearly 300 m. These developments also 

dramatically increased extraction of live and dead rhodoliths 

(maërl) for commercial purposes, an activity that has occurred 

since the seventeenth century along French and U.K. coasts (Grall 

and Hall-Spencer, 2003; see the “Rhodolith Systems: Communities and Conservation” section in this paper).

While large rhodolith beds have long been known in the 

northeast Atlantic, the surge in ocean exploration beginning in 

the twentieth century revealed the presence of coralline banks 

in Malaysia (Weber-van Bosse, 1904), the Galapagos (Lemoine, 

1930), the eastern Pacific (Dawson 1960a, 1960b), and Brazil, 

where beds cover hundreds of square km (Kempf, 1970; see the 

“Deep Beds in Brazil” section in this paper). These explorations 

were followed by extensive surveys in Brazil (Lavrado, 2006) 

and around the Hawaiian Islands (Adey et al., 1982). Hundreds 

of species were described from deeper areas, strongly suggesting 

that more species would be found as surveys continued. However, these collections were all made by dredging, and the few 

specimens obtained may not have been representative of local 

variation. Taxonomic analyses could be biased by describing new 

species based on a limited number of specimens.

This situation greatly improved in the 1950s when E.Y. 

Dawson started to use scuba for his research, diving with only 

mask, fins, tank, regulator, and a very rudimentary buoyancy 

compensator, with shorts and a shirt for a diving suit (Norris, 

2010: figs. 7, 8). Dawson could observe and collect numerous 

representative specimens under water, including what became 

Porolithon castellum and Sporolithon pacificum, the latter a very 

distinctive species (Dawson, 1960b). The allure of the visual record meant that underwater photography began to be used in 

the early days of diving. Dawson soon added a camera to his 

equipment, and his dive partner took one of the first underwater 

photographs of a coralline alga. Scuba diving quickly became 

part of the usual collecting approach for many researchers. It 

was a boon for taxonomists, who need to collect hundreds of 

individuals for rigorous morphological, anatomical, and now 

molecular analyses. 
146 • smithsonian contributions to the marine sciences

As scuba was recognized as an essential tool for marine 

scientists, scientific diving facilities and training programs, both 

fixed and portable, were developed around the world. There are 

a number of excellent examples of the success of such facilities in 

helping contribute to our knowledge of coralline taxonomy and 

diversity, including the descriptions of Tenarea tesselatum (Littler, 1971) from the tropics and Ezo eppiyessoense (Adey et al., 

1974) from a temperate region. Scuba investigations continue to 

discover new and interesting subtidal coralline species, including 

Synarthrophyton schielianum (Woelkerling and Foster, 1989), 

which has one of the strangest morphologies among the red algae.

In situ ecological studies of rhodolith-forming species began

in the 1970s, including the seminal studies of Bosellini and Ginsburg (1971) and Bosence (1976). These studies documented the 

large effects of the environment, especially variation in water 

motion, on rhodolith shape and branching characteristics. The 

results enlightened paleoenvironmental interpretations but also 

served as a warning to taxonomists that many described rhodolith 

species might be morphological variants of the same species. For 

Mediterranean waters, Ballesteros (1988) wrote the first review of 

rhodolith species using information obtained by diving, and Basso 

(1998) critically evaluated species boundaries. Taxonomic evaluations based on scuba collections using research stations in the 

western Pacific were done by Verheij (1993) in Indonesia and Ballesteros and Afonso-Carrillo (1995) in the Indo-Pacific. In the eastern Pacific, the diving study of Steller and Foster (1995) further 

showed the influence of the environment on rhodolith morphology. This environmentally induced morphological plasticity (Figure 2) obscured the real taxonomic boundaries used for the species 

until detailed anatomical work was done (Riosmena-Rodríguez et

FIGURE 2. Growth-form variation in the rhodolith Lithophyllum margaritae from the Gulf of California. The small rhodolith in lower left 

corner is 1.5 cm wide. From Riosmena-Rodríguez et al., 1999.
number 39 • 147

al., 1999). Additional genetic information from Schaeffer et al. 

(2002) has shown that some isolation occurs among populations. 

New descriptions and studies of rhodolith beds (e.g., Harvey et 

al., 2005; Konar et al., 2006) and collections and species analyses 

of the rhodoliths found are helping to refine our understanding of 

growth forms, species, and species distributions.

Rhodolith beds are distributed worldwide but a thorough 

bathymetric evaluation has not been produced at the global 

scale. Harvey and Woelkerling (2007) did an excellent review 

of the rhodolith-forming species in the coralline algae, concluding that there are 8 genera and 71 species cited in modern 

studies. Most of the records in this review came from dredging, 

not scuba collection, again suggesting that more of the latter is 

needed to clarify the boundaries between species. New technologies for working under water, along with the traditional methods 

of ocean exploration, provide very exciting opportunities that 

will contribute to understanding the evolutionary history of 

rhodolith-forming species via comparisons of subtidal findings 

with the geological record of well-preserved coralline red algae.

Collections using scuba diving and/or remotely operated 

underwater vehicles (ROVs) have already provided new records 

and evolutionary insights based on research occurring around 

the world (e.g., Brazilian continental shelf, Farias et al., 2010, 

and Bahia et al., 2011; Galician estuaries, Peña et al., 2011; Gulf 

of California, Riosmena-Rodríguez et al., 2010). In the future, it 

might be particularly interesting to examine very old fossil deposits along the coast of the Bahamas where Littler et al. (1985) 

described the deepest known plant life, a coralline alga. Coralline 

algae originated in the Cambrian (Woelkerling, 1988) and are one 

of the oldest clades in red algae. New studies will likely change 

our current views on rhodolith taxonomy and systematics due to 

probable discoveries of presently unknown evolutionary clades. 

The current challenge with regard to rhodolith systematic 

biology is to use information from field collections in combination with genetic analyses to better resolve species and answer 

evolutionary questions. This needs to involve the use of nuclear, 

chloroplast, and mitochondrial genes to delimit the number of 

clades among rhodoliths. These genetic approaches, combined 

with correlations between molecular clock and isotopic ages 

from carbonate deposits, should allow the construction of a 

model based on evolution and development (EVO DEVO), as 

suggested by Aguirre et al. (2010). The origins and development 

of rhodolith deposits can also be explored using mitochondrial 

genes to determine the origins of populations and the relative importance to bed persistence of fragmentation versus recruitment 

from spores. This is the edge of taxonomy and evolution, and 

scuba will therefore continue to be essential to advances. 

RHODOLITH SYSTEMS: 

COMMUNITIES AND CONSERVATION

Individual rhodoliths, or “nodules,” can form intricately 

branched structures, and large aggregations of nodules form 

beds, complex biogenic matrices of hard branches that create numerous interstitial spaces. Beds typically form as a living layer on 

top of an otherwise sedimentary bottom (Figure 1) and harbor 

a diverse and often unique assemblage of associated species (Cabioch, 1969; Keegan, 1974). In addition to being considered biodiversity hot spots, rhodolith beds are also settlement sites and 

nursery grounds for important commercial species. Fleshy macroalgae are found on the rhodolith surfaces; invertebrates are 

found among or bored into rhodolith branches (cryptofauna), 

moving over and among the rhodoliths, or burrowed into underlying sediments (infauna) (Grall and Glemarec, 1997; Steller et 

al., 2003). Burrowing fish add further benthic complexity, making these habitats rich sites for ecological exploration. 

Rhodolith beds are generally more species rich and support 

higher population densities than adjacent sedimentary habitats 

(Birkett et al., 1998; Steller et al., 2003). For example, stratified 

sampling of subhabitats in a rhodolith bed and a sand flat found 

richness to be 1.7 times, and total abundance 900 times, greater 

in a rhodolith bed than in adjacent non-rhodolith habitat (Steller 

et al., 2003). This has been attributed to the higher number of 

available niches in rhodoliths relative to sand. Beds support complex food webs of predators, suspension feeders, detritivores, 

and micrograzers in the eastern Atlantic (Grall et al., 2006). 

Early studies using scuba were largely devoted to determining the distribution of rhodoliths and associated species (Keegan, 

1974; Bosence, 1979), and such studies encouraged the development of diver-operated sampling devices such as suction dredges 

to more precisely sample soft-bottom species (Keegan and Konnecker, 1973). This ecological community research continues as 

new beds are discovered and explored, and many recent studies 

have shifted their focus to understanding the mechanisms underlying ecological relationships, reflecting the evolution of ecological research as well as changes in research methods. Traditional 

ship-based benthic sampling with dredges and grabs has been 

useful in establishing general patterns of distribution and diversity. Combining this type of sampling with scuba allows for (1) 

efficient visual surveys of large areas, (2) more precise habitat 

sampling, (3) enhanced detection of rare, seasonal, and fragile 

associated species and species interactions, and (4) in situ environmental measurements and experimental manipulations. As a 

result, surveys worldwide now report that the greatest contributors to high richness and abundance are cryptofauna (primarily 

arthropods, annelids, and cnidarians) that increase as live cover 

and rhodolith size and branching increases. Such microhabitat 

associations can be obscured or eliminated in homogenized samples from dredges, grabs, and cores.

Large-scale studies comparing species in rhodolith beds to 

those in entirely sedimentary habitats have measured species 

diversity of either the entire community or a dominant group 

of organisms. In general, higher diversity and abundance of a 

community (Grall et al., 2006), or of specific invertebrate groups 

(e.g., polychaetes; Figueiredo et al., 2007), has been correlated 

with higher density and cover of live rhodoliths and more complex habitat. This pattern is not consistent for all species; infauna 
148 • smithsonian contributions to the marine sciences

such as soft-sediment meiofaunal bivalves can be more diverse 

on dead (versus live) rhodolith substrate (Jackson et al., 2004).

When rhodoliths grow as distinct, densely branched, spherical individuals (Figure 2) rather than mats of intertwined, jacklike structures, the richness and abundance of species in and on 

them increases with rhodolith size, branching, and available space 

(Steller et al., 2003; Hinojosa-Arango and Riosmena-Rodríguez,

2004; Foster et al., 2007). Elucidating such relationships requires 

using scuba to carefully collect individual specimens, followed by 

proper fixation and careful dissection. Such studies have shown 

that 2–6 cm–diameter, highly branched Lithophyllum margaritae and 5–9 cm–diameter, knobby, branched Lithothamnion 

muellerii from the Gulf of California can harbor 10–90 cryptofaunal species per rhodolith, with more species in larger individuals. Rhodolith densities can beupwards of 5,000–10,000 m−2

(D. Steller, personal observation), resulting in exceptionally high 

cryptofaunal abundance. The most abundant taxa often include 

crustaceans, polychaetes, ophiuroids, and mollusks. Collectively, 

these findings support the notion that large, old individuals act 

as “old-growth rhodoliths,” and are inhabited by species such as 

stomatopods and burrowing clams not found on and in smaller 

rhodoliths (Foster et al., 2007).

Diving studies have also revealed rare and new species, and 

some unique and interesting ecological relationships. Eight species of small (2–10 mm) cryptofaunal chitons were collected 

from between the branches of Lithophyllum margaritae in the 

Gulf of California, four of which were previously undescribed 

(Clark, 2000). Reports of complex, fragile nests built by the mollusk Limaria hians, a gaping file shell, came from in situ observations (Hall-Spencer et al., 2003). Macroinvertebrates such as the 

urchin Toxopneustes roseus can cover themselves with rhodoliths and also prefer to eat them rather than fleshy algae (James, 

2000). The burrowing crustacean Upogebia deltaura creates extensive burrows among the rhodoliths that can withstand disturbance (Hall-Spencer and Atkinson, 1999). Such investigations 

are still few but the use of standardized scuba-enabled subtidal 

sampling designs and methods (Steller et al., 2007) promises to 

reveal more new species, as well as ecological and biogeographic 

insights.

The productivity of rhodolith beds is enhanced by a diverse 

associated flora that grows on the hard substrata they provide 

(Jacquotte, 1962; Grall et al., 2006), and some algal species appear to be confined to rhodolith habitat (Leliaert et al., 2009). The 

associated flora often changes seasonally, as well as with depth. 

These changes are correlated with variation in rhodolith characteristics such as cover, depth, and the amount of live material. The 

changes are also correlated with changing oceanographic conditions, such as water motion, which can turn and roll rhodoliths, 

as well as temperature (Cabioch, 1969; Lieberman et al., 1979; 

Hily et al., 1992; Birkett et al., 1998; Steller et al., 2003; AmadoFilho et al., 2007; Riul et al., 2009; Peña and Barbara, 2010). In 

a subtropical Gulf of California bed, Steller et al. (2003) reported 

up to thirty common macroalgal species in winter, but a maximum of eight species in summer. Year-long sampling at 11⁄2-month

intervals has shown similar large seasonal changes in the flora of 

a European Atlantic bed, as well as relationships between these 

changes and the depth of the living rhodolith layer and the live/

dead rhodolith ratio (Peña and Barbara, 2010). 

Qualitative in situ observations in the Gulf of California 

and elsewhere suggest that the diversity of large fishes in the 

water column above rhodolith beds is generally low, probably 

because there is little structure above the bottom. Reports of 

numerous associated water column fishes (e.g., Aburto-Oropeza 

and Balart, 2001) are likely an artifact of the beds being in close 

proximity to reefs that provide macrostructure. Numerous cryptic demersal, benthic, and/or burrowing species such as gobies 

and blennies are found on, in, and among rhodoliths, and juveniles of species such as cod have been reported to use rhodolith 

beds as feeding areas (Hall-Spencer et al., 2003). Large, bottomdwelling or burrowing species can be quite common, including sheephead (Semicossyphus pulcher) in California, and tiger 

snake eels (Myrichthys maculosus), bullseye electric (Diplobatis 

ommanata) and other rays, and Cortez garden eels (Taeniconger 

digueti) in the Gulf of California (D. Steller and M. Foster, pers. 

obs.). The distribution of rhodolith beds appears to be largely 

constrained by abiotic variables such as water motion and light, 

but within-bed structure and perhaps even bed persistence may 

be strongly affected by biological interactions. Bioturbation by 

invertebrates and fishes moves rhodoliths and resuspends fine 

sediment, likely facilitating rhodolith growth and bed maintenance (Marrack, 1999). 

Rhodolith beds may act as nursery habitat for a variety of 

species. Bivalves are abundant in rhodolith beds in areas such as 

Georges Bank (Thouzeau, 1991), the Gulf of California (Steller 

and Caceras-Martinez, 2009), and the eastern Atlantic (Hily et 

al., 1992; Hall-Spencer, 1998; Hall-Spencer and Moore, 2000), 

and rhodolith beds may play a role as nursery habitats for scallops. Scallop–rhodolith bed interactions have been of particular 

interest because scallops are commercially harvested and their 

life history is well known. Scallop larvae have been shown to 

preferentially settle on living (versus dead) rhodoliths (Steller 

and Caceras-Martinez, 2009). This preference likely contributes 

to high juvenile scallop densities (Kamenos et al., 2004a)h@ due 

to greater scallop selection, attachment, and growth (Kamenos et 

al., 2004b, 2004c). Rhodolith beds may also benefit adult scallops by providing a refuge from predation (Steller et al., 2003; 

Kamenos et al., 2006). Patterns of water motion responsible for 

rhodolith maintenance may also influence larval delivery of a 

number of associated species, a mechanism that remains to be 

investigated. 

While natural disturbances are an essential feature of rhodolith ecosystems, anthropogenic disturbances can be catastrophic. 

This is readily clear from diving observations made over a oncethriving rhodolith bed that had been crushed by a scallop dredge.

Beds have been entirely or partially destroyed by extraction of 

calcareous sediment, bottom fisheries, and degraded water quality from fish farms (De Grave, 1999; Hall-Spencer and Moore,

2000; Hall-Spencer et al., 2006). Smaller-scale disturbances such 
number 39 • 149

as anchoring or mooring in coastal bays also occur, but have 

received less attention. 

In addition to localized destruction, rhodolith beds worldwide will likely be impacted by decreasing ocean pH linked to 

rising atmospheric CO2

 (Kleypas et al., 2006). Coralline algae, 

with their very soluble high-Mg calcite, are predicted to be in 

the first suite of species severely impacted by ocean acidification 

(Kuffner et al., 2007; Jokiel et al., 2008). Chemical dissolution 

could make them more susceptible to other physical and biological disturbances and decrease post-disturbance recovery rates. 

The positive relationship between biodiversity and rhodolith 

density, nodule size, and branching strongly suggests that factors 

negatively impacting nodule characteristics would likely lead to 

negative community-level impacts.

The need for protecting rhodolith beds from dredging, 

trawling, and other relatively small-scale disturbances has been 

recognized by conservation directives in the European Union,

Australia, New Zealand, and Mexico (review in RiosmenaRodríguez et al., 2010). On the largest scale, however, little progress has been made toward reducing CO2

 emissions. It remains to 

be seen how effective local conservation measures will be in the 

face of global change. 

DEEP BEDS IN BRAZIL

The Brazilian coast supports the largest known rhodolith 

beds in the world, covering extensive areas of the north, northeastern, and southeastern Brazilian continental shelf (Kempf, 

1970; Milliman, 1977; Amado-Filho et al., 2007). However, 

our understanding of the latitudinal distribution and community structure of these beds is still in its infancy. Many rhodolith 

studies in Brazil, especially the early ones, were focused on the 

characterization of shelf sediments and prospects for potential 

commercial exploitation (Milliman and Amaral, 1974; Dias, 

2000). Only a few published studies have considered the beds 

in a biological context that includes consistent information 

about meso- and small-scale distribution, bed structure, associated organisms, and the species composition of the rhodoliths 

(e.g., Gherardi, 2004; Riul et al., 2009; Villas-Boas et al., 2009; 

Amado-Filho et al., 2010).

These latter studies have found a high diversity of organisms 

associated with rhodolith beds and highlight their ecological relevance. A general evaluation of the marine biota in the Brazilian 

exclusive economic zone (the marine area extending 320 km offshore) indicated rhodolith beds increase the diversity of epibenthic organisms, with Shannon diversity indices (H’) of 4.0–5.1 

found to depths of 250 m in this ecosystem (Lavrado, 2006). 

These and other data obtained during the 1990s and the early 

2000s were, however, based on dredging and the analyses were 

largely qualitative. Most rhodolith beds in Brazil still remain unexplored or poorly known ecologically. This is largely because 

the beds occur mostly in mesophotic habitats (~30–120 m depth) 

that are difficult to adequately access with standard scuba.

As pointed out by Bridge et al. (2010), information on biotic and abiotic aspects of mesophotic habitats remains extremely 

scarce due to logistical and technological restrictions, particularly 

when compared with shallow-water habitats. This is true for 

rhodolith beds in Brazil, but recent advances in mixed-gas diving techniques (Figure 3), complemented by ROV observations 

and high-resolution, multibeam, bathymetric mapping systems, 

allow us to begin determining their extent, structure, and dynamics. These tools are now being used to investigate extensive areas 

of the continental shelf (e.g., Abrolhos Bank), tops of seamounts 

(Vitoria-Trindade Ridge), and around oceanic islands (e.g., Trindade Island and Fernando de Noronha Island; Figure 4).

One of the most interesting features of these mesophotic 

habitats, recently investigated using technical diving, are rhodolith beds inhabited by populations of the deep water endemic 

kelp Laminaria abyssalis. This kelp occurs on the continental 

shelf at latitudes of 19°–23° S and depths of 45–120 m where 

the bottom is completely covered by rhodoliths (Amado-Filho 

et al., 2007). Kelp populations are closely associated with the 

rhodoliths; all L. abyssalis holdfasts are attached to one or more 

rhodoliths. Graham et al. (2007) suggested that such deep water 

kelp refugia are potential hot spots of tropical marine diversity 

and productivity. This suggestion has been confirmed in the Brazilian deep water rhodolith–kelp beds, as endemic species of different taxonomic groups have been cited to this area. 

The northern limit of Brazilian L. abyssalis populations is 

determined by the southern edge of Abrolhos Bank. The Abrolhos Shelf (16°50′S–19°45′S; Figure 4) is an ~6,000 km2 enlargement of the eastern Brazilian continental shelf, and encompasses 

the largest (~325 km2

) and richest reefs in the South Atlantic 

(Leão and Ginsburg, 1997). These reefs are well known for their 

unique coral assemblages dominated by Brazilian-endemic, Neogene relics belonging to the genus Mussismilia. Investigations 

combining side scan sonar, ROV images, and scuba diving show 

that rhodolith beds are the predominant feature from north to 

south across the Abrolhos Shelf at depths from ~25 m to ~110 m.

These beds are composed of at least five non-geniculate coralline 

species.

The Vitoria-Trindade Ridge (VTR; 20°S–21°S) is a 

1,150 km east–west chain of nine seamounts in the South Atlantic that includes two small and highly isolated islands at its 

eastern end (Figure 4). Previous biological sampling on the VTR 

was largely restricted to (1) dredging, (2) data from commercial 

fisheries, and (3) a few scientific diving operations in the shallow waters surrounding Trindade Island. The mesophotic zone 

on the top of two seamounts (Davis and Jaseur) were surveyed 

in March 2009 using a combination of ROVs, mixed-gas technical dives, and a single-beam bathymetry system. The seamounts 

have predominantly flattened tops that result from alternating 

periods of growth and erosion of carbonate algal deposits over 

volcanic pedestals during periods of high and low sea level (Almeida, 1965). At present sea level, the flattened summits of the 

seamounts are all situated in relatively shallow water, with minimum depths ranging from 40 m to 110 m. The seamount tops 
150 • smithsonian contributions to the marine sciences

rise up to 50 m from the bottom, and are dominated by rhodoliths with a high diversity of associated species including seaweeds, sponges, corals, black corals, octocorals, and reef fishes. 

Rhodolith beds are also the main feature surrounding Fernando 

de Noronha, a typical tropical island (03°50′S, 32°25′W, about 

345 km east of the coast of Brazil; Figure 4) known as the best 

diving location in Brazil. These beds, found down to 120 m at the 

edge of the island shelf, were also discovered using technical diving. The ongoing description and study of these unique coralline 

environments will provide essential information for understanding the ecology, biodiversity, and connectivity of South Atlantic 

reef communities. 

RHODOLITHS AS 

ENVIRONMENTAL RECORDERS

Coralline algae have several characteristics that make them 

ideal candidates for recording the environment in which they 

grow. When these algae grow, they lay down annual and subannual carbonate-derived growth bands composed of high-Mg 

calcite (Figure 5; Henrich et al., 1996; Kamenos et al., 2008). 

Groups of subannual primary growth bands resulting from variation in cell size and wall thickness can be grouped into dark 

FIGURE 3. Technical diving equipment being used to take video images at 60 m on Fernando de Noronha Island 

shelf, Brazil. Photo by Z. Matheus, courtesy of G. M. Amado Filho.

FIGURE 4. Locations of mesophotic rhodolith beds on the Brazilian 

Shelf.
number 39 • 151

and light pairs that form higher-order annual banding patterns 

(Freiwald and Henrich, 1994). While Lithothamnion glaciale

and Clathromorphum compactum show clear annual banding 

patterns (Halfar et al., 2008; Kamenos et al., 2008), other species 

such as Phymatolithon calcareum show clearer subannual banding patterns (Blake and Maggs, 2003). In some species, growth 

is not hampered by prolonged periods of low temperature (e.g., 

L. glaciale; Henrich et al., 1996) or darkness (e.g., L. glaciale; 

Freiwald and Henrich, 1994), while in others there is reduced 

growth in winter (e.g., C. compactum; Halfar et al., 2008). As 

new thalli grow at the surface of the rhodolith bed, older thalli 

become covered by sediment, die, and form part of the dead deposit. Individual coralline algal thalli can live to at least ~850 

years (Frantz et al., 2005) and accumulations of these algal thalli 

have created maërl deposits spanning the last 20,000 years (Figure 6; Bosence, 1983). Unlike most carbonate-depositing organisms, which have a more restricted distribution, coralline algae 

occur from polar (Schwarz et al., 2005) to tropical (Littler et al., 

1991) shallow seas.

Three key steps are typically used in the development of 

an environmental recorder (known as a proxy; Kamenos et al., 

2009). For coralline algae this involves the following: (1) calibration, which involves understanding the biology of the algae and 

experimentally determining how growth, for example, responds 

to environmental stimuli such as temperature (Kamenos et al., 

2008); (2) validation of the algae as proxies, which requires appropriate biogeochemical analyses to determine if the observed 

response of the alga’s physical or chemical characteristics to environmental change are a direct response to that change or the 

record of a tertiary response to a related physiological process 

(Kamenos et al., 2009); and, (3) application, which establishes 

that the coralline algae are recording a specific environmental 

stimulus and can be used to reconstruct and understand environmental changes that occurred before the availability of instrumental records (Kamenos, 2010; Burdett et al., 2011). 

Unfortunately, many proxies do not undergo this rigorous and 

important three-step process, rendering their utility questionable. 

Scuba has been instrumental in the development of rhodoliths as environmental recorders. Because of their fragile nature, 

hand collection is the only suitable technique for calibrating the 

algae in the field or collecting them for calibration in the laboratory. Subsequent to calibration, collection of samples for paleoenvironmental reconstruction involves determination of the 

most suitable sampling location (e.g., the location likely to provide the longest record) and precise manipulation of sampling 

apparatus (e.g., corer placement or airlift attachment). These 

tasks can only be reliably achieved using on-site sampling via 

scuba. Remote mechanical collection is not suitable due to the 

absence of specific sampling location information (e.g., what was 

the orientation of the surface algae on collection?). While suitable remote coring equipment can be used in softer sediments 

(e.g., vibra corer), the dense nature of rhodolith deposits requires 

coring techniques capable of penetrating the sediment without 

causing excessive disturbance. At present, scuba is the ideal tool 

for conducting such coring activities.

FIGURE 6. A Lithothamnion glaciale bed and associated fauna on 

the west coast of Scotland. Scale = 5 cm. Photo by N. Kamenos.

FIGURE 5. Annual banding patterns in a transverse sectioned Lithothamnion glaciale branch. Scale = 1 mm. Photo by N. Kamenos.
152 • smithsonian contributions to the marine sciences

Relationships between environmental parameters and 

growth have been observed in coralline algae. Significant negative relationships are present between temperature and calcite 

density in Lithothamnion glaciale (Kamenos and Law, 2010), as 

well as temperature and growth-band width in Clathromorphum 

compactum (Halfar et al., 2011). In both species growth characteristics were correlated to decadal-scale temperature records at 

collection sites but were characterized by noticeable variability. 

That variability was attributed to localized control of incident 

radiation (e.g., algal blooms) and thus it is likely that growth 

contains a record of both temperature and irradiance (Kamenos 

and Law, 2010). This was addressed by the development of a 

growth-environment model that accounts for both temperature 

and light (as photosynthetically active radiation or PAR; Burdett et al., 2011). By combining a record of summer calcification 

within individual Lithothamnion glaciale growth bands with 

known temperature records for the area, cloud cover (indicative 

of PAR) history on the west coast of Scotland was reconstructed 

that indicated a modest increase in cloud cover trends since 1910 

(Burdett et al., 2011). 

The chemistry of the calcite deposited by coralline algae 

within their growth bands also serves as an environmental recorder. Initial observations indicated elemental concentrations 

within coralline algae varied directly (Chave and Wheeler, 1965) 

and indirectly (Moberly, 1968) with environmental fluctuations. 

More recently, Mg concentrations within Lithothamnion glaciale

have been observed to represent ambient temperature of the seawater in which the algae grew at fortnightly resolutions (Kamenos

et al., 2008), as well as sea-surface temperature at seasonal resolution (Halfar et al., 2000). This response allowed Lithothamion 

glaciale to be validated as a paleotemperature recorder (Kamenos 

et al., 2009), enabling the first biweekly resolution reconstruction 

of Atlantic marine temperatures since ~1350 (Kamenos, 2010). 

δ18O in Clathromorphum nereostratum and Lithothamnion glaciale represents ambient seawater temperature at seasonal resolutions and has been used to reconstruct northeastern Atlantic 

sea-surface temperature since 1970 (Halfar et al., 2000, 2008). 

Lithothamnion muellerii and C. nereostratum have been shown 

to record atmospheric 14C concentrations (Frantz et al., 2000, 

2005), which are critical for determining long-term growth rates

and age in coralline algae as well as dating the exact timing of climatic events recorded by the growth-banding structure or chemistry within the algae. Overall, coralline algae are ideally suited 

as chemical environmental recorders because (1) they do not suffer diagenetic effects due to the presence of the living membrane 

covering the carbonate skeleton (Alexandersson, 1974); (2) there 

is no stress-related geochemical deviation in Mg/Ca–temperature

relationships (Kamenos et al., 2008); and, (3) there is no nonequilibrium-associated oxygen isotope fractionation in maërl

(Rahimpour-Bonab et al., 1997; Halfar et al., 2007). 

Scuba has played a central role in facilitating an understanding of how coralline algae act as environmental recorders 

through their utility in paleoenvironmental reconstructions. With 

the need for increasingly resolved spatio-temporal paleoclimate 

records to better understand recent climate trends, these algae 

are beginning to receive increased attention as environmental 

recorders.

CONCLUSIONS

As they have for other shallow subtidal environments, in 

situ investigations using scuba have improved our understanding 

of rhodoliths and rhodolith beds far beyond that achievable by 

dredging and other remote research techniques. Scuba enabled 

detailed sampling that continues to clarify the taxonomy and 

evolutionary relationships of rhodoliths and associated species. 

It has allowed the direct determination of bed distribution and 

abundance patterns, and field experiments to test hypotheses 

about the causes of these patterns. Such studies, including those 

in deep water that use technical diving, continue to provide new 

insights into bed structure and function. Careful collection and 

underwater experimentation have also revealed rhodoliths to be 

exceptional environmental recorders. Beds are, however, very 

susceptible to disturbance and climate change. Their conservation must be a priority if we are to continue to enjoy, better understand, and learn from these remarkable communities and the 

plants that dominate them. 

ACKNOWLEDGMENTS

We thank the diving community for providing locations and 

in situ observations of new rhodolith beds that have contributed to understanding rhodolith distribution and provided new 

opportunities for research. Coauthor GAF thanks the Brazilian 

research agencies CNPq, CAPES, and FAPERJ for financial support for development projects. Coauthor NK is in receipt of a 

Royal Society of Edinburgh/Scottish Government Personal Research Fellowship (RSE 48704/1).

This chapter is dedicated to the memory of Isabella A. Abbott 

(1919–2010), who contributed enormously to our knowledge of 

marine algae, championed international scientific collaboration, 

and always encouraged searches for subtidal seaweeds. 

REFERENCES

Aburto-Oropeza, O., and E. F. Balart. 2001. Community structure of reef fish in 

several habitats of a rocky reef in the Gulf of California. PSZNI Marine Ecology, 22:283–305.

Adey, W. H., T. Masaki, and H. Akioka. 1974. Ezo epiyessoense, a new parasitic genus and species of Corallinaceae (Rhodophyta, Cryptonemiales). Phycologia, 

13:329–344. http://dx.doi.org/10.2216/i0031-8884-13-4-329.1.

Adey, W. H., R. A. Townsend, and W. T. Boykins. 1982. The crustose coralline algae 

(Rhodophyta: Corallinaceae) of the Hawaiian Islands. Smithsonian Contributions to Marine Science, No. 15. Washinton, D.C.: Smithsonian Institution 

Scholarly Press.

Aguirre, J., F. Perfectti, and J. C. Braga. 2010. Integrating phylogeny, molecular 

clocks and the fossil record in the evolution of coralline algae (Corallinales, 

Rhodophyta). Paleobiology, 36:519–533. http://dx.doi.org/10.1666/09041.1.
number 39 • 153

Alexandersson, T. 1974. Carbonate cementation in coralline algal nodules in 

Skagerrak, North Sea: Biochemical precipitation in undersaturated waters. 

Journal of Sedimentary Petrology, 44:7–26.

Almeida, F. F. M. 1965. As ilhas oceânicas brasileiras e uma hipótese sobre a origem 

do Atlântico. Anais da Academia Brasileira Ciencias, 37:141–145.

Amado-Filho, G. M., G. Maneveldt, R. C. C. Manso, B. V. Marins-Rosa, M. R. 

Pacheco, and S. Guimarães. 2007. Structure of rhodolith beds from 4 to 55 

meters deep along the southern coast of Espírito Santo State, Brazil. Ciencias 

Marinas, 32:399–410.

Amado-Filho, G. M., G. W. Maneveldt, G. H. Pereira-Filho, R. C. C. Manso, R. G.

Bahia, M. B. Barros-Barreto, and S. M. P. B. Guimarães. 2010. Seaweed diversity associated with a Brazilian tropical rhodolith bed. Ciencias Marinas,

36(4):371–391. http://dx.doi.org/10.7773/cm.v36i4.1782.

Bahia, R. G., R. Riosmena-Rodríguez, G. W. Maneveldt, and G. M. Amado-Filho.

2011. First report of Sporolithon ptychoides (Sporolithales, Corallinophycidae, Rhodophyta) for the Atlantic Ocean. Phycological Research, 59:64–69. 

http://dx.doi.org/10.1111/j.1440-1835.2010.00599.x.

Ballesteros, E. 1988. Composición y estructura de los fondos de maërl de tossa de 

Mar (Gerona, España). Collectanea Botanica, 17:161–182. http://dx.doi.org

/10.3989/collectbot.1989.v17.137.

Ballesteros, E., and J. Afonso-Carrillo. 1995. Species records and distribution of 

shallow-water coralline algae in a western Indian Ocean coral reef (Trou 

d’Eau Douce, Mauritius). Botanica Marina, 38:203–213. http://dx.doi.org/10

.1515/botm.1995.38.1-6.203.

Bassi, D., J. H. Nebelsick, A. Checconi, J. Hohenegger, and Y. Iryu. 2009. Presentday and fossil rhodolith pavements compared: Their potential for analyzing 

shallow-water carbonate deposits. Sedimentary Geology, 214:74–84. http://

dx.doi.org/10.1016/j.sedgeo.2008.03.010.

Basso, D. 1998. Deep rhodolith distribution in the Pontian Islands, Italy: A model for 

the paleoecology of a temperate sea. Paleogeography, Paleoclimatology, Paleoecology, 137:173–187. http://dx.doi.org/10.1016/S0031-0182(97)00099-0.

Birkett, D., C. Maggs, and M. Dring. 1998. Maërl, Volume V : An overview of dynamic and sensitivity characteristics for conservation management of marine 

SACs. Oban, UK: Scottish Association for Marine Science.

Blake, C., and C. Maggs. 2003. Comparative growth rates and internal banding periodicity of maërl species (Corallinales, Rhodophyta) from northern Europe. 

Phycologia, 42:606–612. http://dx.doi.org/10.2216/i0031-8884-42-6-606.1.

Bosellini, A., and R. N. Ginsburg. 1971. Form and internal structure of recent algal 

nodules (Rhodolites) from Bermuda. Journal of Geology, 79: 669–682. http://

dx.doi.org/10.1086/627697.

Bosence, D. W. J. 1976. Ecological studies on two unattached coralline algae from 

western Ireland. Paleontology, 19:365–395.

———. 1979. Live and dead faunas from coralline algal gravels, Co. Galway. Paleontology, 22:449–478.

———. 1983. The occurrence and ecology of recent rhodoliths: A review. In Coated 

grains, ed. T. M. Peryt, pp. 225–242. Berlin: Springer-Verlag. http://dx.doi

.org/10.1007/978-3-642-68869-0.

Bridge, T. C. L., T. J. Done, R. J. Beaman, A. Friedman, S. B. Williams, O. Pizarro, 

and J. M. Webster. 2010. Topography, substratum and benthic macrofaunal 

relationships on a tropical mesophotic shelf margin, central Great Barrier 

Reef, Australia. Coral Reefs, doi:10.1007/s00338-010-0677-3. http://dx.doi

.org/10.1007/s00338-010-0677-3.

Burdett, H. L., N. A. Kamenos, and A. Law. 2011. Using coralline algae to understand historic marine cloud cover. Paleogeography, Paleoclimatology, Paleoecology, 302:65–70. http://dx.doi.org/10.1016/j.palaeo.2010.07.027.

Cabioch, J. 1969. Les fonds de maërl de la Baie de Morlaix et leur peuplement 

vegetal. Cahiers de Biologie Marine, 9:139–161.

Chave, K. E., and B. D. Wheeler. 1965. Mineralogic changes during growth in red 

algae, Clathromorphum compactum. Science, 147:621. http://dx.doi.org/10

.1126/science.147.3658.621.

Clark, R. N. 2000. The chiton fauna of the Gulf of California rhodolith beds (with 

descriptions of four new species). Nemouria, 43:1–20.

Darwin, C. R. 1844. Geological observations on the volcanic islands visited during 

the voyage of H.M.S. Beagle. London: Smith Elder and Co.

Dawson, E. Y. 1960a. New records of marine algae from Pacific Mexico and Central America. Pacific Naturalist, 1:31–52.

———. 1960b. Marine red algae of Pacific Mexico. Part III. Cryptonemiales, Corallinaceae, subf. Melobesioideae. Pacific Naturalist, 2:3–125.

De Grave, S. 1999. The influence of sedimentary heterogeneity on within maërl bed 

differences in infaunal crustacean community. Estuarine, Coastal and Shelf 

Science, 49:153–163. http://dx.doi.org/10.1006/ecss.1999.0484.

Dias, G. T. M. 2000. Granulados bioclásticos – algas calcárias. Brazilian Journal of 

Geophysics, 18:307–318.

Ehrhold, A., D. Hamon, and B. Buillaumont. 2006. The REBENT monitoring 

network, a spatially integrated, acoustic approach to surveying nearshore 

macrobenthic habitats: Application to the Bay of Concarneau (South Brittany, France). ICES Journal of Marine Science, 63:1604–1615. http://dx.doi

.org/10.1016/j.icesjms.2006.06.010.

Farias, J., R. Riosmena-Rodríguez, and P.A. Horta. 2010. Lithothamnion superpositum (Corallinales, Rhodophyta): First description for Brazil or a rediscovery 

of a species? Phycological Research, 51:210–216. http://dx.doi.org/10.1111/j

.1440-1835.2010.00581.x.

Figueiredo, M. A. D. O., K. Santos de Menezes, E. M. Costa-Paiva, P. C. Paiva, and 

C. R. R. Ventura. 2007. An experimental evaluation of rhodoliths as living substrata for infauna in the Abrolhos Bank, Brazil. Ciencias Marinas, 33: 427–440.

Foslie, M. 1900. Die Systematik der Melobesieae. (Eine Berichtigung). Berichte der 

Deutschen Botanischen Gesellschaft, 18:239–241. 

Foster, M. S. 2001. Rhodoliths: Between rocks and soft places. Journal of Phycology, 37:659–667. http://dx.doi.org/10.1046/j.1529-8817.2001.00195.x.

Foster, M. S., L. M. McConnico, L. Lundsten, T. Wadsworth, T. Kimball, L. B. 

Brooks, M. Medina-Lopez, R. Riosmena-Rodríguez, G. Hernandez-Carmona,

R. Vasquez-Elisando, S. Johnson, and D. L. Steller. 2007. The diversity and 

natural history of a Lithothamnion muelleri–Sargassum horridum community in the Gulf of California. Ciencias Marinas, 33:367–384.

Foster, M. S., R. Riosmena-Rodríguez, D. L. Steller, and W. J. Woelkerling. 1997. 

Living rhodolith beds in the Gulf of California and their implications for 

paleoenvironmental interpretation. In Pliocene carbonates and related facies 

flanking the Gulf of California, Baja California, Mexico, ed. M. E. Johnson 

and J. Ledesma-Vazquez, pp.127–139. Geological Society of America Special 

Paper 318. Boulder, Colo.: Geological Society of America. http://dx.doi.org/10

.1130/0-8137-2318-3.127.

Frantz, B. R., M. S. Foster, and R. Riosmena-Rodríguez. 2005. Clathromorphum 

nereostratum (Corallinales, Rhodophyta): The oldest alga? Journal of Phycology, 41:770–773. http://dx.doi.org/10.1111/j.1529-8817.2005.00107.x.

Frantz, B. R., M. Kashgarian, K. H. Coale, and M. S. Foster. 2000. Growth rate 

and potential climate record from a rhodolith using C-14 accelerator mass 

spectrometry. Limnology and Oceanography, 45:1773–1777. http://dx.doi

.org/10.4319/lo.2000.45.8.1773.

Freiwald, A., and R. Henrich. 1994. Reefal coralline algal build-ups within the Arctic circle: Morphology and sedimentary dynamics under extreme environmental seasonality. Sedimentology, 41:963–984. http://dx.doi.org/10.1111/j.1365

-3091.1994.tb01435.x.

Gherardi, D. F. M. 2004. Community structure and carbonate production of a 

temperate rhodolith bank from Arvoredo Island, southern Brazil. Brazilian 

Journal of Oceanography, 52:207–224.

Graham, M. H., B. P. Kinlan, L. D. Dreuhl, L. E. Garske, and S. Banks. 2007. Deepwater kelp refugia as potential hotspots of tropical marine diversity and 

productivity. Proceedings of the National Academy of Sciences, 104:16576–

16580. http://dx.doi.org/10.1073/pnas.0704778104.

Grall, J., and M. Glemarec. 1997. Biodiversite des fonds de maërl en Bretagne: approache fonctionnelle et impacts anthropogeniques. VIE MILIEU, 47:339–349.

Grall, J., and J. M. Hall-Spencer. 2003. Problems facing maërl conservation in Brittany. Aquatic Conservation: Marine and Freshwater Ecosystems, 13:55–64. 

http://dx.doi.org/10.1002/aqc.568.

Grall, J., F. Le Loc’h, B. Guyonnet, and P. Riera. 2006. Community structure and 

food web based on stable isotopes (DELTA15N and DELTA13C) analysis of a 

North Eastern Atlantic maërl bed. Marine Ecology Progress Series, 338:1–15.

Halfar, J., S. Hetzinger, W. H. Adey, T. Zack, G. Gamboa, B. Kunz, B. Williams, and 

D. E. Jacob. 2011. Coralline algal growth-increment widths archive North 

Atlantic climate variability. Paleogeography, Paleoclimatology, Paleoecology, 

302:71–80. http://dx.doi.org/10.1016/j.palaeo.2010.04.009.

Halfar, J., R. S. Steneck, M. Joachimski, A. Kronz, and A. D. Wanamaker. 2008. Coralline red algae as high-resolution climate recorders. Geology, 36:463–466. 

http://dx.doi.org/10.1130/G24635A.1.

Halfar, J., R. Steneck, B. Schone, G. W. K. Moore, M. Joachimski, A. Kronz, 

J. Fietzke, and J. Estes. 2007. Coralline alga reveals first marine record of 

subarctic North Pacific climate change. Geophysical Research Letters, 

34:L07702. http://dx.doi.org/10.1029/2006GL028811.

Halfar, J., T. Zack, A. Kronz, and J. C. Zachos. 2000. Growth and high resolution paleoenvironmental signals of rhodoliths (coralline red algae): A new 

biogenic archive. Journal of Geophysical Research, C, Oceans, 105: 22,107–

22,116. http://dx.doi.org/10.1029/1999JC000128.
154 • smithsonian contributions to the marine sciences

Hall-Spencer, J. M. 1998. Conservation issues relating to maërl beds as habitats for 

molluscs. Journal of Conchology, Special Publication, 2:271–286.

Hall-Spencer, J. M., and R. J. A. Atkinson. 1999. Upogebia deltaura (Crustacea: 

Thalassinidea) in Clyde Sea maërl beds, Scotland. Journal of the Marine Biological Association of the United Kingdom, 79:871–880. http://dx.doi.org/10

.1017/S0025315498001039.

Hall-Spencer, J. M., J. Grall, P. G. Moore, and R. J. A. Atkinson. 2003. Bivalve fishing and maërl-bed conservation in France and the UK: Retrospect and prospect. Aquatic Conservation: Marine and Freshwater Ecosystems, 13:S33–

S41. http://dx.doi.org/10.1002/aqc.566.

Hall-Spencer, J. M., and P. G. Moore. 2000. Scallop dredging has profound, longterm impacts on maërl habitats. ICES Journal of Marine Science, 57:1407–

1415. http://dx.doi.org/10.1006/jmsc.2000.0918.

Hall-Spencer, J. M., N. White, E. Gillespie, K. Gillham, and A. Foggo. 2006. Impact 

of fish farms on maërl beds in strongly tidal areas. Marine Ecology Progress 

Series, 326:1–9. http://dx.doi.org/10.3354/meps326001.

Harvey, A. S., and W. J. Woelkerling. 2007. A guide to nongeniculate coralline red 

algal (Corallinales, Rhodophyta) rhodolith identification. Ciencias Marinas,

33:411–426.

Harvey, A. S., W. J. Woelkerling, T. Farr, K. Neill, and W. Nelson. 2005. Coralline Algae of Central New Zealand: An Identification Guide to Common ‘Crustose’ 

Species. Wellington, New Zealand: NIWA. 

Henrich, R., A. Freiwald, A. Wehrmann, P. Schafer, C. Samtleben and H. Zankl. 

1996. Nordic cold water carbonates: Occurrence and controls. In Global and 

Regional Controls on Biogenic Sedimentation, ed. J. Reitner, F. Neuweiler, 

and F. Gunkel, pp. 35–53. Gottingen, Germany: Gottinger Arbeiten Geologie und Paläontologie.

Hily, C., P. Potin, and J.-Y. Floc’h. 1992. Structure of subtidal algal assemblages on 

soft-bottom sediments: Fauna/flora interactions and role of disturbances in 

the Bay of Brest, France. Marine Ecology Progress Series, 85:115–130. http://

dx.doi.org/10.3354/meps085115.

Hinojosa-Arango, G., and R. Riosmena-Rodríguez. 2004. Influence of rhodolithforming species and growth form on associated fauna of rhodolith beds in the 

central west Gulf of California, Mexico. Marine Ecology, 25:109–127. http://

dx.doi.org/10.1111/j.1439-0485.2004.00019.x.

Jackson, C. M., N. A. Kamenos, P. G. Moore, and M. Young. 2004. Meiofaunal bivalves in maërl and other substrata: Their diversity and community structure. 

Ophelia, 58:49–60. http://dx.doi.org/10.1080/00785236.2004.10410212.

Jacquotte, R. 1962. Etude des fonds de maërl de Mediterranee. Recueil des Travaux 

de la Station Marine D’Endoume, Bulletin, 26:143–235.

James, D. W. 2000. Diet, movement, and covering behavior of the sea urchin Toxopneustes roseus in rhodolith beds in the Gulf of California, Mexico. Marine 

Biology, 137:913–923. http://dx.doi.org/10.1007/s002270000423.

James, D. W., M. S. Foster, and J. O’Sullivan. 2006. Bryoliths (Bryozoa) in the Gulf 

of California. Pacific Science, 60:117–124. http://dx.doi.org/10.1353/psc

.2005.0057.

Jokiel, P. L., K. S. Rodgers, I. B. Kuffner, A. J. Andersson, E. F. Cox, and F. T. Mackenzie. 2008. Ocean acidification and calcifying reef organisms: A mesocosm investigation. Coral Reefs, 27:473–483. http://dx.doi.org/10.1007/s00338-008

-0380-9.

Kamenos, N. A. 2010. North Atlantic summers have warmed more than winters 

since 1353 and the response of marine zooplankton. Proceedings of the National Academy of Sciences, 107:22442–22447. http://dx.doi.org/10.1073

/pnas.1006141107.

Kamenos, N. A., P. Calosi, and P. G. Moore. 2006. Substratum-mediated heart rate 

responses of an invertebrate to predation threat. Animal Behaviour, 71:809–

813. http://dx.doi.org/10.1016/j.anbehav.2005.05.026.

Kamenos, N. A., M. Cusack, T. Huthwelker, P. Lagarde, and R. E. Scheibling. 2009. 

Mg-lattice associations in red coralline algae. Geochimica et Cosmochimica 

Acta, 73:1901–1907. http://dx.doi.org/10.1016/j.gca.2009.01.010.

Kamenos, N. A., M. Cusack, and P. G. Moore. 2008. Red coralline algae are global 

paleothermometers with bi-weekly resolution. Geochimica et Cosmochimica 

Acta, 72:771–779. http://dx.doi.org/10.1016/j.gca.2007.11.019.

Kamenos, N. A., and A. Law. 2010. Temperature controls on coralline algal skeletal growth. Journal of Phycology, 46:331–335. http://dx.doi.org/10.1111/j

.1529-8817.2009.00780.x.

Kamenos, N. A., P. G. Moore, and J. M. Hall-Spencer. 2004a. Nursery-area function 

of maërl grounds for juvenile queen scallops Aequipecten opercularis and 

other invertebrates. Marine Ecology Progress Series, 274:183–189. http://dx

.doi.org/10.3354/meps274183.

———. 2004b. Attachment of the juvenile queen scallop (Aequipecten opercularis

L.) to maërl in mesocosm conditions; juvenile habitat selection. Journal of 

Experimental Marine Biology and Ecology, 306:139–155. http://dx.doi.org

/10.1016/j.jembe.2003.10.013.

———. 2004c. Maërl grounds provide both refuge and high growth potential for 

juvenile queen scallops (Aequipecten opercularis L.). Journal of Experimental Marine Biology and Ecology, 313:241–254. http://dx.doi.org/10.1016/j

.jembe.2004.08.007.

Keegan, B. F. 1974. The macrofauna of maërl substrates on the west coast of Ireland. Cahiers de Biologie Marine, 4:513–530.

Keegan, B. F., and G. Konnecker. 1973. In situ quantitative sampling of benthic 

organisms. Helgolander Wissenschaftliche Meeresuntersuchungen, 24:256–

263. http://dx.doi.org/10.1007/BF01609516.

Kempf, M. 1970. Notes on the benthic bionomy of the N-NE Brazilian Shelf. Marine Biology, 5: 213–224. http://dx.doi.org/10.1007/BF00346909.

Kleypas, J. A., R. A. Feely, V. J. Fabry, C. Langdon, C. L. Sabine, and L. L. Robbins. 

2006. Impacts of ocean acidification on coral reefs and other marine calcifers: 

A guide for future research. Seattle: NOAA/Pacific Marine Environmental 

Laboratory.

Konar, B., R. Riosmena-Rodríguez, and K. Iken. 2006. Rhodolith bed: A newly 

discovered habitat in the North Pacific Ocean. Botanica Marina, 49:355–359. 

http://dx.doi.org/10.1515/BOT.2006.044.

Kuffner, I. B., A. J. Andersson, P. L. Jokiel, K. S. Rodgers, and F. T. Mackenzie. 2007. 

Decreased abundance of crustose coralline algae due to ocean acidification. 

Nature Geoscience, 1:114–117. http://dx.doi.org/10.1038/ngeo100.

Lavrado, H. P. 2006. Caracterização do ambiente e da comunidade bentônica. In 

Biodiversidade da costa central da zona econômica exclusiva brasileira, ed. 

H. P. Lavrado and B. L. Ignácio, pp. 19–66. Rio de Janeiro: Museu Nacional.

Leão, Z. M., and R. N. Ginsburg. 1997. Living reefs surrounded by siliciclastic sediments: The Abrolhos coastal reefs, Bahia, Brazil. Proceedings of the eighth 

International Coral Reef Symposium, 2:1767–1772. 

Leliaert, F., C. Boedeker, V. Peña, F. Bunker, H. Verbruggen, and O. De Clerck. 2009. 

Cladophora rhodolithicola sp. Nov. (Cladophorales, Chlorophyta), a diminutive species from European maërl beds. European Journal of Phycology, 

44:155–169. http://dx.doi.org/10.1080/09670260802573113.

Lemoine, M. 1930. Les Corallinacées de l’archipel des Galapagos et du Golfe de 

Panama. Archives du Muséum National d’Histoire Naturelle, Paris, séries, 

6, 4:37–88. 

Lieberman, M., D. M. John, and D. Lieberman. 1979. Ecology of subtidal algae on 

seasonally devastated cobble substrates off Ghana. Ecology, 60:1151–1161. 

http://dx.doi.org/10.2307/1936963.

Littler, M. M. 1971. Tenarea tesselatum (Lemoine) Littler comb. nov., an unusual 

crustose coralline (Rhodophyceae, Cryptonemiales) from Hawaii. Phycologia, 10:355–359. http://dx.doi.org/10.2216/i0031-8884-10-4-355.1.

Littler, M. M., D. S. Littler, S. M. Blair, and J. N. Norris. 1985. Deepest known plant 

life discovered on an uncharted seamount. Science, 227:57–59. http://dx.doi

.org/10.1126/science.227.4682.57.

Littler, M. M., D. S. Littler, and M. D. Hanisak. 1991. Deep-water rhodolith distribution, productivity, and growth history at sites of formation and subsequent 

degradation. Journal of Experimental Marine Biology and Ecology, 150:163–

182. http://dx.doi.org/10.1016/0022-0981(91)90066-6.

Marrack, E. 1999. The relationship between water motion and living rhodolith 

beds in the southwestern Gulf of California, Mexico. Palaios, 14:159–171. 

http://dx.doi.org/10.2307/3515371.

Milliman, J. D. 1977. Role of calcareous algae in Atlantic continental margin segmentation. In Fossil algae, ed. E. Flugel, pp. 232–247. Berlin: Springer-Verlag. 

http://dx.doi.org/10.1007/978-3-642-66516-5_26.

Milliman, J. D., and C. A. B. Amaral. 1974. Economic potential of Brazilian continental margin sediments. Anais do Congresso Brasieiro de Geologia, 28:335–

344.

Moberly, R. J. 1968. Composition of magnesian calcites of algal and pelecypods 

by electron microprobe analysis. Sedimentology, 11:61–82. http://dx.doi.org

/10.1111/j.1365-3091.1968.tb00841.x.

Norris, J. N. 2010. Marine algae of the Northern Gulf of California: Chlorophyta 

and Phaeophyceae. Smithsonian Contributions to Botany, No. 94. Washington, D.C.: Smithsonian Institution Scholarly Press.

Peña, V., W. Adey, R. Riosmena-Rodríguez, H. G. Choi, J. Afonso-Carrillo, and 

I. Bárbara. 2011. Mesophyllum sphaericum sp. nov. (Corallinales, Rhodophyta): A new maërl-forming species from the NE Atlantic. Journal of Phycology, 47(4):911–927. http://dx.doi.org/10.1111/j.1529-8817.2011.01015.x.

Peña, V., and I. Bárbara. 2010. Seasonal patterns in the maërl community of shallow European Atlantic beds and their use as baseline for monitoring studies. European Journal of Phycology, 45:327–342. http://dx.doi.org/10.1080

/09670261003586938.
number 39 • 155

Rahimpour-Bonab, H., Y. Bone, R. Moussavi-Harami, and K. Turnbull. 1997. 

Geochemical comparisons of modern cool-water calcareous biota, Lacepede 

Shelf, south Australia. Society for Sedimentary Geology, Special Publication, 

56:77–92.

Riosmena-Rodríguez, R., D. L. Steller, G. Hinojosa-Arango, and M. S. Foster. 2010. 

Reefs that rock and roll: Biology and conservation of rhodolith beds in the Gulf 

of California. In Marine biodiversity and conservation in the Gulf of California, ed. R. Brusca, pp. 49–71. Tucson, Ariz.: University of Arizona Press.

Riosmena-Rodríguez, R., W. J. Woelkerling, and M. S. Foster. 1999. Taxonomic reassessment of rhodolith-forming species of Lithophyllum (Corallinales, Rhodophyta) in the Gulf of California, México. Phycologia, 38:401–417. http://

dx.doi.org/10.2216/i0031-8884-38-5-401.1.

Riul, P., P. Lacouth, P. R. Pagliosa, M. L. Christoffersen, and P. A. Horta. 2009. 

Rhodolith beds at the easternmost extreme of South America: Community 

structure of an endangered environment. Aquatic Botany, 90:315–320. http://

dx.doi.org/10.1016/j.aquabot.2008.12.002.

Schaeffer, T. N., G. J. Smith, M. S. Foster, and A. DeTomaso. 2002. Genetic differences between two growth-forms of Lithophyllum margaritae (Rhodophyta) 

in Baja California Sur, México. Journal of Phycology, 38:1090–1098. http://

dx.doi.org/10.1046/j.1529-8817.2002.01108.x.

Schwarz, A. M., I. Hawes, N. Andrew, S. Mercer, V. Cummings, and S. Thrush. 

2005. Primary production potential of non-geniculate coralline algae at Cape 

Evans, Ross Sea, Antarctica. Marine Ecology Progress Series, 294:131–140. 

http://dx.doi.org/10.3354/meps294131.

Setchell, W. A. 1893. On the classification and geographical distribution of the 

Laminariaceae. Transactions of the Connecticut Academy of Arts and Sciences, 9:333–375. 

Steller, D. L., and C. Caceras-Martinez. 2009. Coralline algal rhodoliths enhance 

larval settlement and early growth of the Pacific calico scallop Argopecten 

ventricosus. Marine Ecology Progress Series, 396:49–60. http://dx.doi.org/10

.3354/meps08261.

Steller, D. L., and M. S. Foster. 1995. Environmental factors influencing distribution 

and morphology of rhodoliths in Bahía Concepción, B.C.S., México. Journal 

of Experimental Marine Biology and Ecology, 194:201–212. http://dx.doi

.org/10.1016/0022-0981(95)00086-0.

Steller, D. L., M. S. Foster, and R. Riosmena-Rodríguez. 2007. Sampling and 

monitoring rhodolith beds. In Sampling biodiversity in coastal communities: NaGISA protocols for seagrass and macroalgal habitats, ed. P. R. Rigby, 

K. Iken, and Y. Shirayama, pp. 93–97. Kyoto: Kyoto University Press.

Steller, D. L., R. Riosmena-Rodriguez, M. S. Foster, and C. A. Roberts. 2003. Rhodolith bed diversity in the Gulf of California: The importance of rhodolith 

structure and consequences of disturbance. Aquatic Conservation: Marine 

and Freshwater Ecosystems, 13:S5–S20. http://dx.doi.org/10.1002/aqc.564.

Thouzeau, G. 1991. Experimental collection of postlarvae of Pecten maximus (L.) 

and other benthic macrofaunal species in the Bay of Saint-Brieuc, France. 

I. Settlement patterns and biotic interactions among the species collected. 

Journal of Experimental Marine Biology and Ecology, 148:159–180. http://

dx.doi.org/10.1016/0022-0981(91)90080-G.

Verheij, E. 1993. The genus Sporolithon (Sporolithaceae fam. nov., Corallinales, 

Rhodophyta) from the Spermonde Archipelago, Indonesia. Phycologia, 32: 

184–196. http://dx.doi.org/10.2216/i0031-8884-32-3-184.1.

Veron, J. E. N. 1995. Corals in space and time: The biogeography and evolution of 

the Scleractinia. Sydney: University of New South Whales Press.

Villas-Boas, A. B., R. Riosmena-Rodríguez, G. M. Amado-Filho, G. W. Maneveldt, 

and M. Figueiredo. 2009. Taxonomy of rhodolith-forming species of Lithophyllum (Corallinales; Rhodophyta) from Espírito Santo State, Brazil. Phycologia, 48:237–248. http://dx.doi.org/10.2216/08-35.1.

Weber-van Bosse, A. 1904. Corallineae verae of the Malay Archipelago. In The Corallinaceae of the Siboga Expedition, Siboga-Expeditie LXI, ed. A. Weber-van 

Bosse and M. Foslie, pp. 78–110. Leiden, Germany: E. J. Brill.

Weber-van Bosse, A., and M. Foslie, eds. 1904. The Corallinaceae of the Siboga 

Expedition. Siboga-Expeditie LXI. Leiden, Germany: E. J. Brill.

Woelkerling, W. J. 1988. The coralline red algae: An analysis of the genera and subfamilies of nongeniculate Corallinaceae. New York: Oxford University Press. 

Woelkerling, W. J., and M. S. Foster. 1989. A systematic and ecographic account 

of Synarthrophyton schielianum sp. nov. (Corallinaceae, Rhodophyta) from 

the Chatham Islands. Phycologia, 28:39–60. http://dx.doi.org/10.2216/i0031

-8884-28-1-39.1.

Woelkerling, W. J, G. Gustavsen, H. E. Myklebost, T. Presto, and S. Såstad. 2005. 

The Coralline Red Algal Herbarium of Mikael Foslie: Revised Catalogue with 

Analyses. Trondheim, Norway: Museum of Natural History and Archaeology, Norwegian University of Science and Technology. 

How Scuba Changed Our Understanding 

of Nature: Underwater Breakthroughs 

in Reef Fish Ecology

Mark H. Carr, Daniel P. Malone, Mark A. Hixon, Sally J. 

Holbrook, and Russell J. Schmitt

ABSTRACT. The development of the self-contained underwater breathing apparatus (scuba) in the 

mid-twentieth century provided ecologists with unprecedented access to reef fishes and their ecosystems. These studies fostered major advances in our understanding of tropical and temperate reef 

fishes through comparisons of disparate systems to identify common ecological and evolutionary 

threads, and through the integration of processes across multiple levels of biological organization. 

For each of these levels (individuals, populations, communities, and entire ecosystems) we describe 

the diversity of research approaches enabled by scuba, the insights they generated, and the resulting 

conceptual contributions to ecology and evolution. Much of the research described here has direct 

and valuable application to management and policy decisions for fisheries and conservation of reef 

species and ecosystems. 

INTRODUCTION

The use of scuba has had such a profound impact on our understanding of the ecology of reef fishes at all levels of biological organization that it is difficult to imagine what 

the state of our understanding would be without it. For many decades, fish assemblages 

associated with shallow reef ecosystems have attracted the attention of ecologists because 

of their natural beauty, great species diversity, economic and cultural importance for both 

consumptive (e.g., fisheries) and nonconsumptive (e.g., tourism) uses, and importantly, 

relative accessibility for conducting ecological experiments and long-term observational 

studies. The adoption of scuba has allowed researchers to observe how individual and 

populations of fishes interact with one another and their environment, to conduct complex experiments, and to deploy and maintain in situ sampling devices (e.g., larval collectors, video systems, oceanographic equipment). Scuba is largely responsible for the great 

advances achieved in the ecology of marine reef fishes. Because scuba has become such a 

cost effective and ubiquitous research tool, observational and experimental studies can 

be conducted across a broad range of spatial (up to hundreds of km) and temporal (up 

to decades) scales. Indeed, the vast majority of publications on the ecology of reef fishes 

over the past several decades has been either empirical studies that employed scuba or 

theoretical work that has been informed by scuba-based studies.

Scientific contributions to our understanding of the environmental, evolutionary, 

and ecological processes that shape the diverse ecological systems of the natural world 

Mark H. Carr and Daniel P. Malone, Department of Ecology and Evolutionary Biology, 

Long Marine Laboratories, 100 Shaffer Road, 

University of California, Santa Cruz, California 

95060, USA. Mark A. Hixon, Department of 

Biology, University of Hawai’i, Honolulu, Hawaii 96822, USA. Sally J. Holbrook and Russell J. Schmitt, Department of Ecology, Evolution & Marine Biology, University of California, 

Santa Barbara, Santa Barbara, California 93106, 

USA. Correspondence: M. Carr, carr@biology

.ucsc.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
158 • smithsonian contributions to the marine sciences

have benefited from two fundamental approaches. The first is the 

comparative approach that contrasts ecological and evolutionary processes in different environments (e.g., tropical vs. temperate forest and reef systems) to derive fundamental insights 

into processes (e.g., biotic vs. abiotic determinants of community 

structure) that underscore the structural (e.g., biodiversity) and 

functional (e.g., nutrient cycling) attributes of ecosystems. This 

approach also can involve application of understanding achieved 

in one ecosystem to a wide range of others. Fish assemblages 

associated with tropical coral reefs and temperate rocky reefs 

have been a focus of ecological investigation not only to better understand those particular species and ecosystems, but also 

to gain insights into broader ecological principles. Indeed, such 

fundamental ecological concepts as open populations, recruitment limitation, lottery models, and the mechanisms of density 

dependence and population regulation generated by studies of 

reef fishes have been applied across marine, freshwater, and terrestrial ecosystems.

The second fundamental approach to ecological understanding entails the investigation and integration of processes 

acting at multiple levels of biological organization: individuals, 

populations, communities, and ecosystems. Studies of individual 

organisms have focused on behavioral and physiological processes that determine growth, survival, reproductive success, 

and other determinants of individual fitness, as well as on a 

variety of population-level attributes (e.g., size and age structure). Such studies reveal the mechanisms governing interactions between individuals and their environment, interactions 

with conspecifics and other species, and the scales of space (e.g., 

neighborhood size) and time (e.g., stages of ontogeny) over 

which these interactions occur. Population studies identify the 

mechanisms that determine population distribution, structure, 

and dynamics, which influence the persistence of populations 

and magnitude of interactions with other species in a community. Studies of genetic patterns and diversity reveal past and 

present patterns and scales of natural selection, gene flow, and 

population connectivity. Studies that examine the interactions 

among co-occurring species identify how species interact, the 

strength of interactions, and the unique functional roles of individual species that all contribute to the structure and functions 

of ecological communities. Ecosystem-level investigations reveal 

the collection of interactions among species and their environment that contribute to the integrity, productivity, and dynamics 

(e.g., resiliency) of ecosystems.

Studies of reef fishes have advanced our understanding of 

ecology and evolution by their integration across all these levels 

of organization. For example, factors that influence variation in 

individual fitness have demographic consequences (size, structure, and dynamics) that in turn affect patterns of species interactions (Johnson et al., 2010). The purpose of this brief overview 

is to highlight the myriad ways in which scuba has contributed 

to ecological studies of tropical and temperate reef fishes across 

the various levels of biological organization and to the field of 

ecology as a whole. 

THE ECOLOGY OF INDIVIDUALS

Ecological studies focused on individual fishes have enlightened our understanding of the behavioral and physiological mechanisms that underlie individual performance and fitness 

and of the spatial scale at which individuals interact with their 

environment. In situ observations and experiments have revealed 

how reef fishes perceive and interact with their environment 

(e.g., foraging and resource utilization), how they respond to 

trade-offs between quantity and quality of resources and predation risk, and what the consequences of these responses are for 

habitat use, growth, and reproductive success (e.g., Holbrook 

and Schmitt, 1988a, 1988b). Not only has scuba allowed many 

researchers to spend countless hours over the course of their careers making observations under natural conditions, it has also 

enabled scientists to experimentally manipulate environmental 

conditions (both biological and physical) and quantify behavioral responses and their consequences for individual fitness. Examples of some biological factors that have been manipulated 

include the density, dispersion, distribution, size range, and quality of prey resources; the presence, density, and size distribution 

of predators and competitors; and combinations of resource and 

predator characteristics. Manipulations of prey resources have 

included the deployment of devices that release planktonic prey 

(Forrester, 1990) and the configuration of portable algal habitats 

with associated invertebrate prey (Holbrook and Schmitt, 1984). 

Refuge manipulations include the alteration of algal structure 

(Levin, 1991, 1993; Carr, 1994a, 1994b; Johnson, 2006), the 

addition of artificial refuges (Hixon and Beets, 1993), and the 

elimination of naturally occurring physical features (cracks and 

crevices). Such experiments have revealed the determinants of 

foraging behavior and habitat use of consumers and how individuals balance the trade-off between the reward of resource acquisition and the risk of mortality with resulting consequences 

(i.e., sublethal effects) on various aspects of individual performance including growth and reproduction. 

Behavioral studies of the reproductive ecology of reef fishes 

have leveraged the great diversity of reproductive modes exhibited by reef fishes and their accessibility for observational and 

experimental studies with scuba. Indeed, coral reef fishes have 

become one of the most prominent model systems for studies of 

reproductive ecology, mating systems, and social structures, as 

evidenced by the expansive literature on these subjects and its 

impact on evolutionary theory (reviewed by Robertson, 1991; 

Shapiro, 1991; Warner, 1991; Petersen and Warner, 2002). Observational studies have described the timing (diel and seasonal; 

Sancho et al., 2000; Gladstone, 2007) of reproduction and the 

location and movements associated with reproductive behavior (e.g., spawning; Domeier and Colin, 1997), and have linked 

these behaviors to environmental cues (e.g., moonlight, tides, 

temperature) and conditions (e.g., ambient light levels, currents) 

that contribute to the successful release and dispersal of larvae. 

Orthogonal manipulations of mate and habitat traits have identified the relative contributions of these cues to spawning success. 
number 39 • 159

Observations of the relative effects of mate attributes (i.e., fish 

size, behavior) and associated habitat attributes (nest size and 

quality) have revealed the determinants of mate choice (Warner, 

1987; Sikkel, 1989). Such studies have also shed light on the relationships between reproductive ecology and social structure, 

including mating systems (e.g., hermaphroditism; Warner and 

Hoffman, 1980; Warner, 1984). 

Research using scuba has contributed greatly to our knowledge of the movement patterns of reef fishes, the environmental 

and ecological determinants of these patterns, and their ecological significance in both tropical and temperate reef ecosystems. 

Scuba has been used widely to describe and quantify movement 

patterns in three primary applications: direct observation of fish 

movement, sighting of tagged individuals, and the use of acoustic 

telemetry equipment. Early studies repeatedly located individually tagged fishes to eventually delimit their home ranges (e.g., 

Larson, 1980; Hixon, 1981; Holbrook and Schmitt, 1986). Diver 

resighting of tagged fishes has facilitated mark-recapture studies of fish movement (Starr et al., 2004). Telemetry studies have 

benefited from scuba by the selective sampling of fishes (e.g., gender, size class) and the deployment and maintenance of arrays 

of acoustic receivers (Holland et al., 1996; Zeller, 1999; Lowe 

and Bray, 2006), thereby allowing intrapopulation differences of 

movement patterns to be ascertained. All of these approaches 

have been complemented by information on biotic (e.g., distribution and density of conspecifics and other species, distribution and composition of corals and macroalgae) and abiotic (e.g., 

geologic composition, relief, and current direction and speed) 

attributes of the reef habitat and used to identify the relative 

importance of these variables in determining movement patterns 

and ranges. Most importantly, scuba has enabled experimental 

manipulations of key biotic and abiotic features to demonstrate 

their causal and interactive effects on patterns and ranges of fish 

movement. 

POPULATION ECOLOGY

Studies of the population ecology of reef fishes have had 

a major influence on our understanding of the relationship between environment, life history, and the distribution, structure, 

and dynamics of populations. Reef fish studies have been a key 

in the development of the concept of open populations, in which 

the dispersal of larvae effectively decouples the relationship between production and replenishment of local populations (Caley 

et al., 1996; Carr and Syms, 2006). This fundamental structure 

of marine populations was revealed by a plethora of studies that 

used scuba to quantify the size of reef-associated fish populations and rates of larval recruitment. From this work emerged 

evidence that the size of a local population can be influenced 

by recruitment limitation—the limitation in supply of larvae 

delivered to a population due to the high mortality larvae experience in the pelagic environment—and the vagaries of ocean 

currents (Doherty, 1981, 1983; Victor, 1983, 1986; reviews by 

Doherty and Williams, 1988; Mapstone and Fowler, 1988; Sale, 

1991; Doherty, 2002). Such observations prompted a great number of empirical studies (both observational and experimental) 

that examined the relative contributions of larval supply versus 

processes acting at settlement and early post-settlement (e.g., 

competition, predation, facilitation) in determining the size and 

dynamics of local populations (Schmitt et al., 1999; Schmitt and 

Holbrook, 2000; Osenberg et al., 2002). Because these processes 

can be density dependent (i.e., rates of growth and survival vary 

with the density of settlers or adults), these studies contributed 

to our understanding of mechanisms for the regulation and persistence of populations (Hixon and Webster, 2002). Studies of 

density dependence further explored the relative and interactive 

effects of competition and predation through a large number of 

complex experiments conducted on both coral and temperate 

rocky reef fishes (e.g., Carr et al., 2002; reviews by Hixon and 

Jones, 2005). Scuba has been instrumental in enabling researchers to conduct multifactorial manipulations of density of recruits, 

competitors, predators, and refuge availability to elucidate the 

interactive effects of these variables on the settlement, growth, 

and survival of young reef fishes, and their ultimate effects on 

population replenishment (Holbrook and Schmitt, 2002; Schmitt 

et al., 2009). Manipulations of fish density and refuge availability have been achieved by the selective removal of individuals on 

natural reefs and by experimentally creating isolated reef habitat 

from natural structures (e.g., corals, shells, rubble, rock, kelps; 

Figure 1a–c) and artificial substrata (e.g., cinder blocks, concrete 

rubble, tubes; Figure 1d–f). Scuba also has enabled ecologists to 

understand how the distribution of predators and refuge from 

predators across landscapes determines the spatial scale of variance in density dependence (Forrester and Steele, 2004; Schmitt 

and Holbrook, 2007).

Having identified the importance of larval recruitment to 

the distribution and dynamics of local reef-associated populations, ecologists investigated the role of larval behavior and 

oceanographic processes in driving variation in larval delivery 

to and settlement in local populations and in contributing to 

geographic variation in population dynamics. Scuba has been 

instrumental in exploring relationships between the spatial and 

temporal variation in larval recruitment and oceanographic 

processes in three key ways. First, scuba-based surveys of larval recruitment through time, within and among reefs, coupled 

with monitoring of local and regional oceanographic processes 

(e.g., tidal currents, upwelling, El Niño, La Niña) enable ecologists to determine the influence of these processes on geographic 

and temporal (seasonal, interannual) variation in larval delivery 

(Schmitt and Holbrook, 2002). Secondly, the efficiency and scale 

of these studies have increased with the development and deployment of larval collectors (e.g., plankton nets, light traps, Standardized Monitoring Units for Recruitment of Fishes [SMURFs]; 

Figure 2a–c) using scuba (e.g., Doherty, 1987; Choat et al., 

1993; Anderson et al., 2002; Caselle et al., 2010, 2011). Finally, 

scuba has been necessary in the deployment and maintenance 

of oceanographic instruments (e.g., swell gauges, current meters, 
160 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 1. Habitat manipulations to create independent isolated experimental treatment levels (e.g., density levels, refuge availability) from 

natural substrata: (A) corals, (B) rock, (C) kelps; and artifi cial substrata: (D) cinder blocks, (E) concrete rubble, (F) tubes. (Photo credits given 

in each image.)
number 39 • 161

thermistors; Figure 3a–c) that resolve oceanographic processes 

(e.g., swell, currents, upwelling) at the spatial scale of individual 

reefs. These studies have identified the importance of local and 

regional variability, including episodic events occurring within 

(e.g., upwelling and relaxation, internal waves) and between 

(e.g., El Niño, La Niña) years, in driving seasonal and interannual variation in reef fish recruitment. 

To determine how larval behavior (e.g., settlement preferences) and variation in habitat types (e.g., different species of 

corals, algae versus rock) contribute to spatial variation in rates 

of larval settlement, ecologists using scuba have measured rates 

of settlement to natural landscapes (reviewed by Leis and McCormick, 2002) and experimental arrays of habitat types (e.g., 

Almany, 2004). These studies demonstrated how aspects of the 

FIGURE 2. Devices for collecting larvae using scuba. (A) Plankton 

nets, (B) light traps, and (C) SMURFs (see text). (Photo credits: A, reprinted from Hobson and Chess, 1976; B, C, as given in each image.)

FIGURE 3. Deployment and maintenance of oceanographic instruments using scuba. (A) Swell gauges, (B) current meters, and (C) 

thermistors. (Photo credits given in each image.)
162 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

local reef habitat could explain variation in settlement rates 

among reefs and how important certain features of reefs are to 

the replenishment of reef fi sh populations. 

Fundamental goals of population genetic studies of reef fi shes 

are to identify individual relatedness, mechanisms of selection, the 

spatial and temporal dynamics of genetic structure, and connectivity of populations via larval dispersal. Scuba has contributed to 

these studies largely through the ability to target individuals at a 

very fi ne scale based on their distribution in space (or habitat), life 

stage, gender, and size. For example, in situ collection of individuals from particular size or age cohorts has allowed determination 

of changes in gene frequencies subsequent to settlement as well as 

identifi cation of intercohort relatedness of social groups (Planes 

et al., 2002; Johnson and Hixon, 2010). Scuba-based sampling 

of adults (using anesthesia, underwater nets, or hook and line 

fi shing; Figure 4a–c) allows researchers to effi ciently and nondestructively sample and characterize geographic patterns of genetic 

dissimilarity, which are used to infer the spatial patterns and scale 

of historic gene fl ow via larval dispersal (Bernardi et al., 2001; 

Leray et al., 2010). In situ collection of recently settled juvenile 

reef fi shes can identify patterns and scales of gene fl ow to estimate dispersal patterns of a single cohort. In combination with 

oceanographic information (e.g., current patterns, productivity), 

patterns of genetic similarity can be linked to the oceanographic 

processes that determine the underlying geographic patterns of 

larval dispersal (Planes, 2002; Bernardi et al., 2003; Almany et 

al., 2007; Christie, 2010; Christie et al., 2010). Collection of individuals using scuba has allowed researchers to repeatedly sample 

cohorts of recently settled reef fi shes through time to determine 

at what stage and under what environmental conditions (habitat 

type, exposure to predators) gene frequencies change and when 

and where natural selection or genetic drift establish patterns of 

local genetic diversity and structure (metapopulations) within 

larger regional populations. Comparisons of juvenile and adult 

genotypes (e.g., parentage analysis) from local populations have 

been used to determine the effect of relatedness on patterns of 

settlement (Avise and Shapiro, 1986), as well as to identify the 

origin location of settled larvae and patterns of larval dispersal 

(Planes, 2002; Almany et al., 2007; Christie et al., 2010).

COMMUNITY ECOLOGY

Ecological studies involving scuba have been particularly 

important in advancing our understanding of the processes that 

structure communities of fi shes on both coral and rocky reefs 

and, by extension, communities of organisms in other marine, 

freshwater, and terrestrial ecosystems. The testing of hypotheses that explain the maintenance of species diversity has been a 

central focus of community ecology. Reef fi sh communities have 

provided highly useful models for such tests and in the process 

have generated several new and infl uential hypotheses. 

One theory for the maintenance of species diversity that has 

been examined by reef fi sh ecologists using scuba is the niche 

diversifi cation hypothesis—that species specialize in order to 

partition available resources and thereby facilitate coexistence. 

FIGURE 4. Methods for collecting reef fi sh using scuba. (A) Hand-netting while using anesthesia (clove oil), (B) BINCKE (Benthic Ichthyofauna 

Net for Coral / Kelp Environments), and (C) hook and line. (Photo credits given in each image.)
number 39 • 163

Scuba studies provided observational and experimental evidence 

for partitioning of habitat and food resources on coral reefs and 

temperate rocky reefs (reviewed by Ross, 1986; Ebeling and 

Hixon, 1991). While testing this theory in an assemblage of damselfishes on coral reefs, Sale (1977) generated the lottery hypothesis. This nonequilibrial hypothesis posits that competing species 

do not partition resources, and that diversity is maintained by 

the random settlement of species within and among reefs. The 

lottery model (versus lottery hypothesis) and storage effect posit 

that changing environmental conditions favoring recruitment 

of each species relative to others maintains coexistence despite 

competitive equality (Warner and Chesson, 1985). Recruitment 

limitation, previously described in relation to population dynamics, has also been cited to explain the coexistence of coral 

reef fishes by preempting competitive exclusion (Doherty, 1983). 

Like the other hypotheses for the maintenance of diversity, the 

recruitment limitation hypothesis was enabled by field studies of 

coral reef fishes using scuba. These hypotheses have since been 

tested in a variety of other systems. Studies of reef fishes have 

also provided evidence of indirect mutualism, whereby a strong 

interspecific competitor can actually promote the coexistence of 

the weaker competitor via indirect positive benefits (Schmitt and 

Holbrook, 2003; Holbrook and Schmitt, 2004). 

In addition to testing hypotheses explaining the maintenance of diversity, reef fish ecologists have used scuba to explore 

the sources of spatial and temporal variation in community 

structure. For example, scuba-based observational and experimental studies of reef fish assemblages have been used to test 

island biogeography theory by comparing diversity among patch 

reefs of varying sizes and isolation (Molles, 1978; Talbot et al., 

1978; Bohnsack, 1979). Reef fish ecology has also contributed 

fundamentally to our understanding of the roles of recruitment, 

competition, predation, and mutualistic relationships in structuring the composition and relative abundance of species in communities. Research on competition has involved the selective 

removal of species on natural reefs as well as manipulation of the 

abundance of species on experimental patch reefs in both coral 

and temperate rocky reef ecosystems (e.g., Carr et al., 2002). 

Similarly, the role of predation in structuring communities has 

been illuminated by the manipulation of predators using isolated 

patch reefs and predator exclusion cages (Figure 5). The number 

of these influential studies is too great to cite (see reviews by 

Hixon, 1991; Hixon and Webster, 2002; Hixon and Jones, 2005; 

Carr and Syms, 2006; Hixon, 2006; Steele and Anderson, 2006). 

In addition to elucidating the consequences of biotic processes, reef fish ecologists have also sought to identify the role 

that environmental factors (particularly disturbance) play in 

the structure and dynamics of reef fish assemblages. Studies 

have capitalized on natural events to study recovery, succession, 

and evidence for alternative stable states of community organization. Examples include the response of fish assemblages to 

storm events (e.g., Ebeling et al., 1985) and climatic variation 

(Stephens et al., 1988; Holbrook et al., 1997). Others include 

the simulated destruction of coral reefs (Syms and Jones, 2000) 

and kelp forests (Bodkin, 1988). Studies designed to identify the 

influence of habitat features on community structure have correlated environmental variables to geographic variation identified 

from scuba surveys of reef fish communities (Williams, 1991; 

MacNeil et al., 2009). 

FIGURE 5. Predator exclusion cages used to study the role of predation in structuring communities. (A) Netting surrounding a patch 

reef to exclude piscivorous reef fish, (B) enclosure placed in the Macrocystis canopy to enclose juvenile rockfish (Sebastes sp.) and exclude their predators, and (C) exclusion cage surrounding a replicate 

unit of natural substrate habitat. (Photo credits given in each image.)
164 • smithsonian contributions to the marine sciences

ECOSYSTEM ECOLOGY

Traditional ecosystem studies focused on understanding 

how energy and nutrients flow through food webs and how interactions between biotic and abiotic components of ecosystems 

determine the pathways and rates of energy and nutrient fluxes. 

Such studies are largely based on defining trophic interactions, 

guilds, and pathways by sampling species diets and rates of key 

ecophysiological processes (production, consumption, and respiration) to parameterize ecosystem models. Scuba studies have 

been fundamental for dietary studies that define species interactions and guilds (e.g., Hiatt and Strasberg [1960] and Randall 

[1967], who extol at length the virtue of underwater observation 

and spear fishing, respectively, for fish diet studies), and for in situ 

collection of fundamental ecophysiological rates. More recently, 

ecologists have focused more on the influences of abiotic drivers (oceanographic, geomorphological) on the productivity and 

structure of fish assemblages and how such variation influences 

both the functional roles of reef fishes and their effects on reef 

ecosystem attributes (e.g., productivity, resiliency). For example, 

several studies have examined or experimentally simulated the 

impact of hurricanes or bleaching events on coral reef systems 

and the subsequent responses of reef fish assemblages (Syms and 

Jones, 2000; Graham et al., 2007). Studies of the influence of 

fishes on other components of reef ecosystems (invertebrates and 

algae) have included both direct (e.g., herbivory, predation) and 

indirect (e.g., bioerosion, trophic cascades) trophic interactions 

(Williams, 1980). For example, Bray et al. (1981) quantified the 

increased availability of nitrogen and rate of macroalgal production in cracks and crevices occupied at night by the planktivorous temperate damselfish Chromis punctipinnis, thereby 

demonstrating the role of planktivorous reef fishes in linking 

pelagic and benthic production in reef ecosystems. Other studies have demonstrated the importance of herbivory in maintaining coral abundance and diversity (Hughes et al., 1987; Choat, 

1991; Hay 1991). Similarly, a substantial body of literature 

based on observational and experimental studies using scuba has 

documented the effects of reef fishes on the distribution, species 

composition, and diversity of invertebrate assemblages (reviewed 

by Jones et al., 1991). More recently, studies have demonstrated 

cascading effects of fish predation on herbivores and resulting 

indirect effects on rates of algal production (Davenport and Anderson, 2007; Perez-Matus and Shima, 2010) and other lower 

trophic levels. How these functional roles of reef fishes contribute to the resiliency of coral and temperate rocky reef ecosystems 

(e.g., Hughes, 1994; Bellwood et al., 2004), especially in the face 

of climate change and other perturbations, is a critical research 

direction (McLeod et al., 2009).

APPLIED ECOLOGY

Much of the research described here has direct and valuable application to management and policy decisions for fisheries 

and conservation of reef species and ecosystems. Among the benefits gained using scuba to study reef fishes is the greater spatial 

resolution of population data for stock assessments, including 

unprecedented opportunity to generate estimates of natural mortality using tagging-and-resighting approaches and of size structure (the relative proportion of small and large individuals) using 

nondestructive visual census techniques. Data generated by these 

studies have been used to document population impacts, especially on hermaphroditic species, of selective fishing techniques 

and the resultant consequences on progeny quantity and quality 

for the fished populations. Similarly, surveys of larval recruitment 

produce time series required to identify oceanographic drivers 

of recruitment variation and predictions of year-class strength. 

The breadth of species surveyed by divers includes fished and 

nonfished species and can identify how the fish assemblage as a 

whole (as well as other species in reef ecosystems) responds to 

the removal of fished species (Stallings, 2008). Knowledge of the 

ecosystem-wide effects of fishing is critical for developing strategies that go beyond single-species management and is essential 

for ecosystem-based fisheries management.

One key tool for ecosystem-based management and conservation is the development of networks of marine protected areas 

(MPAs), including marine reserves (e.g., Murray et al., 1999; 

Gaines et al., 2010). These areas provide critical reference sites 

to compare with fished areas to identify population-level and 

ecosystem-wide effects of fishing, as well as social, cultural, and 

nonconsumptive services. Surveys and research conducted with 

scuba enable nondestructive sampling approaches that can assist 

in evaluating how effective MPAs are at protecting reef-associated species and ecosystems from the effects of fishing. Monitoring programs inside and outside MPAs designed in conjunction 

with oceanographic monitoring programs can track ecosystem 

responses to a changing ocean climate and identify the interactive effects of fishing and climate change on the productivity and 

resiliency of reef ecosystems (Ling et al., 2009; Carr et al., 2010). 

FUTURE DIRECTIONS

One fundamental direction in ecology is the rapidly developing field of spatial ecology. Central to our understanding of 

patterns and processes at all levels of biological organization is 

improved understanding of the spatial scales at which ecological processes occur (e.g., interactions between organisms and 

between organisms and their environment). Similarly, the configuration of habitat in a coastal ocean “landscape” modifies the 

distribution and strength of ecological processes. Knowledge of 

the relationships between habitat configuration and these processes is critical to our understanding of how these processes 

vary spatially and their effects on the structure and dynamics of 

metapopulations and metacommunities. The current scarcity of 

studies that have utilized GPS to georeference the location of divers as they collect data, especially in structurally complex habitats (e.g., kelp forests), is a crucial impediment to advancing the 
number 39 • 165

spatial ecology of reef ecosystems and linking ecological data 

with the rapid generation of high resolution seafloor maps. This 

problem is arguably the greatest hindrance to subtidal ecology 

relative to recent advances in freshwater and terrestrial ecology.

Another fundamental hindrance is the paucity of coordinated, large-scale, long-term, multidisciplinary (i.e., ecological, 

physiological, genetic, and oceanographic) monitoring studies for 

understanding the geographic and long-term scales of variation in 

dynamics of reef ecosystems. Models for the development of such 

geographically integrated programs include the U.S. National Science Foundation’s Long-Term Ecological Research (LTER) program and the Partnership for Interdisciplinary Studies of Coastal 

Oceans (PISCO). These programs provide not only information 

fundamental to advancing our understanding of tropical and temperate reef ecosystems, but also information applicable to ecosystem-based management, including how reef ecosystems and their 

services respond to a changing global climate. 

Despite these challenges, it is clear that scuba-based research 

has contributed critically to many major advances in the ecology 

of tropical and temperate reef fishes at all levels of biological 

organization, from genes to ecosystems. Many of these conceptual advances, such as the understanding of ecological processes 

that maintain biodiversity and their influence on the resiliency 

of ecosystems, have been so fundamental that they have shed 

light on the function of ecosystems in general, including those 

in terrestrial and freshwater settings. Based on the rich history 

of contributions and the growing number of research programs 

involving scuba, the advancement of both basic and applied marine and ecological research through scuba is certain to continue 

at an ever faster pace. The opportunities that scuba provides for 

scientists to observe reef fishes and their environments firsthand 

have had profound results that reinforce the importance of 

training future generations of scientists in the use and applications of scuba, and in doing so safely, through programs like the 

American Association of Underwater Scientists (AAUS). With 

continued advances in scuba and associated technology, scientific 

breakthroughs in these ecologically and economically important 

marine ecosystems are limited by only our intellectual curiosity 

and scientific creativity. 

ACKNOWLEDGMENTS

This article benefited from valuable critique and recommendations offered by anonymous reviewers, to whom we express 

our appreciation. The authors express their deep gratitude to 

the National Science Foundation, the David and Lucile Packard 

Foundation, the Gordon and Betty Moore Foundation, Conservation International, National Geographic Society, the W. M. 

Keck Foundation, and the National Oceanic and Atmospheric 

Administration’s National Undersea Research Program. Without their relentless support of scuba-based research, many of the 

advances and discoveries described here would not have been 

possible.

We dedicate this paper to the memory of Conrad “Connie” 

Limbaugh, whose pioneering efforts studying temperate and 

tropical reef fishes with scuba led so many of us to follow after 

him. His great impact on the field of reef fish ecology will be appreciated always and never forgotten.

REFERENCES

Almany, G. R. 2004. Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia,

141:105–113. http://dx.doi.org/10.1007/s00442-004-1617-0.

Almany, G. R., M. L. Berumen, S. R. Thorrold, S. Planes, and G. P. Jones. 2007. Local replenishment of coral reef fish populations in a marine reserve. Science,

316:742–744. http://dx.doi.org/10.1126/science.1140597.

Anderson, T. W., C. T. Bartels, M. A. Hixon, E. Bartels, M. H. Carr, and J. Shenker. 

2002. Current velocity and catch efficiency in sampling settlement-stage larvae of coral-reef fishes. Fishery Bulletin, 100:404–413.

Avise, J. C., and D. Y. Shapiro. 1986. Evaluating kinship of newly settled juveniles 

within social groups of the coral reef fish Anthias squamipinnis. Evolution,

40:1051–1059. http://dx.doi.org/10.2307/2408763.

Bellwood, D. R., T. P. Hughes, C. Folke, and M. Nyström. 2004. Confronting the 

coral reef crisis. Nature, 429:827–833. http://dx.doi.org/10.1038/nature02691.

Bernardi, G., S. J. Holbrook, and R. J. Schmitt. 2001. Gene flow at three spatial 

scales in a coral reef fish, the three-spot dascyllus, Dascyllus trimaculatus. 

Marine Biology, 138:457–465. http://dx.doi.org/10.1007/s002270000484.

Bernardi, G., S. J. Holbrook, R. J. Schmitt, and N. L. Crane. 2003. Genetic evidence 

for two distinct clades in a French Polynesian population of the coral reef 

three-spot damselfish Dascyllus trimaculatus. Marine Biology, 143:485–490. 

http://dx.doi.org/10.1007/s00227-003-1091-y.

Bodkin, J. L. 1988. Effects of kelp forest removal on associated fish assemblages 

in central California. Journal of Experimental Marine Biology and Ecology,

117:227–238. http://dx.doi.org/10.1016/0022-0981(88)90059-7.

Bohnsack, J. A. 1979. The ecology of reef fishes on isolated coral heads: An experimental approach with an emphasis on island biogeography theory. Ph.D. 

diss., University of Miami, Florida.

Bray, R. N., A. C. Miller, and G. G. Geesey. 1981. The fish connection: A trophic 

link between planktonic and rocky reef communities? Science, 214:204–205. 

http://dx.doi.org/10.1126/science.214.4517.204.

Caley, M. J., M. H. Carr, M. A. Hixon, T. P. Hughes, G. P. Jones, and B. A. Menge. 

1996. Recruitment and the local dynamics of open marine populations. Annual Review of Ecology and Systematics, 27:477–500. http://dx.doi.org/10

.1146/annurev.ecolsys.27.1.477.

Carr, M. H. 1994a. Effects of macroalgal dynamics on recruitment of a temperate 

reef fish. Ecology, 75:1320–1333. http://dx.doi.org/10.2307/1937457.

———. 1994b. Predicting recruitment of temperate reef fishes in response to 

changes in macrophyte density caused by disturbance. In Theory and application in fish feeding ecology, ed. D. J. Stouder, K. L. Fresh, and R. J. Feller, pp. 

255–269. Columbia, S.C.: University of South Carolina Press.

Carr, M. H., T. W. Anderson, and M. A. Hixon. 2002. Biodiversity, population regulation, and the stability of coral-reef fish communities. Proceedings of the 

National Academy of Sciences, 99:11241–11245. http://dx.doi.org/10.1073

/pnas.162653499.

Carr, M. H., and C. Syms. 2006. Recruitment. In The ecology of marine fishes: California and adjacent waters, ed. L. G. Allen, D. J. Pondella II, and M. H. Horn, 

pp. 411–427. Berkeley: University of California Press.

Carr, M. H., C. B. Woodson, O. M. Cheriton, D. Malone, M. A. McManus, and 

P. T. Raimondi. 2010. Knowledge through partnerships: Integrating marine 

protected area monitoring and ocean observing systems. Frontiers in Ecology 

and the Environment, http://dx.doi.org/10.1890/090096.

Caselle, J. E., M. H. Carr, D. P. Malone, J. R.Wilson, and D. E. Wendt. 2010. Can we 

predict interannual and regional variation in delivery of pelagic juveniles to 

nearshore populations of rockfishes (genus Sebastes) using simple proxies of 

ocean conditions? CalCOFI Reports, 51:191–205.

Caselle, J. E., S. L. Hamilton, D. M. Schroeder, M. S. Love, J. D. Standish, J. A. RosalesCasian, and O. Sosa-Nishizaki. 2011. Geographic variation in density, demography, and life history traits of a harvested, sex-changing, temperate reef fish. 

Canadian Journal of Fisheries and Aquatic Sciences, 68 (2):288–303.
166 • smithsonian contributions to the marine sciences

Choat, J. H. 1991. The biology of herbivourous fishes on coral reefs. In The ecology 

of fishes on coral reefs, ed. P. F. Sale, pp. 120–155. San Diego: Academic Press.

Choat, J. H., P. J. Doherty, B. A. Kerrigan, and J. M. Leis. 1993. A comparison of 

towed nets, purse seine, and light-aggregation devices for sampling larvae and 

pelagic juveniles of coral reef fishes. Fishery Bulletin, 91:195–209.

Christie, M. R. 2010. Parentage in natural populations: Novel methods to detect 

parent–offspring pairs in large data sets. Molecular Ecology Resources,

10:115–128. http://dx.doi.org/10.1111/j.1755-0998.2009.02687.x.

Christie, M. R., D. W. Johnson, C. D. Stallings, and M. A. Hixon. 2010. Self-recruitment 

and sweepstakes reproduction amid extensive gene flow in a coral-reef fish. 

Molecular Ecology, 19:1042–1057. http://dx.doi.org/10.1111/j.1365-294X

.2010.04524.x.

Davenport, A. C., and T. W. Anderson. 2007. Positive indirect effects of reef fishes 

on kelp performance: The importance of mesograzers. Ecology, 88:1548–

1561. http://dx.doi.org/10.1890/06-0880.

Doherty, P. J. 1981. Coral reef fishes: Recruitment-limited assemblages? Proceedings of the fourth International Coral Reef Symposium, 2:465–470.

———. 1983. Tropical territorial damselfishes: Is density limited by aggression or 

recruitment? Ecology, 64:176–190. http://dx.doi.org/10.2307/1937339.

———. 1987. Light traps: Selective but useful devices for quantifying the distributions and abundances of larval fishes. Bulletin of Marine Science, 41:423–431.

———. 2002. Variable replenishment and the dynamics of reef fish populations. 

In Coral reef fishes: Dynamics and diversity in a complex ecosystem, ed. P. F. 

Sale, pp. 327–355. San Diego: Academic Press.

Doherty, P. J., and D. M. Williams. 1988. The replenishment of coral reef fish populations. Oceanography and Marine Biology Annual Review, 26:487–551.

Domeier, M. L., and P. L. Colin. 1997. Tropical reef fish spawning aggregations: 

Defined and reviewed. Bulletin of Marine Science, 60:698–726.

Ebeling, A. W., and M. A. Hixon. 1991. Tropical and temperate reef fishes: Comparison of community structures. In The ecology of fishes on coral reefs, ed. 

P. F. Sale, pp. 509–563. San Diego: Academic Press.

Ebeling, A. W., D. R. Laur, and R. J. Rowley. 1985. Severe storm disturbances and 

reversal of community structure in a southern California kelp forest. Marine 

Biology, 84:287–294. http://dx.doi.org/10.1007/BF00392498.

Forrester, G. E. 1990. Factors influencing the juvenile demography of a coral reef 

fish. Ecology, 71:1666–1681. http://dx.doi.org/10.2307/1937576.

Forrester, G. E., and M. A. Steele. 2004. Predators, prey refuges, and the spatial 

scaling of density-dependent prey mortality. Ecology, 85:1332–1342. http://

dx.doi.org/10.1890/03-0184.

Gaines, S. D., C. White, M. H. Carr, and S. R. Palumbi. 2010. Designing marine 

reserve networks for both conservation and fisheries management. Proceedings of the National Academy of Sciences, 107:18286–18293. http://dx.doi

.org/10.1073/pnas.0906473107.

Gladstone, W. 2007. Temporal patterns of spawning and hatching in a spawning 

aggregation of the temperate reef fish Chromis hypsilepis (Pomacentridae). Marine Biology, 151:1143–1152. http://dx.doi.org/10.1007/s00227-006-0555-2.

Graham, N. A. J., S. K. Wilson, S. Jennings, N. V. C. Polunin, J. Robinson, J. P. 

Bijoux, and T. M. Daw. 2007. Lag effects in the impacts of mass coral bleaching on coral reef fish, fisheries, and ecosystems. Conservation Biology, 21(5): 

1291–1300.

Hay, M. E. 1991. Fish–seaweed interactions on coral reefs: Effects of herbivorous 

fishes and adaptations of their prey. In The ecology of fishes on coral reefs, ed. 

P. F. Sale, pp. 96–119. San Diego: Academic Press.

Hiatt, R. W., and D. W. Strasburg. 1960. Ecological relationships of the fish fauna 

on coral reefs of the Marshall Islands. Ecological Monographs, 30:65–127. 

http://dx.doi.org/10.2307/1942181.

Hixon, M. A. 1981. An experimental analysis of territoriality in the California 

reef fish Embiotoca jacksoni (Embiotocidae). Copeia, 1981:653–665. http://

dx.doi.org/10.2307/1444571.

———. 1991. Predation as a process structuring coral reef fish communities. In 

The ecology of fishes on coral reefs, ed. P. F. Sale, pp. 475–508. San Diego: 

Academic Press.

———. 2006. Competition. In The ecology of marine fishes: California and adjacent waters, ed. L. G. Allen, D. J. Pondella II, and M. H. Horn, pp. 449–465. 

Berkeley: University of California Press.

Hixon, M. A., and J. P. Beets. 1993. Predation, prey refuges, and the structure of 

coral-reef fish assemblages. Ecological Monographs, 63:77–101. http://dx

.doi.org/10.2307/2937124.

Hixon, M. A., and G. P. Jones. 2005. Competition, predation, and density-dependent 

mortality in demersal marine fishes. Ecology, 86:2847–2859. http://dx.doi

.org/10.1890/04-1455.

Hixon, M. A., and M. S. Webster. 2002. Density dependence in reef fish populations. In Coral reef fishes: Dynamics and diversity in a complex ecosystem, ed. 

P. F. Sale, pp. 303–325. San Diego: Academic Press. http://dx.doi.org/10.1016

/B978-012615185-5/50018-9.

Hobson, E. S., and J. R. Chess. 1976. Trophic interactions among fishes and zooplankters near shore at Santa Catalina Island, California. Fishery Bulletin, 

74:567–598.

Holbrook, S. J., and R. J. Schmitt. 1984. Experimental analyses of patch selection 

by foraging surfperch (Embiotoca jacksoni Agassiz). Journal of Experimental Marine Biology and Ecology, 79:39–64. http://dx.doi.org/10.1016/0022

-0981(84)90029-7.

———. 1986. Food acquisition by competing surfperch on a patchy environmental gradient. Environmental Biology of Fishes, 16:135–146. http://dx.doi

.org/10.1007/BF00005166.

———. 1988a. The combined effects of predation risk and food reward on patch 

selection. Ecology, 69:125–134. http://dx.doi.org/10.2307/1943167.

———. 1988b. Effects of predation risk on foraging behavior: Mechanisms altering patch choice. Journal of Experimental Marine Biology and Ecology,

121:151–163. http://dx.doi.org/10.1016/0022-0981(88)90252-3.

———. 2002. Competition for shelter space causes density-dependent predation 

mortality in damselfishes. Ecology, 83:2855–2868. http://dx.doi.org/10

.1890/0012-9658(2002)083[2855:CFSSCD]2.0.CO;2.

———. 2004. Population dynamics of a damselfish: Effects of a competitor that 

also is an indirect mutualist. Ecology Letters, 85:979–985. http://dx.doi

.org/10.1890/03-0406.

Holbrook, S. J., R. J. Schmitt, and J. S. J. Stephens. 1997. Changes an assemblage 

of temperate reef fishes associated with a climate shift. Ecological Applications, 7:1299–1310. http://dx.doi.org/10.1890/1051-0761(1997)007[1299

:CIAAOT]2.0.CO;2.

Holland, K. N., C. G. Lowe, and B. M. Wetherbee. 1996. Movements and dispersal patterns of blue trevally (Caranx melampygus) in a fisheries conservation zone. Fisheries Research, 25:279–292. http://dx.doi.org/10.1016/0165

-7836(95)00442-4.

Hughes, T. P. 1994. Catastrophes, phase shifts, and large-scale degradation of a 

Caribbean coral reef.  Science, 265:1547–1551. http://dx.doi.org/10.1126

/science.265.5178.1547.

Hughes, T. P., D. C. Reed, and M. J. Boyle. 1987. Herbivory on coral reefs: Community structure following mass mortalities of sea urchins. Journal of Experimental Marine Biology and Ecology, 113:39–59. http://dx.doi.org/10

.1016/0022-0981(87)90081-5.

Johnson, D. W. 2006. Predation, habitat complexity, and variation in densitydependent mortality of temperate reef fishes. Ecology, 87:1179–1188. 

http://dx.doi.org/10.1890/0012-9658(2006)87[1179:PHCAVI]2.0.CO;2.

Johnson, D. W., M. R. Christie, and J. Moye. 2010. Quantifying evolutionary potential of marine fish larvae: Heritability, selection, and evolutionary constraints. Evolution, 64:2614–2628. http://dx.doi.org/10.1111/j.1558-5646

.2010.01027.x.

Johnson, D. W., and M. A. Hixon. 2010. Ontogenetic and spatial variation in sizeselective mortality of a marine fish. Journal of Evolutionary Biology, 23:724–

737. http://dx.doi.org/10.1111/j.1420-9101.2010.01938.x.

Jones, G. P., D. J. Ferrell, and P. F. Sale. 1991. Fish predation and its impact on the 

invertebrates of coral reefs and adjacent sediments. In The ecology of fishes 

on coral reefs, ed. P. F. Sale, pp. 156–179. San Diego: Academic Press.

Larson, R. J. 1980. Competition, habitat selection, and the bathymetric segregation of two rockfish (Sebastes) species. Ecological Monographs, 50:221–239. 

http://dx.doi.org/10.2307/1942480.

Leis, J. M., and M. I. McCormick. 2002. The biology, behavior, and ecology of the 

pelagic, larval stage of coral reef fishes. In Coral reef fishes: Dynamics and 

diversity in a complex ecosystem, ed. P. F. Sale, pp. 171–199. San Diego: Academic Press. http://dx.doi.org/10.1016/B978-012615185-5/50011-6.

Leray, M., R. Beldade, S. J. Holbrook, R. J. Schmitt, S. Planes, and G. Bernardi. 2010. 

Allopatric divergence and speciation in coral reef fish: The three-spot dascyllus, Dascyllus trimaculatus, species complex. Evolution, 64:1218–1230.

Levin, P. S. 1991. Effects of microhabitat on recruitment variation in a Gulf of 

Maine reef fish. Marine Ecology Progress Series, 75:183–189. http://dx.doi

.org/10.3354/meps075183.

———. 1993. Habitat structure, conspecific presence and spatial variation in the 

recruitment of a temperate reef fish. Oecologia, 94:176–185. http://dx.doi

.org/10.1007/BF00341315.

Ling, S. D., C. R. Johnson, S. D. Frusher, and K. R. Ridgway. 2009. Overfishing 

reduces resilience of kelp beds to climate-driven catastrophic phase shift. 
number 39 • 167

Proceedings of the National Academy of Sciences, 106:22341–22345. http://

dx.doi.org/10.1073/pnas.0907529106.

Lowe, C. G., and R. N. Bray. 2006. Movement and activity patterns. In The ecology of 

marine fishes: California and adjacent waters, ed. L. G. Allen, D. J. Pondella II,

and M. H. Horn, pp. 524–553. Berkeley: University of California Press.

MacNeil, M. A., N. A. J. Graham, N. V. C. Polunin, M. Kulbicki, R. Galzin, 

M. Harmelin-Vivien, and S. P. Rushton. 2009. Hierarchical drivers of reef-fish 

metacommunity structure. Ecology, 90:252–264. http://dx.doi.org/10.1890

/07-0487.1.

Mapstone, B. D., and A. J. Fowler. 1988. Recruitment and the structure of assemblages of fish on coral reefs. Trends in Ecology and Evolution, 3:72–77. 

http://dx.doi.org/10.1016/0169-5347(88)90020-1.

McLeod, E., R. Salm, A. Green, and J. Almany. 2009. Designing marine protected 

area networks to address the impacts of climate change. Frontiers in Ecology 

and the Environment, 7:362–370. http://dx.doi.org/10.1890/070211.

Molles, M. C., Jr. 1978. Fish species diversity on model and natural reef patches: 

Experimental insular biogeography. Ecological Monographs, 48:289–305. 

http://dx.doi.org/10.2307/2937232.

Murray, S. N., R. F. Ambrose, J. A. Bohnsack, L. W. Botsford, M. H. Carr, G. E. 

Davis, P. K. Dayton, D. Gotshall, D. R. Gunderson, M. A. Hixon, J. Lubchenco, 

M. Mangel, A. MacCall, D. A. McArdle, J. C. Ogden, J. Roughgarden, R. M. 

Starr, M. J. Tegner, and M. M. Yoklavich. 1999. No-take reserve networks: 

Protection for fishery populations and marine ecosystems. Fisheries, 24:11–

25. http://dx.doi.org/10.1577/1548-8446(1999)024<0011:NRN>2.0.CO;2.

Osenberg, C. W., C. M. S. Mary, R. J. Schmitt, S. J. Holbrook, P. Chesson, and 

B. Byrne. 2002. Rethinking ecological inference: Density dependence in reef 

fishes. Ecology Letters, 5:715–721. http://dx.doi.org/10.1046/j.1461-0248

.2002.00377.x.

Perez-Matus, A., and J. S. Shima. 2010. Density and trait-mediated effects of fish 

predators on amphipod grazers: Indirect benefits for the giant kelp, Macrocystis pyrifera. Marine Ecology Progress Series, 417:151–158. http://dx.doi

.org/10.3354/meps08820.

Petersen, C. W., and R. R. Warner. 2002. The ecological context of reproductive behavior. In Coral reef fishes: Dynamics and diversity in a complex ecosystem, 

ed. P. F. Sale, pp. 103–120. San Diego: Academic Press. http://dx.doi.org/10

.1016/B978-012615185-5/50007-4.

Planes, S. 2002. Biogeography and larval dispersal inferred from population genetic 

analysis. In Coral reef fishes: Dynamics and diversity in a complex ecosystem, 

ed. P. F. Sale, pp. 201–220. San Diego: Academic Press. http://dx.doi.org/10

.1016/B978-012615185-5/50012-8.

Planes, S., G. Lecaillon, P. Lenfant, and M. Meekan. 2002. Genetic and demographic variation in new recruits of Naso unicornis. Journal of Fish Biology, 

61:1033–1049. http://dx.doi.org/10.1111/j.1095-8649.2002.tb01861.x.

Randall, J. E. 1967. Food habits of reef fishes of the West Indies. Studies in Tropical 

Oceanography, 5:665–847.

Robertson, D. R. 1991. The role of adult biology in the timing of spawning of 

tropical reef fishes. In The ecology of fishes on coral reefs, ed. P. F. Sale, pp. 

356–386. San Diego: Academic Press.

Ross, S. T. 1986. Resource partitioning in fish assemblages: A review of field studies. 

Copeia, 1986:352–388. http://dx.doi.org/10.2307/1444996.

Sale, P. F. 1977. Maintenance of high diversity in coral reef fish communities. American Naturalist, 111:337–359. http://dx.doi.org/10.1086/283164.

———. 1991. Reef fish communities: Open nonequilibrial systems. In The ecology 

of fishes on coral reefs, ed. P. F. Sale, pp. 564–598. San Diego: Academic Press.

Sancho, G., A. R. Solow, P. S. Lobel. 2000. Environmental influences on the diel 

timing of spawning in coral reef fishes. Marine Ecology Progress Series,

206:193–212. http://dx.doi.org/10.3354/meps206193.

 Schmitt, R. J., and S. J. Holbrook. 2000. Habitat-limited recruitment of coral reef 

damselfish. Ecology, 81:3479–3494. http://dx.doi.org/10.1890/0012-9658

(2000)081[3479:HLROCR]2.0.CO;2.

———. 2002. Spatial variation in concurrent settlement of three damselfishes: 

Relationships with near-field current flow. Oecologia, 131:391–401. http://

dx.doi.org/10.1007/s00442-002-0893-9.

———. 2003. Mutualism can mediate competition and promote coexistence. 

Ecology Letters, 6:898–902. http://dx.doi.org/10.1046/j.1461-0248.2003

.00514.x.

———. 2007. The scale and cause of spatial heterogeneity in the strength of temporal density dependence. Ecology, 88:1241–1249. http://dx.doi.org/10

.1890/06-0970.

Schmitt, R. J., S. J. Holbrook, A. J. Brooks, and J. C. P. Lape. 2009. Intraguild 

predation in a structured habitat: Distinguishing multiple-predator effects 

from competitor effects. Ecology Letters, 90:2434–2443. http://dx.doi.org

/10.1890/08-1225.1.

Schmitt, R. J., S. J. Holbrook, and C. W. Osenberg. 1999. Quantifying the effects 

of multiple processes on local abundance: A cohort approach for open 

populations. Ecology Letters, 2:294–303. http://dx.doi.org/10.1046/j.1461

-0248.1999.00086.x.

Shapiro, D. Y. 1991. Intraspecific variability in social systems of coral reef fishes. 

In The ecology of fishes on coral reefs, ed. P. F. Sale, pp. 331–355. San Diego: 

Academic Press.

Sikkel, P. C. 1989. Egg presence and developmental stage influence spawning-site 

choice by female garibaldi. Animal Behaviour, 38:447–456. http://dx.doi

.org/10.1016/S0003-3472(89)80038-7.

Stallings, C. D. 2008. Indirect effects of an exploited predator on recruitment of 

coral-reef fishes. Ecology, 89:2090–2095. http://dx.doi.org/10.1890/07

-1671.1.

Starr, R. M., V. O’Connell, and S. Ralston. 2004. Movements of lingcod (Ophiodon 

elongatus) in southeast Alaska: Potential for increased conservation and yield 

from marine reserves. Canadian Journal of Fisheries and Aquatic Sciences,

61:1083–1094. http://dx.doi.org/10.1139/f04-054.

Steele, M. A., and T. W. Anderson. 2006. Predation. In The ecology of marine fishes: 

California and adjacent waters, ed. L. G. Allen, D. J. Pondella II, and M. H. 

Horn, pp. 428–448. Berkeley: University of California Press.

Stephens, J. S., J. E. Hose, and M. S. Love. 1988. Fish assemblages as indicators of 

environmental change in nearshore environments. In Marine organisms as 

indicators, ed. D. Soule and G. S. Kleppel, pp. 91–105. Berlin: Springer-Verlag. 

http://dx.doi.org/10.1007/978-1-4612-3752-5_5.

Syms, C., and G. P. Jones. 2000. Disturbance, habitat structure, and the dynamics of a coral-reef fish community. Ecology, 81:2714–2729. http://dx.doi

.org/10.1890/0012-9658(2000)081[2714:DHSATD]2.0.CO;2.

Talbot, F. H., B. C. Russell, and G. R. V. Anderson. 1978. Coral reef fish communities: Unstable, high-diversity systems? Ecological Monographs, 48:425–440. 

http://dx.doi.org/10.2307/2937241.

Victor, B. C. 1983. Recruitment and population dynamics of a coral reef fish. Science, 219:419–420. http://dx.doi.org/10.1126/science.219.4583.419.

———. 1986. Larval settlement and juvenile mortality in a recruitment-limited 

coral reef fish population. Ecological Monographs, 56:145–160. http://dx

.doi.org/10.2307/1942506.

Warner, R. R. 1984. Mating systems and hermaphroditism in coral reef fish. American Scientist, 72:128–136.

———. 1987. Female choice of sites versus mates in a coral reef fish, Thalassoma 

bifasciatum. Animal Behaviour, 35:1470–1478. http://dx.doi.org/10.1016

/S0003-3472(87)80019-2.

Warner, R. R. 1991. The use of phenotypic plasticity in coral reef fishes as tests of 

theory in evolutionary ecology. In The ecology of fishes on coral reefs, ed. P. F. 

Sale, pp. 387–398. San Diego: Academic Press.

Warner, R. R., and P. L. Chesson. 1985. Coexistence mediated by recruitment fluctuations: A field guide to the storage effect. American Naturalist, 125:769–

787. http://dx.doi.org/10.1086/284379.

Warner, R. R., and S. G. Hoffman. 1980. Local population size as a determinant 

of mating system and sexual composition in two tropical marine fishes (Thalassoma spp.). Evolution, 34:508–518. http://dx.doi.org/10.2307/2408220.

Williams, A. H. 1980. The threespot damselfish: A noncarnivorous keystone species. American Naturalist, 116:138–142. http://dx.doi.org/10.1086/283616.

Williams, D. M. 1991. Patterns and process in the distribution of coral reef fishes. 

Pp. 437-474. In The ecology of fishes on coral reefs, ed. P. F. Sale, pp. 437–

474. San Diego: Academic Press.

Zeller, D. 1999. Ultrasonic telemetry: Its application to coral reef fisheries research. 

Fisheries Bulletin, 97:1058–1065.

Research Facilitated by Scuba

Introduction

Michael A. Lang, Roberta L. Marinelli, Susan J. Roberts, 

and Phillip R. Taylor

S

cuba has played a critical role in marine research. The use of scuba as a research tool 

has been validated by the quantity and quality of scientific output published in highimpact journals that is cited in this volume. This volume further endorses the strong 

integration of scientific diving within the overall science domain: “The history of marine 

research has provided numerous examples of mysteries that would still be unsolved and 

findings that would have been misinterpreted with confidence if not for direct observation on scuba” (Witman et al., this volume).

The first thirteen papers reported research findings and discoveries around the world 

in environments such as coral reefs, oceanic blue water, under-ice polar habitats, and 

temperate kelp forests, providing perspectives on ecological scales and function, physiology, symbiosis and chemistry, biodiversity and behavior, and structured populations. 

These papers weave scuba through the science, often with a historical and developmental 

perspective on methods and techniques. 

The end product of scientific diving activities is the advancement of science. The 

following six papers are illustrative of underwater research that was not only greatly 

facilitated by scuba, but could perhaps not have been accomplished without it. The biology of several marine systems is reported in research involving substantial, often decadal, 

scuba use. The topics include biological studies on the coral holobiont, ecological roles of 

major algal groups on reefs, the significance of synchronized sexual reproduction in green 

algae, and the functional role of small and cryptic metazoans on coral reefs. The research 

facilitated by scuba and reported in these papers focuses on the scientific results, not necessarily on the research methodologies using scuba to obtain those data and observations, 

and includes several case studies. Where appropriate, laboratory studies complementary 

to underwater field observations are referenced.

Michael A. Lang, formerly with Smithsonian 

Institution; now at The Ocean Foundation, 

1990 M Street NW, Suite 250, Washington, D.C. 

20036, USA. Roberta L. Marinelli, National 

Science Foundation, Antarctic Sciences Division, 

Antarctic Organisms and Ecosystems Program; 

now at University of Southern California, Wrigley Institute for Environmental Studies. Susan

J. Roberts, National Research Council, Ocean 

Studies Board. Phillip R. Taylor, National 

Science Foundation, Ocean Sciences Division, 

Ocean Section; now at University of Southern 

California, Research Advancement and Federal 

Relations. Correspondence: M. Lang, langm@

cox.net.

Manuscript received 25 January 2012; accepted 5 March 2013.

Understanding the Coral Holobiont 

through Science and Scuba

Steve V. Vollmer, Andrew C. Baker, Mary-Alice Coffroth,

C. Drew Harvell, and Mónica Medina

ABSTRACT. Reef-building corals are a holobiont composed of the coral animal host and its associated eukaryotic and bacterial microbes. Symbiotic dinoflagellates in the genus Symbiodinium, which 

form the basis of the coral–algal symbiosis and provide the coral host with most of its nutrition, 

are one of the most familiar members of the coral holobiont. Yet reef-building corals also possess 

diverse communities of bacteria that play important roles in processes such as nutrient cycling and 

coral immunity. Understanding the complex relationships between the coral, its algal symbionts, 

and associated microbes is critical because breakdowns in these relationships result in coral bleaching and coral disease outbreaks, both of which are increasing due to global climate change. Here 

we review recent advances in scuba-based research on the coral holobiont that have expanded our 

understanding of coral–algal and coral–microbe relationships as well as the role of the coral host in 

these interactions.

INTRODUCTION

Tropical coral reef ecosystems harbor well known and arguably unrivaled biological 

diversity that supports the marine world (Knowlton, 2001a, 2001b; Hughes et al., 2003). 

The macroscopic, or visible, diversity of life on coral reefs, including the array of tropical fish, seaweeds, and invertebrates, is readily apparent to anyone who has snorkeled 

or scuba dived on reefs. This visible biodiversity tends to capture the most scientific and 

public interest. Yet there is a greater diversity of microorganisms on reefs that goes unseen (Rohwer et al., 2002; Rosenberg et al., 2007; Dinsdale et al., 2008a, 2008b; Bourne 

et al., 2009; Ainsworth et al., 2010). This hidden diversity of microbes is arguably more 

important to the function of coral reef ecosystems because these microorganisms are instrumental in critical ecosystem services like nutrient cycling (Rohwer et al., 2002; Alongi 

and McKinnon, 2005; Wegley et al., 2007; Thurber et al., 2009). 

Reef-building corals are the foundation of coral reef ecosystems. These reef-building 

coral species are host to an amazing diversity of organisms including representatives 

from all three domains of life (eukarya, bacteria, archaea) and viruses (Rohwer et al., 

2002; Rosenberg et al., 2007; Ainsworth et al., 2010). Eukaryotic organisms associated 

with the coral host include the well-known, phototrophic, symbiotic dinoflagellates in the 

genus Symbiodinium (Rowan, 1991; Trench, 1993; Baker, 2003; Stat et al., 2006), which 

translocate fixed carbon to the host (Muscatine, 1973; Muscatine et al.,1981; Falkowski 

et al., 1984; Edmunds and Davies, 1986) as well as other eukaryotes associated with the 

coral tissue and skeleton, including endolithic algae, fungi, and sponges (Rohwer et al., 

2002; Rosenberg et al., 2007; Bourne et al., 2009). Corals house a high abundance and 

diversity of bacterial and archaeal groups in their tissue, surface mucus, and skeleton 

(Rohwer et al., 2002; Wegley et al., 2004; Rosenberg et al., 2007; Bourne et al., 2009). 

Steve V. Vollmer, Marine Science Center, Northeastern University, 430 Nahant Road, Nahant, 

Massachusetts 01908, USA. Andrew C. Baker,

Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, 

University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149, USA. Mary-Alice 

Coffroth, Department of Geology, 411 Cooke 

Hall, University at Buffalo, Buffalo, New York 

14226, USA. C. Drew Harvell, Department 

of Ecology and Evolutionary Biology, Cornell University, 321 Corson Hall, Ithaca, New 

York 14853, USA. Mónica Medina, School of 

Natural Sciences, University of California, Merced, 5200 North Lake Road, Merced, California 95343, USA. Correspondence: S. Vollmer, 

s.vollmer@neu.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
174 • smithsonian contributions to the marine sciences

These bacteria and archaea can benefit the coral by cycling nutrients (Rohwer et al., 2002; Lesser et al., 2004; Wegley et al., 

2004; Beman et al., 2007; Wegley et al., 2007) and producing 

antimicrobial compounds (Kelman et al., 1998; Ritchie, 2006; 

Nissimov et al., 2009). However, some of the coral-associated 

bacteria are also detrimental to the coral, including pathogenic 

bacteria that cause disease (Kushmaro et al., 1996; Rohwer et al., 

2002; Sutherland et al., 2004; Harvell et al., 2007; Rosenberg et 

al., 2007; Bourne et al., 2009; Ainsworth et al., 2010).

The collection of organisms associated with and including 

the host coral animal has been called the coral holobiont (Rohwer et al., 2002). The concept of the coral holobiont (Rohwer 

et al., 2002) originated in part from the need to understand the 

newly discovered diversity of microorganisms on corals in a 

more comprehensive or holistic way, (i.e., by viewing the coral 

as the sum of its parts—the animal host plus all of the associated eukarya, bacteria, and archaea). This expanded view of the 

coral organism began to emerge as it became apparent that the 

symbiotic dinoflagellates within corals, which were once thought 

to be one species, Symbiodinium microadriaticum (Taylor, 1971, 

1974), actually comprised many diverse lineages (or clades) of 

Symbiodinium (Rowan, 1991; Rowan and Powers, 1991), even 

within a single coral (Rowan and Knowlton, 1995; Rowan et al., 

1997). The diversity of algal symbionts led to the view that the 

coral and its algal symbionts represent a holosymbiont (IglesiasPrieto and Trench, 1997). Rohwer et al. (2002) further defined 

the coral holobiont to include the coral host, its symbiotic algae, 

and other associated microbes. 

The coral holobiont concept not only represents an assemblage of microbes and a host, but also allows us to better understand how the associations among the groups composing the 

coral holobiont benefit each other, as well as how breakdowns in 

these associations might impact the coral and the holobiont community (Figure 1). The holobiont perspective helps to solidify a 

departure from the earlier tendency in the study of coral biology 

to focus separately on each component—coral, symbiont, and 

other microbes. The two most familiar symptoms of breakdowns 

in the associations between the coral host and its associated microorganisms include (1) coral bleaching caused primarily by the 

breakdown in the coral–algal symbiosis (Brown, 1997; HoeghGuldberg, 1999; Douglas, 2003), and (2) coral disease resulting 

from the breakdowns between the coral and its associated bacteria (Sutherland et al., 2004; Harvell et al., 2007; Rosenberg et 

al., 2007; Bourne et al., 2009).

The goal of this paper is not to provide a comprehensive 

review of the literature on the coral holobiont since there are 

already many excellent and recent reviews on the coral–algal 

symbiosis (e.g., Baker, 2003; Stat et al., 2006) and coral–microbe 

interactions (e.g., Sutherland et al., 2004; Rosenberg et al., 2007; 

Bourne et al., 2009; Ainsworth et al., 2010). Instead, our goal is 

to highlight recent findings, as well as to characterize the state of 

knowledge of the coral holobiont, including knowledge gaps that 

warrant further investigation. Scuba diving research has played a 

prominent role in all of this work, particularly because it allowed 

for the experimental manipulation and collection of specimens 

from the reef environment. We begin by discussing recent advances in our knowledge of the nature of the coral–algal symbiosis, and in particular their ontogeny. We then discuss recent 

advances in understanding coral–microbe interactions. We conclude by highlighting the role of the coral host as a key member 

of the coral holobiont. 

THE CORAL–ALGAL SYMBIOSIS

All reef-building corals exhibit mutualistic associations with 

symbiotic dinoflagellates in the genus Symbiodinium. These algae 

were originally identified as Gymnodinium-like dinoflagellates 

by Kawaguti (1944), axenically cultured by McLaughlin and 

Zahl (1959), and formally described (from the scyphozoan Cassiopeia sp.) as Symbiodinium microadriaticum by Freudenthal 

(1962). Despite early cautions to the contrary (e.g., McLaughlin 

and Zahl, 1966), all symbiotic dinoflagellates were initially classified as members of a single pandemic species adapted to life in a 

symbiotic state (Taylor, 1971; Taylor, 1974). However, beginning 

in the mid-1970s evidence drawn independently from a variety 

of approaches (biochemical, physiological, behavioral, morphological, and genetic) indicated that these dinoflagellates were in 

fact unusually diverse. Then, in the 1990s, our understanding 

of diversity in Symbiodinium was revolutionized by the application of contemporary PCR-based molecular genetics. The use of 

scuba allowed scientists to collect a wide variety of symbiotic 

hosts from a broad range of habitats and environmental conditions. These two factors greatly improved our understanding of 

how Symbiodinium diversity can influence the physiology and 

ecology of various hosts, particularly corals.

Algal Diversity and Distribution

Rowan and Powers (1991) were the first to PCR-amplify 

and sequence Symbiodinium from reef corals. They recognized 

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FIGURE 1. Schematic view of the coral holobiont (modified from

Rohwer et al., 2002, and Thurber et al., 2009) showing some of the 

potential benefits and breakdowns between the coral host and its 

associated eukaryotes, bacteria, and archaea.
number 39 • 175

three distinct clades of Symbiodinium (named A, B, and C) and 

demonstrated that the genetic distance between these clades was 

comparable to that between some nonsymbiotic dinoflagellate 

orders. In the 20 years since these articles appeared, further evidence of the extraordinary diversity of this genus has accumulated, with six additional clades now recognized: D (Carlos et 

al., 1999), E and F (LaJeunesse, 2001; Pochon et al., 2001), G 

(Pochon et al., 2001), H (Pochon et al., 2004), and I (Pochon and 

Gates, 2010). However, of the nine clades of Symbiodinium (A–I) 

that have been documented to date, only six have been identified 

from corals: A, B, and C (first recorded by Rowan, 1991), D 

(Baker, 1999; see also Rowan, 1991; Baker, 2003), F (LaJeunesse, 

2001), and G (Van Oppen et al., 2005). The majority of these 

studies depended on the use of scuba to collect specimens (Figure 2), and the ready access to diverse specimens obtained using 

this technology has played an important role in these discoveries. 

Previously, Symbiodinium researchers tended to be restricted to 

working on cultures, which are highly selected and thus can limit 

studies of diversity by favoring symbionts that can be cultured 

over others (Santos et al., 2001). 

Our knowledge of how different Symbiodinium are distributed within and among different coral species has progressed rapidly over the last decade. Additional clades have been documented, 

and the diversity of subcladal Symbiodinium types within some 

FIGURE 2. Phylogenetic reconstructions of the genus Symbiodinium inferred using maximum likelihood analysis 

of (A) nuclear large subunit ribosomal DNA (nr28S-rDNA) and (B) chloroplast large subunit ribosomal DNA 

(cp23S-rDNA) (modified from Pochon and Gates, 2010). Next to each of the nine Symbiodinium clades (A–I) are 

the year each clade was first reported (left) and the year each was first recorded in hexacorals or octocorals (right). 

Discoveries marked in red indicate those that involved scuba to collect field samples. Question marks (?) indicate 

that Symbiodinium in clades E, H, and I have not been detected yet in corals.
176 • smithsonian contributions to the marine sciences

clades has been shown to be spectacularly rich (e.g., LaJeunesse, 

2002, 2005; Coffroth and Santos, 2005). A long-standing tenet in

algal symbiosis holds that different invertebrate host species are 

specific to particular Symbiodinium (Trench, 1989, 1992), and 

that although a particular symbiont taxon might be found in a 

variety of diverse hosts, each host species uniquely associates with 

only one algal type. The use of scuba, combined with the development of PCR-based molecular methods, has allowed researchers 

to directly test this theory by obtaining snapshots of algal symbiont diversity in corals over time and space. These surveys have 

shown that while most corals indeed tend to be dominated by 

particular symbionts (LaJeunesse, 2001, 2002; LaJeunesse et al., 

2004a, 2004b; Goulet, 2006; Goulet et al., 2008), many host species show a surprising degree of intraspecific symbiont diversity 

and exhibit considerable variability over time and space, with 

ontogenetic and environmental factors often driving observed 

specificity (Baker, 2003; Baker and Romanski, 2007). The use of 

scuba has been essential in this research by allowing coral species to be sampled from a variety of different sites, habitats, and 

depths. Coral species that routinely host multiple symbiont taxa 

(variously described as “flexible,” “generalist,” or “polymorphic” 

coral host species) have been distinguished from other species 

that have (to date) been found to contain only one particular 

symbiont type (“specific,” “specialist,” or “monomorphic” coral 

species). The reported diversity of symbionts from corals depends 

to a large degree on the breadth and depth of sampling effort, as 

well as the taxonomic and numeric resolution of the molecular 

methods used (Baker and Romanski, 2007). Scuba-based surveys

of Symbiodinium diversity have therefore been a very active area 

of research for the last decade. 

Rowan and Knowlton (1995) and Rowan et al. (1997) provide early examples of how scuba was employed to reveal these 

relationships. Their work showed that the dominant Caribbean 

corals Montastraea annularis and M. faveolata each contained

Symbiodinium in three clades (A, B, and C), and that the distribution of clades in these coral species was determined by irradiance, 

both among colonies at different depths and within individual 

colonies. Moreover, during bleaching, symbionts in different 

clades varied in their sensitivity to high-temperature bleaching as

a result of differences in their irradiance sensitivity. Together, the 

two studies convincingly showed that irradiance affects symbiont 

distribution over a coral landscape. The latter study also showed 

for the first time the important conclusion that symbiont genotype can directly influence fitness of the coral host. 

Symbiodinium distributions also show strong biogeographic 

patterns. In scleractinian corals, perhaps the most obvious pattern is the contrast between the Atlantic and Indo-Pacific, with 

corals in the tropical western Atlantic (Caribbean) being codominated by Symbiodinium in clades A, B, and C but corals in the 

Indo-Pacific being dominated by clade C (Baker and Rowan, 

1997; LaJeunesse, 2002). In both oceanic provinces, clade D is 

commonly found in environments characterized by chronic temperature stress (Chen et al., 2003; Baker et al., 2004; Fabricius 

et al., 2004) or in coral hosts that have recently experienced 

bleaching (Glynn et al., 2001; Baker et al., 2004; Jones et al., 

2008; LaJeunesse et al., 2009a). 

More recently, diversity assessments have focused on the 

identification of symbionts at finer taxonomic scales. LaJeunesse 

(2001) first formalized these investigations by proposing the Internal Transcribed Spacer 2 region of ribosomal DNA (rDNA) 

as a suitable marker for investigating subcladal diversity in Symbiodinium. This marker has since been extensively used to investigate diversity in samples of natural populations worldwide that 

were collected using scuba (e.g., LaJeunesse et al., 2010). Additional investigations of fine-scale diversity have used length heteroplasmy in chloroplast large subunit ribosomal DNA (rDNA) 

to survey symbiont diversity in Caribbean octocorals (Santos et 

al., 2004) and variation in microsatellite flanking sequences to 

further assess variation within these types (Santos et al., 2004). 

Allelic variation in microsatellite loci have been used to screen 

intraspecific variation in soft corals on the Great Barrier Reef 

(Howells et al., 2009) and octocorals in the Bahamas and the 

Florida Keys (Santos et al., 2003; Kirk et al., 2009), and to study 

reef endemism, stability, and fine-scale host specificity of symbionts in Montastraea spp. in the Florida Keys and the Bahamas 

(Thornhill et al., 2009). 

The findings from these studies have revealed that Symbiodinium is extraordinary, not just for its taxonomic breadth (nine 

clades, each of which might ordinarily be considered a genus in 

its own right), but also for the taxonomic richness within many 

of these clades, with some (such as clade C) potentially containing dozens of distinct taxa (species), each of which is characterized by additional intraspecific variation. Some debate exists 

over the functional role of this Symbiodinium genetic diversity 

(Van Oppen and Gates, 2006; Apprill and Gates, 2007), but this 

has not prevented several new species of Symbiodinium from 

being introduced informally into the literature even though from 

a genetic standpoint they differ very little (e.g., LaJeunesse et al., 

2009b). Drawing generalized conclusions from this sometimes 

bewildering level of diversity has proved difficult, as evidenced 

by the fact that no review has yet attempted to reconcile the data 

from the many dozens of papers published over the last decade. 

It seems clear that some degree of taxonomic revision is required 

when one compares diversity within Symbiodinium to that found 

in other groups (Stern et al., 2010), yet there is surprisingly little 

consensus on how to proceed. 

Stability in Coral–Algal Symbiosis through Time

One area where scuba has contributed significantly to our 

understanding of coral–algal symbiosis is the degree to which the 

composition of symbiont assemblages in individual coral colonies can change over time. Of particular interest are the role of 

the environment in controlling potential changes and the importance of human-mediated disturbance, including global climate 

change, in determining the rate at which change might occur. 

These ideas were first introduced as the adaptive bleaching hypothesis (Buddemeier and Fautin, 1993). This hypothesis posited 
number 39 • 177

that recovery from bleaching provides an opportunity for corals 

to become populated with different symbionts, and that changes 

in symbionts might prove beneficial to the coral host (i.e., have 

adaptive value). These ideas were further refined (Ware et al., 

1996) and clarified to include quantitative changes in mixed 

symbiont assemblages as a result of bleaching (Baker, 2003; Buddemeier et al., 2004; Fautin and Buddemeier, 2004). 

Numerous studies have tested this hypothesis and found 

evidence both in support of it (Baker, 2001; Kinzie et al., 2001; 

Berkelmans and van Oppen, 2006; Jones et al., 2008) and against 

it (Goulet and Coffroth, 2003a, 2003b; Rodriguez-Lanetty and 

Hoegh-Guldberg, 2003; Iglesias-Prieto et al., 2004; LaJeunesse et 

al., 2004a, 2004b; Kirk et al., 2005; LaJeunesse, 2005; Hannes 

et al., 2009). Although a consensus has not yet been reached, 

the combined evidence suggests that changes in symbiont assemblages that occur following bleaching are the result of changes 

in the relative abundance of preexisting symbionts, not the result of the acquisition of symbionts from external sources during 

bleaching or initial recovery (Baker, 2004). Although adult corals have been shown to be capable of acquiring symbionts from 

the environment (Lewis and Coffroth, 2004), these symbionts 

may be transient (Coffroth et al., 2010) and might not be able 

to achieve dominance within colonies regardless of environmental conditions or disturbance regime. Consequently, the extent 

to which bleaching can lead to new symbiotic combinations 

hypothetically depends largely on which symbionts are already 

present in the symbiotic assemblage of different coral species. In 

this context, attempts to identify and quantify background symbionts using real-time PCR are essential in determining whether 

corals routinely host a variety of symbionts at low abundance, 

or whether most coral species exclusively host specific symbiont 

types. An improved understanding of corals’ specificity and the 

molecular, environmental, and ontogenetic factors that drive this 

specificity will allow us to critically assess the potential for adaptive bleaching in response to changing environmental conditions. 

Ontogeny of Coral–Algal Symbiosis

The tremendous dinoflagellate diversity that exists among 

and often within host species is first established during the early 

ontogeny of the coral–algal symbiosis. Although in some cnidarian symbioses the symbiont is passed from parent to offspring 

(vertical or closed symbiont transmission), among the majority 

of corals, especially corals that free-spawn eggs and sperm, the 

offspring lack symbionts (aposymbiotic) and must obtain them 

anew each generation from the surrounding environment (horizontal or open transmission; Stat et al., 2006). Laboratory studies have demonstrated that in corals and other cnidarians initial 

uptake is relatively nonspecific and a range of different symbiont types can be acquired (Schwarz et al., 1999; Coffroth et al., 

2001; Weis et al., 2001; Rodriguez-Lanetty et al., 2004; Poland, 

2010). For example, Montastraea faveolata and Acropora palmata larvae acquired nine of eleven Symbiodinium types offered 

(Table 1) although only a subset of these types are dominant 

in the adult holobiont. These studies generally demonstrate that 

although juvenile corals can take up a broad range of potential 

symbionts early in ontogeny, not all symbionts are ultimately incorporated (or acceptable) to the coral species as adult colonies. 

These findings are similar to other laboratory studies that show 

that while newly settled corals and other cnidarians can harbor 

a diverse range of symbiont types, there is a degree of selectivity 

within the coral host such that not all types offered are taken up 

and even fewer are able to establish and sustain the symbiosis 

(Coffroth et al., 2001; Weis et al., 2001; Rodriguez-Lanetty et al., 

2006; Mieog et al., 2009; Voolstra et al., 2009b).

While these laboratory studies are informative of the potential symbiont diversity within cnidarian symbioses, in nature the 

symbiont pool is more diverse. Field studies enabled by scuba of 

initial host infection have shown that the developing coral acquires a wide assortment of Symbiodinium by accepting not only 

multiple strains from the same clade, but also multiple clades. 

This diversity is recorded both within and among juveniles (Coffroth et al., 2001; Little et al., 2004; Coffroth et al., 2006; Thornhill et al., 2006; del C. Gómez-Cabrera et al., 2008; Abrego et 

al., 2009a, 2009b; Mieog et al., 2009; Poland et al., 2013. For 

example, using scuba to deploy recruits to the reef and then 

monitor symbiont uptake over time, Poland et al. (2013) found 

between five and nine symbiont types among newly settled octocoral recruits (Briareum asbestinum) at any site or during any 

year (symbiont richness). Within the individual recruits, however, 

the majority hosted one or two symbiont types simultaneously. 

Fewer recruits (0.2% or less) harbored five or six symbionts simultaneously, even when the total number of symbiont types 

found across all juveniles at a particular site and/or year was 

TABLE 1. Different strains of Symbiodinium used to infect larvae of Montastraea faveolata (6d) and Acropora palmata (8d). 

Strain nomenclature is based on sequence variation in the 23S 

rDNA gene. Symbols: (-) indicates no infection observed; (+) and 

(++) indicate intensity of infection observed.

Culture Strain M. fav. A. pal.

Control None - -

ELI A198 - -

KB8 A194 ++ ++

04-503 A194 ++ ++

Acp343 B184 - -

Mf1.05b B184 ++ ++

Mf1.05b.01 B184 ++ ++

Mf10.14b.02 B224 ++ ++

Mf11.05b.01 B224 ++ ++

Mf6.07B F178 + +

Mf8.3T F178 ++ +

Mf10.08 D206 ++ ++
178 • smithsonian contributions to the marine sciences

higher (i.e., the diversity of available symbionts was higher than 

in hospite diversity within a single juvenile (Poland et al., 2013). 

This leads to a symbiont complement within and among newly 

settled recruits that is more diverse than that within the adult holobiont (Coffroth et al., 2001; Little et al., 2004; Coffroth et al., 

2006; del C. Gómez-Cabrera et al., 2008; Abrego et al., 2009a, 

2009b; Thornhill et al., 2009). 

Many studies confirm that the symbiont type initially acquired by a host is often not the symbiont type that predominates 

in the adult symbiosis. Some host species may acquire the symbiont types found within the adult along with other symbiont types 

(Coffroth et al., 2001; Weis et al., 2001; del C. Gómez-Cabrera et 

al., 2008), while in other host species the symbiont type that predominates in the adult symbiosis is not detected initially in symbiont assemblages of the juveniles (Little et al., 2004; Thornhill 

et al., 2006; Abrego et al., 2009a; Poland, 2010; Poland et al., 

2013). For example, in a study utilizing clade-level analysis (del 

C. Gómez-Cabrera et al., 2008), newly settled recruits (10d) of

Acropora longicyathus harbored mainly clade A Symbiodinium

although clade C Symbiodinium dominated the adult symbiosis. 

After 83d, the proportion of Symbiodinium clade A decreased, 

Symbiodinium type C increased, and Symbiodinium type D was 

also observed. Similar observations have been reported for other 

acroporids (A. tenuis and A. millepora) where juveniles quickly 

acquired Symbiodinium within clade D although adults of these 

species predominantly harbor Symbiodinium types within clade 

C (Little et al., 2004; Abrego et al., 2009a, 2009b). Contrasting symbiont diversity among juveniles (higher) versus adult 

(lower) hosts is also seen in other groups such as octocorals, 

scyphozoans, and tridacnid clams (Coffroth et al., 2001; BeldaBaillie et al., 2002; Thornhill et al., 2009). In each of these studies, the use of scuba enabled the high-resolution sampling of the 

adult colonies, the detailed placement of new recruits at different 

sites, and the careful monitoring of symbiont uptake. These studies imply that over time (hours to years) a winnowing process occurs (sensu Nyholm and McFall-Ngai, 2004), so that only one to 

a few types establish and sustain the long-term symbioses found 

in the adults (Coffroth et al., 2001; Weis et al., 2001; Belda-Baille 

et al., 2002; Little et al., 2004). In some species this winnowing 

process involves large-scale, clade-level changes (e.g., Abrego et 

al., 2009a, 2009b) whereas among other groups the change is 

seen at the subcladal level (e.g., Poland, 2010). In some corals, 

the symbiont assemblage that is typical of an adult host colony 

does not become established until three to four years into the 

coral’s ontogeny (Abrego et al., 2009b; Poland, 2010). It is not 

presently resolved at this time if this is the case in the majority 

of host species.

Future Directions

Scuba has enabled us to routinely sample symbiont diversity within important reef symbioses and to conduct careful in 

situ experiments to elucidate mechanisms that might be driving 

this diversity. However, we are still faced with many unanswered 

questions. Although numerous studies have contributed knowledge of processes involved in the initial infection and winnowing 

(e.g., Lin et al., 2000; Rodriguez-Lanetty et al., 2004; WoodCharlson et al., 2006; Dunn and Weis, 2009; Voolstra et al., 

2009a), the underlying processes and the ecological significance 

of initially accepting multiple types and then narrowing the assemblage to a single or a few types remains to be elucidated.

Coral–Microbial Associations

Corals possess a high abundance and diversity of associated bacteria and archaea in their tissues, carbon-rich surface 

mucus layers, and skeletons (Ferrer and Szmant, 1988; Banin et 

al., 2000; Frias-Lopez et al., 2002; Rosenberg, 2007; Rosenberg 

et al., 2007; Shnit-Orland and Kushmaro, 2009). The diversity of 

coral-associated microbes has now been reasonably well documented using a variety of culture-independent gene surveys of 

microbial diversity (Rohwer et al., 2002; Bourne and Munn, 

2005; Wegley et al., 2007; Thurber et al., 2009; Sunagawa et al., 

2010). These surveys indicate that it is typical for a single coral 

to house many of the known divisions of bacteria. We now recognize this diversity, yet the functional roles and influences (positive, negative, or neutral) of the different microbes within these 

diverse coral–microbial assemblages are still poorly understood. 

There are clear examples of microbes negatively impacting 

the coral host, most notably the pathogenic microbes associated 

with more than twenty documented coral diseases (Sutherland et 

al., 2004; Rosenberg et al., 2007; Bourne et al., 2009) and the 

case of Vibrio-induced coral bleaching (Kushmaro et al., 1996; 

Rosenberg et al., 2007). There are also clear examples of positive 

impacts of coral-associated microbes (Mouchka et al., 2010), 

including their roles in nutrient cycling (Rohwer et al., 2002; 

Lesser et al., 2004; Wegley et al., 2004; Beman et al., 2007; Wegley et al., 2007) and the production of antimicrobial compounds 

(Kelman et al., 1998; Ritchie, 2006; Nissimov et al., 2009; MaoJones et al., 2010; Rypien et al., 2010). In many cases, however, 

we still do not have a good picture of what natural, versus perturbed, coral–microbial assemblages look like, and it has been 

difficult to document clear species-specific associations between 

microbes and their coral host, including symbiotic microbial associations. Despite these knowledge gaps, coral–microbiological 

research has made great strides over the last 20–30 years. Here 

we focus on two recent advances in coral–microbial research: 

(1) increased knowledge of the ontogeny of coral–microbe associations and (2) the use of coral metagenomics to characterize 

microbial diversity and function. Both promise to transform our 

understanding of coral–microbial interactions.

The Ontogeny of Coral–Microbe Associations

While our understanding of the nature of the coral–algal 

symbiosis has improved greatly in recent years, only recently has 

research focused on the ontogeny of coral–microbial associations. 
number 39 • 179

Pioneering work on this subject comes from two studies (Apprill 

et al., 2009; Sharp et al., 2010) wherein the authors followed 

the establishment of the microbial assemblage through the early 

stages of larval development in multiple broadcast-spawning corals. The first study, by Apprill et al. (2009), examined the ontogeny of microbial associations in the Hawaiian coral Pocillopora 

meandrina, a broadcast-spawning coral that vertically transmits 

its algal symbionts by seeding its eggs with Symbiodinium cells. 

Apprill et al. (2009) found that unlike vertically transmitted algal 

symbionts, bacteria are not taken up vertically but instead are 

acquired horizontally from the environment by the planula larvae after approximately 79 hours in the water column. Interestingly, they discovered that a clade of Roseobacteria in the genus 

Jannaschia consistently associated with the coral planula larvae. 

Roseobacteria are known to form associations with both phytoplankton and Symbiodinium (Littman et al., 2009b; Littman et 

al., 2010). This suggests that they might be associated with Symbiodinium inside the coral host, and yet if that is the case it is 

not clear why they would not be transmitted vertically with the 

Symbiodinium in Pocillopora eggs.

The second study, by Sharp et al. (2010), examined the ontogeny of microbes associated with seven species of broadcastspawning corals (both Pacific and Caribbean species) that do 

not vertically transmit Symbiodinium in their eggs. By following 

the development of bacterial associations from the coral gametes through the swimming planulae to the newly settled polyps 

by using fluorescence in situ hybridization (FISH) techniques, 

Sharp et al. (2010) showed that microbes were only prevalent in 

the corals in the settled polyp stage (i.e., postsettlement), rather 

than established in the planula larvae as observed by Apprill et 

al. (2009) in Pocillopora. Taken together, these early results indicate that the ontogeny of these microbial associations differ 

in their timing depending on the coral. Nothing is known yet 

about microbial transmission in coral species that brood larvae, 

where vertical transmission of Symbiodinium is the most common mode. 

Work by Littman also sheds light on how microbial assemblages change during ontogeny. Newly settled corals have a far 

more diverse microbial assemblage than older recruits, which are 

characterized by relatively more predictable, lower-variance assemblages (Littman et al., 2009b). This suggests a winnowing 

process whereby the more diverse microbial assemblage of juveniles is gradually replaced by the more characteristic adult microbial assemblage, much like what is seen with Symbiodinium. 

This ontogenetic pattern coupled with persistent variation in 

composition among sites (Littman et al., 2009b) provides a large 

role for environment in determining final composition. 

Coral Metagenomics

Next-generation sequencing techniques are providing unprecedented access to and information about the genetic diversity of coral-associated microbes. Culture-independent genetic 

profiles of coral–microbial assemblages have become a mainstay 

of coral microbiology and are the primary tool used to examine 

the diversity, abundance, and associations of microbes on corals. The first genetic surveys relied heavily on Sanger sequencing 

bacterial 16s rDNA diversity from coral microbe clone libraries. 

Sequencing 16s rDNA clone libraries from corals revealed the 

high microbial diversity on corals (Rohwer et al., 2002; Bourne 

and Munn, 2005; Pantos and Bythell, 2006; Sunagawa et al., 

2009), but the depth of sequencing has typically been limited to 

tens to hundreds of sequences per coral sample because of the 

high cost. Recent advances in high-throughput sequencing techniques now allow us to profile coral microbial diversity across 

hundreds of thousands, even millions, of sequences (Sunagawa 

et al., 2010) using either a target gene approach, like 16s rDNA 

sequencing (Sunagawa et al., 2009, 2010), or a metagenomic approach where the DNA or RNA content of an entire sample is 

shotgun sequenced, assembled, and annotated by bacterial group 

and gene function (Dinsdale et al., 2008a; Vega Thurber et al., 

2008, 2009).

Deep-sequencing profiles of microbial 16s rDNA diversity 

from seven Caribbean corals (Sunagawa et al., 2010) uncovered 

even greater levels of novel coral-associated microbial diversity 

than had been seen with traditional Sanger 16s rDNA sequencing efforts. The Sunagawa et al. (2010) study also indicates that 

each coral species harbors an unprecedented level of endemic 

microbial diversity, toppling prior estimates of diversity in coral 

reef ecosystems (Sunagawa et al., 2009, 2010). While there was 

an overlapping of the microbial lineages from the adjacent water 

column and those from the sampled coral species, the large number of microbial taxa that were present on each coral species 

suggests that coral research will continue to contribute newly 

discovered microbes to science (Sogin et al., 2006; Pedros-Alio,

2007). These findings add an important microbial diversity–

based perspective to the significance of conserving coral reefs.

Recent metagenomic approaches applied to corals demonstrate that it is possible to simultaneously profile coral microbes 

with rDNA sequences and categorize and annotate functional 

genes (Wegley et al., 2007; Dinsdale et al., 2008a, 2008b; Marhaver et al., 2008; Vega Thurber et al., 2008, 2009). Wegley et 

al. (2007) first demonstrated that metagenomics could be used 

to successfully profile the coral microbiome—including the algal, 

fungal, bacterial, and viral components—as well as to characterize the responses of members of the coral holobiont based on the 

function of particular gene sequences. The Wegley et al. (2007) 

study documented the high abundance of viral phages on corals 

plus an underappreciated role of fungi in nitrogen fixation. 

Thurber et al. (2009) extended this coral metagenomic approach and profiled the changes in coral–microbial assemblages 

on Porites compressa associated with four important coral stressors: increased temperature, increased nutrients, increased dissolved organic carbon, and higher acidity (i.e., lower pH). They 

observed strong shifts in the microbial assemblages between 

healthy and stressed corals, as well as shifts to genes involved 

in virulence and stress resistance due to coral stress. Interestingly, their results indicate that Vibrios caused strong shifts in 
180 • smithsonian contributions to the marine sciences

the microbiome metabolic profiles during the temperature-stress 

treatment.

Future Research Directions for

Coral–Microbial Interactions

New insights into the ontogeny of coral–microbial interactions and metagenomic approaches are allowing us to characterize the onset and dynamics of coral–microbial assemblages with 

more depth than ever before. Significant questions remain about 

the specific roles of particular microbial groups in corals. For 

instance, what is the role of the microbial assemblage in host 

fitness? How flexible is the partnership between corals and their 

microbial assemblage in coping with climate change? How flexible is the partnership between the a coral host’s Symbiodinium of 

choice and its algal-associated microbes? If the coral–algal symbiosis is being threatened by chronic stress, are there microbialantagonistic effects driven by the holobiont or are opportunistic 

microbes driving the holobiont physiology?

Emerging Role of the Coral Host

Although great strides have been made that increase our understanding of the importance and roles of Symbiodinium and 

microbial diversity in corals, we know far less concerning the 

role of the coral host in regulating and maintaining this diversity. This lack of knowledge about the role of the coral host has 

in some cases led to bias in favor of the importance of algae or 

microbes in the relationship (Baird et al., 2009). For example, 

studies of Symbiodinium diversity and flexibility have suggested 

that changes in algal symbiont assemblages will help corals survive environmental change but have tended to downplay how 

coral specificity might limit this process (Baker, 2001; Baker et 

al., 2004; Berkelmans and van Oppen, 2006; Jones et al., 2008). 

Similarly, with coral–microbe interactions, the probiotic hypothesis championed by some coral microbiologists proposes that 

microbes regulating microbes act as the de facto coral immune 

system (Ben-Haim et al., 2003; Rosenberg et al., 2007a, 2007b) 

even though there is clear evidence that coral have innate immune systems as well (Mydlarz et al., 2006, 2010; Miller et al., 

2007; Dunn, 2009). Yet new data from coral genomics and transcriptomics are providing novel insights into the genetic mechanisms controlling the relationship between the coral host and its 

algal symbionts, and into the nature of coral immunity. 

The Role of Coral Genomics

Recent advances in coral genomics and transcriptomics are 

elevating our understanding of the role that the coral host plays 

in maintaining the stability of the coral holobiont. Gene expression analyses using microarrays have examined the response of 

the coral host to a variety of environmental stimuli during early 

ontogeny (Grasso et al., 2008; Reyes-Bermudez et al., 2009; 

Voolstra et al., 2009a; Polato et al., 2010; Portune et al., 2010) as 

well as in adult colonies (DeSalvo et al., 2008; Reyes-Bermudez et 

al., 2009; DeSalvo et al., 2010a, 2010b). Transcriptome profiles 

of larvae exposed to different choices of Symbiodinium strains 

were correlated with the profiles of unsuccessfully infected larvae, and the profiles of control larvae were correlated with those 

of successfully infected larvae (Voolstra et al., 2009b), suggesting 

that successful Symbiodinium strains enter the host in a stealth 

manner rather than triggering a cellular response (Voolstra et al., 

2009b). In the case of adult symbioses under slight stress (e.g., 

thermal), particularly in the coral Montastraea faveolata, which 

harbors multiple strains at once, the transcriptome response 

seems to be driven mainly by the algal complement (DeSalvo et 

al., 2010a). In contrast, when the stress is severe the transcriptome profiles indicate clear cellular responses driven by the host 

coral (DeSalvo et al., 2008).

Recently there has been an explosion of next-generation 

sequencing that is expanding this initial set of coral and algal 

transcriptomes, but few are published (Meyer et al., 2009; Meyer 

and Matz, 2010). With costs dropping and high-throughput capacity increasing exponentially, de novo whole-genome shotgun 

sequencing is now within reach for coral reef science. Several 

coral, Symbiodinium, and microbial genome projects are expected to come online in the near future. Once host, algal, and 

microbe genomes are complete, and as transcriptome sequencing 

becomes more commonplace, our ability to move coral research 

to a systems biology level will be greatly enhanced and new 

“-omic” technologies can be brought into the study of the coral 

holobiont.

Coral Immunity

Recent progress also has been made in understanding the 

coral immune response in fighting off disease (reviewed by Mydlarz et al., 2006, 2010; Miller et al., 2007; Dunn, 2009) as well 

as in the coral–algal symbiosis (Weis, 2008; Weis et al., 2008; 

Weis and Allemand, 2009). Like other invertebrates, corals have 

innate immune systems capable of self-/non-self-recognition 

(Hildemann et al., 1975; Neigel and Avise, 1983) and the ability 

to identify and react to pathogen infection (Mydlarz and Harvell, 

2007; Mydlarz et al., 2008, 2009, 2010). Recent genetic surveys 

demonstrate that corals and their anthozoan relatives possess a 

relatively full set of the genes and gene pathways involved in innate immunity (Miller et al., 2007; Dunn, 2009; Mydlarz et al., 

2010), including the three major innate immune pathways: the 

Toll-like receptor (TLR) pathway (Miller et al., 2007), the Lectin Complement pathway (Miller et al., 2007; Kvennefors et al., 

2010), and the Prophenoloxidase (PPO) pathway (Mydlarz et al., 

2008). Corals lack adaptive immunity (i.e., immune specificity 

and memory), which is restricted to jawed vertebrates.

To date, most of the information that we know about the 

immune responses of corals (hard and soft) comes from histological and biochemical data focused on specific immune assays 

from a few coral species (Mydlarz et al., 2010). Histological data 
number 39 • 181

suggest that mobile amoebocytes, which move between the coral 

ectoderm and endoderm in the mesoglea, act like immune cells 

and aggregate at regions where tissues are damaged (Mydlarz et 

al., 2008, 2009; Palmer et al., 2008). For example, Mydlarz et al. 

(2008) documented aggregations of these mobile amoebocytes in 

the sea fan Gorgonia ventalina at the site of infection by pathogenic Aspergillus sydowii fungus. Likewise, in the reef coral 

Acropora millepora Palmer et al. (2008) documented amoebocyte aggregations associated with inflammation and melanization in abnormally pigmented coral tissues. Other studies reveal 

potential for antioxidant activity associated with coral fluorescent proteins (Palmer et al., 2009). Recent work increases the 

taxonomic range of comparison to 10 coral families and shows 

links between susceptibility to bleaching and disease and sizes of 

melanin granules, levels of PPO activity, and fluorescent proteins 

(Palmer et al., 2010). 

At the biochemical or genetic level, characterizations of the 

coral immune response thus far have focused primarily on the 

Prophenoloxidase (PPO) pathway using biochemical assays of 

enzymatic activity. Prophenoloxidase immune response acts via 

the PPO pathway, which causes pathogens to be targeted, encapsulated in melanin, and ultimately degraded by phagocytosis 

(Mydlarz et al., 2006, 2008, 2010). Increased PPO activity and 

melanization has been detected in Aspergillus-infected sea fans 

(Mydlarz and Harvell, 2007; Mydlarz et al., 2008), as well as in 

the pigment anomalies in the reef coral A. millepora (Palmer et 

al., 2008) and in bleached Montastraea faveolata corals (Mydlarz et al., 2009). These data suggest that melanization and degradation by the PPO pathway is an important innate immune 

response in both soft and hard corals. No one has yet profiled 

the immune response of an infected coral using gene-expression 

approaches across the full range of possible immune pathways, 

and thus it is not yet known what other pathways might be important in coral immunity in general.

Weis and colleagues (Weis, 2008; Weis et al., 2008) have 

begun to focus on the potential links between the coral innate 

immune response and the relationship between the coral host 

and its symbiotic algae. According to the current hypotheses, one 

key to the maintenance of the coral–algal symbiosis is the ability 

of symbionts to modify the host’s immune response. Algal symbionts are contained in specialized vacuoles in the coral endoderm 

and are acquired through a process similar to phagocytosis of 

pathogens. Early data suggest that the acquisition of the symbionts is mediated by pattern recognition receptors (PRR) (Weis 

et al., 2008), such as lectins (Wood-Charlson et al., 2006; Kvennefors et al., 2010), that are down-regulated during the early 

ontogeny of the coral–algal symbiosis (Wood-Charlson et al.,

2006). Phagocytosis also appears to be arrested during symbiont 

acquisition (Chen et al., 2005; Schwarz et al., 2008) and reactivated when nonspecific symbiont types enter the host cells (Dunn 

and Weis, 2009). These preliminary data suggest that there is a 

strong and important link between the coral immune system and 

the evolution of the coral–algal symbiosis that warrants further 

investigation.

Future Directions

These recent studies demonstrate that the coral host has a 

viable innate immune system and can respond to pathogen infection. Genetic data examining the relationship between the 

coral host and its symbionts also indicate clear links between 

the innate immune response of the coral and the mechanisms 

by which algal symbionts become established within their hosts. 

These early findings are just beginning to elucidate how the coral 

immune system operates and how symbionts evade or modify 

the host’s immune response during uptake. Many questions 

remain unanswered. For example, does the innate immune response show specificity according to the type of pathogens (i.e., 

viral, bacterial, or fungal)? If so, what innate immune pathways 

are involved? Similarly, if Symbiodinium modifies the immune 

response during uptake, what genes or gene pathways are also 

modified and how does this impact coral innate immunity? In the 

future, experimental work combining infection experiments and 

genetics promises to answer these questions about the nature of 

coral innate immunity and the role of the coral host in responding to pathogen and symbiont infection. 

CONCLUSIONS

Great progress has been made in understanding the nature 

of the interactions within the coral holobiont since Rohwer et 

al. (2002) proposed the concept. We now have a much stronger 

understanding of the coral–algal symbiosis, including knowledge 

about its ontogeny, specificity, and flexibility. Knowledge about 

the nature of coral–microbe interactions is growing by leaps 

and bounds with increasing interest in coral microbiology and 

the incorporation of new (meta) genomic techniques to address 

questions about the makeup and dynamics of coral microbial 

assemblages. Knowledge about the role of the coral host is growing as we gain insights into the nature of coral innate immunity, 

including how pathogens are detected and how eukaryotic and/

or microbial symbionts modify response or elude detection. As 

we continue to progress, the concept of the coral holobiont will 

remain important because the greatest strides in the field will 

be made by understanding how the complex sets of organisms 

making up the coral holobiont— the coral host and associated 

eukarya, bacteria, archaea, and viruses—interact and function 

both synergistically and sometimes antagonistically as a community or ecosystem. 

ACKNOWLEDGMENTS

We thank Michael Lang, Phil Taylor, Roberta Marinelli, 

and Susan Roberts for organizing the symposium, the Smithsonian Institution and the National Science Foundation for 

providing funding and logistical support, and all our fellow 

participants. Additional funding was provided by National 
182 • smithsonian contributions to the marine sciences

Science Foundation grants to SVV (OCE-0848345), ACB (OCE0099301 and 0527184), MAC (04-24994 and 09-26822), MAC 

and MM (03-13708), and CDH and LM (OCE-0849799). ACB 

was also supported by grants from the Lenfest Ocean Program, 

the Tiffany and Co. Foundation, and a Pew Fellowship in Marine 

Conservation. 

REFERENCES

Abrego, D., M. J. H. van Oppen, and B. L. Willis. 2009a. Highly infectious symbiont 

dominates initial uptake in coral juveniles. Molecular Ecology, 18(16):3518–

3531. http://dx.doi.org/10.1111/j.1365-294X.2009.04275.x.

———. 2009b. Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Molecular Ecology,

18(16):3532–3543. http://dx.doi.org/10.1111/j.1365-294X.2009.04276.x.

Ainsworth, T. D., R. V. Thurber, and R. D. Gates. 2010. The future of coral reefs: 

A microbial perspective. Trends in Ecology and Evolution, 25(4):233–240. 

http://dx.doi.org/10.1016/j.tree.2009.11.001.

Alongi, D., and A. McKinnon. 2005. The cycling and fate of terrestrially-derived 

sediments and nutrients in the coastal zone of the Great Barrier Reef shelf.

Marine Pollution Bulletin, 51(1–4):239–252. http://dx.doi.org/10.1016/j

.marpolbul.2004.10.033.

Apprill, A. M. Y. M., and R. D. Gates. 2007. Recognizing diversity in coral symbiotic dinoflagellate communities. Molecular Ecology, 16(6):1127–1134. http://

dx.doi.org/10.1111/j.1365-294X.2006.03214.x.

Apprill, A., H. Marlow, M. Martindale, and M. Rappé. 2009. The onset of microbial associations in the coral Pocillopora meandrina. The ISME Journal,

3(6):685–699. http://dx.doi.org/10.1038/ismej.2009.3.

Baird, A. H., R. Bhagooli, P. J. Ralph, and S. Takahashi. 2009. Coral bleaching: the 

role of the host. Trends in Ecology and Evolution, 24(1):16–20.

Baker, A., and R. Rowan. 1997. Diversity of symbiotic dinoflagellates (zooxanthellae) in scleractinian corals of the Caribbean and eastern Pacific. Proceedings 

of the eighth International Coral Reef Symposium, 2:1301–1305. 

Baker, A. C. 1999. The symbiosis ecology of reef-building corals. Ph.D. diss., University of Miami, Coral Gables, Florida.

———. 2001. Reef corals bleach to survive change. Nature, 411:765–766. http://

dx.doi.org/10.1038/35081151.

———. 2003. Flexibility and specificity in coral–algal symbiosis: Diversity, ecology, 

and biogeography of Symbiodinium. Annual Review of Ecology, Evolution, 

and Systematics, 34:661–689. http://dx.doi.org/10.1146/annurev.ecolsys.34

.011802.132417.

———. 2004. Symbiont diversity on coral reefs and its relationship to bleaching 

resistance and resilience. In Coral health and disease, ed. E. Rosenberg and 

Y. Loya, pp. 177–194. Berlin: Springer. http://dx.doi.org/10.1007/978-3-662

-06414-6.

Baker, A. C., and A. M. Romanski. 2007. Multiple symbiotic partnerships are 

common in scleractinian corals, but not in octocorals: Comment on Goulet 

(2006). Marine Ecology Progress Series, 335:237–242. http://dx.doi.org/10

.3354/meps335237.

Baker, A. C., C. J. Starger, T. R. McClanahan, and P. R. Glynn. 2004. Corals’ 

adaptive response to climate change. Nature, 430:741. http://dx.doi.org/10

.1038/430741a.

Banin, E., T. Israely, A. Kushmaro, Y. Loya, E. Orr, and E. Rosenberg. 2000. Penetration of the coral-bleaching bacterium Vibrio shiloi into Oculina patagonica. 

Applied and Environmental Microbiology, 66(7):3031–3036. http://dx.doi

.org/10.1128/AEM.66.7.3031-3036.2000.

Belda-Baillie, C. A., B. K. Baillie, and T. Maruyama. 2002. Specificity of a model 

cnidarian–dinoflagellate symbiosis. The Biological Bulletin, 202(1):74. http://

dx.doi.org/10.2307/1543224.

Beman, J. M., K. J. Roberts, L. Wegley, F. Rohwer, and C. A. Francis. 2007. Distribution and diversity of archaeal ammonia monooxygenase genes associated 

with corals. Applied and Environmental Microbiology, 73(17):5642. http://

dx.doi.org/10.1128/AEM.00461-07.

Ben-Haim, Y., M. Zicherman-Keren, and E. Rosenberg. 2003. Temperatureregulated bleaching and lysis of the coral Pocillopora damicornis by the novel 

pathogen Vibrio coralliilyticus. Applied and Environmental Microbiology,

69(7):4236–4242. http://dx.doi.org/10.1128/AEM.69.7.4236-4242.2003.

Berkelmans, R., and M. J. H. van Oppen. 2006. The role of zooxanthellae in the 

thermal tolerance of corals: A ‘nugget of hope’ for coral reefs in an era of 

climate change. Proceedings of the Royal Society B: Biological Sciences,

273(1599):2305–2312. http://dx.doi.org/10.1098/rspb.2006.3567.

Bourne, D. G., M. Garren, T. M. Work, E. Rosenberg, G. W. Smith, and C. D. Harvell. 2009. Microbial disease and the coral holobiont. Trends in Microbiology, 17(12):554–562. http://dx.doi.org/10.1016/j.tim.2009.09.004.

Bourne, D. G., and C. B. Munn. 2005. Diversity of bacteria associated with the coral 

Pocillopora damicornis from the Great Barrier Reef. Environmental Microbiology, 7(8):1162–1174. http://dx.doi.org/10.1111/j.1462-2920.2005.00793.x.

Brown, B. 1997. Coral bleaching: Causes and consequences. Coral Reefs, 16(5): 

129–138. http://dx.doi.org/10.1007/s003380050249.

Buddemeier, R. W., A. C. Baker, D. G. Fautin, and J. R. Jacobs. 2004. The adaptive 

hypothesis of bleaching. In Coral health and disease, ed. E. Rosenberg and 

Y. Loya, pp. 427–444. Berlin: Springer. http://dx.doi.org/10.1007/978-3-662

-06414-6_24.

Buddemeier, R. W., and D. G. Fautin. 1993. Coral bleaching as an adaptive mechanism: A testable hypothesis. Bioscience, 43(5):320–326. http://dx.doi.org

/10.2307/1312064.

Carlos, A. A., B. K. Baillie, M. Kawachi, and T. Maruyama. 1999. Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living 

strain. Journal of Phycology, 35(5):1054–1062. http://dx.doi.org/10.1046/j

.1529-8817.1999.3551054.x.

Chen, C. A., K. K. Lam, Y. Nakano, and W. S. Tsai. 2003. A stable association 

of the stress-tolerant zooxanthellae, Symbiodinium clade D, with the lowtemperature-tolerant coral, Oulastrea crispata (Scleractinia: Faviidae) in subtropical non-reefal coral communities. Zoological Studies, 42:540–550.

Chen, C. A., J. T. Wang, L. S. Fang, and Y. W. Yang. 2005. Fluctuating algal symbiont 

communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. 

Marine Ecology Progress Series, 295:113–121. http://dx.doi.org/10.3354

/meps295113.

Coffroth, M. A., C. F. Lewis, S. R. Santos, and J. L. Weaver. 2006. Environmental 

populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Current Biology, 16(23):R985–R987. 

http://dx.doi.org/10.1016/j.cub.2006.10.049.

Coffroth, M. A., D. M. Poland, E. L. Petrou, D. A. Brazeau, and J. C. Holmberg. 

2010. Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals. PLoS One 5(10): e13258. http://dx.doi.org

/10.1371/journal.pone.0013258.

Coffroth, M. A., and S. R. Santos. 2005. Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist, 156(1):19–34. http://dx.doi.org

/10.1016/j.protis.2005.02.004.

Coffroth, M. A., S. R. Santos, and T. L. Goulet. 2001. Early ontogenetic expression 

of specificity in a cnidarian–algal symbiosis. Marine Ecology Progress Series,

222:85–96. http://dx.doi.org/10.3354/meps222085.

del C. Gómez-Cabrera, M., J. Ortiz, W. K. W. Loh, S. Ward, and O. Hoegh-Guldberg.

2008. Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of 

the coral Acropora longicyathus. Coral Reefs, 27(1):219–226. http://dx.doi

.org/10.1007/s00338-007-0315-x.

DeSalvo, M. K., S. Sunagawa, P. L. Fisher, C. R. Voolstra, R. Iglesias-Prieto, and M. 

Medina. 2010a. Coral host transcriptomic states are correlated with Symbiodinium genotypes. Molecular Ecology, 19(6):1174–1186. http://dx.doi

.org/10.1111/j.1365-294X.2010.04534.x.

DeSalvo, M. K., S. Sunagawa, C. R. Voolstra, and M. Medina. 2010b. Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora 

palmata. Marine Ecology Progress Series 402:97–113. http://dx.doi.org/10

.3354/meps08372.

DeSalvo, M. K., C. R. Voolstra, S. Sunagawa, J. A. Schwarz, J. H. Stillman, M. A.

Coffroth, A. M. Szmant, and M. Medina. 2008. Differential gene expression 

during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Molecular Ecology 17(17):3952–3971. http://dx.doi.org/10.1111/j

.1365-294X.2008.03879.x.

Dinsdale, E. A., R. A. Edwards, D. Hall, F. Angly, M. Breitbart, J. M. Brulc, M. Furlan, C. Desnues, M. Haynes, L. Li, L. McDaniel, M. A. Moran, K. E. Nelson, 

C. Nilsson, R. Olson, J. Paul, B. R. Brito, Y. Ruan, B. K. Swan, R. Stevens, D. L. 

Valentine, R. V. Thurber, L. Wegley, B. A. White, and F. Rohwer. 2008a. Functional metagenomic profiling of nine biomes. Nature, 452(7187):629–632. 

http://dx.doi.org/10.1038/nature06810.

Dinsdale, E. A., O. Pantos, S. Smriga, R. Edwards, F. Angly, L. Wegley, M. Hatay, 

D. Hall, E. Brown, M. Haynes, L. Krause, E. Sala, S. A. Sandin, R. V. Thurber, 
number 39 • 183

B. L. Willis, F. Azam, N. Knowlton, and F. Rohwer. 2008b. Microbial ecology 

of four coral atolls in the Northern Line Islands. PLoS One 3(2), http://dx

.doi.org/10.1371/journal.pone.0001584.

Douglas, A. 2003. Coral bleaching: How and why? Marine Pollution Bulletin, 

46(4):385–392. http://dx.doi.org/10.1016/S0025-326X(03)00037-7.

Dunn, S. R. 2009. Immunorecognition and immunoreceptors in the Cnidaria. Invertebrate Survival Journal, 6:7–14.

Dunn, S. R., and V. M. Weis. 2009. Apoptosis as a post-phagocytic winnowing 

mechanism in a coral–dinoflagellate mutualism. Environmental Microbiology, 11(1):268–276. http://dx.doi.org/10.1111/j.1462-2920.2008.01774.x.

Edmunds, P. J., and P. S. Davies. 1986. An energy budget for Porites porites (Scleractinia). Marine Biology, 92:339–347. http://dx.doi.org/10.1007/BF00392674.

Fabricius, K., J. Mieog, P. Colin, D. Idip, and M. H. van Oppen. 2004. Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with 

contrasting bleaching, temperature and shading histories. Molecular Ecology,

13(8):2445–2458. http://dx.doi.org/10.1111/j.1365-294X.2004.02230.x.

Falkowski, P. G., Z. Dubinsky, L. Muscatine, and J. W. Porter. 1984. Light and the 

bioenergetics of a symbiotic coral. Bioscience, 34(11):705–709. http://dx.doi

.org/10.2307/1309663.

Fautin, D. G., and R. W. Buddemeier. 2004. Adaptive bleaching: A general phenomenon. Hydrobiologia, 530(1):459–467.

Ferrer, L. M., and A. M. Szmant. 1988. Nutrient regeneration by the endolithic 

community in coral skeletons. Proceedings of the sixth International Coral 

Reef Symposium, 3:1–4.

Freudenthal, H. D. 1962. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: Taxonomy, life cycle and morphology. Journal 

of Protozoology, 9:45–52.

Frias-Lopez, J., A. L. Zerkle, G. T. Bonheyo, and B. W. Fouke. 2002. Partitioning 

of bacterial communities between seawater and healthy, black band diseased, 

and dead coral surfaces. Applied Environmental Microbiology, 68(5):2214–

2228. http://dx.doi.org/10.1128/AEM.68.5.2214-2228.2002.

Glynn, P. W., J. L. Mate, A. C. Baker, and M. O. Calderon. 2001. Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Nino–

Southern Oscillation event: Spatial/temporal patterns and comparisons with 

the 1982–1983 event. Bulletin of Marine Science, 69(1):79–109.

Goulet, T. L. 2006. Most corals may not change their symbionts. Marine Ecology 

Progress Series, 321:1–7. http://dx.doi.org/10.3354/meps321001.

Goulet, T. L., and M. A. Coffroth. 2003a. Genetic composition of zooxanthellae between and within colonies of the octocoral Plexaura kuna, based on 

small subunit rDNA and multilocus DNA fingerprinting. Marine Biology,

142(2):233–239.

———. 2003b. Stability of an octocoral–algal symbiosis over time and space. Marine Ecology Progress Series, 250:117–124. http://dx.doi.org/10.3354/meps

250117.

Goulet, T. L., T. C. LaJeunesse, and K. E. Fabricius. 2008. Symbiont specificity and 

bleaching susceptibility among soft corals in the 1998 Great Barrier Reef 

mass coral bleaching event. Marine Biology, 154(5):795–804. http://dx.doi

.org/10.1007/s00227-008-0972-5.

Grasso, L. C., J. Maindonald, S. Rudd, D. C. Hayward, R. Saint, D. J. Miller, and 

E. E. Ball. 2008. Microarray analysis identifies candidate genes for key roles in 

coral development. BMC Genomics, 9:540. http://dx.doi.org/10.1186/1471

-2164-9-540.

Hannes, A. R., M. Barbeitos, and M. A. Coffroth. 2009. Stability of symbiotic dinoflagellate type in the octocoral Briareum asbestinum. Marine Ecology Progress Series, 391:65–72. http://dx.doi.org/10.3354/meps07990.

Harvell, D., E. Jordán-Dahlgren, S. Merkel, E. Rosenberg, L. Raymundo, G. Smith, 

E. Weil, and B. Willis. 2007. Coral disease, environmental drivers, and the 

balance between coral and microbial associates. Oceanography, 20:172–195. 

http://dx.doi.org/10.5670/oceanog.2007.91.

Hildemann, W. H., D. S. Linthicum, and D. C. Vann. 1975. Transplantation and immunoincompatibility reactions among reef-building corals. Immunogenetics,

2(3):269–284. http://dx.doi.org/10.1007/BF01572295.

Hoegh-Guldberg, O. 1999. Climate change, coral bleaching and the future of the 

world’s coral reefs. Marine and Freshwater Research, 50(8):839–866. http://

dx.doi.org/10.1071/MF99078.

Howells, E. J., M. J. H. van Oppen, and B. L. Willis. 2009. High genetic differentiation and cross-shelf patterns of genetic diversity among Great Barrier Reef 

populations of Symbiodinium. Coral Reefs, 28(1):215–225.

Hughes, T. P., A. H. Baird, D. R. Bellwood, M. Card, S. R. Connolly, C. Folke, 

R. Grosberg, O. Hoegh-Guldberg, J. B. C. Jackson, J. Kleypas, J. M. Lough, 

P. Marshall, M. Nystrom, S. R. Palumbi, J. M. Pandolfi, B. Rosen, and 

J. Roughgarden. 2003. Climate change, human impacts, and the resilience 

of coral reefs. Science, 301(5635):929–933. http://dx.doi.org/10.1126/science

.1085046.

Iglesias-Prieto, R., V. H. Beltran, T. C. LaJeunesse, H. Reyes-Bonilla, and P. E. 

Thome. 2004. Different algal symbionts explain the vertical distribution of 

dominant reef corals in the eastern Pacific. Proceedings of the Royal Society B: Biological Sciences, 271(1549):1757–1763. http://dx.doi.org/10.1098

/rspb.2004.2757.

Iglesias-Prieto, R., and R. K. Trench. 1997. Photoadaptation, photoacclimation and 

niche diversification in invertebrate–dinoflagellate symbiosis. Proceedings of 

the eighth International Coral Reef Symposium, 2:1319–1324.

Jones, A. M., R. Berkelmans, M. J. H. van Oppen, J. C. Mieog, and W. Sinclair. 2008. 

A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: Field evidence of acclimatization. Proceedings of the Royal Society B: Biological Sciences, 275(1641):1359–1365. 

http://dx.doi.org/10.1098/rspb.2008.0069.

Kawaguti, S. 1944. On the physiology of reef corals. VII. Zooxanthellae of the reef 

corals is Gymnodinium sp. dinoflagellata; its culture in vitro. Palao Tropical 

Biological Station Studies, 2:675–680.

Kelman, D., A. Kushmaro, Y. Loya, Y. Kashman, and Y. Benayahu. 1998. Antimicrobial activity of a Red Sea soft coral, Parerythropodium fulvum fulvum: 

Reproductive and developmental considerations. Marine Ecological Progress 

Series, 169:87–95. http://dx.doi.org/10.3354/meps169087.

Kinzie, R. A., M. Takayama, S. R. Santos, and M. A. Coffroth. 2001. The adaptive 

bleaching hypothesis: Experimental tests of critical assumptions. Biological 

Bulletin, 200(1):51–58. http://dx.doi.org/10.2307/1543084.

Kirk, N. L., J. P. Andras, C. D. Harvell, S. R. Santos, and M. A. Coffroth. 2009. 

Population structure of Symbiodinium sp. associated with the common sea 

fan, Gorgonia ventalina, in the Florida Keys across distance, depth, and time. 

Marine Biology, 156(8):1609–1623. http://dx.doi.org/10.1007/s00227-009

-1196-z.

Kirk, N. L., J. R. Ward, and M. A. Coffroth. 2005. Stable Symbiodinium composition in the sea fan Gorgonia ventalina during temperature and disease stress. 

The Biological Bulletin, 209(3):227. http://dx.doi.org/10.2307/3593112.

Knowlton, N. 2001a. Ecology: Coral reef biodiversity—habitat size matters. Science, 292(5521):1493–1495. http://dx.doi.org/10.1126/science.1061690.

———. 2001b. The future of coral reefs. Proceedings of the National Academy 

of Sciences, 98(10):5419–5425. http://dx.doi.org/10.1073/pnas.091092998.

Kushmaro, A., Y. Loya, M. Fine, and E. Rosenberg. 1996. Bacterial infection and coral 

bleaching. Nature, 380(6573):396. http://dx.doi.org/10.1038/380396a0.

Kvennefors, E. C. E., W. Leggat, C. C. Kerr, T. D. Ainsworth, O. Hoegh-Guldberg,

and A. C. Barnes. 2010. Analysis of evolutionarily conserved innate immune 

components in coral links immunity and symbiosis. Developmental & Comparative Immunology, 34(11):1219–1229. http://dx.doi.org/10.1016/j.dci

.2010.06.016.

LaJeunesse, T. C. 2001. Investigating the biodiversity, ecology, and phylogeny of 

endosymbiotic dinoflagellates in the genus Symbiodinium using the its region: 

In search of a “species” level marker. Journal of Phycology, 37(5):866–880. 

http://dx.doi.org/10.1046/j.1529-8817.2001.01031.x.

———. 2002. Diversity and community structure of symbiotic dinoflagellates 

from Caribbean coral reefs. Marine Biology, 141(2):387–400. http://dx.doi

.org/10.1007/s00227-002-0829-2.

———. 2005. “Species” radiations of symbiotic dinoflagellates in the Atlantic and 

Indo-Pacific since the miocene–pliocene transition. Molecular Biology and 

Evolution, 22(3):570–581.

LaJeunesse, T. C., R. Bhagooli, M. Hidaka, L. DeVantier, T. Done, G. W. Schmidt, 

W. K. Fitt, and O. Hoegh-Guldberg. 2004a. Closely related Symbiodinium

spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Marine Ecology Progress 

Series, 284:147–161. http://dx.doi.org/10.3354/meps284147.

LaJeunesse, T. C., W. Loh, and R. K. Trench. 2009a. Do introduced endosymbiotic 

dinoflagellates ‘take’ to new hosts? Biological Invasions, 11(4):995–1003. 

http://dx.doi.org/10.1007/s10530-008-9311-5.

LaJeunesse, T. C., D. T. Pettay, E. M. Sampayo, N. Phongsuwan, B. Brown, D. O. 

Obura, O. Hoegh-Guldberg, and W. K. Fitt. 2010. Long-standing environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of 

coral endosymbionts in the genus Symbiodinium. Journal of Biogeography,

37(5):785–800. http://dx.doi.org/10.1111/j.1365-2699.2010.02273.x.

LaJeunesse, T. C., R. T. Smith, J. Finney, and H. Oxenford. 2009b. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean 
184 • smithsonian contributions to the marine sciences

mass coral ‘bleaching’ event. Proceedings of the Royal Society B: Biological 

Sciences, 276(1676):4139–4148. http://dx.doi.org/10.1098/rspb.2009.1405.

LaJeunesse, T. C., D. J. Thornhill, E. F. Cox, F. G. Stanton, W. K. Fitt, and G. W. 

Schmidt. 2004b. High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs,

23(4):596–603.

Lesser, M. P., C. H. Mazel, M. Y. Gorbunov, and P. G. Falkowski. 2004. Discovery 

of symbiotic nitrogen-fixing cyanobacteria in corals. Science, 305(5686):997. 

http://dx.doi.org/10.1126/science.1099128.

Lewis, C. L., and M. A. Coffroth. 2004. The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science, 304(5676):1490–1492. http://dx

.doi.org/10.1126/science.1097323.

Lin, K. L., J. T. Wang, and L. S. Fang. 2000. Participation of glycoproteins on zooxanthellal cell walls in the establishment of a symbiotic relationship with the 

sea anemone Aiptasia pulchella. Zoological Studies, 39:172–178.

Little, A. F., M. J. H. van Oppen, and B. L. Willis. 2004. Flexibility in algal endosymbioses shapes growth in reef corals. Science, 304(5676):1492–1494. http://

dx.doi.org/10.1126/science.1095733.

Littman, R. A., D. G. Bourne, and B. L. Willis. 2010. Responses of coral associated 

bacterial communities to heat stress differ with Symbiodinium type on the 

same coral host. Molecular Ecology, 19(9):1978–1990. http://dx.doi.org/10

.1111/j.1365-294X.2010.04620.x.

Littman, R. A., B. L. Willis, and D. G. Bourne. 2009a. Bacterial communities of 

juvenile corals infected with different Symbiodinium(dinoflagellate) clades. 

Marine Ecology Progress Series, 389:45–59. http://dx.doi.org/10.3354/meps

08180.

Littman, R. A., B. L. Willis, C. Pfeffer, and D. G. Bourne. 2009b. Diversities of coral 

associated bacteria differ with location, but not species, for three acroporid 

corals on the Great Barrier Reef. FEMS Microbiology Ecology, 68(2):152–

163. http://dx.doi.org/10.1111/j.1574-6941.2009.00666.x.

Mao-Jones, J., K. B. Ritchie, L. E. Jones, and S. P. Ellner. 2010. How microbial 

community composition regulates coral disease development. PLoS Biology,

8(3):e1000345. http://dx.doi.org/10.1371/journal.pbio.1000345.

Marhaver, K. L., R. A. Edwards, and F. Rohwer. 2008. Viral communities associated 

with healthy and bleaching corals. Environmental Microbiology, 10(9):2277–

2286.

McLaughlin, J. J. A., and P. A. Zahl. 1959. Axenic zooxanthellae from various invetebrate hosts. Annals of the New York Academy of Sciences, 77(2):55–72. 

http://dx.doi.org/10.1111/j.1749-6632.1959.tb36892.x.

———. 1966. Endozoic algae. Symbiosis 1:257–297.

Meyer, E., G. V. Aglyamova, S. Wang, J. Buchanan-Carter, D. Abrego, J. K. Colbourne, B. L. Willis, and M. V. Matz. 2009. Sequencing and de novo analysis 

of a coral larval transcriptome using 454 GSFlx. BMC Genomics, 10:209. 

http://dx.doi.org/10.1186/1471-2164-10-219.

Meyer, E., and M. V. Matz. 2010. Expression profiling coral responses to thermal 

stress and settlement cues using RNA-Seq. Integrative and Comparative Biology, 50:E117.

Mieog, J. C., M. J. H. van Oppen, R. Berkelmans, W. T. Stam, and J. L. Olsen. 

2009. Quantification of algal endosymbionts (Symbiodinium) in coral tissue 

using real-time PCR. Molecular Ecology Resources, 9(1):74–82. http://dx.doi

.org/10.1111/j.1755-0998.2008.02222.x.

Miller, D. J., G. Hemmrich, E. E. Ball, D. Hayward, K. Khalturin, N. Funayama, 

K. Agata, and T. C. G. Bosch. 2007. The innate immune repertoire in Cnidaria -

ancestral complexity and stochastic gene loss. Genome Biology, 8(RS59):1–13.

Mouchka, M. E., I. Hewson, and C. D. Harvell. 2010. Coral-associated bacterial assemblages: Current knowledge and the potential for climate-driven impacts.

Integrative and Comparative Biology, http://dx.doi.org/10.1093/icb/icq061.

Muscatine, L. 1973. Nutrition of corals. In Biology and geology of coral reefs, ed. 

O. A. Jones and R. Endean, pp. 77–115. New York: Academic Press. http://

dx.doi.org/10.1016/B978-0-12-395526-5.50012-2.

Muscatine, L., L. R. McCloskey, and R. E. Marian. 1981. Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnology 

and Oceanography, 26:601–611. http://dx.doi.org/10.4319/lo.1981.26.4.0601.

Mydlarz, L. D., C. S. Couch, E. Weil, G. Smith, and C. D. Harvell. 2009. Immune 

defenses of healthy, bleached and diseased Montastraea faveolata during a 

natural bleaching event. Diseases of Aquatic Organisms, 87(1–2):67–78. 

http://dx.doi.org/10.3354/dao02088.

Mydlarz, L. D., and C. D. Harvell. 2007. Peroxidase activity and inducibility in the 

sea fan coral exposed to a fungal pathogen. Comparative Biochemistry and 

Physiology Part A: Molecular & Integrative Physiology, 146(1):54–62. http://

dx.doi.org/10.1016/j.cbpa.2006.09.005.

Mydlarz, L., S. Holthouse, E. Peters, and C. Harvell. 2008. Cellular responses in sea 

fan corals: Granular amoebocytes react to pathogen and climate stressors. 

PLoS One, 3(3). http://dx.doi.org/10.1371/journal.pone.0001811.

Mydlarz, L. D., L. E. Jones, and C. D. Harvell. 2006. Innate immunity environmental drivers and disease ecology of marine and freshwater invertebrates. 

Annual Review of Ecology, Evolution and Systematics, 37:251–288. http://

dx.doi.org/10.1146/annurev.ecolsys.37.091305.110103.

Mydlarz, L. D., E. S. McGinty, and C. D. Harvell. 2010. What are the physiological 

and immunological responses of coral to climate warming and disease? Journal of Experimental Biology, 213(6):934–945. http://dx.doi.org/10.1242/jeb

.037580.

Neigel, J. E., and J. C. Avise. 1983. Clonal diversity and population structure in a 

reef-building coral, Acropora cervicornis: Self-recognition analysis and demographic interpretation. Evolution, 37(3):437–453. http://dx.doi.org/10

.2307/2408259.

Nissimov, J., E. Rosenberg, and C. B. Munn. 2009. Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiology Letters, 292(2):210–215. http://dx.doi.org/10.1111/j.1574-6968.2009.01490.x.

Nyholm, S., and M. McFall-Ngai. 2004. The winnowing: Establishing the squid–

Vibrio symbiosis. Nature Reviews Microbiology, 2(8):632–642. http://dx.doi

.org/10.1038/nrmicro957.

Palmer, C. V., L. D. Mydlarz, and B. L. Willis. 2008. Evidence of an inflammatorylike response in non-normally pigmented tissues of two scleractinian corals.

Proceedings of the Royal Society B: Biological Sciences, 275(1652):2687–

2693. http://dx.doi.org/10.1098/rspb.2008.0335.

Palmer, C. V., C. K. Modi, and L. D. Mydlarz. 2009. Coral fluorescent proteins as 

antioxidants. PLoS ONE, 4:e7298.

Palmer, C. V., J. C. Bythell, and B. L. Willis. 2010. Levels of immunity parameters 

underpin bleaching and disease susceptibility of reef corals. The Federation 

of American Societies for Experimental Biology Journal, 24(6):1935–1946.

Pantos, O., and J. C. Bythell. 2006. Bacterial community structure associated with 

white band disease in the elkhorn coral Acropora palmata determined using 

culture-independent 16S rRNA techniques. Diseases of Aquatic Organisms,

69(1):79–88. http://dx.doi.org/10.3354/dao069079.

Pedros-Alio, C. 2007. Ecology: Dipping into the rare biosphere. Science,

315(5809):192–193. http://dx.doi.org/10.1126/science.1135933.

Pochon, X., and R. D. Gates. 2010. A new Symbiodinium clade (Dinophyceae) 

from soritid foraminifera in Hawai’i. Molecular Phylogenetics and Evolution, 

56:492–497. http://dx.doi.org/10.1016/j.ympev.2010.03.040.

Pochon, X., T. C. LaJeunesse, and J. Pawlowski. 2004. Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts 

(Symbiodinium; Dinophyta). Marine Biology, 146(1):17–27. http://dx.doi

.org/10.1007/s00227-004-1427-2.

Pochon, X., J. Pawlowski, L. Zaninetti, and R. Rowan. 2001. High genetic diversity 

and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Marine Biology, 139(6):1069–1078. http://dx

.doi.org/10.1007/s002270100674.

Poland, D. M. 2010. Specificity versus flexibility in cnidarian–algal symbioses. Master’s thesis, State University of New York at Buffalo, Buffalo.

Poland, D. M,, J. M. Mansfield, A. R. Hannes, C. L. F. Lewis, T. L. Shearer, S. J. 

Connelly, N. L. Kirk, and M. A. Coffroth. 2013. Variation in Symbiodinium

communities in juvenile Briareum asbestinum (Cnidaria: Octocorallia) over 

temporal and spatial scales. Marine Ecology Progress Series, 476:23–37.

Polato, N. R., C. R. Voolstra, J. Schnetzer, M. K. DeSalvo, C. J. Randall, A. M. Szmant, M. Medina, and I. B. Baums. 2010. Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata. PLoS 

One, 5(6). http://dx.doi.org/10.1371/journal.pone.0011221.

Portune, K. J., C. R. Voolstra, M. Medina, and A. M. Szmant. 2010. Development 

and heat stress–induced transcriptomic changes during embryogenesis of the 

scleractinian coral Acropora palmata. Marine Genomics, 3(1):51–62. http://

dx.doi.org/10.1016/j.margen.2010.03.002.

Reyes-Bermudez, A., M. K. DeSalvo, C. R. Voolstra, S. Sunagawa, A. M. Szmant, R. 

Iglesias-Prieto, and M. Medina. 2009. Gene expression microarray analysis 

encompassing metamorphosis and the onset of calcification in the scleractinian coral Montastraea faveolata. Marine Genomics, 2(3–4):149–159. http://

dx.doi.org/10.1016/j.margen.2009.07.002.

Ritchie, K. B. 2006. Regulation of microbial populations by coral surface mucus 

and mucus- associated bacteria. Marine Ecology Progress Series, 322:1–14. 

http://dx.doi.org/10.3354/meps322001.

Rodriguez-Lanetty, M., and O. Hoegh-Guldberg. 2003. Symbiont diversity within 

the widespread scleractinian coral Plesiastrea versipora across the north-
number 39 • 185

western Pacific. Marine Biology, 143(3):501–509. http://dx.doi.org/10.1007

/s00227-003-1105-9.

Rodriguez-Lanetty, M., D. A. Krupp, and V. M. Weis. 2004. Distinct ITS types of 

Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Marine Ecology Progress Series, 275:97–102. 

http://dx.doi.org/10.3354/meps275097.

Rodriguez-Lanetty, M., W. S. Phillips, and V. M. Weis. 2006. Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of 

host gene expression. BMC Genomics, 7:23. http://dx.doi.org/10.1186/1471

-2164-7-23.

Rohwer, F., V. Seguritan, F. Azam, and N. Knowlton. 2002. Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series, 243:1–10. 

http://dx.doi.org/10.3354/meps243001.

Rosenberg, E. 2007. Coral microbiology. Oceanography, 20:146–154. http://dx

.doi.org/10.5670/oceanog.2007.60.

Rosenberg, E., O. Koren, L. Reshef, R. Efrony, and I. Zilber-Rosenberg. 2007. The 

role of microorganisms in coral health, disease and evolution. Nature Reviews Microbiology, 5(5):355–362. http://dx.doi.org/10.1038/nrmicro1635.

Rowan, R. 1991. Molecular systematics of symbiotic algae. Journal of Phycology,

27:661–666. http://dx.doi.org/10.1111/j.0022-3646.1991.00661.x.

Rowan, R., and N. Knowlton. 1995. Intraspecific diversity and ecological zonation 

in coral–algal symbiosis. Proceedings of the National Academy of Sciences, 

92(7):2850–2853. http://dx.doi.org/10.1073/pnas.92.7.2850.

Rowan, R., N. Knowlton, A. Baker, and J. Jara. 1997. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature,

388(6639):265–269. http://dx.doi.org/10.1038/40843.

Rowan, R., and D. Powers. 1991. Molecular genetic identification of symbiotic 

dinoflagellates (zooxanthellae). Marine Ecology Progress Series, 71:65–73. 

http://dx.doi.org/10.3354/meps071065.

Rypien, K. L., J. R. Ward, and F. Azam. 2010. Antagonistic interactions among coralassociated bacteria. Environmental Microbiology, 12(1):28–39. http://dx.doi

.org/10.1111/j.1462-2920.2009.02027.x.

Santos, S. R., C. Gutierrez-Rodriguez, H. R. Lasker, and M. A. Coffroth. 2003. Symbiodinium sp. associations in the gorgonian Pseudopterogorgia elisabethae

in the Bahamas: High levels of genetic variability and population structure 

in symbiotic dinoflagellates. Marine Biology, 143(1):111–120. http://dx.doi

.org/10.1007/s00227-003-1065-0.

Santos, S. R., T. L. Shearer, A. R. Hannes, and M. A. Coffroth. 2004. Fine-scale 

diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyceae) of the Caribbean. Molecular Ecology,

13(2):459–469. http://dx.doi.org/10.1046/j.1365-294X.2003.02058.x.

Santos, S. R., D. J. Taylor, and M. A. Coffroth. 2001. Genetic comparisons of freshly 

isolated versus cultured symbiotic dinoflagellates: Implications for extrapolating to the intact symbiosis. Journal of Phycology, 37(5):900–912. http://

dx.doi.org/10.1046/j.1529-8817.2001.00194.x.

Schwarz, J. A., P. B. Brokstein, C. R. Voolstra, A. Y. Terry, D. J. Miller, A. M. Szmant, 

M. A. Coffroth, and M. Medina. 2008. Coral life history and symbiosis: 

Functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. BMC Genomics, 9(1):97. http://dx

.doi.org/10.1186/1471-2164-9-97.

Schwarz, J. A., D. A. Krupp, and V. M. Weis. 1999. Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biological Bulletin

196(1):70–79. http://dx.doi.org/10.2307/1543169.

Sharp, K. H., K. B. Ritchie, P. J. Schupp, R. Ritson-Williams, and V. J. Paul. 2010. 

Bacterial acquisition in juveniles of several broadcast spawning coral species. 

PLoS One, 5(5). http://dx.doi.org/10.1371/journal.pone.0010898.

Shnit-Orland, M., and A. Kushmaro. 2009. Coral mucus-associated bacteria: A 

possible first line of defense. FEMS Microbiology Ecology, 67(3):371–380. 

http://dx.doi.org/10.1111/j.1574-6941.2008.00644.x.

Sogin, M. L., H. G. Morrison, J. A. Huber, D. M. Welch, S. M. Huse, P. R. Neal, J. M. 

Arrieta, and G. J. Herndl. 2006. Microbial diversity in the deep sea and the 

underexplored “rare biosphere.” Proceedings of the National Academy of Sciences, 103(32):12115–12120. http://dx.doi.org/10.1073/pnas.0605127103.

Stat, M., D. Carter, and O. Hoegh-Guldberg. 2006. The evolutionary history of 

Symbiodinium and scleractinian hosts: Symbiosis, diversity, and the effect 

of climate change. Perspectives in Plant Ecology Evolution and Systematics,

8(1):23–43. http://dx.doi.org/10.1016/j.ppees.2006.04.001.

Stern, R. F., A. Horak, R. L. Andrew, M. A. Coffroth, R. A. Andersen, F. C. Küpper, 

I. Jameson, M. Hoppenrath, B. Véron, and F. Kasai. 2010. Environmental 

barcoding reveals massive dinoflagellate diversity in marine environments. 

PLoS One, 5(11):e13991. http://dx.doi.org/10.1371/journal.pone.0013991.

Sunagawa, S., T. DeSantis, Y. Piceno, E. Brodie, M. DeSalvo, C. Voolstra, E. Weil, 

G. Andersen, and M. Medina. 2009. Bacterial diversity and White Plague 

Disease-associated community changes in the Caribbean coral Montastraea 

faveolata. The ISME Journal, 3(5):512–521. http://dx.doi.org/10.1038/ismej

.2008.131.

Sunagawa, S., C. M. Woodley, and M. Medina. 2010. Threatened corals provide underexplored microbial habitats. PLoS One 5(3):e9554. http://dx.doi.org/10

.1371/journal.pone.0009554.

Sutherland, K. P., J. W. Porter, and C. Torres. 2004. Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Marine Ecology Progress Series,

266:273–302. http://dx.doi.org/10.3354/meps266273.

Taylor, D. L. 1971. Ultrastructure of the ‘Zooxanthella’ Endodinium Chattonii in 

Situ. Journal of the Marine Biological Association of the United Kingdom,

51(01):227–234. http://dx.doi.org/10.1017/S0025315400006585.

———. 1974. Symbiotic marine algae: Taxonomy and biological fitness. Columbia, 

S.C.: University of South Carolina Press.

Thornhill, D. J., M. W. Daniel, T. C. LaJeunesse, G. W. Schmidt, and W. K. Fitt. 2006. 

Natural infections of aposymbiotic Cassiopea xamachana scyphistomae 

from environmental pools of Symbiodinium. Journal of Experimental Marine Biology and Ecology, 338(1):50–56. http://dx.doi.org/10.1016/j.jembe

.2006.06.032.

Thornhill, D. J., Y. Xiang, W. K. Fitt, and S. R. Santos. 2009. Reef endemism, host 

specificity and temporal stability in populations of symbiotic dinoflagellates 

from two ecologically dominant Caribbean corals. PLoS One 4(7). http://

dx.doi.org/10.1371/journal.pone.0006262.

Thurber, R. V., D. Willner-Hall, B. Rodriguez-Mueller, C. Desnues, R. A. Edwards, 

F. Angly, E. Dinsdale, L. Kelly, and F. Rohwer. 2009. Metagenomic analysis 

of stressed coral holobionts. Environmental Microbiology, 11(8):2148–2163. 

http://dx.doi.org/10.1111/j.1462-2920.2009.01935.x.

Trench, R. K. 1989. The genetic basis of specificity in dinoflagellate–invertebrate 

symbiosis: Separation of dinoflagellate cell wall proteins. First Annual Report, 

Office of Naval Research contract #N00014-88-K0463.

———. 1992. Microalgal–invertebrate symbiosis: Current trends. Encyclopedia of 

Microbiology, 3:129–142.

———. 1993. Microalgal–invertebrate symbioses: A review. Endocytobiosis Cell 

Research, 9:135–175.

Van Oppen, M. J. H., and R. D. Gates. 2006. Conservation genetics and the resilience of reef-building corals. Molecular Ecology, 15(13):3863–3883. http://

dx.doi.org/10.1111/j.1365-294X.2006.03026.x.

Van Oppen, M. J. H., J. C. Mieog, C. A. Sanchez, and K. E. Fabricius. 2005. Diversity of algal endosymbionts (zooxanthellae) in octocorals: The roles of geography and host relationships. Molecular Ecology, 14(8):2403–2417. http://dx

.doi.org/10.1111/j.1365-294X.2005.02545.x.

Vega Thurber, R., D. Willner-Hall, B. Rodriguez-Mueller, C. Desnues, R. A. Edwards, 

F. Angly, E. Dinsdale, L. Kelly, and F. Rohwer. 2009. Metagenomic analysis 

of stressed coral holobionts. Environmental Microbiology, 11(8):2148–2163. 

http://dx.doi.org/10.1111/j.1462-2920.2009.01935.x.

Vega Thurber, R. L., K. L. Barott, D. Hall, H. Liu, B. Rodriguez-Mueller, C. Desnues, 

R. A. Edwards, M. Haynes, F. E. Angly, L. Wegley, and F. L. Rohwer. 2008. 

Metagenomic analysis indicates that stressors induce production of herpeslike viruses in the coral Porites compressa. Proceedings of the National 

Academy of Sciences, 105(47):18413–18418. http://dx.doi.org/10.1073/pnas

.0808985105.

Voolstra, C. R., J. Schnetzer, L. Peshkin, C. J. Randall, A. M. Szmant, and M. Medina. 2009a. Effects of temperature on gene expression in embryos of the 

coral Montastraea faveolata. BMC Genomics, 10:627. http://dx.doi.org/10

.1186/1471-2164-10-627.

Voolstra, C. R., J. A. Schwarz, J. Schnetzer, S. Sunagawa, M. K. DeSalvo, A. M. Szmant,

M. A. Coffroth, and M. Medina. 2009b. The host transcriptome remains unaltered during the establishment of coral–algal symbioses. Molecular Ecology,

18(9):1823–1833. http://dx.doi.org/10.1111/j.1365-294X.2009.04167.x.

Ware, J. R., D. G. Fautin, and R. W. Buddemeier. 1996. Patterns of coral bleaching: 

Modeling the adaptive bleaching hypothesis. Ecological Modelling, 84(1–3): 

199–214. http://dx.doi.org/10.1016/0304-3800(94)00132-4.

Wegley, L., R. Edwards, B. Rodriguez-Brito, H. Liu, and F. Rohwer. 2007. Metagenomic analysis of the microbial community associated with the coral 

Porites astreoides. Environmental Microbiology, 9(11): 2707–2719. http://dx

.doi.org/10.1111/j.1462-2920.2007.01383.x

Wegley, L., Y. N. Yu, M. Breitbart, V. Casas, D. I. Kline, and F. Rohwer. 2004. 

Coral-associated archaea. Marine Ecology Progress Series, 273:89–96. http://

dx.doi.org/10.3354/meps273089.
186 • smithsonian contributions to the marine sciences

Weis, V. M. 2008. Cellular mechanisms of Cnidarian bleaching: Stress causes the 

collapse of symbiosis. Journal of Experimental Biology, 211(19):3059–3066. 

http://dx.doi.org/10.1242/jeb.009597.

Weis, V. M., and D. Allemand. 2009. Physiology: What determines coral health? 

Science, 324(5931):1153–1155. http://dx.doi.org/10.1126/science.1172540.

Weis, V. M., S. K. Davy, O. Hoegh-Guldberg, M. Rodriguez-Lanetty, and J. R.

Pringe. 2008. Cell biology in model systems as the key to understanding 

corals. Trends in Ecology & Evolution, 23(7):369–376. http://dx.doi.org/10

.1016/j.tree.2008.03.004.

Weis, V. M., W. S. Reynolds, M. D. deBoer, and D. A. Krupp. 2001. Host–symbiont 

specificity during onset of symbiosis between the dinoflagellates Symbodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral 

Reefs, 20(3):301–308. http://dx.doi.org/10.1007/s003380100179.

Wood-Charlson, E. M., L. L. Hollingsworth, D. A. Krupp, and V. M. Weis. 2006. Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cellular Microbiology, 8(12):1985–1993. http://dx.doi.org/10.1111/j

.1462-5822.2006.00765.x.
The Nature of Macroalgae 

and Their Interactions on Reefs

Mark M. Littler and Diane S. Littler

ABSTRACT. What was known about tropical reef algae prior to the use of scuba came largely 

from dredging studies or drift collections, which usually resulted in highly mutilated specimens and 

questionable habitat data. Scuba allows a precise determination of ecological conditions and permits 

in situ photography, two techniques our group has relied on during the past three decades for quantitative studies and field guide production. A goal of this review is to familiarize the scientific diving 

community with the kinds and roles of algae on tropical reefs, with the hope that seaweeds will be 

utilized more fully as tools for addressing important ecological questions.

Because of the rapid degradation of tropical reefs worldwide, it is imperative that 

the role and diversity of macroalgae be studied in a timely, efficient, and scientifically verifiable manner. It is of paramount importance to characterize the world’s 

coral reef environments and to understand the responses of foundation species. The fleshy 

macroalgal forms are the food of herbivores, and only become abundant when their production rate exceeds the capacity of herbivores to consume them. On healthy oligotrophic 

coral reefs, even very low nutrient increases may shift relative dominance from corals 

(Cnidaria) to macroalgae by both stimulating macroalgal production and inhibiting corals. As a result, frondose macroalgae are generally recognized as harmful to the longevity 

of coral reefs due to the link between excessive blooms and coastal eutrophication.

Reef plant complexity has evolved along very different evolutionary lines. The range 

of sizes, shapes, life histories, pigments, and biochemical and physiological pathways is 

remarkable. The biodiversity of coral reef plant life is unequalled. Macroalgae from four 

evolutionary lines dominate and, in conjunction with coelenterate corals, are the primary 

producers and builders of coral reef habitats and carbonate architecture. Previously, marine plants were understudied on coral reefs; however, new scuba-based field guides are 

alleviating this problem. Their rapid growth and short generation time make them ideal 

subjects for experimental studies.

INTRODUCTION

While extensive taxonomic and distributional data were derived before diving was 

common in the collection of algae (Boergesen, 1916; Taylor, 1960), scuba has afforded 

science the opportunity to greatly expand the understanding of the nature of macroalgal 

diversity with new species, new distribution data, and the mechanisms by which diversity 

is produced and maintained in reef systems. This of course is true for all three groups of 

eukaryotic algae—Rhodophyta (red algae), Chlorophyta (green algae), and Phaeophyceae 

Mark M. Littler and Diane S. Littler, formerly 

of Department of Botany, National Museum of 

Natural History, Smithsonian Institution, P.O. 

Box 37012, MRC 166, Washington, District of 

Columbia 20013-7012, USA.

Manuscript received 25 January 2012; accepted 5 March 2013.
188 • smithsonian contributions to the marine sciences

(brown algae)—as well as the larger prokaryotic, colony-forming 

cyanobacteria/Cyanophyta (blue-green algae). These four groups 

do not have a common ancestor (i.e., collectively polyphyletic) 

although chloroplasts—common to all the eukaryotes—appear 

to have had a single blue-green algal (cyanobacteria) origin. The 

presence of chloroplasts and subsequent capacity for photosynthesis gives marine macroalgae ecological roles as primary 

producers that are similar to other marine plants, notably sea 

grasses. Sea grasses are not seaweeds; rather, they are rooted 

flower- and seed-bearing “higher” plants (Angiosperms). 

The macroalgal thallus (i.e., plant body) consists of filaments, sheets and blades (leaflike laminae), reproductive sori 

(spore clusters), gas bladders (floatation organs on blades in 

rockweeds, and between lamina and stipes in kelps), stipes (stemlike structures [may be absent]), and holdfasts (with or without 

haptera, fingerlike extensions anchored to substrates). The stipe 

and blade combined are known as the frond.

Macroalgae grow attached to stable substrata in seawater 

(or brackish water) under light levels sufficient for photosynthesis. Seaweeds are most commonly found in shallow waters 

on rocky shores; however, the giant-celled green algal group 

Bryopsidales includes rhizoidal forms adapted to proliferating 

in sedimentary environments. At the shallowest level are algae 

that inhabit the high-intertidal spray zone whereas at the deepest level are forms attached to the seabed under as much as 295 

m of water (Littler and Littler, 1994; see Littler and Littler, this 

volume: “Coralline Algae,” fig. 13,). The deepest macroalgae are 

calcified crustose coralline species (Rhodophyta).

HUMAN UTILIZATION OF MACROALGAE

Macroalgae have a variety of uses. They are utilized extensively as food by coastal cultures, particularly in Southeast Asia. 

Seaweeds are also harvested or cultivated using scuba or hookah 

for the extraction of alginate, agar, and carrageenan—gelatinous 

substances collectively known as hydrocolloids or phycocolloids. 

Colloids have great commercial importance, especially in the production of food additives. The gelling, water-retention, emulsifying, and other physical properties of colloids are critical to the 

food industry. Agar is used in foods such as candies, canned meats, 

desserts, bottled drinks, and gelatin molds. Carrageenan is used in 

the manufacture of salad dressings, condiments, and dietary foods, 

and as a preservative in canned meat and fish, milk products, and 

bakery goods. Alginates are utilized for many of the same purposes as carrageenan, but are also used in the production of paper 

sizings, glues, colorings, gels, explosive stabilizers, fabric prints, 

hydrosprays, and drill lubricants. Macroalgae have long been used 

as fertilizers and soil conditioners. Seaweeds are currently being 

investigated as sources of biodiesel and biomethane. Algal extracts 

are also widely used in toothpastes, cosmetics, and paints.

In the biomedical and pharmaceutical industries, alginates 

are used in wound dressings and production of dental molds. In 

diagnostic microbiological research, agar is the culture substrate 

of choice for pathogens. Seaweeds are also sources of iodine, an 

element necessary for human thyroid function. The vast array of 

natural products that algae produce represents a gold mine of 

potential medicinal compounds and is presently being investigated using both scuba and submersibles.

ECOLOGICAL SIGNIFICANCE 

OF MACROALGAE

The concepts of top-down and bottom-up controls have 

long been used (e.g., Atkinson and Grigg, 1984; Carpenter et al., 

1985) to describe mechanisms where either the actions of predators or resource availability regulates the structure of aquatic 

communities. These opposing concepts can be particularly useful in understanding complex coral reef ecosystems. The Relative 

Dominance Model (RDM; first proposed by Littler and Littler, 

1984) predicts that the competitive outcomes determining the 

relative abundances of corals, crustose coralline algae, microalgal turfs, and frondose macroalgae on coral reefs are most often 

controlled by the complex interactions of environmental factors 

(bottom-up controls such as nutrient levels) and biological factors (top-down controls such as grazing).

The study of top-down control of macroalgae by abundant 

populations of large mobile herbivores is particularly well developed for coral reefs, beginning over five decades ago with the 

caging study of Stephenson and Searles (1960). As examples, 

Sammarco et al. (1974), Ogden and Lobel (1978), Sammarco 

(1983), Carpenter (1986), Lewis (1986), Morrisson (1988), and 

numerous other researchers (reviewed by McCook et al., 2001) 

have demonstrated that lowering herbivory usually results in 

rapid increases in fleshy algae. However, when coral reefs are exposed to increases in nutrients, fleshy macroalgae (Figure 1) may 

be favored over the slower-growing but highly desirable corals 

(Lapointe et al., 1997). On healthy oligotrophic coral reefs, even 

very low nutrient increases may exceed critical levels and shift 

relative dominances by stimulating macroalgal biomass production while inhibiting corals (Littler and Littler, 1984). Large biomasses/standing stocks of slow-growing perennial macroalgae 

(e.g., rockweeds) can, given sufficient time, develop even under 

low inorganic nutrient concentrations (McCook, 1999). Also, 

Sargassum spp. can coexist with corals in oligotrophic waters 

by utilizing particulate organic sources of nutrients (Schaffelke, 

1999). This information suggests that large macroalgal biomasses do not necessarily require, nor indicate, detrimentally 

abundant dissolved nutrients. 

Fleshy macroalgae can outcompete corals (Birkeland, 1977; 

Bellwood et al., 2006), many of which are inhibited under elevated nutrient levels (reviewed in Marubini and Davies, 1996). 

Fast-growing macroalgae are opportunists that benefit from 

disturbances, which release space resources from established, 

longer-lived organisms. They can also take over space from living 
number 39 • 189

corals (Birkeland, 1977) when provided with sufficient nutrients. 

As a result, frondose macroalgae (those that form carpets of 

horizontal thalli) are generally recognized as harmful to coral 

reefs due to the link between excessive blooms of these algae and 

coastal eutrophication (Anderson, 1995). The competitive dominance of fast-growing macroalgae is inferred from their overshadowing canopy heights as well as from inverse correlations in 

abundances between algae and other benthic producers (Lewis, 

1986), particularly under elevated nutrient concentrations (e.g., 

Littler et al., 1993; Lapointe et al., 1997). Macroalgae, such as 

Halimeda spp. (Figure 2), also can gain competitive advantage 

by serving as carriers of coral diseases (Nugues et al., 2004). 

The fleshy 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 lowered or 

swamped by excessive algal growth (chemically defended forms 

such as cyanobacteria [Figure 3; Paul et al., 2007] are exceptions). Overcompensation with high levels of herbivory may 

explain some of the reported cases (e.g., Smith et al., 2001) of 

specific corals surviving high-nutrient coral reef environments.

FIGURE 1. Ecological interactions (competition) between coral and algae. Top left: Coelothrix irregularis. Top right: Laurencia obtusa. Bottom 

left: Dictyota cervicornis. Bottom right: Halimeda opuntia. (Photos by D. Littler.)
190 • smithsonian contributions to the marine sciences

MAJOR MACROALGAL GROUPS

What was known about tropical reef algae prior to the use 

of scuba came largely from shipboard dredging studies or drift 

collections. These often produced highly mutilated specimens 

and lacked habitat data since the scope of the dredge cable varied greatly. Scuba allows a precise determination of ecological 

conditions and permits in situ photography, two techniques our 

group has relied on during the past three decades for quantitative 

studies and field guide production. A goal of our three reviews 

in this volume is to familiarize the scientific diving community 

with the kinds and roles of algae on tropical reefs, with the hope 

that seaweeds will be utilized more fully as tools for addressing 

important ecological questions. The critical role that seaweeds 

play in reef ecosystems overlaps other fields of marine sciences, 

such as fisheries resources, marine chemistry, ecology, geology, 

and coral reef conservation.

Rhodophyta (Red Algae)

Rhodophyta generally have large quantities of the red pigment phycoerythrin in their photosynthetic cells. This red pigment in combination with various other pigments is responsible 

for the vast array of colors ranging from translucent pale pink, 

lavender, purple, maroon, and burgundy to iridescent blue (Figure 4). The pigment phycoerythrin is water soluble; therefore, 

red algae immersed in hot water will stain the liquid red or 

pink and the thalli will eventually turn green. Other red-algal 

cellular characteristics include eukaryotic cells lacking motile 

gametes (without flagella and centrioles), floridean starch as the 

food reserve, and (if present) chloroplasts containing unstacked 

thylakoids without an external endoplasmic reticulum. Pit connections and pit plugs are unique and distinctive features of red 

algae that form during the process of cytokinesis following mitosis. Most red algae are also multicellular, macroscopic, and reproduce sexually. They display alternation of life-history phases 

including a gametophyte phase and two sporophyte phases.

The red algae are almost exclusively marine and are the 

largest and most diversified group of tropical reef plants, with 

population estimates of up to 10,000 species. The diversity of 

their forms is astonishing, ranging from small filamentous turfs 

to some of the larger and most beautifully delicate organisms on 

coral reefs (Figure 4). Calcareous red algae can dominate some 

reefs and often surpass corals in reef-building importance (e.g.,

Porolithon (Hydrolithon) craspedium; Figure 5). Most often, 

corals (Cnidaria) supply the bulk building blocks whereas coralline algae do much of the cementing together of debris. The 

crustose coralline algae (forms that deposit a type of calcium 

carbonate [calcite] that is harder and denser than the aragonite 

of corals) also build the algal ridge (see Littler and Littler, this 

volume: “Coralline Algae,” fig. 9) on many reef systems. By absorbing wave energy, the raised algal ridge not only protects land 

masses that would otherwise erode, but also shelters the more 

delicate corals and other reef organisms. 

FIGURE 2. Halimeda opuntia overgrowing coral. (Photo by 

D. Littler.)

FIGURE 3. Lyngbya polychroa, a chemically defended blue-green

alga. (Photo by D. Littler.)
number 39 • 191

FIGURE 4. Different forms and colors of red algae. Top left: Halymenia sp. Top right: Osmudea pinnatifida. Middle left: Dasya iridescens. 

Middle right: Halymenia maculata. Bottom left: Carpopeltis maillardii. Bottom right: Dudresnaya hawaiiensis. (Photos by D. Littler.)
192 • smithsonian contributions to the marine sciences

Phaeophyceae (Brown Algae)

Phaeophyceae contain large quantities of the brown pigment 

fucoxanthin. They have cellulose walls; alginic acid and fucoidin 

are also important components. Brown algae are unique among 

macroalgae in their developing into multicellular forms with differentiated tissues, and they reproduce by means of motile flagellated spores. Most brown algae have a life history that consists 

of an alternation between morphologically similar haploid and 

diploid plants. Scytosiphon lomentaria alternates between four 

distinct morphological generations, which is considered to be a 

bet-hedging survival strategy (Littler and Littler, 1983).

The Phaeophyceae comprise about 2,000 species and are 

almost exclusively marine algae. Tropical brown algae include 

microscopic filament, sheet, coarsely branched, and crust forms 

(Figure 6). Nearly all brown algae have fine (microscopic) hairs 

emanating from their surfaces that may serve to increase surface 

area for nutrient uptake. Kelps attain their greatest abundance, 

size, and diversity in cold temperate to polar waters. They occur 

from the intertidal (Fucales) to 115 m depth (Sargassum hystrix; 

Littler and Littler, 1994) on reefs. 

Brown algae are also well represented in coral reef ecosystems, particularly in back-reef areas. For example, Sargassum 

and Turbinaria (Figure 7) can form small-scale forests up to several meters high that provide biomass, habitat, and shelter for 

numerous fishes and invertebrates. 

Chlorophyta (Green Algae)

Chlorophyta generally have predominantly green chlorophyll pigments. The green algae also contain subordinate carotenoid and xanthophyll pigments and are the ancestral relatives 

of vascular plants (grasses, trees, sea grasses, etc.), which also 

contain these same basic pigments. Green seaweeds range from 

microscopic threadlike filaments to thin sheets; can be spongy, 

gelatinous, papery, leathery, or brittle in texture; and reach up 

to 1.5 m in length (Figure 8). The green algae store their energy 

reserves as starch. All produce flagellated spores and gametes, 

giving them the advantage of motility (Hoek et al., 1995). 

Green algae are always present on tropical coral reefs and 

lagoon floors, often intermixed among sea grass shoots. Chlorophyta are usually the siphonaceous (giant-celled) forms of 

Bryopsidales, such as Halimeda, Avrainvillea, Udotea, and Caulerpa, that employ a unique cytoplasmic streaming/blade abandonment mechanism to eliminate epiphytes (Littler and Littler, 

1999). Most Bryopsidales have a rhizophytic, rooted growth 

form and readily take up pore-water nutrients by cytoplasmic 

streaming (Williams, 1984). The deepest-occurring fleshy upright 

alga (Rhipiliopsis profunda) is a member of this group and was 

found by submersible attached to bedrock at a depth of 210 m 

(Littler and Littler, 1994). Many of these same very deep living 

species were later found by scuba divers in shallower shaded locations. Some genera of filamentous or sheetlike green algae are 

extremely tolerant of stressful conditions and can be indicators 

of freshwater seeps, recently disturbed areas (as early colonizers 

of newly exposed substrates), habitats of low herbivory (high 

herbivory eliminates palatable greens), and especially areas with 

an overabundance of nutrients (e.g., bird roosting islands, polluted areas).

Calcified green algae are major contributors to the production of marine sediments. Some genera, such as Udotea and 

Penicillus, produce enormous amounts of fine silt and other sediments due to continual sloughing of thalli and the subsequent 

disintegration. In many tropical locales, the sparkling white sand 

beaches are mostly bleached and eroded calcium carbonate (aragonite) skeletons of Halimeda. Halimeda “hash” (i.e., the coarse 

oatmeal-like accumulations of Halimeda segments, Figure 9) has 

been used in power plants and other fossil fuel industries as a 

smokestack scrubber/neutralizer to precipitate sulfurous acid 

and other precursors to acid rain.

FIGURE 5. The reef-building calcareous macrophyte Porolithon

(Hydrolithon) craspedium. (Photo by D. Littler.)
number 39 • 193

FIGURE 6. Different forms and colors of brown algae. Top left: Dictyota humifusa. Top right: Asteronema breviarticulatus. Middle left: Distromium flabellatum. Middle right: Cutleria sp. Bottom left: Iyengaria stellata. Bottom right: Ralfsia extensum. (Photos by D. Littler.)
194 • smithsonian contributions to the marine sciences

Figure 7. Top left and middle: Sargassum hystrix. Top right: Turbinaria turbinata. Bottom: Sargassum polyceratium forming vast, dense beds 

on the windward side of Bonaire. (Photos by D. Littler.)
number 39 • 195

Figure 8. An array of different green algal forms. Top left: Codium intertextum. Top right: Halimeda copiosa. Middle left: 

Ventricaria ventricosa. Bottom left: Udotea cyathiformis. Bottom right: Caulerpa sertularioides f. farlowii. (Photos by D. Littler.)
196 • smithsonian contributions to the marine sciences

Cyanobacteria (Blue-Green Algae)

This ancient, highly controversial, and difficult group is 

prokaryotic, and not a member of the true plants. Cyanobacteria’s simple, mostly filamentous, colonial thalli lack sophisticated 

characters, making their taxonomy highly technical. Saltwater 

species at scuba depths have seldom been collected and their important roles are only recently being appreciated. Cyanobacteria 

were the first group to evolve aerobic photosynthesis, the process 

that generates food for most of the biological world. On tropical reefs, cyanobacteria form masses of microscopic organisms 

that are strung together into large filamentous clumps or colonies (Figure 10), and they have specific colors, shapes, or growth 

forms that are distinctive. However, these are lost in preserved 

specimens, and before scuba went unappreciated by earlier museum/herbarium–bound taxonomists. Most commonly, the color 

of blue-green algae is some peculiar shade of pink to purple to 

black—a combination of red from the pigment phycoerythrin,

blue from phycocyanin, and green from chlorophyll.

Figure 9. Halimeda “hash” (i.e., dead calcareous segments). 

(Photo by D. Littler.)

Figure 10. An array of different blue-green algal forms. Top left: Rivularia nitida. Bottom left: Schizothrix minuta. Right: unidentified. (Photos 

by D. Littler.)
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Some filamentous colonies show the ability to differentiate 

into several specialized cell types: vegetative cells (the normal, 

photosynthetic cells that are formed under favorable growing 

conditions); akinetes (the stress-resistant, long-lived spores that 

form when environmental conditions become harsh); and thickwalled heterocysts, which contain the enzyme nitrogenase for nitrogen fixation (Herrero and Flores, 2008). Many cyanobacteria 

also produce motile reproductive filaments called hormogonia 

that glide free from the parent colony and disperse to form new 

colonies. 

High standing biomass of cyanobacteria is usually considered detrimental to the health of both coral reef systems and people. They produce chemical compounds that can be toxic to fish, 

plankton, and invertebrates. For example, one type of swimmer’s 

itch, a skin irritation that beach-goers commonly experience,

can be caused by blooms of the blue-green alga Lyngbya majuscula (Figure 11). Black band disease of corals (Figure 12),found 

throughout all tropical oceans, is caused by blue-green algae and 

associated microorganisms (Ruetzler et al., 1983). Certain cyanobacteria produce neurotoxins, hepatotoxins, cytotoxins, and 

endotoxins that can be dangerous to animals and humans (Paul 

et al., 2007).

The nitrogen-fixing capacity of some blue-green algae is extremely important. Heterocyst-forming species bind nitrogen gas 

into ammonia (NH3

), nitrite (NO2−), or nitrate (NO3−) that can 

be absorbed by all plants. This role is crucial for tropical reef 

systems and especially nutrient-depauperate atoll reefs, which 

are extremely low in fixed nitrogen. Some of these cyanobacteria contribute significantly to global ecology and the oxygen 

cycle. For example, the marine cyanobacterium Prochlorococcus

(0.5–0.8 μm diameter) accounts for >50% of the total photosynthetic production of the open ocean and 20% of the planet’s 

atmospheric oxygen (Partensky et al., 1999). Cyanobacteria are 

the only group of organisms that are able to reduce nitrogen and 

carbon in aerobic conditions, a feature that may be responsible 

for their evolutionary and ecological success in certain coral reef 

habitats.

Blue-green algae are abundant worldwide and ubiquitous 

on coral reefs, where they often occur under extreme environmental conditions. The universally present black band in the 

splash zones that make rocks or boat ramps slippery is a layer 

of microscopic blue-green algae. Such blue-greens can withstand 

exposure to severe drying, extreme salinity, rain, bright sun, and 

high heat and still flourish. Cyanobacteria are among the oldest 

known life forms on Earth. Stromatolites containing fossilized 

Figure 12. Black band disease, Phormidium corallyticum, attacking a brain coral. (Photos by D. Littler.)

Figure 11. Lyngbya majustula, the cyanobacteria (blue-green

alga) that causes one type of swimmer’s itch. (Photo by D. Littler.)
198 • smithsonian contributions to the marine sciences

oxygen-producing cyanobacteria date to 1.5 billion years ago 

(Zhang and Golubic, 1987). 

REFERENCES

Anderson, D. M. 1995. ECOHAB – The ecology and oceanography of harmful 

algal blooms—A national research agenda. Woods Hole, Mass.: Woods Hole 

Oceanographic Institution.

Atkinson, M. J., and R. W. Grigg. 1984. Model of a coral reef ecosystem. II. Gross 

and net benthic primary production at French Frigate Shoals, Hawaii. Coral 

Reefs, 3:13–22. http://dx.doi.org/10.1007/BF00306136.

Bellwood, D. R., T. P. Hughes, and A. S. Hoey. 2006. Sleeping functional group 

drives coral reef recovery. Current Biology, 16:2434–2439. http://dx.doi.org

/10.1016/j.cub.2006.10.030.

Birkeland, C. 1977. The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits. Proceedings of the third International Coral Reef Symposium, 1:15–21.

Boergesen, F. 1916. The marine algae of the Danish West Indies. Part III. Rhodophyceae (2). Dansk Botanisk Arkiv, 3:81–144.

Carpenter, R. C. 1986. Partitioning herbivory and its effects on coral reef algal communities. Ecological Monographs, 56:345–363. http://dx.doi.org/10.2307

/1942551.

Carpenter, S. R., J. F. Kitchell, and J. R. Hodgson. 1985. Cascading trophic interactions and lake productivity. BioScience, 35:634–639. http://dx.doi.org/10

.2307/1309989.

Hay, M. E. 1981. Spatial patterns of grazing intensity on a Caribbean barrier reef: 

Herbivory and algal distribution. Aquatic Botany, 11:97–109. http://dx.doi

.org/10.1016/0304-3770(81)90051-6.

Hoek, C. van den, D. G. Mann, and H. M. Jahns. 1995. Algae: an introduction to 

phycology. Cambridge: Cambridge University Press.

Herrero, A., and F. Flores, eds. 2008. The cyanobacteria: Molecular biology, genomics and evolution. Norfolk, UK: Caister Academic Press.

Lapointe, B. E., M. M. Littler, and D. S. Littler. 1997. Macroalgal overgrowth of 

fringing coral reefs at Discovery Bay, Jamaica: Bottom-up versus top-down 

control. Proceedings of the eighth International Coral Reef Symposium, 

1:927–932.

Lewis, S. M. 1986. The role of herbivorous fishes in the organization of a Caribbean reef community. Ecological Monographs, 56:183–200. http://dx.doi.org

/10.2307/2937073.

Littler, M. M., and D. S. Littler. 1983. Heteromorphic life history strategies in the 

brown alga Scytosiphon lomentaria (Lyngb.). Journal of Phycology, 19:425–

431. http://dx.doi.org/10.1111/j.0022-3646.1983.00425.x.

———. 1984. Models of tropical reef biogenesis: The contribution of algae. In 

Progress in phycological research, Vol. 3., ed. F. E. Round and D. J. Chapman, 

pp. 323–364. Bristol, UK: Biopress. 

———. 1994. Algenwachstum in ozeanischen Tiefen [Plant life of the deep ocean 

realm]. Biologie in Unserer Zeit, 24(6):330–335. 

———. 1999. Blade abandonment/proliferation: A novel mechanism for rapid epiphyte control in marine macrophytes. Ecology, 80:1736–1746. http://dx.doi

.org/10.1890/0012-9658(1999)080[1736:BAPANM]2.0.CO;2.

Littler, M. M., D. S. Littler, and B. E. Lapointe. 1993. Modification of tropical reef 

community structure due to cultural eutrophication: The southwest coast of 

Martinique. Proceedings of the seventh International Coral Reef Symposium, 

1:335–143.

Littler, M. M., D. S. Littler, and P. R. Taylor. 1983a. Evolutionary strategies in a 

tropical barrier reef system: Functional-form groups of marine macroalgae.

Journal of Phycology, 19:229–237. http://dx.doi.org/10.1111/j.0022-3646

.1983.00229.x.

Littler, M. M., P. R. Taylor, and D. S. Littler. 1983b. Algal resistance to herbivory on 

a Caribbean barrier reef. Coral Reefs, 2:111–118. http://dx.doi.org/10.1007/

BF02395281.

Marubini, F., and P. S. Davies. 1996. Nitrate increases zooxanthellae population 

density and reduces skeletogenesis in corals. Marine Biology, 127:319–328. 

http://dx.doi.org/10.1007/BF00942117.

McCook, L. J. 1999. Macroalgae, nutrients and phase shifts on coral reefs: Scientific issues and management consequences for the Great Barrier Reef. Coral 

Reefs, 18:357–367. http://dx.doi.org/10.1007/s003380050213.

McCook, L. J., J. Jompa, and G. Diaz-Pulido. 2001. Competition between corals 

and algae on coral reefs: A review of evidence and mechanisms. Coral Reefs,

19:400–417. http://dx.doi.org/10.1007/s003380000129.

Morrison, D. 1988. Comparing fish and urchin grazing in shallow and deeper 

coral reef algal communities. Ecology, 69:1367–1382. http://dx.doi.org/10

.2307/1941634.

Nugues, M. M., G. W. Smith, R. J. van Hooidonk, M. I. Seabra, and R. P. M. Bak. 

2004. Algal contact as a trigger for coral disease. Ecology Letters, 7:919–923. 

http://dx.doi.org/10.1111/j.1461-0248.2004.00651.x.

Ogden, J. C., and P. S. Lobel. 1978. The role of herbivorous fishes and urchins 

in coral reef communities. Environmental Biology of Fishes, 3:49–63. http://

dx.doi.org/10.1007/BF00006308.

Partensky, F., W. R. Hess, and D. Vaulot. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiology and Molecular Biology Reviews, 63:106–127.

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. http://dx.doi.org/10.2307/25066642.

Ruetzler, K., D. L. Santavy, and A. Antonius. 1983. The black band disease of Atlantic reef corals. III. Distribution, ecology, and development. Publicazione 

Stazione Zoologica di Napoli: Marine Ecology, 4:329–358. http://dx.doi.org

/10.1111/j.1439-0485.1983.tb00118.x.

Sammarco, P. W. 1983. Effects of fish grazing and damselfish territoriality on coral 

reef algae. I. algal community structure. Marine Ecology Progress Series, 

13:1–14. http://dx.doi.org/10.3354/meps013001.

Sammarco, P. W., J. S. Levinton, and J. C. Ogden. 1974. Grazing and control of coral 

reef community structure by Diadema antillarum Phillipi (Echinodermata: 

Echinoidea): A preliminary study. Journal of Marine Research, 32:47–53.

Schaffelke, B. 1999. Particulate organic matter as an alternative nutrient source for 

tropical Sargassum species (Fucales, Phaeophyceae). Journal of Phycology, 

35:1150–1157. http://dx.doi.org/10.1046/j.1529-8817.1999.3561150.x.

Smith, J. E., C. M. Smith, and C. L. Hunter. 2001. An experimental analysis of the 

effects of herbivory and nutrient enrichment on benthic community dynamics 

on a Hawaiian reef. Coral Reefs, 19:332–342.

Stephenson, W., and R. B Searles. 1960. Experimental studies on the ecology of 

intertidal environments at Heron Island. I. Exclusion of fish from beach rock. 

Australian Journal of Marine and Freshwater Research, 2:241–267. http://

dx.doi.org/10.1071/MF9600241.

Taylor, W. R. 1960. Marine algae of the eastern tropical and subtropical coasts of 

the Americas.Ann Arbor: University of Michigan Press. 

Williams, S. L. 1984. Uptake of sediment ammonium and translocation in a marine green macroalga Caulerpa cupressoides. Limnology and Oceanography, 

29:374–379. http://dx.doi.org/10.4319/lo.1984.29.2.0374.

Zhang, Y., and S. Golubic. 1987. Endolithic microfossils (Cyanophyta) from early 

proterozoic stromatolites, Hebei, China. Acta Micropaleontologia Sinica,

4:1–12.
The Nature of Crustose Coralline Algae 

and Their Interactions on Reefs

Mark M. Littler and Diane S. Littler

ABSTRACT. What was known about crustose coralline algae (CCA) prior to the use of scuba came 

mostly from dredging collections. This method usually resulted in damaged specimens and questionable habitat data. Scuba has allowed a more accurate determination of ecological conditions and 

facilitated in situ photography, two techniques our group has relied on during the past three decades 

for quantitative ecological studies and field guide production. A goal of this review is to familiarize 

the scientific diving community with the kinds and roles of CCA on tropical reefs, with the hope that 

the diving community will more fully appreciate the role of this important group of organisms that 

is so critical to healthy reef structure and function.

Crustose (nongeniculate) coralline algae occur worldwide from polar to tropical 

regions, reaching their highest diversity in tropical reef environments. Coralline 

algae occupy the entire depth range inhabited by photosynthetic organisms, from 

upper-intertidal regions to depths as great as 295 m. The great abundances of corallines in the poorly known deep-sea realm underscore their widespread contributions to 

productivity, the marine food web, sedimentology, and reef biogenesis in clear tropical 

seas. The diversity of CCA forms is astonishing, ranging from small filamentous strands 

to some of the larger and most beautiful head-forming organisms on coral reefs. The 

predominant members of this functional indicator group tend to be slow-growing, competitively subordinate taxa that are abundant in most reef systems. As an indicator group 

they are functionally resilient and able to expedite the recovery and restoration of coral 

reef systems relatively quickly since some thin forms of crustose coralline algae accelerate 

colonization and chemically attract and facilitate the survival of coral larvae; the other 

two fleshy algal functional indicator groups (i.e., turfs and macroalgae) tend to overgrow 

and inhibit coral settlement, survival, and recovery. Because most crustose coralline algae 

continually slough off upper surface layers, they play a key cleaning role and physically 

prevent the settlement and colonization of many fleshy fouling organisms on coral reefs.

INTRODUCTION

Prior to scuba, studies by dredging provided most of the sparse knowledge of crustose coralline algae (CCA), which focused primarily on taxonomy and distributional 

records. Scuba has enabled studies on ecology, physiology, interactions, etc., that were 

impossible before its development (Figure 1). Since crustose coralline algae are often 

overlooked or ignored due to their complex taxonomy and life histories, it is now paramount to understand their fundamental structure and development so that we can utilize 

Mark M. Littler and Diane S. Littler, formerly 

of Department of Botany, National Museum of 

Natural History, Smithsonian Institution, P.O. 

Box 37012, MRC 166, Washington, District of 

Columbia 20013-7012, USA.

Manuscript received 25 January 2012; accepted 5 March 2013.
200 • smithsonian contributions to the marine sciences

this important functional group to answer many questions about 

marine biology and ecology. 

Coralline algae (also “corallines”) are red algae (Rhodophyta) characterized by a thallus that is stony because of calcareous deposits contained within and between the cell walls. The 

extensive crystalline calcium carbonate (calcite) deposits provide 

a geological history of reefs and an excellent fossil record. These 

algae are typically pink or other shades of red, but some species 

can be variations of purple, blue, gray-green, or brown.

Corallines rank among the major reef builders in coral reef 

systems. Coralline algae are exclusively marine plants and occur 

throughout all of the world’s oceans, attached to substrates by 

cellular adhesion or root-like holdfasts. Many corallines are epiphytic (on other plants) or epizoic (on animals), and some are 

even endophytic parasites within other corallines. Despite their 

ubiquity, all aspects (e.g., taxonomy, biology, ecology) of the coralline algae remain poorly understood, and corallines are often 

overlooked or intentionally ignored by coral reef scientists.

When they were discovered in 1707 (Sloane), corallines 

were thought to be animals. In 1837, Philippi recognized that 

coralline algae were plants and proposed the two generic names 

Lithophyllum (for flat forms) and Lithothamnium (for erect, 

branched forms). However, in an overlooked earlier treatment 

Bory de Saint-Vincent (1832) had recognized Tenarea undulosa 

as a crustose calcareous alga, making it the oldest species name 

originally applied to the group in a botanical context. Coralline 

algae were included in the order Cryptonemiales as the family 

Corallinaceae until 1986 (Silva and Johansen), when they were 

elevated to the order Corallinales.

LIFE HISTORIES

Corallines reproduce by sori, which are specialized, volcanoshaped, domed conceptacles containing haploid tetraspores, diploid bispores, or either male or female gametes. Gametes fuse to 

form the parasitic diploid carposporophyte stage within the female conceptacles, and the resultant carpospores germinate into 

diploid tetrasporophytes. Haploid tetraspores germinate to produce the male and female gametophytes. Some crustose coralline 

populations are unusual in that uninucleate bispores (diploid) are 

commonly the sole means of reproduction. The plant body (thallus) is composed of strands of pit-connected cells (filaments) that

may fuse laterally or form secondary pit connections. Pit connections and pit plugs are translocational structures characteristic of 

red algae (Rhodophyta). These reproductive and vegetative structures provide the critical anatomical characters used in coralline 

algal taxonomy, but also create major obstacles for researchers, 

since complicated decalcification techniques and microtome sectioning of infrequently present cryptic features are required.

Articulated (geniculate) corallines are upright or pendulous 

branched, bushy plants (Figure 2), with shallower and warmer 

FIGURE 1. The research team surveying an extensive rhodolith bed at 30 m. (Photo by D. E. Hurlbert.)
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distributions than nongeniculate species. The multiple clumped 

thalli are flexible due to noncalcified zones (genicula, joints) separating longer calcified segments (intergenicula). Many articulated 

and upright crustose corallines can also form extensive twodimensional adherent crusts, allowing them to spread laterally, 

and thereby providing those species with multiple bet-hedging 

ecological survival strategies (called heterotrichy; Figure 3) (Littler and Kauker, 1984). The upright portions receive relatively 

more light and nutrients, and are faster growing with increased 

fertility; horizontal crusts are more resistant to physical forces 

such as grazing, wave shearing, and sand scouring, and allow the 

plants to regenerate and invade horizontal primary space. 

Crustose (nongeniculate) corallines range in thickness from 

a few micrometers to many centimeters (Figures 4–7). The thinner forms are faster-growing early colonizers and occur on all 

hard substrates and other marine organisms. Crustose corallines 

span a spectrum of morphotypes from thin, sheetlike crusts to 

thick, slow-growing massive pavements (Figure 4) and from 

shelf forms (Figure 5) to upright branched (Figure 6) and columnar coral-like heads and nodules (Figure 7) that contribute 

to both cementation and bulk. On oceanic reefs, the highest part 

of the reef is often a massive intertidal algal ridge of crustose 

corallines in the reef’s breaker zone (Dawson, 1961). Thalli of 

thicker forms often consist of three recognizable layers: an attached lower hypothallus, a middle perithallus, and an upper 

epithallus. Trichocytes (hair cells, megacells) occur as horizontal 

plates within the epithallus layer in some genera such as Porolithon. The protected meristematic (growing) region is usually 

located as a layer beneath the uppermost intercalary perithallus cells, a feature which is unusual in the Rhodophyta, whose 

Figure 2. Spectrum of articulated (jointed, geniculate) coralline algal forms. Top left: Amphiroa foliacea. Top right: Jania rubens. Middle left: 

Cheilosporum acutilobum. Middle right: Amphiroa beauvoisii. Bottom left: Corallina berteroi. Bottom right: Amphiroa ephedraea. (Photos by 

D. Littler.)
202 • smithsonian contributions to the marine sciences

Figure 3. Heterotrichy: multiple bet-hedging ecological survival strategies. Left: Jointed corallines with the upright 

portions receive relatively more light and nutrients and are faster growing, whereas horizontal crusts are more resistant

to physical forces and invade horizontal space. Right: Knob-forming coralline with two-dimensional leading crust invading and overgrowing neighboring species. (Photos by D. Littler.)

Figure 4. Spectrum of simple two-dimensional forms of nongeniculate (crustose) corallines. Top left: Titanoderma

tessellatum. Top right: Titanderma pustulatum. Bottom left: Porolithon onkodes. Bottom right: Neogoniolithon fosliei

showing synchronous sloughing. (Photos by D. Littler.)
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members (except for Delesseriaceae) typically show strictly apical cell growth. Because of the upright branched head formers 

(Figures 6, 7), some specialists prefer the term nongeniculate over 

crustose; however, all have extensive crustose bases and whether 

branched or simple they are still elaborations of crusts.

RHODOLITHS

In the absence of hard substrates, many nongeniculate species can propagate as free-living rhodolith nodules colonizing 

sedimentary seafloors (Figure 8). Some of the attached crustose 

corallines break free and then continue spherical growth as they 

are tumbled by wave action and bioturbation to ultimately cover 

vast areas as free-living rhodoliths (also called nodules, rhodolites, maërl, red algal balls, algaliths). Rhodolith beds have been 

found throughout all of the world’s oceans. Globally, rhodoliths 

fill an important niche in marine ecosystems, serving as transitional habitats between rocky substrates and barren sedimentary 

areas (Littler and Littler, 2008). Under favorable preservation 

conditions, rhodoliths can be the predominant contributors 

of carbonate sediments, often forming rudstone or floatstone 

depositional beds consisting of large fragments of rhodoliths 

contained in grainy matrices. Although they can be rolled by 

infrequent tropical storms, stationary rhodoliths nevertheless 

provide a three-dimensional microhabitat by intercellular translocation onto the lower shaded layers that continue to expand. 

A wide variety of species attach to rhodoliths, including other 

algae, corals, and commercial species such as clams, oysters, and 

scallops. Rhodoliths are a common feature of modern and ancient carbonate shelves worldwide. Fossil rhodoliths commonly 

are used to derive paleoecological and paleoclimatic information, and rhodolith communities contribute significantly to the 

global calcium carbonate budget.

Quantitative submersible studies in conjunction with scubabased research (Littler et al., 1985, 1986, 1991; Littler and Littler, 

1994) on deep-water rhodolith development, distribution, abundance, and primary productivity, at sites of both active formation 

and breakdown, provided the following detailed case study. The 

1.27 km2

 upper platform (67 to 91 m deep) of a ~1,000 m high 

Bahamian seamount (San Salvador Seamount) averaged 95.8% 

cover of rhodoliths, contributing an impressive 391 tons of organic 

Figure 5. Spectrum of shelf-forming crustose corallines. Top left: Mesophyllum funafutiense. Top right: Mesophyllum 

mesomorphum. Bottom left: Mesophyllum cf. lichenoides. Bottom right: Mesophyllum sp. Note abundant examples of 

conceptacles in bottom left image. (Photos by D. Littler.)
204 • smithsonian contributions to the marine sciences

carbon per year to deep-sea productivity. The predominant crustose coralline alga was acclimated to extremely low light ranges, 

with an extremely narrow photosynthesis versus irradiance (PI) 

curve of net primary productivity (0.005 to slightly beyond 0.24 

μmol per meter square per second of photosynthetically active 

radiation). Horizontal platform areas contained accumulations 

up to five rhodoliths deep (about 45 cm thick), with their visible planer (two-dimensional) crustose algal cover (68.5%) being

composed of 41% Lithophyllum sp., 14.9% mixed crustose corallines, and 12.6% Peyssonnelia sp. The platform rhodoliths also 

contained an average 25% cover of the foraminiferan Gypsina

sp.; by contrast, Gypsina cover was minimal on the slope rhodoliths. Rhodoliths that had spilled down from the relatively flat 

platform tended to be concentrated in fan-shaped deposits that

were more prevalent near the tops of the slopes. Cover of living crustose algae on the deeper slope rhodoliths averaged only 

22.8% and was made up of 14.8% unidentified crustose corallines, 6% Lithophyllum sp., and 2% Peyssonnelia sp. 

Throughout platform depths from 67 to 91 m, rhodoliths 

were fairly uniform in composition and abundance. They ranged 

from 4 to 15 cm in diameter, with an average diameter of about 9 

cm, and were roughly spherical with smooth living surfaces. The 

rugose rhodoliths spilling down the steep slopes of the seamount 

to depths below 200 m were characteristically smaller (about 5 

cm average diameter), much rougher, and pitted by boring organisms. Cross-sections through the centers of upper platform nodules showed relatively thin (1–3 cm thick), well-preserved, outer 

envelopes overlying dead laminated crustose layers. These layers 

surrounded much thicker cores of biotically altered carbonates 

(comprised mostly of corallines, foraminiferans, and corals) that 

had been extensively reworked by boring sponges, boring algae, 

polychaetes, and pelecypods. Radiocarbon dating indicated that 

the outermost unaltered envelopes beneath actively growing 

platform crusts averaged 429 years old (range = 112 to 880 ybp), 

while the innermost unaltered layers showed an average age of 

731 ybp (range = 200 to 1,100 ybp).

GEOLOGY AND EVOLUTION

Crustose coralline algae appeared in the early Cretaceous and 

have been important components of shallow marine communities 

Figure 6. Spectrum of head-forming crustose corallines with upright branched excrescences. Top left: Lithophyllum bamleri. Top right: Mastophora pacifica. Bottom left: Neogoniolithon spectabile. Bottom right: Lithophyllum pygmaeum. (Photos by D. Littler.)
number 39 • 205

Figure 7. Spectrum of crustose coralline that form knoblike branched excrescences. Top left: Mesophyllum erubescens. Top 

right: Lithothamnion proliferum. Bottom left: Hydrolithon reinboldii. Bottom right: Lithophyllum congestum. (Photos by 

D. Littler.)

Figure 8. Examples of coralline algal rhodoliths. (Photos by D. Littler.)
206 • smithsonian contributions to the marine sciences

throughout the Cenozoic, mostly showing long-term increases in

species richness during much of their history. There are currently 

over 1,600 described species of crustose coralline algae (Woelkerling, 1988) and ~649 fossil species (Aguirre et al., 2000). Interestingly, Miocene coastal carbonate habitats are characterized by a 

worldwide bloom of coralline red algal deposits (termed rhodalgal facies). These extensively developed facies (i.e., characteristic 

sedimentary deposits) temporarily replaced corals throughout the 

tropics and subtropics as dominant carbonate producers (e.g., Esteban, 1996). By calibrating modern carbonate assemblages to 

local oceanographic conditions in the Gulf of California, Halfar 

et al. (2004) demonstrated that the predominance of rhodalgal facies occurred under mesotrophic to slightly eutrophic conditions. 

In the Mediterranean region, early to middle Miocene carbonates 

contain more rhodalgal components than coral reef deposits (Esteban, 1996). In addition to being widespread globally, fossil coralline algae also exhibited their greatest species richness during 

the early and middle Cenozoic (early Miocene peak of 245 species; Aguirre et al., 2000), with a collapse to a late Pleistocene low 

of 43 species. In reviewing 37 representative late-Pliocene studies, 

Halfar and Mutti (2005) concluded that although rhodalgal facies were clearly the dominant components at specific study sites, 

they often were not emphasized as extensively as the much better 

known coral assemblages. A number of the above studies focused 

mainly on coral reef components although rigorous reanalyses 

of the facies studied actually indicated a relatively low percentage of corals and a predominance of rhodoliths. Esteban (1996) 

noted a similar bias in a review of Miocene Mediterranean coral 

reefs and rhodalgal facies. Such discrepancies can be attributed 

mostly to poor knowledge of coralline red algae and rhodolith 

facies in conjunction with the tendency for researchers to apply 

classic coral reef depositional models, even in settings where corals were sparse.

Throughout the world’s oceans during the late-early to 

early-late Miocene, while many phototrophs declined globally, 

coralline red algae radiated and diversified greatly. In fact, corallines have shown a long-term overall increase in species richness 

throughout most of their history. Despite this, coralline species 

diversification was not sustained after the Miocene (Aguirre 

et al., 2000) and coralline algae suffered a series of extinction 

events, each of which eliminated at least 20% of the species. In 

fact, during the two largest extinction events of the late Cretaceous and late Miocene–Pliocene, about 66% of all coralline species were lost. Each extinction event was followed by substantial 

episodes of rapid radiation and speciation, particularly in the 

early Paleocene and Pleistocene.

The conspicuous Miocene shift from coral- to rhodolithdominated carbonate communities has been attributed to global 

climate changes. Halfar and Mutti (2005) argued that the prevalence of rhodolith facies, which developed under broader nutrient and temperature ranges than did the coral reef facies, was 

initially triggered by a global enhancement of nutrient resources. 

In the middle Miocene, nutrient availability was apparently augmented by increased upwelling- and erosion-related nutrient 

inputs into coastal ecosystems. These nutrient increases together 

with declining temperatures following the early to middle Miocene climatic optimum led to further expansion of rhodalgal 

facies. Hence, a global phase shift in dominance occurred in 

nearshore shallow-water carbonate producers from corals to 

coralline species that were tolerant of the higher nutrient levels 

(in accordance with the Relative Dominance Model [RDM]; Littler et al., 2006). Geological deposits of coralline algae contain 

organic carbon compounds such as cellulose (due to photosynthesis), as well as massive calcareous compounds due to calcification (precipitation of inorganic CaCO3

). The resultant carbon 

stores may be among the most important in the biosphere as 

neutralizers of global oceanic acidification and as reservoirs of 

excess greenhouse CO2

.

A striking geological pattern is an inverse relationship in 

the species richness of two of the families of Corallinales. From 

the Cretaceous to Pleistocene, Corallinaceae (both warm- and 

cold-water species) increased, while the tropical Sporolithaceae 

declined. This climatic link for Sporolithaceae and Corallinaceae 

was supported by both direct and inverse correlations, respectively, between species diversity and documented Cretaceous to 

Cenozoic paleotemperatures. Coralline diversification since the 

Cretaceous (Steneck, 1983, 1985) may have been driven by simultaneous coevolutionary increases in herbivores (mainly limpets, echinoids, and grazing fishes) that physically scrape and 

remove fleshy algal competitors, though that remains to be more 

firmly established.

DISTRIBUTIONAL PATTERNS AND 

FUNCTIONAL SIGNIFICANCE

Crustose (nongeniculate) coralline algae occur worldwide 

from polar to tropical regions, reaching their highest diversity 

in tropical reef environments. Three subgroups of Corallinales 

show characteristic distributions (Aguirre et al., 2000): (1) Sporolithoideae, low latitude/mainly deep waters; (2) Melobesioideae, high latitude/shallow waters to low latitude/deep waters; 

and (3) Lithophylloideae/Mastophoroideae, mid to low latitude/

shallow waters.

The abundant occurrence of crustose corallines (and corals) 

in Indo-Pacific reefs was initially recognized by Darwin (1842); 

however, their important role as reef builders was first emphasized by Agassiz (1888). Most often, corals (Cnidaria) supply the 

bulk building blocks whereas coralline algae do much of the cementing together of debris. Barrier, fringing, and atoll reefs are 

complex ecosystems that depend on calcareous coralline algae 

for the development and maintenance of wave-resistant outer 

fronts (Figure 9). The crustose coralline algae, which deposit a 

type of calcium carbonate (calcite limestone) that is harder and 

denser than the aragonite of corals, build this raised algal ridge 

(Dawson, 1961). The intertidal–outer algal ridge habitat, to 

which crustose corallines (mainly species of Porolithon) are crucial for constructing the framework, characterizes surf-pounded 
number 39 • 207

windward coral reefs of tropical Indo-Pacific and, to a lesser extent, Atlantic regions. The Pacific algal ridge builder Porolithon

onkodes fixes a remarkable 3.2 mg of organic carbon per square 

meter per hour and 1.9 mg calcium per square meter per hour 

during an average-daylight day (Littler, 1973). By extending 

above the waterline, the algal ridge absorbs tremendous wave 

energy, not only protecting coastal shorelines that would otherwise erode, but also sheltering the more delicate corals and other 

reef organisms. Algal ridges develop intertidally and, therefore, 

require intense and persistent wave action to form, so are best 

developed on windward areas where there are consistent trade 

wind conditions.

Some of the coralline algae that develop into shelf-like 

crusts (Figure 5), upright branches (Figure 6), or thick knobby 

crusts (Figure 7) provide microhabitats for countless vulnerable invertebrates that would otherwise suffer increased mortality due to fish predation. Coralline algae also constitute a food 

source in the energy webs of coral reefs. Sea urchins, parrotfishes, 

surgeonfishes, limpets, and chitons all readily feed on coralline 

algae, which are usually not destroyed due to sunken, intercalary meristems that replenish the upper, damaged areas. Crustose corallines accelerate colonization by chemically attracting 

and facilitating the survival of coral larvae (Harrington et al., 

2004), as well as the larvae of certain grazing invertebrates. This 

is beneficial for the corallines because the herbivores then remove epiphytes that might preempt available light or otherwise 

smother the crusts. Because of their stony texture, indigestible 

acid-neutralizing CaCO3

, and covered intercalary meristematic 

layer, corallines are uniquely resistant to considerable levels of 

grazing. As examples, the most common Indo-Pacific crustose 

coralline, Porolithon onkodes, often forms an intimate relationship with the chiton Cryptoplax larvaeformis (Littler and Littler, 

1999), as does the Atlantic coralline H. pachydermum and the 

chiton Choneplax lata (Littler et al., 1995). The chitons live in 

Figure 9. Right: A well-developed algal ridge from windward Guam. Top left: close-up of the pink crustose Porolithon craspedium. Bottom 

left: close-up of the head-forming Lithophyllum kotschyanum. (Photos by D. Littler.)
208 • smithsonian contributions to the marine sciences

burrows that are overgrown by Porolithon and graze nocturnally 

on the surfaces of the corallines (Figure 10). The pattern of grazing causes rapid meristematic differentiation and redirection in 

which the coralline produces an abundance of vertical, bladelike lamellae, resulting in a spectacular growth form resembling 

castles. This type of relationship is unique in the marine environment, whereby the predator actually increases the biomass, surface area, and reproductive capacity (i.e., fitness) of its principal 

prey (Littler et al., 1995).

PATHOGENS

Instances of coralline algal pathogens were unknown until 

1993, when Coralline Lethal Orange Disease (CLOD) was first 

discovered using scuba (Littler and Littler, 1995) on Aitutaki 

Atoll, Cook Islands (Figure 11). The occurrence of CLOD at 25 

Great Astrolabe, Fiji, sites increased from 0% in 1992 to 100% 

in 1993, indicating that the pathogen was in an early stage of 

virulence and dispersal. The bright orange bacterial pathogen 

grows as fan-shaped or circular bands at a mean linear rate of 1.5

mm per day, totally consuming host corallines that are in its path. 

All species of articulated and crustose species tested to date are 

easily infected by CLOD, and it has now become circumtropical 

throughout all coral reef habitats. In recent years, a white CLODlike pathogen has become even more abundant worldwide; this

is in addition to the recently recorded dispersion of a virulent 

black fungal pathogen (Figure 12) of coralline algae first found in 

American Samoa (Littler and Littler, 1998) and an unknown species of target-shaped coralline pathogen (Figure 13) first reported

from the Great Astrolabe Reef (Littler et al., 2007). Without 

scuba, none of the above pathogens would have been discovered.

Figure 10. Castle forms of the crustose corallines created by their association with herbivorous chitons. Left and top right: Hydrolithon pachydermum/Choneplax lata (Pacific). Bottom right: H. onkodes/Cryptoplax larvaeformus (Atlantic). (Photos by D. Littler.)
number 39 • 209

Figure 12. In situ images of black fungus disease in the Pacific. (Photos by D. Littler.)

Figure 11. In situ images of the worldwide CLOD pathogen. (Photos by D. Littler.)
210 • smithsonian contributions to the marine sciences

IMPORTANCE AND ROLE

The findings reviewed here are based mainly on extensive 

scuba research. Crustose (nongeniculate) coralline algae occur 

worldwide from polar to tropical regions, reaching their highest 

diversity in tropical reef environments. Coralline algae occupy the 

entire depth range inhabited by photosynthetic organisms, from 

upper-intertidal regions to depths as great as 295 m (Figure 14;

Littler and Littler, 1994). The great abundances of corallines in 

the poorly known deep-sea realm underscore their widespread

contributions to productivity, the marine food web, sedimentology, and reef biogenesis in clear tropical seas. The diversity of coralline algal forms is astonishing, ranging from small filamentous 

strands to some of the larger and most beautiful head-forming

organisms on coral reefs (Figures 4–7). The predominant members of this functional indicator group (Littler and Littler, 2007) 

tend to be slow-growing, competitively subordinate taxa that are 

abundant in most reef systems. As an indicator group they are 

functionally resilient and able to expedite the recovery and restoration of a particular coral reef system relatively quickly since 

some thin forms of crustose coralline algae accelerate colonization and chemically attract and facilitate the survival of coral 

larvae (Harrington et al., 2004); the other two fleshy algal functional indicator groups (i.e., turfs and macroalgae) tend to overgrow and inhibit coral settlement, survival, and recovery. Because 

most crustose coralline algae continually slough off upper surface 

layers (bottom left, Figure 4), they play a key cleaning role and 

physically prevent the settlement and colonization of many fleshy 

fouling organisms on coral reefs (Littler and Littler, 1997).

Crustose corallines, because of their slow growth, tolerate 

a wide range of nutrient levels and generally are conspicuous, 

but not as predominant as corals, under low concentrations of 

nutrients and high levels of herbivory (Littler and Littler, 2007). 

Accordingly, they do well in the presence of both low and elevated nutrients (i.e., 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 

(Littler and Littler, 2007); instead, the degree to which they rise 

to dominance is largely controlled indirectly by the factors influencing the abundances of other functional groups, primarily 

the corals and fleshy macroalgae. The key point is that crustose 

corallines dominate mainly by default (i.e., under conditions of 

minimal competition) where corals are inhibited (e.g., by elevated nutrients or by strong wave action) and where fleshy algae 

are removed by intense herbivory. The wave-pounded intertidal 

algal ridges are built predominantly by Porolithon (Hydrolithon) 

onkodes, P. gardineri, P. craspedium, and Lithophyllum kotschyanum in the Indo-Pacific and by P. pachydermum and L. congestum in the Atlantic; all are coralline species that appear uniquely 

tolerant of aerial exposure. The transition from frondose- to 

turf- to coralline-algal communities has been reported (Steneck,

1989) to closely correlate with increasing herbivory gradients on 

coral reefs. 

In addition to their protective reef-building nature, coralline algae provide a number of other goods and services. Since 

the eighteenth century, unattached corallines (maërl) have been 

harvested as acid-soil pH conditioners. In Britain and France, 

hundreds of thousands of tons of Phymatolithon calcareum and 

Lithothamnion corallioides continue to be dredged annually. 

Enormous maërl beds several km2 in area, mainly composed of 

species belonging to the genera Lithothamnion and Lithophyllum, are present off the coast of Brazil and have begun to be 

Figure 13. In situ images of target pathogen in the Pacific. (Photos by D. Littler.)
number 39 • 211

commercially harvested. Maërl is also used as a mineral food 

additive for cows, hogs, and other livestock, as well as in the 

filtration and neutralization of acidic drinking water. Corallines 

are used in modern medical science in the preparation of dental bone implants (Shors, 1999). The cellular carbonate skeleton 

provides an ideal matrix for the adherence and regeneration of 

bone and tooth structures. Coralline algal fossils have proven 

to be extremely beneficial in deriving paleoecological and paleoclimatic information, and also have been employed as stratigraphic markers of particular significance in petroleum geology. 

As a spectacularly colorful component of live rock for the flourishing marine aquarium trade, coralline algae are highly desired 

for their architectural and attractive aesthetic qualities. However, the most important contribution of coralline algae worldwide may well prove to be in ameliorating the greenhouse CO2

buildup associated with global climate change. It is the balance 

between calcification and respiration—which produces carbon 

dioxide—and the consumption of CO2

 by photosynthesis that 

will determine whether corallines act as a “sink” (absorbing 

CO2

) or as a source of CO2. Experiments that studied how various calcifying systems take up and give off carbon dioxide have 

shown that the rise in CO2

 produced by calcification is mitigated 

by its removal through increased photosynthesis (Ohde, 1999; 

Iglesias-Rodriguez et al., 2008), with a net effect that is unlikely 

to either greatly contribute to or significantly reduce the rise in 

atmospheric CO2

. However, rising levels of CO2 and concomitant 

acidification of seawater inhibit all reef builders, including coralline algae (Kleypas et al., 1999). By binding vast accumulations 

of CaCO3

 during calcification and photosynthesis, corallines 

may play a role in slowing future acidification of marine habitats 

such as coral reefs. 

REFERENCES

Agassiz, A. 1888. Three cruises of the United States coast and geodetic survey 

steamer “Blake.” Boston: Houghton Mifflin Co. 

Aguirre, J., R. Riding, and J. C. Braga. 2000. Diversity of coralline red algae: Origination and extinction patterns from the early Cretaceous to the Pleistocene.

Figure 14. Rock taken by submersible from >200 m depth off San Salvador Seamount, Bahamas, showing the deepest plant life (a 

crustose coralline alga) on Earth. (Photo by D. Littler.)
212 • smithsonian contributions to the marine sciences

Paleobiology, 26(4):651–667. http://dx.doi.org/10.1666/0094-8373(2000)

026<0651:DOCRAO>2.0.CO;2.

Bory de Saint-Vincent, J. B. 1832. Notice sur les Polypiers de la Grèce. Expédition 

Scientifique de Morée (Section des Sciences Physiques), 3(1):204–209, pl. 54.

Darwin, C. R. 1842. The structure and distribution of coral reefs. Being the first 

part of the geology of the voyage of the Beagle, under the command of Capt. 

FitzRoy, R.N. During the years 1832 to 1836. London: Smith Elder and Co. 

i–xii, 1–214, pls I–II.

Dawson, E. Y. 1961. The rim of the reef. Natural History, 70:8–17.

Esteban, M. 1996. An overview of miocene reefs from Mediterranean areas: General trends and facies models. In Models for carbonate stratigraphy from Miocene reef complexes of the Mediterranean regions, ed. E. Franseen, M. Esteban, W. C. Ward, and J. M. Rouchy. Society of Economic Paleontologists and 

Mineralogists: Concepts in Sedimentology and Paleontology Series, 5:3–53.

Halfar, J., L. Godinez-Orta, M. Mutti, J. Valdez-Holguin, and J. Borges. 2004. Nutrient and temperature controls on modern carbonate production: an example from the Gulf of California, Mexico. Geology, 32(3):213–216.

Halfar, J., and M. Mutti. 2005. Global dominance of coralline red-algal facies: A 

response to Miocene oceanographic events. Geology, 33(6):481–484. http://

dx.doi.org/10.1130/G21462.1.

Harrington, L., K. Fabricius, G. De’Ath, and A. Negri. 2004. Recognition and selection of settlement substrata determine post-settlement survival in corals.

Ecology, 85:3428–3437. http://dx.doi.org/10.1890/04-0298.

Iglesias-Rodriguez, M. D., P. R. Halloran, E. M. Rosalind, R. E. M. Rickaby, I. R.

Hall, E. Elena Colmenero-Hidalgo, J. R. Gittins, D. R. H. Green, T. Tyrrell, S. J. 

Gibbs, P. von Dassow, E. Rehm, E. V. Armbrust, and K. P. Boessenkool. 2008. 

Phytoplankton calcification in a high-CO2 world. Science, 320(5874):336–

340. http://dx.doi.org/10.1126/science.1154122.

Johnson, C. R., and K. H. Mann. 1986. The crustose coralline alga, Phymatolithon

Foslie, inhibits the overgrowth of seaweeds without relying on herbivores. 

Journal of Experimental Marine Biology and Ecology, 96(2):127–146. http://

dx.doi.org/10.1016/0022-0981(86)90238-8.

Kleypas, J. A., R. W. Buddemeier, D. Archer, J. P. Gattuso, C. Langdon, and B. N. 

Opdyke. 1999. Geochemical consequences of increased atmospheric CO2 on 

coral reefs. Science, 284(5411):118–120. http://dx.doi.org/10.1126/science

.284.5411.118.

Littler, M. M. 1973. The population and community structure of Hawaiian 

fringing-reef crustose corallinaceae (Rhodophyta, Cryptonemiales). Journal 

of Experimental Marine Biology and Ecology, 11:103–120. http://dx.doi.org

/10.1016/0022-0981(73)90050-6.

Littler, M. M., and B. Kauker. 1984. Heterotrichy and survival strategies in the 

red alga Corallina officinalis L. Botanica Marina, 27:37–44. http://dx.doi.org

/10.1515/botm.1984.27.1.37.

Littler, M. M., and D. S. Littler. 1994. Algenwachstum in ozeanischen Tiefen [Plant 

life of the deep ocean realm]. Biologie in Unserer Zeit, 24(6):330–335. http://

dx.doi.org/10.1002/biuz.19940240627.

———. 1995. CLOD spreading in the sea-surface microlayer: Response. Science,

270:897. http://dx.doi.org/10.1126/science.270.5238.897.

———. 1997. Disease-induced mass mortality of crustose coralline algae on coral 

reefs provides rationale for the conservation of herbivorous fish stocks. Proceedings of the eighth International Coral Reef Symposium, 1:719–724.

———. 1998. An undescribed fungal pathogen of reef-forming crustose coralline 

algae discovered in American Samoa. Coral Reefs, 17(2):144. http://dx.doi

.org/10.1007/s003380050108.

———. 1999. Castles built by a chiton from the Great Astrolabe Reef, Fiji. Coral 

Reefs, 18(2):146.

———. 2007. Assessment of coral reefs using herbivory/nutrient assays and indicator groups of benthic primary producers: A critical synthesis, proposed protocols, and critique of management strategies. Aquatic Conservation: Marine 

and Freshwater Ecosystems, 17:195–215. http://dx.doi.org/10.1002/aqc.790.

———. 2008. Coralline algal rhodoliths form extensive benthic communities in 

the Gulf of Chiriqui, Pacific Panama. Coral Reefs 27:553. http://dx.doi.org

/10.1007/s00338-008-0368-5.

Littler, M. M., D. S. Littler, S. M. Blair, and J. N. Norris. 1985. Deepest known 

plant life is discovered on an uncharted seamount. Science, 227:57–59. http://

dx.doi.org/10.1126/science.227.4682.57.

———. 1986. Deepwater plant communities from San Salvador Seamount, Bahamas: New records of distribution, abundance and primary productivity. 

Deep-Sea Research, 33:882–892. 

Littler, M. M., D. S. Littler, and B. L. Brooks. 2006. Harmful algae on tropical coral 

reefs: bottom-up eutrophication and top-down herbivory. Harmful Algae,

5(5):565–585. http://dx.doi.org/10.1016/j.hal.2005.11.003.

———. 2007. Target phenomena on South Pacific reefs: Strip harvesting by prudent 

pathogens? Reef Encounter, 34:23–24.

Littler, M. M., D. S. Littler, and M. D. Hanisak. 1991. Deep-water rhodolith distribution, productivity and growth history at sites of formation and subsequent degradation. Journal of Experimental Marine Biology and Ecology, 

1991:1–20.

Littler, M. M., D. S. Littler, and P. R. Taylor. 1995. Selective herbivore increases biomass of its prey: A chiton–coralline reef-building association. Ecology, 76(5): 

1661–1681. http://dx.doi.org/10.2307/1938167.

Ohde, S. 1995. Calcium carbonate production and carbon dioxide flux on a coral 

reef, Okinawa. In Biogeochemical processes and ocean flux in the western 

Pacific, ed. H. Sakai and Y. Nozaki, pp. 93–98. Tokyo: Terra Scientific Publishing Company (TERRAPUB).

Philippi, R. A. 1837. Beweis, dass die Nulliporen Pflanzen sind. Archiv Für Naturgeschicthe, 3:387–393.

Shors, E. C. 1999. Coralline bone graft substitutes. Orthopedic Clinics of North 

America, 30:599–613. http://dx.doi.org/10.1016/S0030-5898(05)70113-9.

Silva, P. C., and H. W. Johansen. 1986. A reappraisal of the order Corallinales 

(Rhodophyceae). European Journal of Phycology, 21:245–254. http://dx.doi

.org/10.1080/00071618600650281.

Sloane, H. 1707. A voyage to the islands, Madera, Barbados, Nieves, S. Christophers and Jamaica. Vol. 1. London: Author. 364 pp.

Steneck, R. S. 1983. Quantifying herbivory on coral reefs: Just scratching the surface and still biting off more than we can chew. In The ecology of deep and 

shallow coral reefs, ed. M. L. Reaka, pp. 103–112. Symposia Series for Undersea Research, Vol. 1. Rockville, Md.: National Oceanographic and Atmospheric Administration.

———. 1985. Adaptations of crustose coralline algae to herbivory: Patterns in 

space and time. In Paleoalgology, ed. D. Toomy and M. Nitecki, pp. 352–366. 

Berlin: Springer-Verlag. http://dx.doi.org/10.1007/978-3-642-70355-3.

———. 1989. Herbivory on coral reefs: A synthesis. Proceedings of the sixth International Coral Reef Symposium, 1:37–49.

Woelkerling, W. J. 1988. The coralline red algae: An analysis of the genera and subfamilies of nongeniculate Corallinaceae. London: British Museum (Natural 

History).
The Nature of Turf and Boring Algae 

and Their Interactions on Reefs

Mark M. Littler and Diane S. Littler

ABSTRACT. A major goal of this short review is to familiarize the scientific diving community 

with the importance, seasonality, and high diversity of juvenile and microalgal turf assemblages and 

rock-boring cyanobacteria on coral reefs to stimulate further interest in research on these groups.

Boring endolith activity not only negatively inflicts damage to living carbonate coral reef hosts, but 

also positively benefits primary productivity and provides the nutritional base for excavating grazers 

in otherwise dead substrates. Algal turfs, like all subtidal assemblages on reefs, are best studied by 

scuba techniques, which have greatly facilitated observation, collection, photographic sampling, and 

manipulative studies. Prior to scuba, studies in the shallow intertidal and by dredging dominated, 

which focused by necessity primarily on taxonomy and distributional records. Scuba has enabled 

studies on ecology, physiology, interactions, etc., that were impossible before its development. 

TURF ALGAE INTERACTIONS

Turf algae are multispecies assemblages of diminutive, mostly filamentous algae that 

attain a vertical height of only 1 mm to 2 cm (Figure 1). Turf algae often exist as assemblages (algal turfs), are ubiquitous in reef systems and are composed of the small, juvenile 

stages of macroalgae (e.g., Gelidium spp., Gelidiella spp., Digenia simplex) along with 

faster-growing filamentous species (usually red algae such as Polysiphonia spp., Herposiphonia spp., and Ceramium spp.; blue-green algae (cyanobacteria); diatoms; brown 

algae; green algae; and coralline algae) and detritus and sediments. The assemblages of 

juvenile and microalgal species have a high diversity, exceeding 100 species in some western Atlantic turfs, although 30–50 species co-occurring is more common (Steneck, 1988). 

Within the turf assemblage, there is often a high turnover of individual turf algal species 

seasonally, and only a few taxa are able to persist or remain abundant throughout the 

year. However, the assemblages, when viewed as a functional indicator group, remain 

relatively stable year round. They are often able to recover rapidly after being partially 

removed by physical disturbance. 

Algal turfs characteristically trap ambient sediments and smother corals and other 

competitors for space by gradual encroachment. These algal forms become predominant under minimal inhibitory top-down (e.g., herbivory) and stimulatory bottom-up 

(e.g., nutrient supply) controls (Littler et al., 2006). Algal turfs have been shown to form 

extensive horizontal mats under reduced nutrient-loading rates (Fong et al., 1987) or 

infrequent nutrient inputs (Fujita et al., 1988). Domination of horizontal reef space by 

turf algae suggests desirably low nutrient levels but an inadequate herbivory component 

required for healthy coral-dominated reefs. Their relatively small size and rapid regeneration from basal remnants (perennation) result in only moderate losses to herbivory at low 

grazing pressures.

Mark M. Littler and Diane S. Littler, formerly 

of Department of Botany, National Museum of 

Natural History, Smithsonian Institution, P.O. 

Box 37012, MRC 166, Washington, District of 

Columbia 20013-7012, USA.

Manuscript received 25 January 2012; accepted 5 March 2013.
214 • smithsonian contributions to the marine sciences

FIGURE 1. Naturally occurring algal turf communities. Top left: Polysiphonia sp. Top right: Laurencia obtusa. Bottom: Gelidium 

pusillum. (Photos by D. Littler.)
number 39 • 215

Turf algal assemblages are very much affected by the behavior of territorial damselfish that chase off any larger herbivores 

that may come into their areas. Because of their preferential grazing and protection, damselfish cultivate more diverse alga turfs 

with higher biomass within their territories.

Turf algae have opportunistic (“weedy”) life-history characteristics, including high surface area to volume ratios and the 

ability to maintain substantial nutrient uptake and growth rates 

under low-nutrient conditions (Rosenberg and Ramus, 1984). 

Turfs also contain populations of nitrogen-fixing cyanobacteria 

(Adey, 1998) that can enrich the other low-growing members 

within the dense turf assemblage in oligotrophic waters. Turf 

algae have been utilized effectively as a functional group in the 

burgeoning saltwater aquarium trade, where they are grown in 

brightly lit, circulating flumes (i.e., patented scrubbers; Adey et 

al., 2011) to remove excessive nutrient pollutants.

BORING CYANOBACTERIA 

INTERACTIONS

Boring cyanobacteria are filamentous, prokaryotic, mostly 

photosynthetic organisms that chemically bore into calcareous 

rock and limestone. Penetrating or boring algae play important 

roles in the bioerosion of coral reefs; these filamentous microorganisms result in the breakdown of carbonate structure both 

directly and indirectly (reviewed by Tribollet, 2008). The most 

common are blue-green algae (Cyanophyta, cyanobacteria) that 

attack calcareous substrates differentially; the aragonite skeletons of corals are most easily penetrated and the denser calcite deposits of coralline algae are most resistant. However, the 

mechanism of carbonate dissolution remains largely unknown 

and actually contradicts geochemical models that predict the 

precipitation of carbonates by photosynthetically induced pH 

increases. As a consequence of variable processes such as selective settling, competition, persistence, and subsequent grazing 

of euendolithic (true endoliths) cyanobacteria, coastal rocks are 

biodegraded differentially, resulting in grotesque, sharp-edged 

features called karsts (Figure 2). These processes act as feedback 

mechanisms by producing diverse microbial habitats with patchy 

water-retention pockets, which further enhance bioerosion and 

endolithic community diversity. 

Boring endoliths colonize all carbonate substrates on coral 

reefs and are distributed throughout the world’s tropical seas. 

Intertidal carbonate coasts are most intensively bioeroded (Figure 3). However, although endolithic activity inflicts damage to 

living hosts, it also can provide positive overall benefits to reefs, 

including important primary productivity yields in otherwise 

FIGURE 2. Irregular and sharp karsts formed from habitats colonized by boring cyanobacteria and their deeply rasping predators. Inset: rasping 

organisms such as chitons and other mollusks. (Photos by D. Littler.)
216 • smithsonian contributions to the marine sciences

dead substrates. Endoliths attract excavating grazers, and this 

contributes to massive biodestruction processes and sediment 

formation. In other words, the bioerosional effect of boring cyanobacteria themselves is secondary; their primary significance is 

in providing the nutritional base for excavating grazers.

Boring cyanobacteria have been important in the destruction of carbonate throughout geological time. They occur from 

the upper intertidal to abyssal depths (Golubic et al., 1984), but 

in general show a decrease with depth. Marine limestone can 

be infested by more than half a million endolithic filaments per 

square centimeter. The oldest recorded endolithic blue-green—

and the earliest known occurrence of bioerosion—was found 

in 1.5 billion-year-old stromatolite rocks in China (Zhang and 

Golubic, 1987).

The diversity of boring microflora is thought to be large, 

comprising not only undiscovered blue-green algae, but also 

other algae (chlorophytes, rhodophytes) and fungi. Although 

their taxonomy has been studied for decades, new species are 

still being discovered, especially with the advent of molecular 

techniques (Gutner-Hoch and Fine, 2011). However, the taxonomy and diversity of boring blue-green algae remain relatively 

unknown and there is still much to be learned regarding this 

important group.

REFERENCES

Adey, W. H. 1998. Coral reefs: Algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. Journal of Phycology, 34:393–406. http://

dx.doi.org/10.1046/j.1529-8817.1998.340393.x.

Adey, W. H., P. C. Kangas, and W. Mulbry. 2011. Algal turf scrubbing: Cleaning surface waters with solar energy while producing a biofuel. Bioscience, 61:434–

441. http://dx.doi.org/10.1525/bio.2011.61.6.5.

Fong, P., R. Rudnicki, and J. B. Zedler. 1987. Algal community response to nitrogen 

and phosphorus loading in experimental mesocosms: Management recommendations for southern California lagoons. San Diego: San Diego Association of Governments.

Fujita, R. M., P. A. Wheeler, and R. L. Edwards. 1988. Metabolic regulation of ammonium uptake by Ulva rigida (Chlorophyta): A compartmental analysis of 

the rate-limiting step for uptake. Journal of Phycology, 24:560–566.

Golubic, S., S. E. Campbell, K. Drobne, B. Cameron, W. L. Balsam, F. Cimerman, 

and L. Dubois. 1984. Microbial endoliths: A benthic overprint in the sedimentary record, and a paleobathymetric cross-reference with foraminifera.

Journal of Paleontology, 58:351–361.

Gutner-Hoch, E., and M. Fine. 2011.Genotypic diversity and distribution of Ostreobium quekettii within scleractinian corals. Coral Reefs, 30:643–650. http://

dx.doi.org/10.1007/s00338-011-0750-6.

Littler, M. M., D. S. Littler, and B. L. Brooks. 2006. Harmful algae on tropical coral 

reefs: Bottom-up eutrophication and top-down herbivory. Harmful Algae,

5(5):565–585. http://dx.doi.org/10.1016/j.hal.2005.11.003.

Rosenberg, G., and J. Ramus. 1984. Uptake of inorganic nitrogen and seaweed 

surface area: Volume ratios. Aquatic Botany, 19:65–72. http://dx.doi.org/10

.1016/0304-3770(84)90008-1.

Steneck, R. S. 1988. Herbivory on coral reefs: a synthesis. Proceedings of the sixth 

International Coral Reef Symposium, Townsville, Australia, 1:37–49.

FIGURE 3. Extreme undercut formed by boring intertidal blue-green algae grazed by deep-rasping chitons. (Photo by D. Littler.)
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Tribollet, A. 2008. The boring microflora in modern coral reef ecosystems: A review 

of its roles. In Current Developments in Bioerosion, ed. M. Wisshak and L. Tapanila, pp. 67–94. Berlin: Springer-Verlag. http://dx.doi.org/10.1007/978-3-

540-77598-0_4.

Zhang, Y., and S. Golubic. 1987. Endolithic microfossils (Cyanophyta) from early 

Proterozoic stromatolites, Hebei, China. Acta Micropaleont Sinica, 4:1–12.

The Ecological Significance of Sexual 

Reproduction by Tropical Green Algae

Kenneth E. Clifton

ABSTRACT. The ability of scuba-equipped scientists to directly observe marine organisms in their 

natural environments has dramatically improved our understanding of marine ecological processes. 

Despite advances on numerous fronts, however, the basic ecology of many important groups, including the tropical green algae, remains relatively unstudied. This paper examines how aspects of sexual 

reproduction by these algae relate to their population dynamics and includes discussions of gamete 

formation, spatial dispersion of males and females, herbivory on fertile algae, the nature and timing 

of gamete release, fertilization success, and zygote dispersal. Further investigations into any of these 

topics promise to shed useful light on an ecologically important group of tropical seaweeds.

INTRODUCTION

The field of subtidal marine ecology owes much of its success to the technology of 

scuba. With the advent of open-circuit air delivery, scientists were no longer forced to 

rely on samples dredged from the depths or washed up on the shore to infer ecological 

processes. Organisms could be observed firsthand in their natural setting, and followed 

through time at a variety of depths and locations. As a result, we have learned a great 

deal about how marine life forms live and die beneath the waves, but there is still much 

to be learned.

Perhaps nowhere is this more apparent than in the study of tropical green algae. Five 

genera of siphonous green algae in the order Byropsidales (Caulerpa in the family Caulerpaceae and Halimeda, Penicillus, Rhipocephalus, and Udotea in the family Udoteacae) 

are particularly notable for their size, their abundance, and the range of habitats they occupy on or near coral reefs (Bold and Wynne, 1985; Littler and Littler, 1994, 2007; Hay, 

1997). Prior to direct observations enabled by the application of scuba, very little was 

known about the ecological role of these algae.

We now know that these seaweeds are extremely important members of shallowwater, tropical marine communities. As primary producers, these algae help sustain many 

reef-associated herbivores (e.g., Morrison, 1988; Niam, 1988; Littler and Littler, 1994; 

Stachowicz and Hay, 1996; Williams and Walker, 1999; Munoz and Motta, 2000). As 

relatively large, structurally complex benthic flora, tropical green algae provide shelter 

for numerous invertebrates (e.g., Stoner, 1985; Hendler and Littman, 1986; Hay et al., 

1990) while competing directly with others for space (e.g., Carpenter, 1986; Hughes et 

al., 1987; Littler et al., 1989; Tanner, 1995; Ceccherelli et al., 2000; Beach et al., 2003; 

Márquez and Diaz, 2005). Correlations between increasing green algal abundance and 

declining coral cover and reef biodiversity further emphasize the ecological significance 

of these seaweeds within coral reef communities (e.g., Porter and Meier, 1992; Hallock et 

Kenneth E. Clifton, Department of Biology, MSC 

53, Lewis and Clark College, Portland, Oregon 

97219, USA. Correspondence: clifton@lclark

.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
220 • smithsonian contributions to the marine sciences

al., 1993; Hughes, 1994a, 1994b; Ogden and Ogden, 1994; Sebens, 1994; Morand and Briand, 1996; Shulman and Robertson, 

1996; Szmant, 2002; Smith et al., 2006; Nelson, 2009). Tropical green seaweeds also produce complex defensive compounds 

that alter the foraging of herbivorous fishes and invertebrates 

(e.g., Paul and Fenical, 1986; Paul, 1987; Paul and Van Alstyne, 

1988; Hay and Fenical, 1992; Stachowicz and Hay, 1996) and 

potentially have useful biomedical properties (e.g., Fischel et al., 

1995; Isassi and Alvarez-Hernandez, 1995). Even after death, the 

heavily calcified thalli of the Udoteacae contribute to sand production, reef building, and other important geological processes 

(e.g., Wefer, 1980; Drew, 1983; Flügel, 1988; Marshall and Davies, 1988; Freile et al., 1995; Braga et al., 1996; Freile and Hillis, 

1997; Martin et al., 1997). 

Despite the obvious relevance of tropical green seaweeds 

to reef-associated ecosystems, their basic biology remains rather 

poorly understood, particularly aspects of their reproductive life 

history. As with many algae, variable, often subtle modes of reproduction obscure many of the most basic aspects of their life 

history (Bold and Wynne, 1985; Brawley and Johnson, 1992; 

Lobban and Harrison, 1994); there is a paucity of careful field 

studies that focus on the algae themselves (Walters et al., 2002; 

Vroom et al., 2003; van Tussenbroek and van Dijk, 2007). Indeed, 

the life cycles of some of the most abundant and important groups 

(e.g., Halimeda) have yet to be followed completely in either the 

lab or the field (see Meinesz, 1980). Put simply, more studies are 

needed that examine how tropical green seaweeds live and die. 

This paper seeks to promote further investigations of this cycle 

by highlighting the potential ecological significance of different 

aspects of sexual reproduction by tropical green macroalgae.

As with many algae, Bryopisdales reproduce both asexually 

and sexually. Early studies of vegetative reproduction via rhizoid 

extension (Hillis-Colinvaux, 1973; Walters and Smith, 1994) 

and, more recently, thallus fragmentation (Smith and Walters, 

1999; Walters et al., 2002) support a general premise that asexual processes contribute significantly to the dynamics of green 

seaweed populations on and around coral reefs (e.g., Friedmann 

and Roth, 1977; Hillis-Colinvaux, 1980; Meinesz, 1980). At the 

same time, observations of seasonal pulses of highly synchronous 

sexual activity by green algae on Caribbean reefs (Clifton, 1997, 

2008; Clifton and Clifton, 1999; van Tussenbroek et al., 2005) 

imply a previously underappreciated role for sexual reproduction in terms of population regulation and ecological influence. 

Because sexually reproducing algae die immediately following 

gamete release, annual peaks of reproduction by tropical green 

seaweeds have immediate effects on algal demography as density and cover percentage decline precipitously, often in a matter of weeks (Clifton and Clifton, 1999). While the synchronous 

nature of gamete release presumably boosts fertilization success 

during episodes of sex, how these bouts of reproduction contribute to subsequent algal recruitment and repopulation of reefs is 

currently unknown. The remainder of this paper examines how 

different aspects of sexual reproduction by green algae may contribute to their ecological significance.

Gamete Formation 

and Sexual Identity

Although easily detected by a trained observer, fertility and 

sexual reproduction in tropical Bryopsidales is a transient, often 

overlooked phenomenon. It begins when, overnight, a fraction of 

the population (tens to thousands of thalli) changes color and/

or develops external gametangia. These macroscopic features are 

clear and reliable indicators of an impending sexual event (Clifton 

and Clifton, 1999). What induces this pulse of fertility remains 

unknown (environmental factors such as tides, moon phase, 

water movement, temperature, and day length are known to organize bouts of synchronous sexual reproduction in other marine 

organisms; see reviews by Harrison and Wallace, 1990; Brawley 

and Johnson, 1992; Levinton, 1995). Within 24 or 48 hours (depending on species) the entire algal protoplasm converts to gametic products that migrate into newly developed gametangia. 

For all species but those in the monoecious genus Caulerpa, the 

gender of a fertile thallus (based on gametangia color and morphology; see Figure 1) becomes apparent during this time (Clifton 

and Clifton, 1999), facilitating measures of local sex ratios and 

nearest-neighbor distances prior to gamete release. For species 

of Caulerpa, macro- and microgametes concentrate in different 

parts of the thallus and can be identified based on color (green = 

microgametes, brown = macrogametes; Figure 2). These general 

patterns of fertility have now been verified for over 30 species in 

6 genera (Clifton and Clifton, 1999; KEC, personal observation).

The spatial dispersion of fertile male or female thalli presumably plays an important role in fertilization success. Proximity to other reproductive individuals coupled with the synchrony 

of release generally influences gamete concentration in broadcast-spawning organisms, and gamete concentration influences 

the likelihood that gametes of opposite sex will encounter one 

another following release (Lotterhos and Levitan, 2010). The 

spatial dispersion of males and females may be especially important for dioeceous, sand-dwelling species that occur in a broad 

range of densities (from isolated individuals to large “meadows” 

with densities of hundreds of individuals/m2

; e.g., Halimeda incrassata, H. monile, H. simulans, Penicillus spp., Rhypocephalus 

phoenix, and Udotea spp.). For these species, small, same-sex 

clusters of two or three individuals (within 5 cm of one another; 

KEC, unpublished data) are commonly encountered. It remains 

to be known whether these represent genetically identical thalli 

derived from vegetative reproduction (ramets), in which case the 

synchronous release of gametes would boost gamete concentrations and reduce the likelihood of gamete limitation (sensu Levitan, 1993), or whether they are genetically distinct thalli (genets) 

derived from sexual reproduction and recruitment into the population, in which case synchronous reproduction would increase 

gamete competition for fertilization. Gender-specific dispersion 

is, at first glance, less relevant for monoeceous species such as 

Caulerpa. However, differential patterns of sexual allocation 

to micro- and macrogamete production coupled with the overall spatial distribution of reproductive thalli could still play an 
number 39 • 221

important ecological role in determining the likelihood of successful zygote formation.

Sexual Reproduction 

and Herbivory

A diverse array of crustaceans, echinoderms, mollusks, and 

fishes consume siphonous green algae as part of their regular 

diet. These seaweeds counter with an evolved combination of 

chemical and physical defenses that deter rates of feeding by different herbivores to varying degrees (e.g., see Hay and Fenical, 

1992; Williams and Walker, 1999; Paul et al., 2001; Molis et al., 

2008; and references therein). To date, studies of herbivory on 

Bryopsidales have focused almost exclusively on the consumption on nonreproductive thalli. 

The potential for chemical and physical defenses to herbivory to be altered by a shift from vegetative to reproductive 

FIGURE 1. Examples of fertility—evident by the presence of gametangia and color change, as well as gender identity—in dioeceous 

species of siphonous green seaweeds. Species by column: (I) Penicillus capitatus (note the white stipe and lighter color of the capitulum 

in fertile seaweeds); (II) Halimeda tuna (external gametangia and white blades denote fertile condition); (III) Udotea caribea (note white 

blade and newly developed gametangia along terminal blade edge). Gender by row: (A) fertile males (lighter green color for all species 

and rounded tip morphology of gametangia for U. caribea); (B) fertile females (darker green/bluish color for all species and spiked tip 

morphology of gametangia for U. caribea); (C) nonfertile thalli for all three species. Photos by Kenneth Clifton.
222 • smithsonian contributions to the marine sciences

state seems high. Uncalcified gametangia, the structures that 

house gametes prior to their release, develop during the initial 

stages of fertility. Thus, they are potentially exposed to herbivores that would normally be deterred by the presence of CaCO3

for one or more night/day cycles, depending on the species of 

algae. The chemical defenses of these seaweeds may be similarly 

altered, as the conversion of the entire thallus from vegetative 

protoplasm to gametes occurs during a similar time span. While 

the phenomenon has not been investigated sufficiently, observations of heavy infestations of the sacoglossan sea slug Elysia tuca

on fertile specimens of sand-dwelling Halimeda incrassata and 

H. monile (hundreds of slugs on a single reproductive thallus 

versus a normal load of one or fewer slugs on a nonreproductive 

thallus; KEC, pers. obs.) indicate that some species of herbivores 

respond directly to the expression of sexual reproduction by 

green algae. Severe herbivory on the gametangia of fertile specimens of Udotea, Penicillus, and Rhypocephalus have also been 

observed (Figure 3). If a shift to fertility does attract a disproportionate level of herbivory, it may represent an additional cost of 

reproduction to the seaweed; the phenomenon certainly merits 

further study.

Gamete Characteristics

The flagellated, anisogamous gametes produced by siphonous green algae are known from a variety of studies (e.g., Goldstein and Morrall, 1970; Meinesz, 1972, 1980; Kajimura, 1977; 

Hillis-Colinvaux, 1980; Enomoto and Ohba, 1987; Clifton and 

Clifton, 1999). The size of biflagellated male microgametes is 

relatively consistent across taxa, whereas female macrogametes 

occur in two forms, depending on species. Halimeda, Caulerpa, 

and one species of Udotea (flabellum) produce biflagellated, phototactic macrogametes that morphologically resemble microgametes but are 2–34 times larger (Clifton and Clifton, 1999) and 

possess an obvious eye-spot. Relative gamete size may play an 

important role in fertilization dynamics in terms of both gamete 

encounter rates (Levitan, 2006) and gamete behavior. Although 

negatively buoyant, biflagellated macrogametes can swim relatively long (1–5 m) distances toward light (Clifton, 1997) prior 

to fertilization. As in other green algae (e.g., Togashi et al., 1998), 

zygotes of these species show negative phototaxis immediately 

after fertilization (KEC, unpublished). In contrast, Penicillus, Rhipocephalus, and three species of Udotea (abbottiorum, 

caribaea, and cyathiformes) produce large (100 μm diameter) 

stephanokont gametes (Figure 4) with flagella arrayed along a 

membranous, sheetlike tail (Clifton and Clifton, 1999). To date, 

these large, macroscopically visible gametes (Figure 5) have not 

been well studied (Meinesz, 1980; Littler and Littler, 1990); however, observations of freshly released material indicate that these 

gametes are relatively immotile. Under calm conditions they 

quickly sink, tail up, to the bottom, where flagellar motion drives 

water past the gamete. This may increase encounter rates with 

microgametes. Upon fusion, the membranous tail quickly (30–90 

s) stops moving and is absorbed into the zygote. Both negative 

phototaxis and negative buoyancy presumably limit the distance 

a zygote disperses, however the extent of this limitation and the 

degree to which it influences local population dynamics following zygote development and recruitment awaits further study. 

Given that siphonous green algae convert their entire protoplasm into gametes, and in keeping with a simple model of quantity versus quality, the number of gametes produced by an alga 

FIGURE 2. Progression of fertility in the monoeceous green alga Caulerpa cupressoides. (A) Cellular contents migrate from 

rhizoids into unspecialized gametangia at terminal ends of blades approximately 48 hours prior to gamete release. (B) Roughly 

24 hours later, segregation of macrogametes (brown, terminal areas of blade) and microgametes (greener, basal sections) occurs, leading to a two-colored appearance. (C) The discharge of both micro- and macrogametes occurs from separate small 

tubular orifices that develop 1–3 hours prior to gamete release. Scale bar = 1 cm (all three images). Photos by Kenneth Clifton.
number 39 • 223

FIGURE 3. Details of protoplasm migration, gametangia development, and gamete release for male and female Penicillus lamourouxii. (1) Fertile male (a) and female (b) thalli showing diagnostic white stipe caused by protoplasmic migration. The darker, blue/

green coloration of the female and the lighter green color of the capitulum are both reliable indicators of fertility and gender. (2) Closer 

view of the top section of a fertile male (a) and female (b) 12 hours prior to gamete release. Note the light green, uncalcified extension 

of siphonous tubes and clearly evident sexually dimorphic colorations. (3) Gamete release from male (a) and female (b) seaweeds. 

Individual macrogametes can be seen wafting away from the female. Photos by Kenneth Clifton.

FIGURE 4. Scanning electron microscope image of stephanokont macrogamete from Rhipocephalus phoenix. Flagellae that line the edge of 

the membranous tail are not visible, probably due to loss during sample 

preparation. Photo by Kenneth Clifton.
224 • smithsonian contributions to the marine sciences

should be related to gamete size. Preliminary investigations support this contention. Samples of total gamete release by a single 

thallus into known volumes of seawater reveal that, as expected, 

larger seaweeds release a greater number of gametes, and further 

that females produce fewer gametes than males for a given thallus size (Figure 6). There appears to be no relationship between 

gamete size and thallus size.

The Timing of Gamete Release

The reproductive synchrony of siphonous green algae can 

be evaluated on several temporal scales. On the diel scale, in 

all species studied to date, both micro- and macrogametes are 

released directly into the water column during a single, brief 

(typically 5–15 min), highly synchronous pulse of early morning 

FIGURE 5. Examples of herbivores known to consume siphonous green algae and herbivory on fertile seaweeds. Clockwise from top left: the saccoglossan sea slug Elysia subornata on nonfertile Caulerpa racemosa; E. crispata on nonfertile 

Penicillus lamourouxii; a close up view of fertile C. racemosa showing unspecialized gametangia along blade bases and an 

apparent bite wound (source unknown) to one blade; parrotfish bite wounds to gametangia of female Udotea caribaea; 

and E. subornata on nonfertile Rhipocephalus phoenix. Photos by Kenneth Clifton.
number 39 • 225

reproduction (Clifton, 1997). The alga dies immediately following gamete release (holocarpy). The timing of release appears to 

be organized around changing light levels associated with the 

onset of daylight, though water temperature also plays a role 

(Clifton, 1997). The duration of gamete release varies between 

species, with larger, epilithic species tending to release their gametes more rapidly (Clifton and Clifton, 1999). With many thalli 

reproducing synchronously, dense gamete clouds may extend 

down-current for tens of meters, though these generally dissipate 

within 5–10 minutes even under the calmest conditions. The precise timing of release relative to sunrise remains consistent for a 

given species across seasons and years. Up to nine species from 

five genera have been observed to release gametes on the same 

morning; however, each species has a specific, narrow time of 

release (Clifton and Clifton, 1999). Some species show overlapping times of gamete release, though more closely related species 

(Hillis et al., 1998; Vroom et al., 1998; Kooistra et al., 1999) 

reproduce at different times (Clifton, 1997). This may reduce hybridization if gamete viability is short lived relative to the time 

between release by different species. 

Green algae may show a broad seasonal peak of sexual reproduction that shifts with latitude (Clifton, 2008), but unlike 

many broadcast-reproducing invertebrates they exhibit no obvious lunar or tidal cycling (Clifton, 1997). During seasonal peaks 

of reproductive activity, populations of green algae undergo iterative bouts of sexual reproduction with varying degrees of intensity. Only a subset of a given population releases gametes on 

a particular morning (generally about 5%, though major bouts 

of sexual reproduction involving more than 45% of the population can occur). Episodes of sexual reproduction typically occur 

on numerous reefs within a given geographic region on the same 

morning, including on reefs several kilometers apart. 

During the seasonal peak of activity, bouts of sex occur on 

roughly two-thirds of mornings; this frequency varies somewhat 

interannually (e.g., bouts of gamete release occurred on 42%, 

80%, and 68% of days during the seasonal reproductive peaks 

in 1995, 1996, and 1997, respectively). When sexual reproduction is observed on a given morning, several species are often involved. On a single Panamanian patch reef in 1996, 16 species of 

green algae collectively underwent 233 bouts of gamete release 

between March and July, with 97 additional events occurring 

between March and mid-May the following year. A recent comparison of algal sexual reproduction in St. Croix and Panama 

indicates that similar levels of activity occur throughout the Caribbean (Clifton, 2008). 

Given the holocarpic life history of these seaweeds, iterative 

bouts of sexual reproduction have a rapid and dramatic impact 

on adult algal distribution and abundance (Clifton and Clifton, 

1999). Algal cover can drop dramatically, freeing up space for 

future colonization, perhaps by the same species, or more likely 

by other members of the benthic community. Our understanding 

of the nature of algal population dynamics and their effect on 

the overall organization and function of coral reefs remains in 

its infancy. Similarly, little is known of how the postreproductive 

disintegration and dissolution of these calcified seaweeds contributes to rates of CaCO3

 input into reef sediments.

Zygote Formation and Dispersal

Very little is currently known about the early life history 

of siphonous green seaweeds. Although mature algae are easily 

maintained in aquaria (e.g., Hillis-Colinvaux, 1980; Drew and 

Abel, 1988; Ohba et al., 1992), zygote development in the laboratory has been described for only Caulerpa serrulata (Price, 

1992) and Halimeda tuna (Meinesz, 1972). After five months 

the latter produced an alga quite different from the parents, and 

the complete life cycle of the genus remains unresolved. Meinesz 

(1980) reported adult-like algae from the zygotes of Flabellia 

petiolata (formerly Udotea) after seven months, and Friedmann 

and Roth (1977) describe an “espera” (non-adult-like) state of 

Penicillus capitatus that arose after months of culturing. It is unclear whether these nonadult morphs represent a natural stage of 

development or simply an artifact of in vivo conditions. 

These laboratory observations should encourage further 

study of zygote development, particularly under natural conditions. Such data are fundamental to an understanding of how 

algal recruitment and rates of growth from zygote to adult thallus influence population dynamics. The relatively slow rates 

of development reported from the lab coupled with field observations of delayed recovery of populations following peaks 

of sexual activity suggest that algal recruitment occurs several 

months after fertilization, with a possible cryptic stage of life 

history occurring before the production of an adult form. Perhaps this allows green algae to persist through unfavorable 

seasonal periods of temperature, salinity, or light in a manner 

FIGURE 6. Number of gametes released versus thallus size for 10 

male (microgametes, open circles) and 10 female (macrogametes, 

filled circles) Udotea flabellum. The effect of sex on the relationship 

between gamete number and thallus size was significant (ANCOVA; 

p = 0.035).
226 • smithsonian contributions to the marine sciences

analogous to terrestrial seed banks (Hoffmann and Santelices, 

1991). Seasonality in Panama (Cubit et al., 1989), where most of 

the longer-term data on temporal patterns of green algal sexual 

reproduction have been obtained, is known to be ecologically 

significant for herbivorous reef fishes and their algal foods (e.g., 

Robertson, 1990; Clifton, 1995).

CONCLUSION

Numerous studies have implied a significant ecological role 

for siphonous green algae within tropical marine communities. 

To date, however, the basic biology of these algae remains poorly 

understood. The presence of complex life-history strategies and 

remarkable interspecific variation in the manner in which different algae reproduce are partly to blame for this dearth of 

information, yet this very same complexity and variation offer 

marine ecologists unparalleled opportunities to explore the ways 

in which factors such as timing and location of reproduction, 

patterns of gamete size and behavior, and fertilization success 

and zygote development ultimately influence where and how 

abundantly these algae occur. Investigations of the origins and 

consequences of algal reproduction remain a critical step toward 

improved understanding of the biological mechanisms that underlie their ecological significance. 

ACKNOWLEDGMENTS

My studies of tropical green seaweeds have been supported 

by numerous sources, including the National Science Foundation, the Smithsonian Institution, the National Geographic Society, the University of California, Santa Cruz, and Lewis and 

Clark College. I thank Lisa Clifton for her keen observation 

skills and assistance with my field studies over the years. Diane 

and Mark Littler also deserve recognition for their willingness to 

share their insights about the Bryopsidales with a recovering vertebrate chauvinist. I thank also the organizers of the “Research 

and Discoveries” symposium for bringing this work together: 

Michael Lang, Roberta Marinelli, Susan Roberts, Phillip Taylor, 

and their respective agencies. Finally, I acknowledge the inspiring 

contributions of those early scientific divers, including my father, 

H. E. Clifton, one of the original Tektite aquanauts, whose pioneering use of scuba as a research tool ushered in a new era of 

scientific inquiry. 

REFERENCES

Beach, K. S., L. J. Walters, H. Borgeas, C. M. Smith, J. A. Coyer, and P. S. Vroom. 

2003. The impact of Dictyota spp. on Halimeda populations of Conch Reef, 

Florida Keys. Journal of Experimental Marine Biology, 297:141–159. http://

dx.doi.org/10.1016/j.jembe.2003.07.003.

Bold, H. C., and M. J. Wynne. 1985. Introduction to the algae: Structure and reproduction. New Jersey: Prentice-Hall, Inc.

Braga, J. C., J. M. Martin, and R. Riding. 1996. Internal structure of segment reefs: 

Halimeda algal mounds in the Mediterranean Miocene. Geology, 24:35–38. 

http://dx.doi.org/10.1130/0091-7613(1996)024<0035:ISOSRH>2.3.CO;2.

Brawley, S. H., and L. E. Johnson. 1992. Gametogenesis, gametes and zygotes: An 

ecological perspective on sexual reproduction in the algae. British Phycological Journal, 27:233–252. http://dx.doi.org/10.1080/00071619200650241.

Carpenter, R. C. 1986. Partitioning herbivory and its effects on coral reef algal communities. Ecological Monographs, 56:345–360 http://dx.doi.org/10.2307

/1942551.

Ceccherelli, G., L. Piazzi, and F. Cinelli. 2000. Response of the non-indigenous 

Caulerpa racemosa (Forsskal) J. Agardh to the native seagrass Posidonia oceanica (L.) Delile: Effect of density of shoots and orientation of edges of meadows. Journal of Experimental Marine Biology, 243:227–240. http://dx.doi

.org/10.1016/S0022-0981(99)00122-7.

Clifton, K. E. 1995. Asynchronous food availability on neighboring Caribbean 

coral reefs determines seasonal patterns of growth and reproduction for an 

herbivorous parrotfish. Marine Ecology Progress Series, 116:39–46. http://

dx.doi.org/10.3354/meps116039.

———. 1997. Mass spawning by green algae on coral reefs. Science, 275:1116–

1118. http://dx.doi.org/10.1126/science.275.5303.1116.

———. 2008. Spatial patterns of reproductive synchrony by four genera of tropical 

green seaweed across a latitudinal gradient in the Caribbean. Proceedings of 

the eleventh International Coral Reef Symposium, 1:351–355.

Clifton, K. E., and L. M. Clifton. 1999. The phenology of sexual reproduction by 

green algae on coral reefs. Journal of Phycology, 35:24–34. http://dx.doi.org

/10.1046/j.1529-8817.1999.3510024.x.

Cubit, J. D., H. M. Caffey, R. C. Thompson, and D. M. Windsor. 1989. Meteorology 

and hydrography of a shoaling reef flat on the Caribbean coast of Panama. 

Coral Reefs, 8:59–66. http://dx.doi.org/10.1007/BF00301804.

Drew, E. A. 1983. Halimeda biomass, growth rates and sediment generation on 

reefs of the central Great Barrier Reef province. Coral Reefs, 2:101–110. 

http://dx.doi.org/10.1007/BF02395280.

Drew, E. A., and K. M. Abel. 1988. Studies on Halimeda II: Reproduction, particularly the seasonality of gametangia formation, in a number of species 

from the Great Barrier Reef province. Coral Reefs, 6:207–218. http://dx.doi

.org/10.1007/BF00302017.

Enomoto, S., and H. Ohba. 1987. Culture studies on Caulerpa (Caulerpales, Chlorophyceae). I. Reproduction and development of C. racemosa var. laetevirens. 

Japanese Journal of Phycology, 35:167–177.

Fischel, J. L., R. Lemee, P. Formento, and C. Caldani. 1995. Cell growth inhibitory 

effects of caulerpenyne, a sequesterpenoid from the marine algae Caulerpa 

taxifolia. Anticancer Research, 15:2155–2160.

Flügel, E. 1988. Halimeda: Paleontological record and palaeoenvironmental significance. Coral Reefs, 6:123–130. http://dx.doi.org/10.1007/BF00302008.

Freile, D., and L. Hillis. 1997. Carbonate productivity by Halimeda incrassata in a 

land proximal lagoon, Pico Feo, San Blas, Panama. Proceedings of the eighth 

International Coral Reef Symposium, 1:762–772.

Freile, D., J. D. Milliman, and L. Hillis. 1995. Leeward bank margin Halimeda

meadows and draperies and their sedimentary importance on the western 

Great Bahama Bank slope. Coral Reefs, 14:27–33. http://dx.doi.org/10.1007

/BF00304068.

Friedmann, E. I., and W. C. Roth. 1977. Development of the siphonous green 

alga Penicillus capitatus and the Espera state. Botanical Journal of the Linnean Society, 74:189–214. http://dx.doi.org/10.1111/j.1095-8339.1977.tb

01176.x.

Goldstein, M., and S. Morrall. 1970. Gametogenesis and fertilization in Caulerpa. 

Annals of the New York Academy of Sciences, 175:660–672. http://dx.doi

.org/10.1111/j.1749-6632.1970.tb45183.x.

Hallock, P., F. E. Mulerkarger, and J. C. Halas. 1993. Coral reef decline. National 

Geographic Society Research and Exploration, 9:358–378. 

Harrison, P. L., and C. C. Wallace. 1990. Reproduction, dispersal, and recruitment 

of scleractinian corals. In Ecosystems of the world: Coral reefs, ed. Z. Dubinski, pp. 133–207. Amsterdam: Elsevier. 

Hay, M. E. 1997. Calcified seaweeds on coral reefs: Complex defenses, trophic relationships, and value as habitats. Proceedings of the eighth International Coral 

Reef Symposium, 1:718–719.

Hay, M. E., J. E Duffy, and W. Fenical. 1990. Host-plant specializations decreases 

predation on a marine amphipod: An herbivore in plant’s clothing. Ecology,

71:733–743. http://dx.doi.org/10.2307/1940326.

Hay, M. E., and W. Fenical. 1992. Chemical mediation of seaweed–herbivore interactions. In Plant–animal interactions in the marine benthos, ed. M. D. John, 
number 39 • 227

S. S. Haskins, and J. H. Price, pp. 319–337. Systematics Association special 

volume. Oxford: Clarendon Press.

Hay, M. E., Q. E. Kappel, and W. Fenical. 1994. Synergisms in plant defenses against 

herbivores: Interactions of chemistry, calcification, and plant quality. Ecology,

75:1714–1726. http://dx.doi.org/10.2307/1939631.

Hendler, G., and B. S. Littman. 1986. The ploys of sex: Relationships among the 

mode of reproduction, body size and habits of coral-reef brittlestars. Coral 

Reefs, 5:31–42. http://dx.doi.org/10.1007/BF00302169.

Hillis, L. W., J. A. Engman, and W. H. C. F. Kooistra. 1998. Morphological and 

molecular phylogenies of Halimeda (Chlorophyta, Bryopsidales) identify 

three evolutionary lineages. Journal of Phycology, 34:669–681. http://dx.doi

.org/10.1046/j.1529-8817.1998.340669.x.

Hillis-Colinvaux, L. 1973. Reproduction in the calcareous green algae of coral 

reefs. Journal of the Marine Biological Association of India, 14:328–334.

———. 1980. Ecology and taxonomy of Halimeda: Primary producer of coral 

reefs. Advances in Marine Biology, Vol. 17. London: Academic Press.

Hoffmann, A. H., and B. Santelices. 1991. Banks of algal microscopic forms: Hypotheses on their functioning and comparisons with seed banks. Marine Ecology Progress Series, 79:185–194. http://dx.doi.org/10.3354/meps079185.

Hughes, T. P. 1994a. Catastrophes, phase shifts, and large-scale degradation of a 

Caribbean coral reef. Science, 265:1547–1551. http://dx.doi.org/10.1126

/science.265.5178.1547.

———. 1994b. Coral Reef Degradation: A long term study of human and natural 

impacts. In Proceedings of the colloquium on global aspects of coral reefs: 

Health, hazards, and history, 1993, ed. R N. Ginsburg, pp. 208–213. Miami: 

University of Miami.

Hughes, T. P., D. C. Reed, and M. Boyle. 1987. Herbivory on coral reefs: Community 

structure following mass mortalities of sea urchins. Journal of Experimental Marine Biology, 113:39–59. http://dx.doi.org/10.1016/0022-0981(87)

90081-5.

Isassi, G. D., and S. Alvarez-Hernandez. 1995. Anticoagulant properties of Mexican 

algal extracts: Heparin-like potency of Halimeda discoidea (Chlorophyta) extract. Cryptogamie Algologie, 16:199–205.

Kajimura, M. 1977. On dioecious and isogamous reproduction of Caulerpa scalpelliformes (R.Br.) Ag. var. denticulata (Decsn.) Wever Van Bosse from the Oki 

Islands, Shimane Prefecture. Bulletin of the Japanese Society of Phycology,

25:27–33.

Kooistra, W. H. C. F., M. Calderon, and L. W. Hillis. 1999. Development of the 

extant diversity in Halimeda is linked to vicariant events. Hydrobiologica,

399:39–45. http://dx.doi.org/10.1023/A:1017084018210.

Levinton, J. S. 1995. Marine Biology: Function, Biodiversity, Ecology. New York: 

Oxford University Press. 

Levitan, D. R. 1993. The importance of sperm limitations to the evolution of egg 

size in marine invertebrates. American Naturalist, 141:517–535. http://dx

.doi.org/10.1086/285489.

———. 2006. Relationship between egg size and fertilization success in broadcast spawning marine invertebrates. Integrative and Comparative Biology,

46:298–311. http://dx.doi.org/10.1093/icb/icj025.

Littler, M. M., and D. S. Littler. 1990. Systematics of Udotea species (Bryopsidales, Chlorophyta) in the tropical western Atlantic. Phycologia, 29:206–252. 

http://dx.doi.org/10.2216/i0031-8884-29-2-206.1.

———. 1994. Tropical reefs as complex habitats for diverse macroalgae. In Seaweed ecology and physiology, ed. C. S. Lobban and P. J. Harrison, pp. 72–75. 

New Jersey: Cambridge University Press. http://dx.doi.org/10.1017/CBO

9780511626210.

———. 2007. Assessment of coral reefs using herbivory/nutrient assays and indicator groups of benthic primary producers: A critical synthesis, proposed protocols and a critique of management strategies. Aquatic Conservation: Marine 

and Freshwater Ecosystems, 17:195–215. http://dx.doi.org/10.1002/aqc.790.

Littler, M. M., P. R. Taylor, and D. S. Littler. 1989. Complex interactions in the 

control of coral zonation on a Caribbean reef flat. Oecologia, 80:331–342. 

http://dx.doi.org/10.1007/BF00379034.

Lobban, C. S., and P. J. Harrison, eds. 1994. Seaweed ecology and physiology. 

New Jersey: Cambridge University Press. http://dx.doi.org/10.1017/CBO

9780511626210.

Lotterhos, K., and D. R. Levitan. 2010. Gamete release and spawning behavior in 

broadcast spawning marine invertebrates. In The evolution of primary sexual 

characters, ed. J. Leonard, pp. 99–120. London: Oxford University Press.

Márquez, J. C., and J. M. Diaz. 2005. Coral and macroalgae interactions: Dependence between involved species. Boletin de Investigaciones Marinas y Costeras, 34:227–242.

Marshall, J. F., and P. J. Davies. 1988. Halimeda bioherms of the northern 

Great Barrier Reef. Coral Reefs, 6:139–148. http://dx.doi.org/10.1007/BF

00302010.

Martin, J. M., J. C. Braga, and R. Riding. 1997. Late Miocene Halimeda algamicrobial segment reefs in the marginal Mediterranean Sorbas Basin, Spain. 

Sediment, 44:441–456. http://dx.doi.org/10.1046/j.1365-3091.1997.d01

-31.x.

Meinesz, A. 1972. Sur le cycle de l’Halimeda tuna (Ellis et Solander) Lamouroux 

(Udoteacae, Caulerpales). Comptes Rendus de l’Académie des Sciences, 275: 

1363–1365.

———. 1980. Connaisances actuelles et contribution a l’etude de la reproduction 

et du cycle des udoteacees (Caulerpales, Chlorophytes). Phycologia, 19:110–

138. http://dx.doi.org/10.2216/i0031-8884-19-2-110.1.

Molis, M., J. Körner, Y. W. Ko, and J. H. Kim. 2008. Specificity of inducible seaweed 

anti-herbivory defenses depends on identity of macroalgae and herbivores. 

Marine Ecology Progress Series, 345:97–105. http://dx.doi.org/10.3354/meps

07255.

Morand, P., and X. Briand. 1996. Excessive growth of macroalgae: A symptom 

of environmental disturbance. Botanica Marina, 39:491–516. http://dx.doi

.org/10.1515/botm.1996.39.1-6.491.

Morrison, D. 1988. Comparing fish and urchin grazing in shallow and deeper 

coral reef algal communities. Ecology, 69:1367–1382. http://dx.doi.org/10

.2307/1941634.

Munoz, R. C., and P. J. Motta. 2000. Interspecific aggression between two parrotfishes (Sparisoma, Scaridae) in the Florida Keys. Copeia, 2000:674–683. 

http://dx.doi.org/10.1643/0045-8511(2000)000[0674:IABTPS]2.0.CO;2.

Nelson, W. A. 2009. Calcified macroalgae—critical to coastal ecosystems and vulnerable to change: A review. Marine and Freshwater Research, 60:787–801. 

http://dx.doi.org/10.1071/MF08335.

Niam, O. 1988. Distributional pattern of mobile fauna associated with Halimeda

in the Tiahura coral-reef complex (Moorea, French Polynesia). Coral Reefs,

6:237–250. http://dx.doi.org/10.1007/BF00302020.

Ogden, J. C., and N. B. Ogden. 1994. The coral reefs of the San Blas Islands: Revisited after 20 years. In Proceedings of the colloquium on global aspects 

of coral reefs: Health, hazards, and history, 1993, ed. R N. Ginsburg, pp. 

267–272. Miami: University of Miami.

Ohba, H., H. Nashima, and S. Enomoto. 1992. Culture studies on Caulerpa

(Caulerpales, Chlorophyceae) III. Reproduction, development, and morphological variation of laboratory-cultured C. racemosa var. peltata. The Botanical Magazine, Tokyo, 105:589–600. http://dx.doi.org/10.1007/BF02489433.

Paul, V. J. 1987. Feeding deterrent effects of algal natural products. Bulletin of 

Marine Science, 41:514–522. 

Paul, V. J., E. Cruz-Rivera, and R. W. Thacker. 2001. Chemical mediation of macroalgal-herbivore interactions: Ecological and evolutionary perspectives. In 

Marine chemical ecology, ed. J. McClintock and W. Baker, pp. 227–265. Boca 

Raton, La.: CRC Press.

Paul, V. J., and W. Fenical. 1986. Chemical defense in tropical green algae, order 

Caulerpales. Marine Ecology Progress Series, 34:157–169. http://dx.doi.org

/10.3354/meps034157.

Paul, V. J., and K. L. Van Alstyne. 1988. Chemical defense and chemical variation 

in some tropical Pacific species of Halimeda (Halimedaceae; Chlorophyta). 

Coral Reefs, 6:263–269. http://dx.doi.org/10.1007/BF00302022.

Porter, J. W., and O. W. Meier. 1992. Quantification of loss and change in Floridian 

reef coral populations. American Zoologist, 32:625–640.

Price, I. R. 1992. Seaweed phenology in a tropical Australian locality (Townsville, 

North Queensland). Botanica Marina, 32:399–406.

Robertson, D. R. 1990. Differences in the seasonalities of spawning and recruitment 

of some small neotropical reef fishes. Journal of Experimental Marine Biology, 144:49–62. http://dx.doi.org/10.1016/0022-0981(90)90019-9.

Sebens, K. P. 1994. Biodiversity of coral reefs: What are we losing and why? American Zoologist, 34:115–133.

Shulman, M. J., and D. R. Robertson. 1996. Changes in the coral reefs of the San 

Blas, Caribbean Panama: 1983–1990. Coral Reefs, 15:231–236.

Smith, C. M., and L. J. Walters. 1999. Fragmentation as a strategy for Caulerpa

species: Fates of fragments and implications for management of an invasive 

weed. Marine Ecology-Pubblicazioni della Stazione Zoologica di Napoli,

30:307–319. http://dx.doi.org/10.1046/j.1439-0485.1999.2034079.x.

Smith , J. E., M. Shaw, R. A. Edwards, D. Obura, O. Pantos, E. Sala, S. A. Sandin, S. Smriga, M. Hatay, and F. L. Rohwer. 2006. Indirect effects of algae 

on coral: Algae-mediated, microbe-induced coral mortality. Ecology Letters,

9:835–845. http://dx.doi.org/10.1111/j.1461-0248.2006.00937.x.
228 • smithsonian contributions to the marine sciences

Stachowicz, J. J., and M. E. Hay. 1996. Facultative mutualism between an herbivorous crab and a coralline alga: Advantages of eating noxious seaweeds. 

Oecologia, 105:377–387. http://dx.doi.org/10.1007/BF00328741.

Stoner, A. W. 1985. Penicillus capitatus: An algal island for macrocrustaceans. Marine Ecology Progress Series, 26:279–287. http://dx.doi.org/10.3354/meps

026279.

Szmant, A. M. 2002. Nutrient enrichment on coral reefs: Is it a major cause of coral 

decline? Estuaries, 25:743–766. http://dx.doi.org/10.1007/BF02804903.

Tanner, J. E. 1995. Competition between scleractinian corals and macroalgae: 

An experimental investigation of coral growth, survival, and reproduction. 

Journal of Experimental Marine Biology, 190:151–168. http://dx.doi.org/10

.1016/0022-0981(95)00027-O.

Togashi, T., T. Motomura, and T. Ichimura. 1998. Gamete dimorphism in Bryopsis 

plumosa: phototaxis, gamete motility and pheromonal attraction. Botanica 

Marina, 41:257–264.

Van Tussenbroek, B. I., M. G. B. Santos, and J. K. van Dijk. 2005. Unusual synchronous spawning by green algae (Bryopsidales), after the passage of Hurricane 

Wilma. Botanica Marina, 49:270–271.

Van Tussenbroek, B. I., and J. K. van Dijk. 2007. Spatial and temporal variability 

in biomass and production of psammophytic Halimeda incrassata (Bryopsidales, Chlorophyta) in a Caribbean reef lagoon. Journal of Phycology, 43:69–

77. http://dx.doi.org/10.1111/j.1529-8817.2006.00307.x.

Vroom, P. S., C. M. Smith, J. A. Coyer, L. J. Walters, C. L. Hunter, K. S. Beach, 

and J. E. Smith. 2003. Field biology of Halimeda tuna (Bryopsidales, Chlorophyta) across a depth gradient: Comparative growth, survivorship, recruitment, and reproduction. Hydrobiologica, 501:149–166. http://dx.doi

.org/10.1023/A:1026287816324.

Vroom, P. S., C. M. Smith, and S. C. Keeley. 1998. Cladistics of the Bryopsidales: a 

preliminary analysis. Journal of Phycology, 34:351–360.

Walters, L. J., and C. M. Smith. 1994. Rapid rhizoid production in Halimeda discoidea Decaisne (Chlorophyta) Fragments: A mechanism for survival after separation from adult thalli. Journal of Experimental Marine Biology, 175:105–

120. http://dx.doi.org/10.1016/0022-0981(94)90178-3.

Walters, L. J., C. M. Smith, J. A. Coyer, C. L. Hunter, K. S. Beach, P. S. Vroom. 2002. 

Asexual propagation in the coral reef macroalga Halimeda (Chlorophyta, 

Bryopsidales): Production, dispersal and attachment of small fragments. Journal of Experimental Marine Biology, 278:47–65. http://dx.doi.org/10.1016

/S0022-0981(02)00335-0.

Wefer, G. 1980. Carbonate production by algae Halimeda, Penicillus and Padina. 

Nature, 285:323–324. http://dx.doi.org/10.1038/285323a0.

Williams, S. L., and D. I. Walker. 1999. Mesoherbivore-macroalgal interactions: 

Feeding ecology of sacoglossan seaslugs and their effects on their food algae. 

Oceanography and Marine Biology: An Annual Review, 37:87–128.
Fine-Scale Interspecific Interactions

on Coral Reefs: Functional Roles 

of Small and Cryptic Metazoans

Peter W. Glynn

ABSTRACT. Direct underwater observations and experiments aided by scuba technology have greatly advanced the science of coral reef ecology. Coral community species 

interactions of small (macrofauna) and cryptic metazoans can exercise pivotal roles in the 

vitality, protection, and perpetuation of reef-building corals. Advances in the understanding of mechanisms underlying coral–metazoan symbiotic and facilitative interactions are 

examined in six invertebrate phyla (Porifera, Cnidaria, Acoelomorpha, Annelida, Mollusca, and Arthropoda) and in fishes, the latter with emphasis on cryptic coral reef fishes 

in the eastern Pacific. Crustacean associates of zooxanthellate corals, especially those 

inhabiting corals with branching morphologies, are notably diverse and can exhibit complex behaviors that greatly benefit their hosts. Several recently proposed positive effects 

of coral associates are reviewed, including evidence for increased colony stabilization, 

asexual fragmentation, interbranch circulation, cleansing of coral surfaces, mineral nutrient regeneration, reduction in the settlement of fouling organisms, and the removal of 

algal overgrowth. In several instances, the shared positive effects resulting from symbiotic 

interactions suggest that formerly regarded relationships of commensalism and parasitism are best viewed as mutualisms. The presence of a diverse and abundant cryptic fauna 

in coral communities suggests important roles in predation, selective recruitment effects, 

scavenging, and nutrient regeneration processes. 

INTRODUCTION

Fine-scale studies of interspecific interactions on coral reefs have demonstrated important roles of small and often inconspicuous invertebrate and fish metazoans. Notable 

advances have been made recently in our understanding of various trophic relationships in 

this often-neglected area. This paper offers a brief overview of biotic interactions of selected 

coral reef metazoans with emphasis on trophic relationships involving small, generally unseen or cryptic fauna. Coral symbioses (beyond the well-known microscopic, symbiotic 

zooxanthellae), reef scavengers, and cryptic fish carnivores are the chief areas addressed 

because of my personal involvement with research on these topics. Consequently, other 

groups of organisms such as herbivores, suspension feeders, deposit feeders, and parasites, 

while of paramount importance to the trophodynamics of reef ecosystems, are considered 

here only peripherally. This treatment considers mainly field-based observations via scuba

diving, a principal method for observation, collection, and experimentation; however, 

Peter W. Glynn, Division of Marine Biology and 

Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 

Rickenbacker Causeway, Miami, Florida 33149, 

USA. Correspondence: pglynn@rsmas.miami

.edu.

Manuscript received 25 January 2012; accepted 5 March 2013.
230 • smithsonian contributions to the marine sciences

relevant laboratory studies are referenced where they shed light 

on particular processes and relationships.

Coral–metazoan symbioses were generally considered to 

be interesting and novel when first reported, but with little if 

any ecological importance. Field studies conducted during the 

past few decades, however, have revealed several pivotal roles of 

coral–metazoan associations that can affect the survivorship of 

both symbionts and hosts and even influence coral community 

structure, reef growth, and recovery from disturbances. 

Several excellent reviews are available on the animal associates of living corals (e.g., Garth, 1964; Patton, 1974, 1976, 1994; 

Bruce, 1976, 1998; Castro, 1976, 1988), however many new 

symbiotic relationships and functions have been described over 

the past two decades. This is due in large measure to a renewed 

interest in biodiversity and the development of new methodologies. To illustrate the breadth and depth of coral–metazoan interactions, examples are selected from documented studies in six 

invertebrate phyla (Porifera, Cnidaria, Acoelomorpha, Annelida, 

Mollusca, and Arthropoda) as well as fishes. Due to the great 

variety of coral–crustacean symbioses, relationships among the 

Cnidaria and Arthropoda are highlighted. 

In addition to the many invertebrates associated with living corals, an abundant and diverse community of sessile and 

vagile metazoans is known to take refuge in dead coral crypts, 

including suspension feeders, necrophagous or scavenging species, carnivorous predators, and grazers (e.g., Jackson and Winston, 1982; Choi and Ginsburg, 1983; Gischler and Ginsburg, 

1996; Wunsch et al., 2000). In most studies there has been a bias 

toward describing sessile taxa due in large measure to their ease 

of collection and quantification. Here I consider predominantly 

ecological interactions of motile cryptic fauna. Assemblages of 

cryptic scavengers from the eastern Pacific are compared with 

those reported from Lizard Island, Great Barrier Reef, Australia. 

Finally, the diets of cryptic reef fishes from 20 families in Colombia and Panama are considered. The data collectively indicate the 

prevalence of predation in cryptic coral reef habitats.

TERMINOLOGY AND PERSPECTIVE

Emphasis in this essay is on the macrofauna (i.e., small invertebrates and fishes in the size range of 1–40 mm body length). 

This group also includes mesograzers and mesoherbivores, herbivorous taxa that are not microscopic but not easily seen when 

undisturbed (Hay et al., 1987; Carpenter, 1997). Occasionally 

reference is made to some taxa (e.g., ostracods, mysids, and isopods) that belong to the microfauna, with body length <1 mm. 

Moreover, some species examined exceed the size limits of the 

macrofauna (e.g., cryptic sponges, bryozoans, and tunicates in 

large cavities that can attain maximum body length in excess 

of 10–20 cm). Also, small postsettlement and juvenile stages of 

species that shelter in reefs are only temporary members of the 

macrofauna, attaining larger size as they grow, mature, and leave 

the confines of reef frameworks. 

Most members of the macrofauna occupy cryptic habitats 

and remain hidden in reef structures that range from intra- to 

interskeletal cavities, borings, and interparticle spaces. The complexity of cryptic habitats in terms of physical conditions and 

biotic composition is highlighted in Ginsburg (1983) and Kobluk 

(1988). While many coelobites (i.e., cryptofauna or cryptic biota) 

remain permanently hidden (e.g., various intraskeletal and benthic species), large numbers also are transient and emerge from 

reefs daily (reef plankton), seasonally, or during development as 

they mature (e.g., mollusks, crustaceans, and fishes). 

Some cautionary remarks are necessary regarding the classification of feeding modes. Clear distinctions between predators, 

scavengers, and parasites are often difficult to determine. Many 

consumer species are opportunists, assuming the role of predators or scavengers depending on the availability, variety, and 

condition of prey. For example, some omnivorous polychaete 

worms will pursue, attack, and consume preferred live prey when 

abundant, but will also resort to feeding on moribund and dead 

animals if their usual prey is in short supply. These feeding modes 

can also change depending on the developmental stage of the 

consumer. Other groups of metazoans exhibit feeding behaviors 

that may be considered to belong to two or more different feeding modes. For example, mesopredators that live in intimate association with coral colonies (e.g., flatworms, prosobranch and 

nudibranch gastropods, copepods, barnacles, crabs, shrimps, and 

gobies) typically consume small amounts of tissue and/or secretory products, causing only partial mortality, and therefore they 

may also be classified as parasites (Castro, 1988; Glynn, 1988). 

They also may be considered omnivores or even deposit feeders if they feed primarily on mucus or other byproducts of their 

coral hosts. Additionally, scavengers and detritivores that feed on 

dead and decaying plant and animal remains differ primarily in 

the relative size and state of degradation (microbial decay) of the 

organic matter ingested, which can vary widely depending on the 

size of the consumers.

Much debate surrounds the definition of symbiosis. Some 

researchers restrict the term to mutualisms (i.e., mutually beneficial relationships resulting from intimate heterospecific associations). Others have applied more restrictive criteria (e.g., 

requiring the demonstration of some degree of metabolic dependency [see Castro, 1988] or dismissing relationships in which a 

host responds to an organism’s presence by forming a kind of 

physical barrier [Pantos and Bythell, 2010]). In this essay Anton 

de Bary’s (1879) broad definition of symbiosis is employed, 

slightly modified as follows: an intimate and prolonged association between two or more organisms in which at least one partner obtains some benefit from the relationship. This definition 

avoids the categorization of relationships and preconceptions 

about outcomes (Saffo, 1993). 

Not all cryptic metazoans are engaged in symbiotic interactions, but they may still benefit from the presence of associated 

species. Positive or facilitative interactions involve encounters 

that are beneficial to at least one of the participants and harmful to neither (Bruno et al., 2003). Facilitation is best regarded 
number 39 • 231

as all encompassing; it can bring about positive effects under 

many guises. Various types of symbioses can have positive effects, and even predation and parasitism can result in indirect 

positive effects. For example, several metazoan symbionts of corals that were formerly regarded as harmful or neutral to their 

hosts are now known to provide various benefits (e.g., defense 

against predators, tissue irrigation, protection from fouling organisms, and nutrient enrichment). Many of the coral–metazoan 

associations considered below that are beneficial to at least one 

member can best be considered under the rubric of facilitation. 

The challenge is to rigorously quantify such positive interactions 

so that they can be related to individual fitness, species population dynamics, and community-scale composition and diversity.

REEF MACROFAUNA: 

CASE STUDIES AND INTERACTIONS

Porifera

Coral–sponge interactions are often perceived to be detrimental to corals because of the destructive effects of bioerosion as well as the competitive dominance and overgrowth of 

corals by sponges. At least two mutually beneficial interactions 

have been reported, however. These were observed by Goreau 

and Hartman (1966), who showed that the demosponge Mycale laevis, which is often present on the undersurfaces of plating Montastraea annularis corals, may provide a benefit to the 

partnership. Sponge and coral growth are in balance, with neither overgrowing the other. The peripheral skeletal folds of the 

coral grow around the oscules of the expanding sponge. Potential competitors of sponges (i.e., fouling organisms) and boring 

organisms capable of penetrating coral skeletons are absent from 

those parts of the colony overgrown by the sponge. Additionally, 

the coral may benefit nutritionally from an enhanced feeding efficiency caused by the sponge’s effluent currents. The sponge in 

turn occupies increasing substrate space as the coral grows.

Even excavating sponges, despite their bioerosive effects, 

may not have a negative influence in all situations. Highsmith 

(1982) noted several studies in which boring sponges were 

shown to promote asexual fragmentation in corals. The carbonate skeletons of most coral species are susceptible to erosion by 

clionaid sponges; both branching and massive coral colonies 

have been shown to shed live fragments that contribute to lateral reef expansion. This has been reported in the Caribbean for 

Acropora spp. and Porites furcata (branching taxa ) and Montastraea annularis (a massive taxon), and in the eastern Pacific for 

Pocillopora damicornis (branching) and Pavona clavus (massive). 

The shedding, survival, and dispersal of fragments following disturbance events can aid in the rapid recovery of coral cover.

Several sponge species contribute to the stabilization of reef 

framework structures (Wulff and Buss, 1979; Rützler, 2004; 

Wulff, 2006). Both epibenthic and cryptic sponges temporarily stabilize coral rubble as they attach to and bind loose coral 

fragments. Field experiments have demonstrated that sponge 

fragments can consolidate coral rubble quickly, within a 10-

month period (Wulff, 1984). Small corals that had originated 

from asexual fragmentation (or sexual recruitment) were dependent on sponge binding. Sponge-mediated substrate stabilization provides an opportunity for the successful settlement and 

survival of corals, bryozoans, vermetid mollusks, and serpulid 

worms. Another result of the sponge-mediated stabilization was 

an increase in topographic relief, which was twice that of experimental rubble piles without sponges. Encrusting coralline algae 

contributed importantly in later stages of the consolidation cycle.

Some quantitative measures of the contribution of cryptic sponge filter feeders to ecosystem-scale trophodynamics 

have been reported for a fringing Red Sea reef by Richter et al. 

(2001). By means of endoscopic exploration, these researchers 

determined that the surface area of reef cavities greatly exceeded 

that of reef surfaces by factors of 2.5–7.4 m2

. Sponge cover predominated in cavities, amounting to 60% of all coelobites, and 

exceeded surface filter feeder biomass by twofold. This study 

concluded that the consumption and mineralization of allochthonous organic matter by cryptic sponges is a principal source 

of nutrients that support endosymbiotic algal and coral growth. 

The magnitude of this cycling could help explain how high coral 

reef productivity occurs in often nutrient-deficient waters.

Cnidaria

Cnidarians offer numerous resources to reef organisms, 

and this is reflected in the great variety of taxa associated with 

zooxanthellate corals, from bacteria and fungi (Rohwer et al., 

2002; Knowlton and Rohwer, 2003) to invertebrates and fishes 

(e.g., Patton, 1976; Castro, 1988; Cole et al., 2008; Glynn and 

Enochs, 2011). Reef-building or zooxanthellate corals (i.e., those 

harboring endosymbiotic photobionts [Symbiodinium]) provide 

shelter and protection (cnidocytes) from predators, and trophic 

resources (mucus, tissues, lipids, zooxanthellae) for their metazoan residents.

Perhaps the most celebrated corals offering shelter and trophic resources to diverse metazoan symbionts are several species in the scleractinian families Acroporidae and Pocilloporidae. 

Their tissues, secretory products, and endosymbiotic algae provide a rich source of nutrition for numerous crustacean associates, many of which are obligate symbionts of specific coral host 

taxa. No fewer than four trophic pathways were identified by 

Rinkevich et al. (1991) for a pocilloporid species (Stylophora pistillata) in the Red Sea (Figure 1). At the base of this food web are 

the microbial community and particulate organic detritus plus 

minute plankton organisms embedded in the coral host’s mucus. 

This organic matrix is consumed by obligate Trapezia crabs and 

other coral symbionts, as well as various facultative and freeliving grazing metazoans. Metabolic byproducts (nutrients) of 

the coral host are utilized by zooxanthellae, which in turn supply corals with photosynthates. Although early investigators surmised that crustacean symbionts fed primarily on coral mucus, 
232 • smithsonian contributions to the marine sciences

Rinkevich et al. (1991) demonstrated conclusively—by employing 

C-14 isotopic labeling—that Trapezia grazes directly on coral host 

tissues. An additional trophic pathway involves predation of crustacean and other symbiont associates by free-living invertebrates

and fishes. Finally, the larvae released by host corals and metazoan 

symbionts into the water column are consumed by planktivores.

Not only are zooxanthellate corals essential for building reef 

frameworks, but they also provide a limestone substrate that is 

actively eroded and occupied by numerous excavating taxa such 

as fungi, microfilamentous algae, sponges, annelid worms, bivalve mollusks, crustaceans, and fishes (Hutchings, 1986; Glynn, 

1996; Perry and Hepburn, 2008; Tribollet and Golubic, 2011). 

Early studies have described the symbiotic relationship between 

endolithic bivalve mollusks and fungiid corals, and how embedded mytilid bivalves engulf various items (e.g., phytoplankton, 

mucus, and extruded zooxanthellae) from the coral host’s coelenteron (Goreau et al., 1970). In a classic study, Goreau and Yonge 

(1968) described the unique relationship between a free-living

dendrophyliid coral (Heteropsammia) and a sipunculid worm 

(Aspidosiphon). The coral host provides a refuge for the sipunculid, which pulls the coral along the muddy-sandy bottom. This 

enhanced mobility increases the feeding efficiency of the coral, 

Trapezia

Stylophora

Zooxanthellae

Planula Predation

Larvae

Predation Predation Predation

Predation

Predation

Zooea

Larvae

Other

Symbionts

Mucus &

Bacteria

Mucus

DOM

POM

Grazing

Predation

Photosynthates

MetabolicNutrients

Trapped Organic

Matter Trapped Organic

Matter

?

Mucus

Collection

FIGURE 1. Multiple trophic pathways in a coral/microbial/zooxanthella/crab symbiosis (modified from Rinkevich et al., 1991).
number 39 • 233

which sweeps its tentacles across the mud surface. The sipunculid 

in turn probes subsurface sediments while feeding—neither partner in competition with the other. 

A diverse suite of nonexcavating organisms also finds refuge in available cavities. This community of hidden organisms, 

including those that occupy interskeletal spaces, is referred to as 

the opportunistic cryptobiota or nestling fauna. Several researchers maintain that the cryptobiota may exceed in diversity and 

biomass the visible surface biota (Ginsburg, 1983; Reaka-Kudla,

1997; Richter et al., 2001). 

Acoelomorpha

Another complex symbiotic association, involving corals, 

epizoic acoel worms, and algal symbionts, is being actively investigated in the northern Red Sea (Barneah et al., 2007). Waminoa brickneri, possibly one of a multispecies complex, has been 

found on the surface tissues of 13 zooxanthellate scleractinian 

coral species at Eilat. The acoel worms generally demonstrate a 

low infestation rate (<5%); however, notably high abundances 

have been observed on some coral hosts. Both Waminoa and 

the coral hosts contain endosymbiotic dinoflagellates. Symbiodinium sp. and ?Amphidinium sp. were present in the worm, as 

was Symbiodinium sp. in the corals. Molecular genetic evidence 

and histological examination indicated that the two genera of 

dinoflagellates in the acoel worm are unique and therefore not 

present in the coral host. The symbionts are independently and 

vertically transmitted by the worm via oocytes during gametogenesis. This is the first evidence of maternal transmission of dinoflagellates in a triploblastic organism. These worms probably 

consume coral mucus and may have a negative impact on their 

host coral’s photophysiology when present in large numbers. 

Annelida

To date, the amphinomid polychaete Hermodice carunculata is the only annelid species known to prey consistently on 

coral tissues (Fauchald and Jumars, 1979). This worm is widely 

distributed on western Atlantic reefs, where it typically preys on 

branching corals within the genera Acropora and Porites. Its preference for these corals is of increasing concern due to population 

declines of acroporids following hurricane disturbances (Knowlton et al., 1990) and disease outbreaks (Williams and Miller, 

2005). In the eastern Mediterranean Sea, H. carunculata preys 

on Oculina patagonica and in the process inadvertently infects 

its prey with Vibrio shiloi, a causative agent of coral bleaching 

(Sussman et al., 2003). It is not presently known if H. carunculata can infect acroporid prey in the tropical western Atlantic.

Pherecardia striata, an eastern Pacific amphinomid, is an aggressive reef predator/scavenger and vigorously attacks wounded 

or moribund Acanthaster planci sea stars (Glynn, 1982). Acanthaster that are wounded by harlequin shrimp (see below) or fish 

predators attract the worms, which enter the sea star’s body cavity and consume soft organs such as hepatic caeca and gonads. 

Pherecardia are cryptic and patchily distributed within pocilloporid reef frameworks; where present, they can attain median 

population densities of 90–380 individuals m−2 (Glynn, 1984).

A sessile polychaete worm that constructs and occupies 

calcareous tubes embedded in massive corals has been shown 

to promote polyp survival following damage from corallivores 

and bleaching. The polychaete in question has been tentatively 

identified as Spirobranchus giganteus, a member of a possibly 

10–12 species complex (Fiege and ten Hove, 1999). Many but 

not all individuals were observed to defend their coral hosts 

(Porites spp.) on the central Great Barrier Reef by thrusting their 

hook-adorned operculum at the tube feet and arms of attacking Acanthaster. This reaction interrupted the sea star’s feeding 

response, resulting in localized polyp survivorship. Surviving polyps contributed to the regeneration of large, old colonies that 

experienced tissue mortality on surfaces lacking defending worm 

symbionts (DeVantier et al., 1986).

Ben-Tzvi et al. (2006) have suggested that Spirobranchus 

giganteus worms living embedded in corals may also benefit 

their hosts during bleaching events. They found that coral tissues 

immediately surrounding the serpulids showed no damage and 

quickly recovered after bleaching events. This led these researchers to hypothesize that sessile tube worms positively influence 

their immediate surroundings by causing (1) improved water 

circulation, (2) more efficient dispersal of waste products, and 

(3) increased availability of nutrients. Additional evidence that 

nutrients from spionid polychaete worms may be involved in 

coral tissue regeneration was offered by Wielgus and Levy (2006) 

in a study at Eilat in the northern Red Sea. Via the application 

of an active fluorescence technique over infested and noninfested 

coral colony surfaces, these researchers observed marked differences in holobiont primary production. Photosynthetic activity 

and coral tissue proliferation were greatest at worm-infested 

sites, leading to the conclusion that spionid waste products contribute to localized eutrophication. Also, the experimental coral, 

Astreopora myriophthalma, showed knobby growth aberrations 

at the sites of infestation. They concluded that this was due to an 

increased nitrogen/carbon ratio near the worms that resulted in 

greater tissue proliferation compared with calcification.

Mollusca

Most studies examining the effects of mollusks on zooxanthellate corals highlight their negative influences. Noteworthy 

are the several species of gastropods that graze on coral tissues 

(Robertson, 1970; Hadfield, 1976; Schuhmacher, 1992; Rotjan 

and Lewis, 2008) and bivalves that bore into coral skeletons 

(Kleemann, 1980; Valentich-Scott and Tongkerd, 2008). Obligate gastropod corallivores—for example Drupella spp. in the 

western Pacific and Indian Oceans, Jenneria pustulata in the 

eastern Pacific, and Coralliophila spp. in the Caribbean—have 

caused significant mortality on some reefs. Additionally, Phestilla lugubris (=sibogae), an aeolid nudibranch, lives its entire life 

and feeds extensively on Porites compressa colonies in Hawaii 
234 • smithsonian contributions to the marine sciences

caused significant mortality on some reefs. Additionally, Phestilla lugubris (=sibogae), an aeolid nudibranch, lives its entire life 

and feeds extensively on Porites compressa colonies in Hawaii 

(Hadfield, 1976). It is highly secretive, which helps it to avoid 

potentially intense fish predation. Remarkably, Haramaty (1991) 

presented indirect evidence that P. lugubris may utilize the photosynthetic products of endosymbiotic zooxanthellae that are 

ingested (and remain viable) along with coral tissues.

Like the corallivorous polychaete noted above (Hermodice 

carunculata), Coralliophila abbreviata was observed to concentrate on remnant corals (Acropora spp.) that survived a severe 

hurricane disturbance (Knowlton et al., 1981, 1990). Field experiments in the Florida Keys have demonstrated that C. abbreviata can transmit a coral disease (tentatively termed “rapid tissue 

loss”) to acroporid corals (Williams and Miller, 2005). Thus, 

acroporid corals that have experienced recent population declines 

due to stress and disturbance events may be subject to additional 

mortality from increased predation and disease outbreaks. 

Epizoic vermetid gastropods have been shown generally to 

reduce coral growth and survival (Colgan, 1985; Shima et al., 

2010). Porites lobata colonies at Moorea, French Polynesia, 

suffered both reduced growth (up to 82%) and survival (up to 

52%) from the smothering effect of the mucus feeding net of 

Dendropoma maxima. This vermetid also has a marked effect 

on the morphology of massive and branching corals, transforming both growth forms to flat-surfaced colonies (Zvuloni et al.,

2008). Trapezia crab symbionts, however, have been observed to 

mitigate the negative effects of vermetids on coral growth (Figure 2; Stier et al., 2010). This is accomplished by Trapezia’s consumption of vermetid mucus, as well as by its both inadvertent 

and directed dislodging of mucus.

Positive effects of bivalve mollusks on corals range from increased asexual reproduction to coral host defense and nutrient 

enrichment. Bivalve borers promote skeletal breakage and disintegration, which can enhance the asexual propagation of corals 

and also provide microhabitats for cryptic metazoans. Similar to 

Spirobranchus giganteus, the polychaete worm noted earlier, the 

scallop Pedum spondyloideum was observed to defend Porites 

spp. colonies on the Great Barrier Reef (DeVantier and Endean, 

1988). This scallop lives embedded in the skeletons of Porites 

spp. and often prevents Acanthaster from feeding on nearby polyps by repeatedly expelling jets of water. Surviving polyps may 

then reproduce asexually and assist in colony recovery. Mokady 

et al. (1998) have questioned the parasitic role of boring bivalves 

in association with coral hosts. From field and laboratory studies 

in the northern Red Sea, they found that ammonium nitrogen 

recycled by Lithophaga simplex supplied a significant amount of 

this nutrient to zooxanthella symbionts in a massive coral (Astreopora). They concluded that this tripartite symbiosis may be 

best regarded as a mutualism.

Arthropoda

Crustaceans are the principal invertebrates present on living 

corals, with numerous species of copepods, barnacles, shrimps, 

and crabs represented. In terms of species richness and abundance, copepod associates of reef-building corals are noteworthy 

(Humes, 1985; Stock, 1988). Also, sessile pyrgomatine barnacles are common on eight major scleractinian and hydrocoral 

higher taxa (updated from Ross and Newman, 1973; Glynn and 

Enochs, 2011). At least 48 species of pontoniine shrimps in 16 

genera are obligate symbionts in several coral genera, especially 

in branching species of Acropora and pocilloporid species of Pocillopora, Stylophora, and Seriatopora (Bruce, 1998). These same 

branching coral taxa are also known to host numerous species 

of obligate trapeziid crab symbionts (Patton, 1966, 1974, 1976; 

Castro, 1988; Castro et al., 2004).

Copepods that belong to the species-rich Xarifiidae inhabit 

the gastrovascular cavity of corals and have been assumed to be 

obligate endoparasites. Up to nine copepod species have been 

found on individual colonies of Acropora, and a single colony 

of Pocillopora was found to host 668 individuals belonging to a 

single copepod species (Humes, 1994). A recent study by Cheng 

and Dai (2010) presented evidence suggesting that Xarifia fissilis 

associated with Pocillopora damicornis consumes zooxanthellae 

from its coral host. Furthermore, their study indicated that ingested algal cells remained photosynthetically active, and in an 

experimental starvation treatment copepod hosts supplied with 

light suffered significantly lower mortality than copepods maintained in the dark. This result suggests that photosynthetically 

0.0030

0.0025

0.0020

0.0015

0.0010

0.0005

0.0000

Coral Growth (gm d )

Vermetid

Absent Present

Trapezia

Absent Present

-1 FIGURE 2. Mean (±1 SE) effects of Dendropoma maximum, a vermetid gastropod, and Trapezia serenei on the growth of Pocillopora 

cf. verrucosa. In the presence of vermetids, Trapezia can prevent the 

negative influence of the gastropod’s mucus feeding net on its coral 

host’s growth (modified from Stier et al., 2010).
number 39 • 235

active algae in the gut may provide photosynthate to the copepod, at least over the short term. If zooxanthellae are still viable 

when voided, it is possible they could disperse to other corals, 

serve as an innoculum source for planular larvae, or assist in the 

repopulation of zooxanthellae in bleached corals. 

With respect to feeding interactions, barnacles interact in 

various ways with their coral hosts. While most are suspension 

feeders, a few barnacles consume coral tissues directly (Ross and 

Newman, 1995, 2000). For example, Pyrgoma monticulariae 

stimulates coral tissue growth into its aperture to facilitate feeding (Ross and Newman, 1969). Species of Lithotrya bore into 

dead coral skeletons and extend their cirri into the surrounding 

water when feeding. They probably play a more important role in 

bioerosion than in any nutritional exchange. Several researchers, 

however, have hypothesized a mutualistic relationship between 

barnacles and their scleractinian and hydrocoral hosts. From 

a study utilizing stable carbon isotopes, Achituv et al. (1997) 

found that several species of coral-inhabiting barnacles assimilate carbon from their coral hosts via coral tissues (presumably 

abraded) and zooxanthellae. Barnacle symbionts can also have a 

positive effect on coral holobionts. The phosphorus and nitrogen 

excreted by barnacles can be absorbed by endosymbiotic zooxanthellae (Cook et al., 1991; Achituv and Mizrahi, 1996). Finally, a provocative experiment testing the effects of filter-feeding 

pyrgomatine barnacles on their hydrocoral host suggested an 

antifouling role (Pasternak et al., 2001). Millepora hydrocorals 

without their barnacle symbionts (experimentally stripped) were 

subject to higher rates of fouling by algae and fungi compared 

to corals with their usual complement of barnacles. These results 

suggest that the filtering capacity of barnacles can offer corals 

protection from fouling by water-borne organisms.

Some hermit crabs—members of the crustacean order 

Anomura—are also known to live symbiotically with corals.

Species of Paguritta live in polychaete tubes present on corals 

(Schuhmacher, 1977) or in self-constructed boreholes in living

coral (Lewinsohn, 1978). Juveniles of Paguritta harmsi were reported to live within the tissue-containing corallites of the massive coral Astreopora (Patton and Robertson, 1980). Since the 

corallites of the host coral lack columellae, the hermit crab is 

able to extend its soft abdomen into the corallite for protection. The crab’s right cheliped is flat and covered with spines, 

thus serving as an operculum when the crab is disturbed and 

withdraws within the corallite. It was hypothesized that small 

hermit crab recruits likely remain in the corallites while the 

coral grows, keeping pace with the growth and thus producing 

an elongated pit. Paguritta spp. possess feathered antennae and 

depend entirely on a filtering mode of feeding. Species recognition is often difficult; at least six species are known in this genus 

(McLaughlin and Lemaitre, 1993).

Gall crabs, members of the order Brachyura, are also sedentary obligate crustacean symbionts of reef-building corals. These 

crabs were long thought to be suspension feeders until Kropp 

(1986) found that they feed on coral mucus and tissues. Evidence 

from a chlorophyll spectral analysis indicates that excreta from 

a gall crab species of Cryptochirus fertilizes the immediate surroundings and thus enhances endosymbiotic zooxanthella production (Simon-Blecher et al., 1996). 

A rich fauna of mobile trapeziid crabs and pontoniine 

shrimps occur as obligate associates on pocilloporid and acroporid corals. Branching coral hosts typically provide quality shelter 

and trophic resources for these crustacean taxa. Early studies 

suggested that crustaceans were the sole beneficiaries of this 

partnership, feeding on coral mucus plus entrapped particulate 

organic matter. Accordingly, these crab and shrimp crustaceans 

were classified as ectoparasites (Knudsen, 1967) or commensals 

(Patton, 1974). More recent studies have demonstrated that Trapezia spp. crabs actually consume coral tissues directly (Rinkevich et al., 1991) as well as “fat bodies” or lipid globules produced 

by the coral hosts (Stimpson, 1990). The crabs harvest this food 

source by inserting their pereopods into polyps. Movements of 

the pereopods stimulate fat body production, which occurs only 

when crab symbionts are present. 

There are now several lines of evidence showing that mobile 

crustaceans provide various levels of facilitation to their hosts. 

Demonstrated positive effects include protection from corallivores (e.g., Glynn, 1983a; Pratchett, 2001); improved water flow 

within interbranch spaces and the removal of foreign organisms 

and contaminants (Glynn, 1983b); and reduced sediment deposition and increased coral growth and survivorship (Stewart et al., 

2006). Crab and shrimp agonistic behaviors also help regulate 

the abundances of potential competitors by preventing the overexploitation of host resources. It is likely that strong and persistent selective forces have resulted in the evolution of aggressive 

behaviors that both reduce competition and limit mortality by 

corallivores.

In the remainder of this section, a few noteworthy obligate 

crab and shrimp interaction effects are considered first, followed 

by selected examples of free-living species that can directly or 

indirectly affect coral survival. Trapeziid crabs typically form 

heterosexual pairs and aggressively defend their coral hosts from 

conspecific individuals (Preston, 1973; Patton, 1974). This aggressive behavior is also directed toward other species that could 

potentially compete for resources or harm the coral host. Trapezia crabs and Alpheus shrimp, however, coexist in stable populations on Pocillopora corals, with both the crabs and shrimp 

defending their coral hosts against intruders of both species. 

Movement between colonies, usually at night, commonly 

occurs in Trapezia crabs (Castro, 1978). At such times, the migrating crabs are vulnerable to fish invertivores and quickly associate with a coral host. Vannini (1985) observed that a Trapezia

crab attempting to enter a coral colony must perform cheliped 

rubbing and body contact with a conspecific resident crab before being accepted (Figure 3A). These appeasement behaviors 

usually allow an alien crab to successfully establish residency in 

the colony. Alpheus shrimp must also perform similar behaviors 

with crabs (i.e., cheliped rubbing and body contact to gain access to a defended colony; Figure 3B). While other behaviors 

occur between resident and intruding (alien) shrimp, cheliped 
236 • smithsonian contributions to the marine sciences

rubbing and body contact are performed almost exclusively between shrimps and crabs and seldom between alpheid shrimps 

themselves. Vannini (1985) speculated that shrimp, the weaker 

of the two combatants, needed to adopt the “language” of the 

stronger crab aggressor. Since crabs tolerate shrimp more than 

their own conspecifics, Vannini further suggested that snapping 

shrimp could be exploited by resident crabs as a clarion warning 

of approaching intruders and predators (see below).

Behavioral interactions among obligate crab, shrimp, and 

gobiid fish symbionts of Pocillopora damicornis colonies have 

been shown to facilitate the coexistence and stability of symbiont 

assemblages (Lassig, 1977). Resident crab–fish interactions were 

generally nonagonistic. Gobies made contact with crabs in various positions and performed shivering movements (rapid flexion 

of the entire body and median fins, particularly the caudal fin) 

similar to those employed in courtship behavior (Figure 4A–C). 

However, nest sites on coral branches were vigorously defended 

by Paragobiodon spp. during the breeding season. There are two 

species of gobiid fishes present in Pocillopora; Paragobiodon lacunicola mostly occurs near the base of corals, where it overlaps 

spatially with Alpheus more than with the other goby species, P. 

echinocephalus. The appeasement signal system—shivering and 

antennal contact—exists between the shrimp and P. lacunicola, 

but not between the shrimp and P. echinocephalus (Figure 4D–E).

The first reported observations of trapeziid crabs defending 

their coral hosts from predator attack were by Pearson and Endean (1969) and Weber and Woodhead (1970). These researchers noted how the obligate crab associates of pocilloporid corals 

could repel attacking sea stars (Acanthaster planci) on southern Pacific reefs. Although I refer to the single taxon A. planci, 

four distinct species of Acanthaster, each with well-defined geographic distributions, are now recognized (Vogler et al., 2008). 

It is possible that these species have different feeding preferences 

and elicit different defensive responses. However, observations in 

the eastern Pacific have demonstrated a repertoire of relatively 

consistent crustacean defensive behaviors when compared with 

coral guards from other Indo-Pacific regions.

Five defensive activities of Trapezia ferruginea on eastern 

Pacific reefs in Panama have also been observed in Guam, American Samoa, and Oman (Glynn, 1976, 1980, 1983a, 1987). An 

approaching Acanthaster typically elicits a startle or meral display in which an alerted crab will move to the coral’s peripheral 

branches and flex its chelipeds widely (Figure 5A). If Acanthaster

attempts to mount the colony, Trapezia may then begin to push 

the sea star away, executing several thrusts per minute (Figure 

5B). If the pushing response is unsuccessful, the defensive behaviors often escalate to the following three patterns: (1) up–down 

jerking, (2) pinching and clipping of spines and tube feet, and 

(3) resisting retreat of Acanthaster (Figure 5C–E). In the last response, a defending crab will grip a pair of spines near the arm 

tip and temporarily prevent the sea star from fleeing. When the 

crab is maximally stretched it will suddenly release its grip, causing the sea star to lurch forward and then quickly retreat from 

the guarded coral.

If attacking sea stars are approaching corals from an upcurrent direction, chemical cues or danger signals (kairomones) 

move down-current and alert the crustacean guards, which 

quickly move to peripheral branches where they assume defensive postures. The first agonistic responses toward attacking 

Acanthaster are pronounced snapping by Alpheus and meral displays by Trapezia, both of which are directed toward the predator from the coral’s peripheral branches (Figure 6). Glynn (1980) 

demonstrated experimentally that some unknown factor diffuses 

from the sea star and arouses the crustaceans. It is possible that 

the high concentrations of saponins in Acanthaster, which function as surfactant repellents to predators, alert the crustacean 

guards, but experimental testing of this hypothesis is necessary 

(Birkeland and Lucas, 1990).

The most common agonistic response of Alpheus lottini was 

a loud snapping sound that culminated in a directed shock wave. 

B

A

1cm

FIGURE 3. Crustacean appeasement interactions preceding acceptance of a nonresident associate into a Pocillopora sp. colony. 

(A) Intruder female Trapezia ferruginea rubbing her right cheliped 

against left cheliped of resident male crab. (B) Intruder Alpheus lottini shrimp rubbing both chelipeds against resident T. ferruginea

(modified from Vannini, 1985).
number 39 • 237

This snapping increased in frequency as an Acanthaster attack 

escalated from approaching a coral to contact and finally mounting. The most extreme response involved the shrimp in rapid succession pinching spines and tube feet, grasping the terminal arm 

spines of Acanthaster, and snapping at the sea star while it was 

in contact with the coral (Figure 5F).

Field observations in Panama indicated that the defensive 

responses of crustacean guards were overwhelmingly directed 

toward Acanthaster and not at other corallivores such as sea 

urchins, hermit crabs, snails, and fishes (Glynn, 1983a). This 

specific, high level of defense against Acanthaster corresponds 

with the level of harm this corallivore could cause to the coral 

host (i.e., death of the entire colony). Culcita spp., sea star corallivores in the Indo-Pacific, commonly feed on small acroporid 

and pocilloporid branching corals. In Hawaii, only about 50% 

of small Pocillopora colonies harbored crustacean guards (Trapezia and Alpheus) compared with 100% of large colonies (Glynn 

and Krupp, 1986). When present in small colonies, the crustacean guards would engage in defensive behaviors when attacked 

by Culcita, but these were generally weak responses that seldom 

curtailed a sea star attack. Thus, unguarded juvenile corals were 

particularly vulnerable to predation by Culcita. 

Scuba-supported field and laboratory studies conducted 

throughout the Indo-Pacific region have demonstrated that 

A B

1cm

1cm

C

D E

FIGURE 4. Behavioral interactions among crab (Trapezia cymodoce), shrimp (Alpheus lottini), and gobiid fish (Paragobiodon echinocephalus) 

associates of the coral Pocillopora damicornis. (A–C) Various contact positions assumed by crab and fish (modified from Lassig, 1977). (D) Antennal and (E) body contact between shrimp and fish. 
238 • smithsonian contributions to the marine sciences

FIGURE 5. Commonly observed defensive responses of crab and shrimp guards toward Acanthaster threatening to mount and feed on their 

coral host. Trapezia ferruginea: (A) startle display, (B) pushing sea star, (C) grasping spines with up–down jerking, (D) clipping spines and tube 

feet, (E) resisting sea star’s retreat. Alpheus lottini: (F) snapping in contact and pinching sea star’s arm tip (from Glynn, 1983a).

d

l

1

d

l

2

d

l

3

d

l

4

d

l

5

d

l

6

0 5 10 15 20

Number of Defensive Responses

3

1 2

Legend d = dead

l = live

Trapezia bouts

Alpheus snaps

FIGURE 6. Defensive responses of Trapezia and Alpheus toward simulated attacks of dead (boiled) and live Acanthaster. 

The frequency of Alpheus snaps per bout is indicated by the 

length of each open horizontal bar; the total frequency of 

Trapezia bouts is indicated by the length of each occluded 

bar (see legend; from Glynn, 1980).
number 39 • 239

metazoan symbionts significantly affect the feeding preferences 

of Acanthaster. Field observations in the Gulf of Oman revealed 

distinct feeding preferences and avoidances of several coral genera (Figure 7). Coral genera in the family Acroporidae (Acropora, Montipora) were significantly preferred over several genera 

in other families (e.g., Astreopora, Goniopora, Porites, and Pocillopora). There was a close relationship between branching coral 

taxa and (1) the colonies avoided, (2) the species and numbers 

of crustacean guards per colony, and (3) the intensity of colony 

defense. For example, pocilloporid colonies hosting large and 

aggressive Trapezia cymodoce and Trapezia tigrina crab guards 

were seldom attacked by Acanthaster, but acroporid colonies 

with small and less aggressive Tetralia cavimana guards were frequently eaten by the sea star. Montipora spp. without crustacean 

guards were preferentially fed upon by Acanthaster. 

In order to quantify the efficacy of defense by symbiotic 

crabs, shrimps, gobies, and the entire symbiont assemblage, 

Pratchett (2001) related coral avoidance interactions of Acanthaster to combinations of symbiotic taxa in controlled feeding 

trials. Two coral species were tested: Acropora nasuta with Tetralia and Coralliocaris guards, and Pocillopora damicornis with 

Trapezia and Alpheus guards. Crab guards elicited the strongest 

Acanthaster avoidance interactions but were not significantly 

different from the avoidance of all symbionts present in the two 

coral species tested (Figure 8). The most pronounced avoidance 

response was to P. damicornis with the aggressive crab guard 

Trapezia cymodoce. The small and weak acroporid crab guard 

Tetralia fulva also performed defensive behaviors, but these were 

less effective compared with Trapezia. Acanthaster avoided Pocillopora colonies with the Alpheus guard alone, but not Acropora

colonies with Coralliocaris shrimp symbionts. Goby symbionts 

alone in both corals were not effective in thwarting Acanthaster

attacks.

The effects of Acanthaster predation on coral community 

structure is complex and depends on several factors, such as 

population size of attacking sea stars, absolute and relative abundances of preferred and nonpreferred coral prey, colony morphology, coral availability, past experience in prey choice, and 

symbiont defenses. In-depth reviews on this subject are offered 

by Moran (1986) and Birkeland and Lucas (1990). Observed effects have involved changes in species richness, diversity (both 

increases and decreases), coral cover (slight to near-total elimination), colony sizes, age distributions, and spatial patterns. Two 

examples of the last have involved symbiont-defended corals in 

Panama and Guam. Symbiont-defended corals in Panama were 

observed to form a protective barrier around preferred, nondefended corals (Glynn, 1985). In this situation, Acanthaster was 

prevented from crossing the barrier and thus denied access to 

a coral (Gardineroseris planulata) ranking high in preference. 

In Guam, Colgan (1987) observed a halo of uneaten corals surrounding a colony defended by crustacean guards.

In addition to defending corals from corallivores, trapeziid 

crabs promote the growth and survival of their host corals by 

increasing interbranch circulation and removing organisms and 

Ac

Ac

Ac

Al

Al

As

As

Gn

Gn

Mn

Mn

Mn Mn Pc

Pc

Pc

Pc

Pc

Pl

Pl

Pr

Pr

Pr

Pr

Pr

Pr St

St

*** ***

***

***

***

***

***

***

***

*** *

*

NS

NS

NS

NS

NS

NS

NS

1

1

2

3

.10

.10

.20

.20

.30

.30

.40

.40

.50

.50

.60

.60

.70

.70

.80

.80

.90

.90

1.00

1.00

Observed Frequency Eaten

Expected Frequency Eaten

Prey Taxa Acropora

Alcyonacea

Astreopora

Goniopora

Montipora

Pocillopora

Platygyra

Porites

Stylophora

AVOIDANCE

PREFERENCE

tests of signicance 2

NS

* ***

nonsignicant

p < 0.05

p < 0.001

FIGURE 7. Field-sampled coral prey preferred and avoided by Acanthaster in the Gulf of Oman. Chi-square significance values are noted 

beside prey genera eaten and compared to their relative abundances 

(from Glynn, 1987).

12

10

8

6

4

2

0

No infauna gobies shrimps crabs All infauna

Acropora nasuta

12

10

8

6

4

2

0

No infauna gobies shrimps crabs All infauna

Pocillopora damicornis

Avoidance (mean rank + SE) FIGURE 8. Avoidance interactions of Acanthaster experimentally 

presented with different metazoan symbiont assemblages apportioned between two potential coral species prey (modified from 

Pratchett, 2001). Acropora nasuta: crabs (Tetralia), shrimps (Coralliocaris, Periclimenes), and gobies (Gobiodon). Pocillopora damicornis: crabs (Trapezia), shrimps (Alpheus), and gobies (Paragobiodon).
240 • smithsonian contributions to the marine sciences

contaminants from coral surfaces (Glynn, 1983b). A recent study 

at Moorea quantified the positive effects of crab symbionts in 

clearing sediments from branching pocilloporid and acroporid 

corals (Stewart et al., 2006). In a 24-day field experiment, corals 

without Tetralia (Acropora hyacinthus) or Trapezia (Pocillopora

verrucosa) experienced ~50% and ~80% mortality, respectively. 

The crab symbionts were experimentally removed from test colonies. Crabs were observed to predominantly remove sediments of 

large particle size (0.5–4.0 mm), which were the most damaging 

to coral tissues. They responded quickly to increased sediment 

loads by removing sediments with their rear pereopods and chelae. The corals that survived without crabs showed significantly 

lower colony growth, increased tissue bleaching, and higher sediment loading. 

Facultative majid crabs living cryptically with branching 

Porites on a Caribbean reef have been shown experimentally to 

benefit their coral host indirectly (Coen, 1988). In treatments 

where Mithrax had access to coral colonies (i.e., crab enclosures 

and natural controls), foliose algae were significantly reduced 

compared to crab exclosure treatments (Figure 9) after about 

one month. The feeding activities of the herbivorous crabs were 

found to prevent algae from overgrowing and killing the corals. 

This study and others suggest that mesograzers, such as amphipods, isopods, and polychaete worms, may exercise strong control over algal abundance and community structure in some reef 

habitats (Brawley, 1992; Carpenter, 1997). 

Field observations on a coral reef in the Gulf of Chiriquí, 

Panama, have revealed an abundance of the painted shrimp, 

Hymenocera picta (Glynn, 1977, 1982). This shrimp lives 

cryptically in reef framework cavities and among the branches of 

both live scleractinians and hydrocorals (Figure 10), but is visible 

when attacking and feeding on adult Acanthaster and other sea 

stars. Population abundances, which were determined in part by 

sea star baiting, reached maximum density estimates of 54–118 

shrimp ha-1

. These shrimp attack asteroid echinoderms only, cutting through the body wall and amputating arm tips with their 

sharp chelae; exposed internal organs such as gonads and hepatic caeca are then consumed (Wickler, 1973). While feeding 

on Acanthaster, the shrimp (often a pair) are carried on the sea 

star’s aboral surface for up to several days as it moves about. 

Pherecardia striata, a cryptic polychaete worm, was often observed entering the wounded sea star’s coelom, where it also fed 

on soft tissues. From Acanthaster immigration and mortality 

rates, Glynn (1982) concluded that the shrimp and polychaete 

worm could control the population size of adult Acanthaster on 

the eastern Pacific study reef. Fiedler (2002) found that the postlarvae of Hymenocera begin eating sea stars only five days after 

metamorphosis. Therefore it is possible that postsettlement and 

juvenile Acanthaster are consumed in cryptic reef habitats before 

they mature and emerge onto exposed reef surfaces.

 Early observations with scuba prompted the pioneer marine ethologist Eibl-Eibesfeldt (1955) to propose that cleaner 

shrimps could benefit reef fishes by removing parasites. Whether 

or not cleaner shrimp can effectively remove ectoparasites from 

coral reef fishes has been vigorously debated (Spotte, 1998). Although this type of interaction is not considered here, convincing 

evidence that cleaner shrimp do remove crustacean (copepod, 

isopod) and monogenean flatworm parasites is presented in 

Bunkley-Williams and Williams (1998) and Becker and Grutter (2004). These new findings, aided by controlled laboratory 

procedures, support a mutualistic relationship between some 

shrimps and fishes.

FIGURE 9. Mean (±1 SE) cover of algae on Porites porites colonies 

in relation to the presence of Mithrax sculptus, a facultative majid 

crab associate. Pre- and posttreatment effects: clear bars indicate

crab enclosures; light gray bars indicate crab exclosures; dark gray 

bars indicate natural controls. The same letter is shared among treatments not significantly different (p > 0.05).

0

10

20

30

40

50

60

70

80

Treatments

Pre Post

Mean macroalgal cover (%)

A

A

a

a

a

B

FIGURE 10. Harlequin shrimp, Hymenocera picta, perched on a 

branch of the hydrocoral Millepora intricata, at Uva Island, Gulf of 

Chiriquí, Panama, 20 m depth. A second member of the pair is only 

partly visible. Photo courtesy of B. Harris.
number 39 • 241

It is apparent that trapeziid crab symbionts have received 

considerable attention from researchers, due mainly to their 

relatively large size, complex behaviors, and extraordinary capacity to defend their coral hosts against predators. The ecological roles of smaller taxa (e.g., copepods and smaller shrimps) 

are still largely unknown with regard to host effects (e.g., tissue 

consumption or protection from micropredators). Similarly, the 

potential importance of crustacean symbionts vis-à-vis predation 

on settling metazoan larvae, recruits, and residents, as well as 

transmission of zooxanthellae and coral diseases, are also research areas in need of further study. These are all vital ecological 

functions that can determine the persistence or demise of particular coral populations. 

Chordata

Relatively few fishes form close or obligate relationships 

with living corals. To illustrate fish–coral symbioses, examples 

are briefly noted from three families, namely Gobeidae (gobies), 

Cirrhitidae (hawkfishes), and Pomacentridae (damselfishes). 

These examples range from obligate to facultative associations 

with branching corals where shelter and food are assumed to 

be the chief resources sought. For additional information on the 

range of fish corallivore diets, see Cole et al. (2008). Since the 

majority of the 128 coral reef fishes (in 11 families) they list are 

relatively large and conspicuous, they fall outside the scope of 

this paper.

Several species in four gobiid genera are closely associated 

with live corals (Munday et al., 1997; Herler, 2007). Among obligate goby symbionts, Gobiodon spp. inhabit acroporid corals and 

Paragobiodon spp. reside in pocilloporid corals. Both coral families exhibit branching colony morphologies. Gut content analysis 

on the Great Barrier Reef has established that three species of 

Gobiodon consume the tissues of their acroporid hosts (Brooker 

et al., 2010). In addition, relatively large amounts of algae are 

consumed, which may benefit the host by preventing algal overgrowth and the fish symbionts by maintaining open living spaces.

Even though gobies alone are not effective in repelling 

Acanthaster (Pratchett, 2001), Lassig (1981) found that Gobiodon quinquestrigatus could effectively reduce predation by butterflyfishes. In field experiments with Acropora colonies with and 

without Gobiodon, Lassig found that the number of bites and 

time spent at colonies by feeding Chaetodon were significantly 

reduced when the goby was present. Gobiodon spp. produce an 

epidermal secretion that is ichthyotoxic and likely plays an important role in reducing the grazing of butterflyfishes. Due to 

the mobility of butterflyfishes feeding around a colony and likely 

rapid dilution of the toxic agent, the efficacy of such a deterrent might be questioned. An ichthyotoxin would be effective, 

however, if accurate delivery were possible. Lassig speculated 

that Gobiodon could be attracted to areas threatened by butterflyfishes and may abrade their epidermis against the coral in 

order to release the repellant at targeted feeding sites. This hypothesized defensive behavior is in need of further study.

Donaldson (1990) lists two species of hawkfishes that are 

obligate coral dwellers, and eight species that occupy either coral 

or other noncoral microhabitats. Paracirrhites arcatus is a facultative associate of Pocillopora meandrina in Hawaii, where it 

finds shelter among this coral’s branches and uses the coral as 

a foraging base (DeMartini, 1996). In Panama, Cirrhitichthys 

oxycephalus is a facultative associate of pocilloporid corals. It 

typically perches on coral branches, from which it locates and 

presumably preys on symbiotic and pelagic crustaceans as well 

as small fishes (Dominici-Arosemena and Wolff, 2006; Robertson and Allen, 2008).

Cole et al. (2008) listed eight species of pomacentrid corallivores; two of these feed exclusively on zooxanthellate corals. 

Some species of zooplanktivorous damselfishes (Dascyllus) seek 

refuge from piscivores in branching corals. The experimental removal of Dascyllus from Stylophora in the Red Sea resulted in 

significantly lowered coral growth compared to colonies hosting fish (Liberman et al., 1995). Similar results were obtained by 

Holbrook et al. (2008) for Dascyllus that shelter in Pocillopora

colonies at Moorea; sheltering damselfish enhanced coral growth 

by about 50% and up to nearly 100% when large groups of fish 

were present. Elevated coral growth was dependent on nutrients 

(ammonium) excreted by the fish. The magnitude of this effect 

was positively related to the biomass of fish resident on each 

coral. Another factor that could indirectly affect coral growth is 

the presence of predatory hawkfish, which can co-occur with and 

prey on Dascyllus in Pocillopora colonies. Hawkfish predation 

would result in a reduction of the number and biomass of Dascyllus, thus resulting in reduced coral growth. A final beneficial 

effect of note is the sleep-swimming behavior of pomacentrids 

(Dascyllus, Chromis) that are closely associated with pocilloporid and acroporid corals (Goldshmid et al., 2004). These fishes 

enhance water replenishment, and hence oxygen availability, in 

the inner branch zones of corals at night (Goldshmid et al., 2004). 

This sleeping behavior, which involves high-frequency fin motion 

even when the fish are at rest, is unique; non-coral-associated 

pomacentrids are motionless during their quiescent period.

When a disturbance disrupts a symbiosis, the proximate 

cause of the breakdown is not always obvious. In a few cases, 

however, the reason(s) for the disappearance of coral symbionts has been revealed. For example, during coral bleaching on 

Panamanian reefs, obligate crustacean symbionts starved and 

died due to the loss of their coral host and nutritional resources 

(Glynn et al., 1985). Coral bleaching in Australia has resulted 

in marked declines of damselfishes that inhabit Pocillopora corals. It has been shown experimentally that the predation rate of 

coral-dwelling damselfishes increased in degraded host colonies 

(Coker et al., 2009). Predation was highest on bleached and 

algal-covered corals. In bleached corals, this was likely a result 

of increased prey visibility against a bleached coral background; 

in algal-covered corals, it was possibly a result of changes in the 

behavior of prey fishes that would increase their susceptibility to 

predation, such as increased movement in search of live corals.
242 • smithsonian contributions to the marine sciences

The contribution of small cryptic fishes to reef assemblages 

and processes is largely unknown (Ackerman and Bellwood, 

2000). Although cryptic reef habitats are often noted to be important as refuges for postsettlement and juvenile life history 

stages of invertebrates and fishes, the presence of diverse cryptic 

predators is usually not acknowledged. A study focused on the 

trophic roles of a cryptobenthic fish community on the Great 

Barrier Reef revealed an abundant carnivore presence (Depczynski and Bellwood, 2003). Five of 16 of the most abundant 

species examined, representing 40.5% of all individuals, were 

carnivores. Detritivores made up a large portion of this cryptic assemblage as well (see below). In two eastern Pacific studies conducted on reefs in Colombia (Mora and Zapata, 2000) 

and Panama (Glynn, 2006), 37 fish species in 20 families were 

found inhabiting experimentally constructed dead coral rubble 

structures (Table 1). Thirty-three (~89%) of these cryptic species belong to carnivore or other consumer guilds (planktivores, 

parasites). The most common dietary items were crustaceans and 

fishes. The fishes sampled in Colombia recruited to cryptic substrates during a maximum time of just two months. This short 

period indicates the rapidity with which cryptic predators can 

invade and become established in newly formed shelters. Thus, 

cryptic fish predators are likely early colonizers in disturbed reef 

communities and effective in modulating recruitment dynamics 

(e.g., species composition and abundances). The presence of particular macropredators could limit the recruitment of species that 

would positively or negatively affect coral growth. 

MESOSCAVENGERS

The first quantitative study of small scavengers on a coral 

reef, carried out at Lizard Island on the Great Barrier Reef, revealed high abundances of crustacean and mollusk species (Keable, 1995). Traps baited with dead fish were deployed overnight 

for 18 hours in three reef zones and surrounding sedimentary 

substrata. From 410 baited traps, 108 crustacean, mollusk, and 

polychaete species were collected, yielding a total of 112,690 

individuals. Amphipod, isopod, and ostracod crustaceans were 

the most abundant taxa, with maximum capture numbers per 

trap reaching hundreds to thousands of individuals. The overall 

mean capture rate was 275 individuals per trap. The dominance 

of crustacean scavengers was evident in traps sampled in leeward 

reef slope and reef flat habitats (Figure 11).

Scavenger trap baiting on Panamanian coral reefs in the 

eastern Pacific revealed a diverse scavenger guild, but with lower 

abundances than those reported at Lizard Island. Since the trapping methodology in Panama was similar to that employed in 

Australia—small entrance aperture, fish baits, and overnight, 18-

hour deployment—a region-wide comparison is justified (Figure 12). Of the 55 traps set on a Panamanian coral reef, a total 

of 1,219 individuals were captured, with a mean capture rate 

of 22 individuals per trap. In addition to the shrimp and crab 

crustaceans, gastropods, and polychaete scavengers that were 

likewise captured in Australia, a few other invertebrate taxa 

were present in Panama, including holothurians, hermit crabs, 

and one individual each of a polyclad flatworm, bivalve mollusk, 

and muraenid eel (Figure 13). One small moray eel (Gymnothorax panamensis) also was observed to enter a trap and consume 

part of the bait. At both Australian and Panamanian study reefs, 

cirolanid isopods were in high abundance and often numerically 

dominant. Ostracod abundances and diversity were higher in 

Australia than in Panama. In traps with scavengers, commonly 

one-half to all of the ~8 cm3

–baits were consumed during the 18-

hour period. The rapidity of this consumption suggests a critical 

role of cryptic reef scavengers in nutrient regeneration processes, 

and possibly a paucity of food resources. 

In the Depczynski and Bellwood (2003) study noted above, 

detritivores were also well represented, especially small gobiid 

fishes. Ten of 16 species and 39.3% of individuals examined 

were assigned to the detritivore guild. Like cryptic invertebrate 

scavengers, cryptic fishes may also contribute importantly to the 

recycling of primary production through detrital pathways.

CONCLUSIONS

This overview has shown that several coral–metazoan interactions that were formerly regarded as neutral or harmful to 

corals are in many instances beneficial. With greater awareness 

of the critical roles played by small, cryptic reef metazoans, new 

insights and research directions have emerged. 

Sponges offer several key ecosystem services, including 

water column filtering, nutrient regeneration, binding and stabilization of reef substrates, and facilitation of coral community 

regeneration and recovery processes. Since sponges represent a 

vital component of coral communities, their abundances and 

diversity should be protected. Polychaete worm and gastropod 

mollusk corallivores can serve as vectors and promote the spread 

of coral diseases. It is also possible that copepod parasites of corals may assist in the transmission of distinct Symbiodinium types 

among potential coral hosts. This may increase the survival of 

certain coral species during bleaching stress events. Crustaceans 

have been highly successful in establishing a variety of facultative and obligate symbiotic associations with live corals. Of note 

are copepods, barnacles, shrimps, hermit crabs, gall crabs, and 

trapeziid crabs. In measures of species richness, abundances, and 

variety of interactions, crustaceans exceed all other metazoans. 

Diverse epizoic taxa and endolithic borers (e.g., sponges, 

polychaete annelids, bivalve mollusks, gall crabs, and barnacles) 

enhance nitrogen sources for use by coral holobionts. This can 

lead to localized eutrophication, increased primary production, 

and elevated coral growth. The activities of epizoic symbionts in 

thinning boundary layers and creating microturbulence can have 

several beneficial effects on massive and branching coral hosts. 

This function has been observed in suspension-feeding sponges,
number 39 • 243

TABLE 1. Juvenile and adult fishes occupying cryptic habitats on eastern Pacific coral reefs. Habitats: G, 0.5 m aggregate of dead 

pocilloporid rubble secured in netting and resting on bottom; M&Z, 0.4 m aggregate of dead pocilloporid rubble secured with line and 

positioned 0.2 m above sand bottom. Trophic roles: CAR, carnivore; PLK, planktivore; PAR, parasite; OMN, omnivore; CLN cleaner; 

HRB, herbivore.

Family Species Trophic role Dieta Habitatb

Muraenidae Anarchias galapagensis c CAR Crustacead, worms, gastropods/bivalves G

Gymnothorax panamensis CAR Crustacea, bony fishes G

Gymnothorax undulata CAR Crustacea, cephalopods, bony fishes G

Gymnothorax dovii e CAR Crustacea, cephalopods, bony fishes G

Muraena lentiginosa CAR Crustacea, bony fishes G

Carapidae Carapus mourlani CAR/PLK Benthic/planktonic crustacea f G

Encheliophis vermicularise PLK/PAR Plankton, echinoderms G

Bythitidae Ogilbia sp.c CAR Crustacea, bony fishes G

Grammonus sp.c CAR Crustacea, bony fishes G

Antennariidae Antennarius sanguineus CAR Crustacea, bony fishes G, M&Z

Antennarius coccineus CAR Crustacea, bony fishes G, M&Z

Antennatus strigatus CAR Crustacea, bony fishes G, M&Z

Scorpaenidae Scorpaena mystes CAR Crustacea, cephalopods, bony fishes G

Scorpaenodes xyrise CAR Crustacea, cephalopods, bony fishes G, M&Z

Scorpaenid sp.c CAR Crustacea, cephalopods, bony fishes G

Serranidae Serranus psittacinuse CAR Crustacea, cephalopods, bony fishes G, M&Z

Paranthias colonus CAR/PLK Pelagic crustacea, zooplankton, bony fishes M&Z

Alphestes immaculatus CAR Crustacea, bony fishes M&Z

Cephalopholis panamensis CAR Crustacea, cephalopods, bony fishes M&Z

Grammistidae Pseudogramma thaumasium CAR Crustacea, bony fishes G

Apogonidae Apogon dovii e PLK Zooplankton, pelagic fish eggs/larvae G, M&Z

Labrisomidae Starksia fulva c CAR Crustacea, worms G

Gobiidae Gobulus hancocki c CAR Benthic worms, crustacea, gastropods/bivalves G

Tetraodontidae Canthigaster punctatissimae OMN Benthic microalgae, sessile invertebrates G, M&Z

Gerreidae Eucinostomus gracilise CAR Benthic worms, crustacea, gastropods/bivalves M&Z

Blenniidae Plagiotremus azaleuse CAR/PAR Crustacea, bony fishes M&Z

Lutjanidae Lutjanus guttatus CAR Crustacea, bony fishes M&Z

Lutjanus viridis CAR Crustacea, cephalopods, bony fishes M&Z

Pomacanthidae Pomacanthus zonipectus CLN/OMN Microalgae, sessile invertebrates M&Z

Pomacentridae Stegastes flavilatus OMN Microalgae, crustacea, sessile worms/crustacea M&Z

Chromis atrilobata PLK Zooplankton, pelagic fish eggs M&Z

Cirrhitidae Cirrhitichthys oxycephalus CAR/PLK Benthic/pelagic crustacea, bony fishes M&Z

Labridae Halichoeres dispilus c CAR/PLK Crustacea, worms, gastropods/bivalves M&Z

Halichoeres nicholsi CAR/PLK Crustacea, worms, gastropods/bivalves, echinoderms M&Z

Thalassoma lucasanum CAR/PLK Crustacea, worms, gastropods/bivalves, echinoderms M&Z

Acanthuridae Acanthurus xanthopterus HRB Microalgae, detritus, soft corals/hydroids M&Z

Balistidae Sufflamen verres CAR Crustacea, worms, gastropods/bivalves, echinoderms M&Z

a After Robertson and Allen (2008) unless otherwise noted. The majority of the dietary items listed are probably mostly for adult fishes. Even though some juvenile carnivores emigrated to reef surface locations as they matured (e.g., serranids, lutjanids, and labrids), their membership in the feeding guilds noted probably remained the same.

b G, Glynn (2006); M&Z, Mora and Zapata (2000).

c Diet and trophic assignment inferred from family-level feeding habits.

d Crustacea noted under carnivore trophic guild are primarily benthic, and those under the planktivore guild are present in the water column. 

e Diet and trophic assignment inferred from genus-level feeding habits.

f

Glynn et al. (2008).
244 • smithsonian contributions to the marine sciences

Cypridinodes sp. A

Cirolana erodiae

Paradoloria spp.

Ichnopus capricornus

Various

Nassarius splendidulus

Nassarius albescens

Skogsbergia spp.

Siphonostra sp.

Reef Slope

Cirolana erodiae

Cypridinodes sp. A

Paradoloria spp.

Skogsbergia spp.

Various

Ichnopus capricornus

Reef Flat

FIGURE 11. Small invertebrate taxa and relative abundances captured in baited scavenger traps, Lizard Island, Australia (1989–1990). Right: 

Leeward reef flat; Left: Leeward reef slope (modified from Keable, 1995).

FIGURE 12. Invertebrate scavengers inside a trap being retrieved after overnight exposure on the Uva Island 

coral reef, Gulf of Chiriquí, Panama, 3 m depth. Arrows 1 and 2 respectively denote captured brachyuran 

crabs and amphinomid worms Pherecardia striata. The polychaete worms are ~1 cm wide. Photo courtesy 

of V. W. Brandtneris.
number 39 • 245

polychaete worms, bivalve mollusks, and barnacles. Mobile crustaceans (e.g., trapeziid crabs and alpheid shrimps) and symbiotic fishes such as gobies and certain pomacentrids also increase 

circulation in the interbranch spaces of corals. Positive effects 

include increased availability of nutrients, dissolved oxygen, and 

food and dispersal of waste products, including reactive oxygen 

species generated during stress events. Overgrowth by fouling 

organisms can also be restricted by filter-feeding barnacles and 

shrimps and crabs that scrape coral surfaces.

Metazoan symbionts of corals employ diverse mechanisms 

to defend their host colony from corallivores. A serpulid polychaete worm thrusts an armed operculum and a scallop directs 

jets of water at attacking Acanthaster. Xanthid crabs employ a 

variety of agonistic responses toward sea stars, including pinching, clipping spines and tube feet, and body thrusts and dislodgment of large corallivores. Alpheid pistol shrimps direct 

aggressive snapping and water jets toward attacking corallivores. 

Gobies limit the grazing of chaetodontids probably by releasing 

an ichthyotoxic repellant.

Care should be exercised in establishing the identity of coral 

reef organisms in light of widespread species-specific interdependencies. For example, molecular genetic studies of the morphospecies of Pocillopora damicornis in the western Indian Ocean 

has shown the existence of two distinct species (Souter, 2010), 

and eight morphospecies of Pocillopora in the far eastern Pacific 

may in fact represent only three species (Pinzón and LaJeunesse, 

2010). Other noted sibling species complexes are Acanthaster 

planci and Spirobranchus giganteus, representing four and 10–12 

species respectively. 

Sampling of cryptic reef scavengers in Australia and Panama suggests that this is a taxonomically diverse feeding group 

dominated by various crustacean orders, especially isopods. 

Mesoscavengers affect the rapid breakdown of reef carrion and 

particulate organic matter, driving nutrient recycling and coral 

reef primary production. Small, cryptic fish carnivores on eastern Pacific reefs (Panama and Colombia) were represented by 

37 species in 20 families, and consisted of adult resident and immature transient members. Crustaceans ranked high in the diets 

of these fishes, as did other invertebrate taxa (e.g., polychaete 

worms, gastropod and bivalve mollusks, and cephalopods) and 

fishes. This cryptic carnivore guild likely exerts heavy consumer 

pressure on other cryptic metazoans, including biota recruiting 

to reefs via planktonic larval stages. Coral reef frameworks and 

associated habitats providing shelter can no longer be perceived 

as predator-free refuges.

From the variety of newly described coral–metazoan symbioses and a clearer understanding of functional interrelationships, it is apparent that small cryptic animals play numerous 

and essential ecological roles in many host corals. Their effects, 

both positive and negative, need to be understood with regard 

to the nature of key ecosystem processes and their influence on 

the dynamics of populations in reef systems and the diversity 

FIGURE 13. Small scavenger taxa and relative abundances captured in 55 baited traps 

set in pocilloporid framework on the Uva Island coral reef, Gulf of Chiriquí, Panama, 

2–4 m depth.

Cirolana parva

Mysida Ostracoda

Polychaeta

Gastropoda

Polycladida

Bivalvia

Muraenidae

Brachyura

Paguroidea

Holothuria
246 • smithsonian contributions to the marine sciences

and structure of coral reef communities overall. The importance 

of understanding the various interactions and nuances involved 

in cryptic reef communities is critical in light of projected and 

unknown responses that are sure to accompany climate change 

impacts on coral reefs.

ACKNOWLEDGMENTS

I especially thank Michael A. Lang for the invitation to participate in this symposium highlighting research through the aid 

of scuba. Diane S. and Mark M. Littler are acknowledged for their 

help in editing this section on ecological interactions. Helpful suggestions for improving this paper were offered by V. W. Brandtneris, I. C. Enochs, T. C. LaJeunesse, and J. Serafy. Symposium 

attendance was supported by the Smithsonian Institution, National 

Research Council, and the National Science Foundation. Research 

support was provided by the U.S. National Science Foundation Biological Oceanography Program grant OCE-0526361 and earlier

awards. I am also grateful for support provided by the Ministry of 

Agriculture and Fisheries, Sultanate of Oman, Omani–American 

Joint Commission for Economic and Technical Cooperation; the 

Department of Marine and Wildlife Resources, American Samoa; 

the Smithsonian Tropical Research Institute and Scholarly Studies Program, Smithsonian Institution; and the Marine Laboratory, 

University of Guam, facilitated by C. Birkeland. 

REFERENCES

Achituv, Y., I. Brickner, and J. Erez. 1997. Stable carbon isotope ratios in Red Sea 

barnacles (Cirripedia) as an indicator of their food source. Marine Biology, 

130:243–247. http://dx.doi.org/10.1007/s002270050244.

Achituv, Y., and L. Mizrahi. 1996. Recycling of ammonium within a hydrocoral 

(Millepora dichotoma): Zooxanthellae–cirripede (Savignium milleporum) 

symbiotic association. Bulletin of Marine Science, 58:856–861.

Ackerman, J. L., and D. R. Bellwood. 2000. Reef fish assemblages: A re-evaluation 

using enclosed rotenone stations. Marine Ecology Progress Series, 206:227–

237. http://dx.doi.org/10.3354/meps206227.

Barneah, O., I. Brickner, M. Hooge, V. M. Weis, and T. C. LaJeunesse. 2007. Three 

party symbiosis: Acoelomorph worms, corals and unicellular algal symbionts 

in Eilat (Red Sea). Marine Biology, 151:1215–1223. http://dx.doi.org/10.1007

/s00227-006-0563-2.

Becker, J. H., and A. S. Grutter. 2004. Cleaner shrimp do clean. Coral Reefs, 23: 

515–520. 

Ben-Tzvi, O., S. Einbinder, and E. Brokovich. 2006. A beneficial association between a polychaete worm and a scleractinian coral? Coral Reefs, 25:98. 

http://dx.doi.org/10.1007/s00338-005-0084-3.

Birkeland, C., and J. S. Lucas. 1990. Acanthaster planci: Major management problem of coral reefs. Boca Raton, Fla.: CRC Press.

Brawley, S. H. 1992. Mesoherbivores. In Plant–animal interactions in the marine 

benthos, ed. D. M. John, S. J. Hawkins, and J. H. Price, pp. 235–263. Systematics Association Special Volume 46. Oxford, U. K.: Clarendon Press.

Brooker, R. M., P. L. Munday, and T. D. Ainsworth. 2010. Diets of coral-dwelling 

fishes of the genus Gobiodon with evidence of corallivory. Journal of Fish Biology, 76:2578–2583. http://dx.doi.org/10.1111/j.1095-8649.2010.02644.x.

Bruce, A. J. 1976. Shrimps and prawns of coral reefs, with special reference to commensalism. In Biology and geology of coral reefs, Volume 3: Biology 2, ed. 

O. Jones and R. Endean, pp. 37–94. New York: Academic Press.

———. 1998. New keys for the identification of Indo-West Pacific coral associated 

pontoniine shrimps, with observations on their ecology. Ophelia, 49:29–46. 

http://dx.doi.org/10.1080/00785326.1998.10409371.

Bruno, J. F., J. J. Stachowicz, and M. D. Bertness. 2003. Inclusion of facilitation 

into ecological theory. Trends in Ecology and Evolution, 18:119–125. http://

dx.doi.org/10.1016/S0169-5347(02)00045-9.

Bunkley-Williams, L., and E. H. Williams, Jr. 1998. Ability of Pederson cleaner 

shrimp to remove juveniles of the parasitic cymothoid isopod, Anilocra haemuli, from the host. Crustaceana, 71:862–869. http://dx.doi.org/10.1163

/156854098X00888.

Carpenter, R. C. 1997. Invertebrate predators and grazers. In Life and death of 

coral reefs, ed. C. Birkeland, pp. 198–229. New York: Chapman & Hall. 

http://dx.doi.org/10.1007/978-1-4615-5995-5_9.

Castro, P. 1976. Brachyuran crabs symbiotic with scleractinian corals: A review of 

their biology. Micronesica, 12:99–110.

———. 1978. Movements between coral colonies in Trapezia ferruginea (Crustacea: Brachyura), an obligate symbiont of scleractinian corals. Marine Biology, 

46:237–245. http://dx.doi.org/10.1007/BF00390685.

———. 1988. Animal symbioses in coral reef communities: A review. Symbiosis, 

5:161–184.

Castro, P., P. K. L. Ng, and S. T. Ahyong. 2004. Phylogeny and systematics of the 

Trapeziidae Miers, 1886 (Crustacea, Brachyura), with the description of a 

new family. Zootaxa, 643:1–70.

Cheng, Y.-R., and C.-F. Dai. 2010. Endosymbiotic copepods may feed on zooxanthellae from their coral host, Pocillopora damicornis. Coral Reefs, 29:13–18. 

http://dx.doi.org/10.1007/s00338-009-0559-8.

Choi, D. R., and R. N. Ginsburg. 1983. Distribution of coelobites (cavity dwellers) 

in coral rubble across the Florida reef tract. Coral Reefs, 2:165–172. http://

dx.doi.org/10.1007/BF00336723.

Coen, L. D. 1988. Herbivory by crabs and the control of algal epibionts on Caribbean host corals. Oecologia, 75:198–203. http://dx.doi.org/10.1007/BF

00378597.

Coker, D. J., M. S. Pratchett, and P. L. Munday. 2009. Coral bleaching and habitat 

degradation increase susceptibility to predation for coral-dwelling fishes.

Behavioral Ecology, 20:1204–1210. http://dx.doi.org/10.1093/beheco

/arp113.

Cole, A. J., M. S. Pratchett, and G. P. Jones. 2008. Diversity and functional importance of coral-feeding fishes on tropical coral reefs. Fish and Fisheries, 

9:286–307. http://dx.doi.org/10.1111/j.1467-2979.2008.00290.x.

Colgan, M. W. 1985. Growth rate reduction and modification of a coral colony by 

a vermetid mollusc Dendropoma maxima. Proceedings of the fifth International Coral Reef Symposium, 6:205–210.

———. 1987. Coral reef recovery on Guam (Micronesia) after catastrophic predation by Acanthaster planci. Ecology, 68:1592–1605. http://dx.doi.org/10

.2307/1939851.

Cook, P. A., B. A. Steward, and Y. Achituv. 1991. The symbiotic relationship between 

the fire coral Millepora dichotoma and the barnacle Savignium milleporum. 

Hydrobiologia, 216/217:285–290. http://dx.doi.org/10.1007/BF00026476.

De Bary, H. A. 1879. Die Erscheinung der Symbiose. Strasburg: Author. 

DeMartini, E. E. 1996. Sheltering and foraging substrate uses of the arc-eye hawkfish Paracirrhites arcatus (Pisces: Cirrhitidae). Bulletin of Marine Science, 

58:826–837.

Depczynski, M., and D. R. Bellwood. 2003. The role of cryptobenthic reef fishes in 

coral reef trophodynamics. Marine Ecology Progress Series, 256:183–191. 

http://dx.doi.org/10.3354/meps256183.

DeVantier, L. M., and R. Endean. 1988. The scallop Pedum spondyloideum mitigates the effects of Acanthaster planci predation of the host coral Porites: 

Host defence facilitation by exaptation. Marine Ecology Progress Series, 47: 

293–301. http://dx.doi.org/10.3354/meps047293.

DeVantier, L. M., R. E. Reichelt, and R. H. Bradbury. 1986. Does Spirobranchus 

giganteus protect Porites from predation by Acanthaster planci: Predator 

pressure as a mechanism of coevolution? Marine Ecology Progress Series, 32: 

307–310. http://dx.doi.org/10.3354/meps032307.

Dominici-Arosemena, A., and M. Wolff. 2006. Reef fish community structure in 

the tropical eastern Pacific (Panamá): Living on a relatively stable rocky reef 

environment. Helgoland Marine Research, 60:287–305. http://dx.doi.org/10

.1007/s10152-006-0045-4.

Donaldson, T. J. 1990. Reproductive behavior and social organization of some Pacific hawkfishes (Cirrhitidae). Japanese Journal of Ichthyology, 36:439–458. 

Eibl-Eibesfeldt, I. 1955. Über Symbiosen, Parasitismus und andere besondere zwischenartliche Beziehungen tropischer Meeresfische. Zeitschrift für Tierpsychologie, 12:203–219. http://dx.doi.org/10.1111/j.1439-0310.1955.tb01523.x.

Fauchald, K., and P. A. Jumars. 1979. The diet of worms: A study of polychaete 

feeding guilds. Oceanography and Marine Biology, an Annual Review, 17: 

193–284.
number 39 • 247

Fiedler, G. C. 2002. The influence of social environment on sex determination in 

harlequin shrimp (Hymenocera picta: Decapoda, Gnathophyllidae). Journal 

of Crustacean Biology, 22:750–761. http://dx.doi.org/10.1651/0278-0372

(2002)022[0750:TIOSES]2.0.CO;2.

Fiege, D., and H. A. ten Hove. 1999. Redescription of Spirobranchus gaymerdi 

(Quatrefages, 1866) (Polychaeta: Serpulidae) from the Indo-Pacific with remarks on the Spirobranchus giganteus complex. Zoological Journal of the 

Linnean Society, 126:355–364.

Garth, J. S. 1964. The crustacean Decapoda (Brachyura and Anomura) of Eniwetok 

Atoll, Marshall Islands, with special reference to the obligate commensals of 

branching corals. Micronesica, 1:137–144.

Ginsburg, R. N. 1983. Geological and biological roles of cavities in coral reefs. In 

Perspectives on coral reefs, ed. D. J. Barnes, pp. 148–153. Manuka, Australia: 

Brian Clouston Publisher.

Gischler, E., and R. N. Ginsburg. 1996. Cavity dwellers (coelobites) under coral 

rubble in Southern Belize barrier and atoll reefs. Bulletin of Marine Science, 

58:570–589.

Glynn, P. W. 1976. Some physical and biological determinants of coral community 

structure in the eastern Pacific. Ecological Monographs, 46:431–456. http://

dx.doi.org/10.2307/1942565.

———. 1977. Interactions between Acanthaster and Hymenocera in the field and laboratory. Proceedings of the third International Coral Reef Symposium, 1:210–215.

———. 1980. Defense by symbiotic crustacea of host corals elicited by chemical 

cues from predator. Oecologia, 47:287–290. http://dx.doi.org/10.1007/BF

00398518.

———. 1982. Acanthaster population regulation by a shrimp and a worm. Proceedings of the fourth International Coral Reef Symposium, 2:607–612.

———. 1983a. Crustacean symbionts and the defense of corals: Coevolution on the 

reef? In Coevolution, ed. M. H. Nitecki, pp. 111–178. Chicago: University of 

Chicago Press.

———. 1983b. Increased survivorship in corals harboring crustacean symbionts. 

Marine Biology Letters, 4:105–111.

———. 1984. An amphinomid worm predator of the crown-of-thorns sea star and 

general predation on asteroids in eastern and western Pacific coral reefs. Bulletin of Marine Science, 35:54–71.

———. 1985. El Niño-associated disturbance to coral reefs and post disturbance 

mortality by Acanthaster planci. Marine Ecology Progress Series, 26:295–

300. http://dx.doi.org/10.3354/meps026295.

———. 1987. Some ecological consequences of coral-crustacean guard mutualisms 

in the Indian and Pacific oceans. Symbiosis, 4:301–324.

———. 1988. Predation on coral reefs: Some key processes, concepts and research 

directions. Proceedings of the sixth International Coral Reef Symposium, 

1:51–62.

———. 1996. Bioerosion and coral growth: A dynamic balance. In Life and death 

of coral reefs, ed. C. Birkeland, pp. 68–94. New York: Chapman & Hall.

———. 2006. Fish utilization of simulated coral reef frameworks versus eroded 

rubble substrates off Panamá, eastern Pacific. Proceedings of the tenth International Coral Reef Symposium, 1:250–256.

Glynn, P. W., and I. C. Enochs. 2011. Invertebrates and their roles in coral reef 

ecosystems. In Coral reefs: An ecosystem in transition, ed. Z. Dubinsky and 

N. Stambler, pp. 273–326. Berlin: Springer. http://dx.doi.org/10.1007/978-94

-007-0114-4_18.

Glynn, P. W., I. C. Enochs, J. E. McCosker, and A. N. Graefe. 2008. First record of 

a pearlfish, Carapus mourlani, inhabiting the aplysiid opisthobranch mollusk Dolabella auricularia. Pacific Science, 62:593–601. http://dx.doi.org/10

.2984/1534-6188(2008)62[593:FROAPC]2.0.CO;2.

Glynn, P. W., and D. A. Krupp. 1986. Feeding biology of a Hawaiian sea star corallivore, Culcita novaeguineae Muller and Troschel. Journal of Experimental Marine Biology and Ecology, 96:75–96. http://dx.doi.org/10.1016/0022

-0981(86)90014-6.

Glynn, P. W., M. Perez, and S. L. Gilchrist. 1985. Lipid decline in stressed corals and 

their crustacean symbionts. Biological Bulletin, 168:276–284. http://dx.doi

.org/10.2307/1541240.

Goldshmid, R., R. Holzman, D. Weihs, and A. Genin. 2004. Aeration of corals by 

sleep-swimming fish. Limnology and Oceanography, 49:1832–1839. http://

dx.doi.org/10.4319/lo.2004.49.5.1832.

Goreau, T. F., N. I. Goreau, and Y. Neumann. 1970. On feeding and nutrition in 

Fungiacava eilatensis (Bivalvia, Mytilidae), a commensal living in fungiid corals. Journal of Zoology, London, 160:159–172. http://dx.doi.org/10.1111

/j.1469-7998.1970.tb02901.x.

Goreau, T. F., and W. D. Hartman. 1966. Sponge: Effect on the form of reef corals. 

Science, 151:343–344. http://dx.doi.org/10.1126/science.151.3708.343.

Goreau, T. F., and C. M. Yonge. 1968. Coral community on muddy sand. Nature

(London), 217:421–423. http://dx.doi.org/10.1038/217421a0.

Hadfield, M. G. 1976. Molluscs associated with living tropical corals. Micronesica, 

12:133–148.

Haramaty, L. 1991. Reproduction effort in the nudibranch Phestilla sibogae: 

Calorimetric analysis of food and eggs. Pacific Science, 45:257–262.

Hay, M. E., J. E. Duffy, and C. A. Pfister. 1987. Chemical defense against different 

marine herbivores: Are amphipods insect equivalents? Ecology, 68:1567–

1580. http://dx.doi.org/10.2307/1939849.

Herler, J. 2007. Microhabitats and ecomorphology of coral- and coral-rock associated gobiid fish (Teleostei: Gobiidae) in the northern Red Sea. Marine Ecology, An Evolutionary Perspective, 28(Suppl. s1):82–94.

Highsmith, R. C. 1982. Reproduction by fragmentation in corals. Marine Ecology 

Progress Series, 7:207–226. http://dx.doi.org/10.3354/meps007207.

Holbrook, S. J., A. J. Brooks, R. J. Schmitt, and H. L. Stewart. 2008. Effects of 

sheltering fish on growth of their host corals. Marine Biology, 155:521–530. 

http://dx.doi.org/10.1007/s00227-008-1051-7.

Humes, A. G. 1985. Cnidarians and copepods: A success story. Transactions of 

the American Microscopical Society, 104:313–320. http://dx.doi.org/10.2307

/3226484.

———. 1994. How many copepods? Hydrobiologia, 292/293:1–7. http://dx.doi

.org/10.1007/BF00229916.

Hutchings, P. A. 1986. Biological destruction of coral reefs. Coral Reefs, 4:239–252. 

http://dx.doi.org/10.1007/BF00298083.

Jackson, J. B. C., and J. E. Winston. 1982. Ecology of cryptic coral reef communities. I. Distribution and abundance of major groups of encrusting organisms. 

Journal of Experimental Marine Biology and Ecology, 57:135–147. http://

dx.doi.org/10.1016/0022-0981(82)90188-5.

Keable, S. J. 1995. Structure of the marine invertebrate scavenging guild of a tropical 

reef ecosystem: Field studies at Lizard Island, Queensland, Australia. Journal of 

Natural History, 29:27–46. http://dx.doi.org/10.1080/00222939500770021.

Kleemann, K. H. 1980. Boring bivalves and their host corals from the Great Barrier 

Reef. Journal of Molluscan Studies, 46:13–54.

Knowlton, N., J. C. Lang, and B. D. Keller. 1990. Case study of natural population 

collapse: Post-hurricane predation on Jamaican staghorn corals. Smithsonian 

Contributions to the Marine Sciences, No. 31. Washington, D.C.: Smithsonian 

Institution Press.

Knowlton, N., J. C. Lang, M. C. Rooney, and P. Clifford. 1981. Evidence for delayed 

mortality in hurricane-damaged Jamaican staghorn corals. Nature, 294:251–

252. http://dx.doi.org/10.1038/294251a0.

Knowlton, N., and E. Rohwer. 2003. Multispecies microbial mutualisms on coral 

reefs: The host as a habitat. American Naturalist, 162:551–562. http://dx.doi

.org/10.1086/378684.

Knudsen, J. W. 1967. Trapezia and Tetralia (Decapoda, Brachyura, Xanthidae) as obligate ectoparasites of pocilloporid and acroporid corals. Pacific Science, 21:51–57.

Kobluk, D. R. 1988. Cryptic faunas in reefs: Ecology and geologic importance. 

Palaios, 3:379–390. http://dx.doi.org/10.2307/3514784.

Kropp, R. K. 1986. Feeding biology and mouthpart morphology of three species of 

coral gall crabs (Decapoda: Cryptochiridae). Journal of Crustacean Biology, 

6:377–384. http://dx.doi.org/10.2307/1548178.

Lassig, B. R. 1977. Communication and coexistence in a coral community. Marine 

Biology, 42:85–92. http://dx.doi.org/10.1007/BF00392016.

———. 1981. Significance of the epidermal ichthyotoxic secretion of coraldwelling gobies. Toxicon, 19:729–735. http://dx.doi.org/10.1016/0041-0101

(81)90068-4.

Lewinsohn, C. 1978. Bemerkungen zur Taxonomie von Paguritta harmsi (Gordon) (Crustacea Decapoda, Anomura) und Beschreibung einer neuen Art der 

gleichen Gattung aus Australien. Zoologische Mededelingen, 53:243–252.

Liberman, T., A. Genin, and Y. Loya. 1995. Effects on growth and reproduction of 

the coral Stylophora pistillata by the mutualistic damselfish Dascyllus marginatus. Marine Biology, 121:741–746. http://dx.doi.org/10.1007/BF00349310.

McLaughlin, P., and R. Lemaitre. 1993. A review of the hermit crab genus Paguritta (Decapoda: Anomura: Paguridae) with descriptions of three new species. 

Raffles Bulletin of Zoology, 41:1–29.

Mokady, O., Y. Loya, and B. Lazar. 1998. Ammonium contribution from boring bivalves to their coral host—A mutualistic symbiosis? Marine Ecology Progress 

Series, 169:295–301. http://dx.doi.org/10.3354/meps169295.

Mora, C., and F. A. Zapata. 2000. Effects of a predatory site-attached fish on abundance

and body size of early post-settled reef fishes from Gorgona Island, Colombia. 

Proceedings of the ninth International Coral Reef Symposium, 1:475–480.

Moran, P. J. 1986. The Acanthaster phenomenon. Oceanography and Marine Biology, An Annual Review, 24:379–480.
248 • smithsonian contributions to the marine sciences

Munday, P. L., G. P. Jones, and M. Julian Caley. 1997. Habitat specialization and 

the distribution and abundance of coral-dwelling gobies. Marine Ecology 

Progress Series, 152:227–239. http://dx.doi.org/10.3354/meps152227.

Pantos, O., and J. C. Bythell. 2010. A novel reef coral symbiosis. Coral Reefs, 

29:761–770. http://dx.doi.org/10.1007/s00338-010-0622-5.

Pasternak, Z., A. Rix, and A. Abelson. 2001. Episymbionts as possible anti-fouling 

agents on reef-building hydrozoans. Coral Reefs, 20:318–319. http://dx.doi

.org/10.1007/s003380100177.

Patton, W. K. 1966. Decapod crustacea commensal with Queensland branching corals.

Crustaceana, 10:271–295. http://dx.doi.org/10.1163/156854066X00180.

———. 1974. Community structure among the animals inhabiting the coral Pocillopora damicornis at Heron Island, Australia. In Symbiosis in the sea, ed. W. B. 

Vernberg, pp. 219–243. Columbia, S.C.: University of South Carolina Press.

———. 1976. Animal associates of living reef corals. In Biology and geology of 

coral reefs, Volume 3: Biology 2, ed. O. A. Jones and R. Endean, pp. 1–36. 

New York: Academic Press.

———. 1994. Distribution and ecology of animals associated with branching corals 

(Acropora spp.) from the Great Barrier Reef, Australia. Bulletin of Marine 

Science, 55:193–211. 

Patton, W. K., and D. R. Robertson. 1980. Pair formation in a coral inhabiting hermit crab. Oecologia, 47:267–269. http://dx.doi.org/10.1007/BF00346831.

Pearson, R. G., and R. Endean. 1969. A preliminary study of the coral predator 

Acanthaster planci (L.) (Asteroidea) on the Great Barrier Reef. Fisheries 

Notes, Department of Harbours and Marine, Queensland, 3:27–68.

Perry, C. T., and L. J. Hepburn. 2008. Syn-depositional alteration of coral reef 

framework through bioerosion, encrustation and cementation: Taphonomic 

signatures of reef accretion and reef depositional events. Earth-Science Reviews, 86:106–144. http://dx.doi.org/10.1016/j.earscirev.2007.08.006.

Pinzón, J. H., and T. C. LaJeunesse. 2010. Species delimitation of common reef 

corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Molecular Ecology, 20:311–325. 

http://dx.doi.org/10.1111/j.1365-294X.2010.04939.x.

Pratchett, M. S. 2001. Influence of coral symbionts on feeding preferences of crownof-thorns starfish Acanthaster planci in the western Pacific. Marine Ecology 

Progress Series, 214:111–119. http://dx.doi.org/10.3354/meps214111.

Preston, E. M. 1973. A computer simulation of competition among five sympatric congeneric species of xanthid crabs. Ecology, 54:469–483. http://dx.doi

.org/10.2307/1935333.

Reaka-Kudla, M. L. 1997. The global biodiversity of coral reefs: a comparison 

with rain forests. In Biodiversity II: Understanding and protecting our biological resources, ed. M. L. Reaka-Kudla, D. E. Wilson, and E. O. Wilson, pp. 

83–108. Washington, D.C.: Joseph Henry Press.

Richter, C., M. Wunsch, M. Rasheed, I. Kötter, and M. I. Badran. 2001. Endoscopic 

exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling 

sponges. Nature, 413:726–730. http://dx.doi.org/10.1038/35099547.

Rinkevich, B., Z. Wolodarsky, and Y. Loya. 1991. Coral-crab Association: A compact domain of a multilevel trophic system. Hydrobiologia, 216/217:279–

284. http://dx.doi.org/10.1007/BF00026475.

Robertson, D. R., and G. R. Allen. 2008. Shorefishes of the tropical eastern Pacific 

online information system. Version 1.0. Balboa, Panama: Smithsonian Tropical Research Institute. www.neotropicalfishes.org/sftep.

Robertson, R. 1970. Review of the predators and parasites of stony corals, with special reference to symbiotic prosobranch gastropods. Pacific Science, 24:43–54.

Rohwer, F., V. Seguritan, F. Azam, and N. Knowlton. 2002. Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series, 243:1–10. 

http://dx.doi.org/10.3354/meps243001.

Ross, A., and W. A. Newman. 1969. A coral eating barnacle. Pacific Science, 23: 

252–256.

———. 1973. Revision of the coral-inhabiting barnacles (Cirripedia: Balanidae).

Transactions of the San Diego Society of Natural History, 17:137–174.

———. 1995. A coral-eating barnacle, revisited (Cirripedia, Pyrgomatidae). Contributions to Zoology, 65:129–175.

———. 2000. A new coral-eating barnacle: The first record from the Great Barrier 

Reef, Australia. Memoirs of the Queensland Museum, 45:585–591.

Rotjan, R. D., and S. M. Lewis. 2008. Impact of coral predators on tropical reefs. 

Marine Ecology Progress Series, 367:73–91. http://dx.doi.org/10.3354

/meps07531.

Rützler, K. 2004. Sponges on coral reefs: A community shaped by competitive cooperation. Bollettino dei Musei e degli Istituti Biologici dell Universita di 

Genova, 68:85–148. 

Saffo, M. B. 1993. Coming to terms with a field: Words and concepts in symbiosis. 

Symbiosis, 14:17–31.

Schuhmacher, H. 1977. A hermit crab, sessile on corals, exclusively feeds by 

feathered antennae. Oecologia, 27:371–374. http://dx.doi.org/10.1007/BF

00345570.

———. 1992. Impact of some corallivorous snails on stony corals in the Red Sea. 

Proceedings of the seventh International Coral Reef Symposium, 2:840–846.

Shima, J. S., C. W. Osenberg, and A. C. Stier. 2010. The vermetid gastropod Dendropoma maximum reduces coral growth and survival. Biological Letters, 

doi:10.1098/rsbl.2010.0291. http://dx.doi.org/10.1098/rsbl.2010.0291.

Simon-Blecher, N., Y. Achituv, and Z. Malik. 1996. Effect of epibionts on the microdistribution of chlorophyll in corals and its detection by fluorescence 

spectral imaging. Marine Biology, 126:757–763. http://dx.doi.org/10.1007

/BF00351342.

Souter, P. 2010. Hidden genetic diversity in a key model species of coral. Marine 

Biology, 157:875–885. http://dx.doi.org/10.1007/s00227-009-1370-3.

Spotte, S. 1998. “Cleaner” shrimps? Helgolander Meeresuntersuchungen, 52:59–

64. http://dx.doi.org/10.1007/BF02908736.

Stewart, H. L., S. J. Holbrook, R. J. Schmitt, and A. J. Brooks. 2006. Symbiotic crabs 

maintain coral health by clearing sediments. Coral Reefs, 25:609–615. http://

dx.doi.org/10.1007/s00338-006-0132-7.

Stier, A. C., C. S. McKean, C. W. Osenberg, and J. S. Shima. 2010. Guard crabs alleviate deleterious effects of vermetid snails on a branching coral. Coral Reefs, 

29:1019. http://dx.doi.org/10.1007/s 00338-010-0663-9.

Stimpson, J. 1990. Stimulation of fat-body production in the polyps of the coral Pocillopora damicornis by the presence of mutualistic crabs of the genus Trapezia. Marine Biology, 106:211–218. http://dx.doi.org/10.1007/BF01314802.

Stock, J. H. 1988. Copepods associated with reef corals: A comparison between 

the Atlantic and the Pacific. Hydrobiologia, 167/168:545–547. http://dx.doi

.org/10.1007/BF00026350.

Sussman, M., Y. Loya, M. Fine, and E. Rosenberg. 2003. The marine fireworm 

Hermodice carunculata is a winter reservoir and spring–summer vector for 

the coral-bleaching pathogen Vibrio shiloi. Environmental Microbiology, 

5:250–255. http://dx.doi.org/10.1046/j.1462-2920.2003.00424.x.

Tribollet, A., and S. Golubic. 2011. Reef bioerosion: Agents and processes. In Coral 

reefs: An ecosystem in transition, ed. Z. Dubinsky and N. Stambler, pp. 435–

449. Berlin: Springer.

Valentich-Scott, P., and P. Tongkerd. 2008. Coral-boring bivalve mollusks of southeastern Thailand with the description of a new species. The Raffles Bulletin 

of Zoology, 18(Suppl.):191–216.

Vannini, M. 1985. A Shrimp that speaks crab-ese. Journal of Crustacean Biology, 

5:160–167. http://dx.doi.org/10.2307/1548228.

Vogler, C., J. Benzie, H. Lessios, P. Barber, and G. Worheide. 2008. A threat to coral 

reefs multiplied? Four species of crown-of-thorns starfish. Biological Letters, 

4:696–699. http://dx.doi.org/10.1098/rsbl.2008.0454.

Weber, J. N., and P. M. J. Woodhead. 1970. Ecological studies of the coral predator Acanthaster planci in the South Pacific. Marine Biology, 6:12–17. http://

dx.doi.org/10.1007/BF00352602.

Wickler, W. 1973. Biology of Hymenocera picta Dana. Micronesica, 9:225–230.

Wielgus, J., and O. Levy. 2006. Differences in photosynthetic activity between coral 

sections infested and not infested by boring spionid polychaetes. Journal 

of the Marine Biological Association of the United Kingdom, 86:727–728. 

http://dx.doi.org/10.1017/S0025315406013622.

Williams, D. E., and M. W. Miller. 2005. Coral disease outbreak: Pattern, prevalence 

and transmission in Acropora cervicornis. Marine Ecology Progress Series, 

301:119–128. http://dx.doi.org/10.3354/meps301119.

Wulff, J. L. 1984. Sponge-mediated coral reef growth and rejuvenation. Coral Reefs, 

3:157–163. http://dx.doi.org/10.1007/BF00301960.

———. 2006. Rapid diversity and abundance decline in a Caribbean coral reef 

sponge community. Biological Conservation, 127:167–176. http://dx.doi.org

/10.1016/j.biocon.2005.08.007.

Wulff, J. L., and L. W. Buss. 1979. Do sponges help hold reefs together? Nature, 

281:374–375. http://dx.doi.org/10.1038/281474a0.

Wunsch, M., S. M. Al-Moghrabi, and I. Kötter. 2000. Communities of coral reef 

cavities in Jordan, Gulf of Aqaba (Red Sea). Proceedings of the ninth International Coral Reef Symposium, 1:595–600.

Zvuloni, A., R. Armoza-Zvuloni, and Y. Loya. 2008. Structural deformation of 

branching corals associated with the vermetid gastropod Dendropoma 

maxima. Marine Ecology Progress Series, 363:103–108. http://dx.doi.org/10

.3354/meps07473.
About the Contributors

Gilberto M. Amado Filho holds a B.S. in biology (1985), an M.S. in biological science 

(1991), and a Ph.D. in biological sciences/biophysics (1996) from the Universidade Federal do Rio de Janeiro (UFRJ). He is Professor at UFRJ and Researcher of the ecology and 

ecophysiology of marine macrophytes at the Jardim Botânico do Rio Janeiro. Gilberto’s 

research interests are the ecology of benthic marine communities, the ecophysiology of 

marine macrophytes, the mineralization of marine organisms, and the effects of marine 

pollutants on marine organisms. Current work is on the biodiversity characterization 

of the mesophotic zone of the continental shelf and oceanic islands of Brazil, Abrolhos 

Bank, and Fernando de Noronha Archipelago. Gilberto advises several postdocs and supervises M.S. and undergraduate students.

Charles D. Amsler is a professor of marine ecophysiology and chemical ecology at the 

University of Alabama at Birmingham. Charles holds a B.A. from Duke University, an 

M.S. from the University of North Carolina at Wilmington, and a Ph.D. in 1989 from 

the University of California, Santa Barbara. His research is centered on chemical interactions between organisms or ways in which organisms perceive, respond to, or otherwise interact with their chemical environment, including understanding the impacts of 

ocean acidification and other climate change factors on marine organisms. Previous work 

has included research on environmental factors governing Antarctic algal seasonality, 

the taxonomy of filamentous brown algae, and bacterial chemotactic signal transduction. Charles is very involved with educational outreach and is a long-term Antarctic researcher, scientific diver, and principal investigator. In 2007, the U.S. Board of Geographic 

Names designated Amsler Island, Antarctica, and he has served as the 2009 president of 

the Phycological Society of America.

Suzanne N. Arnold attended Bates College in Lewiston, Maine, and graduated in 1999 

with a B.S. in biology. During her semester abroad she studied marine ecology in Zanzibar. It was this experience that spurred her interest in coral reef ecosystems and the people 

who are dependent on them. After completing her undergraduate degree, Susie worked as 

a Natural Resource Officer on Cape Cod and a Research Associate for a climate change 

mitigation consulting firm in Oregon, studied coral reefs and seamanship in Southeast 

Asia, and worked in Florida at Mote Marine Laboratory’s Center for Tropical Research. 

In 2003, she relocated to the University of Maine’s Darling Marine Center to do subtidal 

lobster and sea urchin research, and in 2007 received Master of Science degrees in marine biology and marine policy from the University of Maine. Susie is currently a Ph.D. 
250 • smithsonian contributions to the marine sciences

candidate under Robert Steneck and was named an International 

Society for Reef Studies fellow in 2008.

Richard B. Aronson is professor and head of the Department 

of Biological Sciences at the Florida Institute of Technology. He 

received his A.B. from Dartmouth College in 1979 and his Ph.D. 

from Harvard University in 1985. His primary research focus 

is understanding how large-scale processes, including climate 

change, disease, overfishing and nutrient loading, control the 

geology and ecology of coral reefs on time scales ranging from 

decades to millennia. To that end, he has been coring reefs under 

water in Belize, Panama, and Jamaica for the past 15 years. A 

second area of interest is climate change in Antarctica and its 

implications for species invasion and community turnover. In 

2004 Rich coauthored a report titled “Coral Reefs and Global 

Climate Change” for the Pew Center on Global Climate Change. 

He is past-president of the International Society for Reef Studies (ISRS). Rich is grateful for the support he has received from 

Smithsonian programs since 1986.

Andrew C. Baker is a marine biologist whose research focuses on 

the effects of climate change on coral reefs. An assistant professor of marine biology and fisheries at the University of Miami’s 

Rosenstiel School of Marine and Atmospheric Science, Andrew 

graduated with a Double First in natural sciences (zoology) from 

Cambridge University in 1993. After coming to the United States 

on a Fulbright Scholarship, he was a predoctoral fellow of the 

Smithsonian Tropical Research Institute in Panama (1995) and 

doctoral fellow of the Australian Museum (1997). He received 

his Ph.D. in marine biology from the University of Miami in 1999 

and worked for the Wildlife Conservation Society (WCS), first at 

the New York Aquarium (1999–2000) and then in the Global 

Marine Program (2001–2005), where he was also a member of 

the adjunct faculty of Columbia University. In 2008 Andrew was 

awarded a Pew Fellowship in marine conservation for his work 

on reef coral symbioses and climate change.

Bill J. Baker holds a B.S. in chemistry from California Polytechnic State University, San Luis Obispo (1982) and a Ph.D. 

in chemistry from the University of Hawaii (1986). Bill is a 

University of South Florida professor of chemistry and director of the USF Center for Drug Discovery and Innovation. His 

research interests include analysis of secondary metabolites 

from marine invertebrates, macroalgae, and microorganisms; 

drug discovery, including tropical (malaria, leishmaniasis, dengue, influenza, river blindness), infective, proliferative, and 

neurodegenerative diseases and multidrug resistance; marine 

biotechnology; chemical ecology of marine organisms; biosynthesis of marine natural products; and agrochemical applications of marine natural products. Bill is a long-term Antarctic 

scientific diver and principal investigator. In 1998, the U.S. 

Board of Geographic Names designated Baker Point, Antarctica. Bill has served as 2007 president of the American Society 

of Pharmacognosy.

Charles H. Baxter’s commitment to holistic biology has grown 

from a career of developing diverse interests in biology to becoming a naturalist and supporting students who ask questions of organisms in nature. Chuck taught biology at Stanford University 

and Hopkins Marine Station from 1961 to 1993. His areas of 

interest focused on the structure and function of animals, how 

they evolved, how they operated in natural systems, and how humans were impacting those systems. From 1988 to 1996 Chuck 

did benthic ecology in the Monterey Canyon with the Monterey 

Bay Aquarium Research Institute’s remotely operated vehicle, 

and from 1996 to 2003 he did concept and content development 

for Sea Studios Foundation television production company. He 

has had a long-standing interest in and participated in ongoing 

collaborations on climate forcing of coastal communities and the 

biogeographic responses of species along the Pacific coast. Chuck 

received the 1993 Dinkelspiel Award for outstanding service to 

undergraduate education and the 2000 Naturalist of the Year 

Award from the Western Society of Naturalists.

Giacomo Bernardi obtained his Master’s and Ph.D. in molecular 

biology from the University of Paris and a postdoc from Stanford 

University. His research on molecular ecology and speciation of 

marine fishes has a strong field component that includes much 

subtidal work. His diving experience started in his early teens 

and was centered in the Mediterranean and the Red Sea. Now 

with University of California, Santa Cruz, his current research 

is primarily done in southern Africa, the tropical eastern Pacific, 

and French Polynesia. He has used a variety of underwater methods, including saturation and technical diving, for his research. 

His commitment to underwater research translated to teaching 

a kelp forest ecology course in California and a subtidal field 

course that has been taught for the past ten years in Mexico, 

French Polynesia, and the Mediterranean.

Charles E. Birkeland earned his doctorate at the University of 

Washington, Seattle. From 1970 to 1975 he was a postdoc at 

the Smithsonian Tropical Research Institute in Panama, where 

he experimented with the effects of nutrient input on the reefs 

of the eastern Pacific in contrast to the reefs in the oligotrophic 

western Atlantic. From 1975 to 2000 he was at the University 

of Guam Marine Laboratory, and from 2000 through 2010 

he was at the Hawaii Cooperative Fishery Research Unit (U.S. 

Geological Survey) at the Department of Biology, University of 

Hawaii at Manoa. His recent research focused mainly on coral 

reef communities, namely (1) how corals acclimatize (physiological or behavioral adjustment of individual colony) or adapt (genetic adjustment of population) to climate change, (2) why some 

reef communities recover from damage by human activities and 

others do not, and (3) how alien populations adjust their realized 

niche dimensions in their new habitats.

Deron E. Burkepile received his Bachelor’s degree from the University of Mississippi in biology in 1999. In 2006, he received his 

Ph.D. under the direction of Dr. Mark Hay from Georgia Tech, 
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where he examined the impacts of herbivorous fish species richness and identity on community structure of coral reefs. After 

finishing his Ph.D., Deron was a Brown Postdoctoral Fellow at 

Yale University, where he did research in Kruger National Park 

in South Africa on the role of different-sized guilds of mammalian herbivores (elephants versus zebra versus impala) in driving 

ecosystem function in African savannas. Deron is currently an 

assistant professor in biological sciences at Florida International 

University in Miami. His lab is currently working on projects 

examining how alterations to herbivore pressure and nutrient 

availability impact coral–microbe interactions and coral disease, 

and he continues to investigate the similarities and differences 

between marine and terrestrial grazing ecosystems.

Mark H. Carr is a professor in the Department of Ecology and 

Evolutionary Biology at the University of California, Santa Cruz. 

Mark received his Master’s degree at Moss Landing Marine 

Laboratories and his Ph.D. at the University of California, Santa 

Barbara. Mark and his graduate students study the behavioral, 

population, and community ecology of temperate marine fishes 

and salmonids, including kelp forest and riparian ecosystems. 

Much of his basic ecological research is designed to inform management and conservation problems, including the design and 

evaluation of marine protected areas, the design of large-scale,

long-term monitoring programs, and ecosystem-based fisheries 

management. Mark is a co–principal investigator with the Partnership for Interdisciplinary Studies of Coastal Oceans (PISCO), 

a multicampus coastal marine research consortium. Mark is also 

a science advisor to California’s Marine Life Protection Act and 

Ocean Protection Council, an editor for the Ecological Society 

of America (Ecology, Ecological Monographs), a member of the 

Society’s Rapid Response Team, and an Aldo Leopold Leadership Fellow. 

Kenneth E. Clifton began diving in 1974 as a skinny 15-year-old,

exploring the kelp beds of Monterey. In 1976 Ken moved to 

La Jolla, where he undertook advanced diver and dive master 

training while earning a B.A. in biology from the University of 

California, San Diego. Ken then moved to UC Santa Barbara, 

receiving a Ph.D. in 1987 from Bob Warner’s lab for studies of 

reef fish behavioral ecology. After a three-year stint studying gazelle foraging in East Africa, he returned to marine studies as a 

postdoctoral researcher with the Smithsonian Tropical Research 

Institute, working out of the San Blas field station for nearly five 

years. It was there that his work on the reproductive ecology of 

green seaweeds began. Ken remains an active research diver who 

continues to focus on the behavior, ecology, and life history of 

various marine organisms. He is currently an associate professor 

of biology at Lewis and Clark College in Portland, Oregon.

Mary-Alice Coffroth completed her undergraduate degree in biology at the College of William and Mary in Virginia. She obtained an M.S. and Ph.D. in biological oceanography from the 

Rosenstiel School of Marine and Atmospheric Science (RSMAS) 

at the University of Miami, where she did a large portion of her 

dissertation work at the Smithsonian Tropical Research Institute’s (STRI) field station in San Blas, Panama. She continued to 

work at STRI as an NSF postdoc and then moved to the University at Buffalo, where she is now a professor. She continues to 

work and dive on reefs, with her work focusing on the establishment and maintenance of coral–algal symbioses.

James A. Coyer received a B.S. in biology from the University 

of Wisconsin-Eau Claire in 1970 and a Ph.D. in biology from 

the University of Southern California in 1979. Jim is Assistant 

Director of Appledore Programs at the Shoals Marine Laboratory (Cornell University/University of New Hampshire). His current research interests include phylogeny and phylogeography of 

Fucus spp. and Zostera spp. in northern Europe, the role of sea 

urchins in determining community structure in giant kelp forests 

off southern California, and the impact of introduced species on 

the kelp beds in the Gulf of Maine. Jim is coauthor of Shoals 

Marine Lab’s The Underwater Catalog: A Guide to Methods in 

Underwater Research.

Paul K. Dayton started diving in the mid-1950s with homemade 

gear that should have killed him. He is now a marine ecologist 

at Scripps Institution of Oceanography. Interested in understanding the processes organizing marine ecosystems, Paul focuses his 

work on the evaluation of important interaction strengths in ecosystems and how they vary in space and time in relation to both 

ecological and physical forcing. He has studied marine systems 

along the eastern rim of the Pacific Ocean from the Arctic to the 

tip of South America and in McMurdo Sound, Antarctica. Paul 

has been awarded both the George Mercer and William Cooper 

awards from the Ecological Society of America, the E. O. Wilson 

Naturalist Award from the American Society of Naturalists, and 

the Ramon Margalef Prize in Ecology and Environmental Sciences in Barcelona. He is proud to have been recognized with a 

Scientific Diving Lifetime Achievement Award from the American Academy of Underwater Sciences.

David O. Duggins is a resident senior research scientist, marine 

technologist, and supervisor of marine operations at the University of Washington Friday Harbor Marine Laboratories (FHL). 

Dave holds a Ph.D. from the University of Washington. He initiated and supervises the FHL Science Outreach Partnership and 

served on the board of directors of the San Juan Nature Institute. 

His research interests are in benthic community ecology, particularly as it relates to intertidal and shallow subtidal habitats and 

population biology and biomechanics of kelps. He pioneered an 

experimental approach to the ecological role of sea otters in relation to sea urchins abundances in kelp forests.

David B. Eggleston is a professor of marine science at North 

Carolina State University, and director of NC State’s Center for 

Marine Sciences and Technology in Morehead City, North Carolina. David began scuba diving in 1974, became an active scuba 
252 • smithsonian contributions to the marine sciences

instructor with the Professional Association of Diving Instructors 

in Florida, and then integrated scuba into his academic research 

and education/outreach programs. David’s areas of expertise are 

marine ecology and conservation, fisheries, and marine science 

education. David has won numerous awards for his research 

and teaching, such as an NSF Early Career Award and induction 

into the North Carolina Academy of Outstanding Teachers. He 

has published more than 90 scientific papers in peer-reviewed 

journals, logged more than 4,000 dives, and used scuba to help 

conserve and restore species and ecosystems in the Florida Keys, 

Bahamas, Caribbean, and North Carolina.

Michael S. Foster is professor emeritus at Moss Landing Marine Laboratories/San Jose State University. He received his B.S. 

from Stanford University and Ph.D. from UC Santa Barbara. 

His research interests center on the ecology of subtidal and intertidal reefs, especially the structure and dynamics of algal assemblages in kelp forests, rhodolith beds, and on rocky shores. 

He is an instructor with the National Association of Underwater Instructors, fellow of the California Academy of Sciences, a 

Fulbright Scholar, and recipient of the Scientific Diving Lifetime 

Achievement Award from the American Academy of Underwater 

Sciences. 

Peter W. Glynn hails from Coronado Island, southern California. 

Peter graduated from Stanford University in 1963 with a Ph.D. 

in biological sciences. Peter’s doctoral research at Stanford was 

performed at the Hopkins Marine Station (Pacific Grove) and 

involved the trophic relationships of an intertidal community; 

Donald P. Abbott served as his advisor. Following graduation 

he joined the Institute of Marine Biology, University of Puerto 

Rico (Mayagüez, 1960–1967), then moved to the Smithsonian 

Tropical Research Institute (Panama, 1967–1983). In 1983 Peter 

joined the faculty of the Rosenstiel School of Marine and Atmospheric Science, University of Miami, where he is currently a 

professor in the Division of Marine Biology and Fisheries. Peter’s 

main research interests have centered on coral reef ecology, with 

specialization in biotic interactions (predation, mutualisms), 

coral community structure, species diversity, reef accretion and 

distribution, biogeography, and disturbances to reefs, especially 

coral reef bleaching and El Niño disturbances.

Steven H. D. Haddock is a research scientist at the Monterey Bay 

Aquarium Research Institute and an adjunct associate professor 

at the University of California, Santa Cruz. His work focuses 

on gelatinous plankton, in particular ctenophores and siphonophores, and on bioluminescence, a common property among 

these animals. He has been conducting blue-water dives as part 

of his research for the last 20 years, since learning from some of 

the pioneers of the technique. Some of his most enjoyable experiences have been night dives to study bioluminescence and 

Humboldt squid behavior, and diversity surveys of plankton in 

Pacific, Atlantic, and Mediterranean habitats. With John Heine 

he has written a book promoting blue-water diving as a unique 

and irreplaceable method of experiencing the open ocean and 

upper water column.

William M. Hamner obtained a B.A. in zoology from Yale (1961) 

and Ph.D. in zoology from UCLA (1965). Bill’s dissertation and 

early research was on photoperiodic control of the annual testicular cycles of birds. He was assistant professor of zoology (1966–

1972) and associate professor of zoology and environmental 

sciences (1972–1974) at UC Davis. From 1971 to 1972 he and 

a group of highly gifted graduate students spent 15 months in 

Bimini scuba diving in the Gulf Stream to investigate gelatinous 

zooplankton; the research was funded by NSF, Guggenheim, and 

the National Geographic Society. He was a principal research scientist at the Australian Institute of Marine Science (1974–1977) 

and adjunct professor (1978–1988) and professor (1988–2004) 

at UCLA. Bill is now a professor emeritus at UCLA and an adjunct senior scientist at Dauphin Island Sea Lab, University of 

South Alabama. Bill and Research Associate Peggy Hamner have 

investigated oceanic zooplankton using scuba in Australia, Palau, 

Antarctica, and the western north Pacific.

Catherine Drew Harvell received her Ph.D. from the University 

of Washington in 1985. After receiving NATO and NSF postdoctoral fellowships she joined the faculty of Cornell University in 

1986 as a professor of ecology and evolutionary biology. Drew is 

recognized for chairing both the World Bank Targeted Research 

Program on Coral Disease and the National Center for Ecological Analysis and Synthesis (NCEAS) Program on the Ecology 

of Marine Disease. Drew’s analyses and papers have led to the 

now-widespread acceptance that diseases in marine ecosystems 

are important, particularly in the very climate-sensitive coral 

reef ecosystems. Drew has worked for many years on coral reefs 

in the Mexican Yucatan and Florida Keys and, more recently, 

in Hawaii, Palau, the Philippines, and Australia. She has been a 

sabbatical fellow at NCEAS and vice president of the Society of 

American Naturalists, is a senior scientist at The Kohala Center 

in Hawaii, and serves on the editorial board of Annual Reviews 

of Ecology, Evolution and Systematics.

William F. Herrnkind received his B.S. in biology in 1961 from 

the State University of New York at Albany. His scientific diving 

career began in 1961 at the University of Miami Marine Laboratory (now Rosenstiel School of Marine and Atmospheric Science), where he earned his M.S. and Ph.D. In 1967, as an assistant 

professor at Florida State University (FSU), he initiated research 

using scuba and other underwater technologies to study mass 

single-file migrations by spiny lobster, which he first witnessed in 

the field as a graduate student. This propelled his career research 

on behavior and ecology of spiny lobsters and other crustaceans. 

Bill taught animal behavior and invertebrate zoology and created 

educational outreach programs at the FSU Marine Laboratory, 

which he directed from 1981 to 1985. Bill was instrumental in 
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establishing FSU’s first scientific diving program for safety and 

training. Florida State University awarded him several prizes for 

both teaching and outreach, as well as a named professorship for 

academic excellence. Bill retired in 2007.

Anson H. “Tuck” Hines is director and marine ecologist at the 

Smithsonian Environmental Research Center on Chesapeake 

Bay, which conducts research and education on linked ecosystems of the coastal zone. He has a B.A. in zoology from Pomona 

College and a Ph.D. in zoology from the University of California, 

Berkeley. He has conducted research on coastal ecosystems in 

Chesapeake Bay, Florida, California, Alaska, Belize, Japan, and 

New Zealand. He has published more than 125 papers and has 

been project leader on a diverse array of research programs, including programs on the effects of thermal discharges of coastal 

power plants; sea otters and kelp forest ecology; long-term ecological change in Chesapeake Bay; blue crab ecology; marine 

food web dynamics; the impacts of fisheries, aquaculture, and 

fishery restoration; crustacean life histories, especially crabs; and 

biological invasions of coastal ecosystems.

Mark A. Hixon was introduced to scuba by Lloyd Bridges (via 

TV’s Sea Hunt), Jacques Cousteau (also via TV), and Bill Brisby 

(his high school marine biology teacher). Starting with undersea 

research as an undergraduate in the early 1970s, Mark has used 

scuba to study kelp forest fishes in California (based at UC Santa 

Barbara) and a variety of coral reef fishes in a broad range of 

Pacific and Atlantic locations (based at the University of Hawaii, 

University of the Virgin Islands, James Cook University, and Oregon State University). An endowed professor at the University 

of Hawai’i at Manoa, Mark is past chair of both the Marine 

Protected Areas Federal Advisory Committee (for the National 

Oceanic and Atmospheric Administration and the Department of 

the Interior) and the Ocean Sciences Advisory Committee for the 

National Science Foundation. He currently studies the invasion 

of Atlantic coral reefs by Pacific lionfish.

Sally J. Holbrook is a professor of ecology in the Department of 

Ecology, Evolution and Marine Biology at the University of California, Santa Barbara. She is co–principal investigator of two NSF 

Long Term Ecological Research (LTER) programs: the Moorea 

Coral Reef LTER and the Santa Barbara Coastal LTER. Sally is 

a member of the NSF LTER Network Executive Committee, is a 

coorganizer of the international Coral Reef Environmental Observatory Network (CREON; www.coralreefeon.org), is the faculty director of the Santa Cruz Island Natural Reserve of the UC 

Natural Reserve System, and has served on the editorial board of 

the Ecological Society of America. Her research explores factors 

that influence population and community dynamics on subtidal 

temperate and tropical marine reefs. She has a particular interest 

in the role of biotic interactions and resource constraints, and in 

the links between individual-, population-, and community-level 

responses to short- and long-term environmental drivers.

Nicholas A. Kamenos received a B.Sc. (Hons) in marine biology 

from the University of Wales, Bangor, in 2000 and his Ph.D. in 

marine biology from the University of London in 2004. Nick is 

a research fellow in the School of Geographical and Earth Sciences and honorary lecturer in the School of Life Sciences at the 

University of Glasgow. His research interests include investigating relationships between global change (e.g., climate variability 

and ocean acidification) and marine ecosystems; development of 

ultra-high-resolution paleoclimatic and paleoecological proxies 

for the Holocene; and investigating if and how fisheries affect 

the expected responses of marine ecosystems to global change.

Brenda Konar is a professor in the School of Fisheries and Ocean 

Sciences at the University of Alaska Fairbanks (UAF). She holds 

a Ph.D. from the University of California, Santa Cruz. Her research expertise is in phycology, biodiversity, and nearshore and 

benthic ecology. She teaches the UAF scientific diving course at 

Kasitsna Bay and is a principal researcher in NaGISA, a Census 

of Marine Life Program. Brenda’s current research includes mapping and characterization of Alaska’s unexplored Arctic coastal 

rocky habitats (funded by NOAA/OE); epifaunal communities 

in the Chukchi and Beaufort Seas (funded by BOEMRE); and 

kelp forest interaction webs in the Aleutian archipelago, namely 

patterns and mechanisms of change following the collapse of an 

apex predator (funded by NSF).

Michael A. Lang is senior fellow at The Ocean Foundation and 

multiterm president of the American Academy of Underwater 

Sciences (AAUS). He was recruited as Smithsonian scientific diving officer in 1990, concurrently served as director of the paninstitutional Marine Science Network from 1998 to 2011, and 

as National Science Foundation Polar Programs Diving Officer 

from 2001 to 2011. Michael was a staff marine biologist at San 

Diego State University from 1982 to 1989. He is the 1991 DAN/

Rolex Diver of the Year and recipient of the 2000 Undersea and 

Hyperbaric Medical Society’s Craig Hoffmann Diving Award, 

the 2008 AAUS Conrad Limbaugh Scientific Diving Leadership 

Award, the 2009 Diving Equipment and Marketing Association’s Reaching Out Award and Diving Hall of Fame admission, 

and the Academy of Underwater Arts and Sciences 2010 NOGI 

Award for Science. Michael received his D.Phil. in environmental 

physiology from the Norwegian University of Science and Technology in Trondheim and pursues research interests in polar regions, marine conservation, and diving safety.

Howard R. Lasker is a marine ecologist whose research focuses 

on Caribbean octocorals as an instrument for studying the processes controlling coral reef cnidarians. A theme in much of 

his research is the manner in which colonization interacts with 

morphology and reproduction in controlling population dynamics. Much of his research has been conducted at the Smithsonian Tropical Research Institute in Panama. He has also worked 

at a variety of other Caribbean sites ranging from Belize to the 
254 • smithsonian contributions to the marine sciences

Bahamas, as well as on the Great Barrier Reef. His current research focuses on the reproduction and population connectivity 

of gorgonians in the Bahamas. All of his work involves extensive 

use of scuba. Howard received B.S. and M.S. degrees from the 

University of Rochester and a Ph.D. from the University of Chicago. He currently is professor of geology and director of the 

Graduate Program in Evolution, Ecology, and Behavior at the 

University at Buffalo. 

Harilaos A. Lessios received his Bachelor’s degree from Harvard 

University in 1973 and his Ph. D. from Yale University in 1979. 

Haris has worked at the Smithsonian Tropical Research Institute (STRI) ever since, rising to the rank of senior scientist. Since 

2007 he has also been an adjunct professor at the Department of 

Biology at McGill University. He also served as deputy director 

and director of marine research at STRI. Most of his field work 

was done in the San Blas Archipelago on the Caribbean coast of 

Panama, and in recent years he has been concentrating on questions of speciation and molecular evolution of marine organisms 

with special emphasis on sea urchins. He has published approximately 70 papers in peer-reviewed journals, and is a fellow of the 

American Association for the Advancement of Science. He was 

the editor of the proceedings of the eighth International Coral 

Reef Symposium, held in Panama in 1996.

Don R. Levitan is a professor in the Department of Biological 

Science at Florida State University. Don is interested in the ecology and evolution of marine invertebrates. His work examines 

the interaction of ecology, behavior, and water flow on shaping 

the evolution of reproductive strategies and patterns of speciation. He addresses these topics by integrating field work with 

molecular analyses and theory. Before entering graduate school, 

he taught diving and how to use scuba as a research tool in the 

Florida Keys and the U.S. Virgin Islands. Spending time under 

water taught Don to appreciate the biology of an organism in 

the context of the environment in which it lives. His current field 

sites are in the cold waters off of British Columbia, Canada, 

where he studies the evolution of gamete traits in sea urchins, 

and in the warm waters of the Caribbean, where he examines 

reproductive isolation and speciation in corals.

Mark M. Littler and Diane S. Littler are marine scientists who 

have developed a unique collaborative relationship. Diane is formerly a Research Associate at the Smithsonian Institution and 

an Adjunct Research Scientist at Harbor Branch Oceanographic 

Institute, Florida Atlantic University. Mark is formerly a Senior 

Scientist at the National Museum of Natural History. Diane and 

Mark each have more than 30 years of scuba experience on coral 

reefs, with more than 195 papers and books published in a wide 

range of disciplines. Their research has taken them around the 

world in search of unexplored marine habitats, often to areas 

of exceptional diversity or places in danger of biodegradation. 

These include Southern California, the Pacific and Atlantic 

coasts of Panama, the Sea of Cortez, the Galapagos Islands, the 

Mediterranean Sea, Morocco, Western Sahara, the Seychelles Archipelago, the Australian Great Barrier Reef, the Hawaiian Islands, Palau, Guam, Tahiti, the Cook Islands, American Samoa, 

Great Astrolabe Reef, Fiji, the Solomon Islands, Papua New 

Guinea, French Guiana, and many island nations of the Caribbean. Mark and Diane’s recent research has focused on relative 

dominance theory, functional morphology, and complex topdown versus bottom-up interactions in coral reef systems. Other 

active research includes monographic, floristic, and phylogenetic 

systematics; seaweed experimental taxonomy; and biodiversity, 

ecology, and conservation of tropical marine ecosystems. Their 

series of user-friendly field guides is now focused on the unique 

and rich flora of Panama, both Caribbean Panama (San Blas Islands, Isla Escudo de Veraguas, and Bocas del Toro) and Pacific 

Panama (Archipelago de las Perlas, Gulf of Panama, Gulf of 

Chiriquí, and Coiba National Park).

Ian G. Macintyre is a research scientist in the Department of 

Paleobiology in the National Museum of Natural History. He 

received his B.Sc. from Queen’s University, Ontario, Canada, in 

1957 and his Ph.D. from McGill University, Montreal, Canada, 

in 1967. He joined the Smithsonian staff in 1970 after three years 

of research at Duke University Marine Laboratory. He is a carbonate petrologist and sedimentologist with a multidisciplinary 

interest in the postglacial history of coral reefs, submarine lithification, skeletal mineralogy of reef organisms, bioerosion, and 

Holocene sea level history. Ian developed the first submersible 

hydraulic drill used in the study of reef history. It enabled him, 

and subsequently many others, to collect cores from reefs at their 

entire depth range. In 1996 he received the Darwin Medal from 

the International Society for Reef Studies. Ian was an original 

member of the scientific team that established Smithsonian’s research activities in Belize in 1972.

Laurence P. Madin is the executive vice president and director 

of research, and a senior scientist, at the Woods Hole Oceanographic Institution (WHOI) in Woods Hole, Massachusetts. Previously Larry has been chair of the WHOI Biology Department 

and director of the WHOI Ocean Life Institute. Larry received 

his A.B. from the University of California, Berkeley and his Ph.D. 

from UC Davis, and has been at WHOI since 1974. His principal research interests are in the biology of oceanic and deep-sea 

zooplankton, particularly medusae, siphonophores, ctenophores, 

and pelagic tunicates. Larry has been a diver since 1970, and was 

among the first biologists to use scuba and submersibles for the 

in situ study of oceanic plankton. He has participated in more 

than 70 research cruises. Larry holds an adjunct appointment at 

the Monterey Bay Aquarium Research Institute, and is a member 

of the American Geophysical Union, Association for the Sciences 

of Limnology and Oceanography, Sigma Xi, and several advisory 

boards.

Daniel P. Malone is a data analyst and field ecologist with an M.S. 

in marine science working at the University of California, Santa 
number 39 • 255

Cruz, as a part of the Partnership for Interdisciplinary Studies 

of Coastal Oceans (PISCO). Dan has used scuba for research in 

African Rift Valley lakes, on coral reefs in the Caribbean and Pacific, under Antarctic ice, and in California kelp forests. During 

the past 15 years he has been involved with long-term monitoring studies of kelp forest ecosystems, including restoration projects on artificial reefs, kelp forest related fisheries, shore-based 

impacts to kelp forests, and other projects. His current research 

activities include integrating a variety of collected data to monitor and evaluate the performance of California’s expanding 

network of marine protected areas, and a study that combines 

oceanographic modeling and genetic parentage analysis to examine the connectivity of fish populations living in kelp forests.

Roberta L. Marinelli is the director of the Wrigley Institute for 

Environmental Studies at University of Southern California and 

the former program director for the Antarctic Organisms and 

Ecosystems Program in the Antarctic Sciences Division at the 

National Science Foundation. Previously she was an associate 

professor at University of Maryland’s Center for Environmental Science, where her research included the ecology and biogeochemistry of nearshore and continental shelf environments 

with funding from the National Science Foundation, the Office 

of Naval Research, and Maryland Sea Grant. Her projects have 

taken her to the Pacific Northwest, the southeastern USA, and 

the shores of Nova Scotia. 

Adam G. Marsh received his Ph.D. in marine science from the 

University of Maryland in 1989 while working at the Chesapeake Biological Laboratory, Solomons Island, Maryland. Recognizing the oncoming revolution in cell and molecular biology 

at that time, he pursued postdoctoral research appointments in 

cell biology, molecular biology, immunology, and molecular ecology. In 2000 he was hired as an assistant professor at the University of Delaware School of Marine Science, where he is currently 

an associate professor. He has been involved with Antarctic research since 1994 and has logged more than 100 dives under 

the sea ice at McMurdo Station. He has authored more than 50 

peer-reviewed journal publications, holds one U.S. patent with 

a second patent now pending, and is the cofounder of a biotech 

startup focusing on microbial gene and protein bioengineering 

under harsh/extreme bioreactor conditions. 

George I. Matsumoto is a senior educational and research specialist at Monterey Bay Aquarium Research Institute. He received his 

Ph.D. from UCLA. His research interests are open ocean and deep 

sea communities; ecology and biogeography of open ocean and 

deep sea organisms; functional morphology; and natural history 

and behavior. He manages several education and outreach programs, including collaborations with the Monterey Bay Aquarium Research Institute’s sister organization, the Monterey Bay 

Aquarium (MBA). Dr. Matsumoto served on the Digital Library 

for Earth System Education (DLESE) Steering Committee and the 

2004 NSF Committee of Visitors for Geoscience Education, and 

is currently serving on the National Ocean Studies Board and the 

national advisory boards for the Center for Microbial Oceanography: Research and Education (C-MORE) and the Centers for

Ocean Sciences Education Excellence (COSEE). He was originally 

certified by the UC Berkeley Scientific Diving Program and used 

scuba extensively for his Ph.D. research. He still dives for both 

research and enjoyment, including volunteering for feeding shows 

in the MBA kelp forest tank.

James B. McClintock is the Endowed University Professor of 

Polar and Marine Biology at the University of Alabama at Birmingham (UAB). Jim received his B.S. degree from the University 

of California, Santa Cruz (UCSC) in 1978 and his doctoral degree from the University of South Florida in 1984. In 1987, after 

completing an NSF Postdoctoral Fellowship at UCSC, he joined 

the faculty of the Department of Biology at UAB. He became a 

full professor at UAB in 1997 and Endowed University Professor 

of Polar and Marine Biology in 2003. Jim’s research focuses on 

aspects of marine invertebrate nutrition, reproduction, and primarily, chemical ecology. He has published more than 230 peerreviewed scientific publications. In 2001 he was selected as the 

winner of the Wright A. Gardner Award for the most outstanding 

scientist in the state of Alabama. He is an elected fellow of the 

American Association for the Advancement of Science. In 1998 

the United States Board on Geographic Names designated the 

geographic feature McClintock Point in honor of his contributions to Antarctic science. 

Mónica Medina obtained her undergraduate degree in biology 

from Universidad de Los Andes in Colombia. However, her fascination with the sea took her to an internship at the Naos Marine 

Laboratory at the Smithsonian Tropical Research Institute in 

Panama. Subsequently, she obtained her Ph.D. in marine biology 

at the University of Miami. Mónica did postdoctoral work at the 

Marine Biological Laboratory in Woods Hole, Massachusetts, 

and at the California Academy of Sciences in San Francisco. She 

spent several years at the Joint Genome Institute as a research 

scientist. In 2005, she became founding faculty of the new campus of the University of California, Merced. She currently studies 

the genomics of coral reef symbioses and the evolution of metazoan biomineralization.

Jessica U. Meir is a comparative physiologist interested in the 

physiology and adaptations of animals in extreme environments. 

Jessica is currently an assistant professor of anesthesia at Harvard Medical School and a former NSF-funded postdoctoral 

researcher at the University of British Columbia, where she researched hypoxia tolerance in the high-flying bar-headed goose.

She received her Ph.D. at the Scripps Institution of Oceanography studying diving physiology of marine mammals and birds. 

Jessica’s work focused on blood oxygen transport and depletion 

in diving emperor penguins in the Antarctic and elephant seals 

in California. Jessica received her bachelor’s degree in biology 

at Brown University and master’s degree from the International 
256 • smithsonian contributions to the marine sciences

Space University in France. Before pursuing her Ph.D. she worked 

as a scientist for human physiology space research at NASA’s 

Johnson Space Center, coordinating, supporting, and training 

astronauts for experiments on the U.S. Space Shuttle and International Space Station. 

Amy L. Moran is professor at University of Hawaii at Manoa’s 

Biology Department and Marine Biology program. Prior to 

2013 she worked in the Department of Biological Sciences at 

Clemson University for eight years as a researcher and teacher 

of marine biology, invertebrate biology, and Antarctic science 

and at the Department of Marine Sciences at the University of 

North Carolina at Chapel Hill. Amy did postdoctoral work on 

marine invertebrate ecology and physiology at the University 

of Southern California and the University of Washington. Her 

research focuses on adaptive responses of marine invertebrate 

animals to environmental change, with particular emphasis on 

the early and most vulnerable life history stages—eggs, embryos, and larvae. Her work has taken her to the tropics, the 

Antarctic, and many temperate parts of the world to examine 

closely related animals living in contrasting and often extreme 

habitats. 

Mark R. Patterson is professor of marine science at the College 

of William and Mary, Virginia Institute of Marine Science. Mark 

holds an A.B., A.M., and Ph.D. in biology from Harvard University. He directs the Autonomous Systems Laboratory, where 

free-swimming robots are designed and built. His research interests are grounded in the interdisciplinary fields of marine ecology 

and biomechanics. Mark uses autonomous underwater vehicles 

to make new discoveries such as coherent structures of lowered 

oxygen over coral reefs, how krill swarms in the Antarctic appear 

on high frequency side scan sonar, and how to identify fishes 

from their side scan sonar images using neural network processing. He also applies chemical engineering theory to the allometry 

of metabolism of lower invertebrates and algae. 

Valerie J. Paul is currently director of the Smithsonian Marine 

Station at Fort Pierce in Florida. She received her B.A. from the 

University of California, San Diego in 1979 with majors in biology and studies in chemical ecology and her Ph.D. in marine 

biology in 1985 from the Scripps Institution of Oceanography. 

Valerie joined the faculty of the University of Guam Marine Laboratory in 1985, serving as director of the laboratory from 1991 

to-1994 and as full professor from 1993 to –2002. Valerie’s research interests include marine chemical ecology, marine plant–

herbivore interactions, coral reef ecology, and marine natural 

products. She was elected a fellow of the American Association 

for the Advancement of Science in 1996 and was elected and 

served as chairperson of the Marine Natural Products Gordon 

Research Conference in 2000. Valerie currently serves on the editorial boards of the journals Coral Reefs and Journal of Natural Products. Valerie and her collaborators have published more 

than 190 research articles in journals and books.

Joseph R. Pawlik received his B.S. in biology from the University 

of Minnesota, Twin Cities (1982), and his Ph.D. in marine biology from Scripps Institution of Oceanography, UC San Diego 

(1988). Joe is a professor in the Department of Biology and Marine Biology at the University of North Carolina, Wilmington, 

where he teaches an undergraduate course in invertebrate zoology and directs a research program involving undergraduate and 

graduate students. He and his collaborators have authored more 

than 100 publications in the scientific literature, primarily on the 

ecology of invertebrates on Caribbean coral reefs. 

John S. Pearse’s undergraduate studies at the University of Chicago (1955–1958) led to Stanford University and marine biology. 

John’s doctoral work examined reproductive timing of marine 

invertebrates at McMurdo Station, Antarctica. A faculty position 

at the American University of Cairo (1964–1967) allowed him 

to continue that work in the Red Sea. In 1968 he joined Wheeler 

North’s program at California Institute of Technology to examine reproductive biology of sea urchins in kelp beds of southern 

California. He joined the faculty of the University of California, 

Santa Cruz in 1971 and began research in nearshore ecology. 

Research and teaching programs took him back to the Antarctic 

as well as to Bermuda and around the tropical western Pacific. 

Among his awards, he is most proud of teaching awards from 

the American University of Cairo and the University of California, Santa Cruz; but he feels the wonderful creatures in his field 

courses deserve the credit. John retired in 1994 but continues to 

teach, conduct research, and write as a professor emeritus.

Daniel C. Reed received his Ph.D. in biological sciences at the 

University of California in 1989. Dan is currently a research biologist in the Marine Science Institute at the University of California, Santa Barbara, and the lead principal investigator of the 

Santa Barbara Coastal Long Term Ecological Research Program 

funded by the National Science Foundation. His primary research 

interests pertain to the ecology of coastal marine ecosystems and 

the ecological and physical processes that structure them. Much 

of Daniel’s work has focused on determining the mechanisms 

that allow these systems to recover from natural disturbance and 

then applying this knowledge to restoration programs designed 

to mitigate impacts caused by human disturbance. Giant kelp 

forests and sea grass beds have been the focal ecosystems for 

most of Dan’s research, which includes studies on dispersal, recruitment, reproduction, population dynamics, community ecology, primary production, and trophic interactions.

Rafael Riosmena-Rodríguez is professor and leader of the Marine Botany Research Group of Universidad Autónoma de Baja 

California Sur in La Paz, Baja California Sur, Mexico. He obtained his Ph.D. from La Trobe University in 2002. Professor 

Riosmena is deeply interested in understanding the role of marine plants and algae in coastal habitats and their evolutionary 

significance. His research includes systematics, biogeography, 

and ecology of marine plants from subtropical habitats. Rodrigo 
number 39 • 257

is an expert in rhodoliths, free-living forms of nongeniculate coralline red algae (Corallinaceae, Rhodophyta) that form extensive 

beds over broad latitudinal and depth ranges with wide morphological variations in response to physical factors. 

Raphael Ritson-Williams is a research technician who has been 

conducting research at the Smithsonian Marine Station at Fort 

Pierce since 2002. He recently became a Ph.D. candidate at the 

University of Hawaii at Manoa. He is interested in the evolutionary ecology of coral reefs. Especially important are the processes that promote reef recovery after a disturbance. Raphael’s 

research expertise is in marine chemical ecology and larval ecology, both of which contribute to coral recruitment, which can 

increase reef resilience. At the University of Hawaii he studies 

population genetics to better understand the role of individual 

variation and resistance in response to stress. This research will 

help illuminate how natural and anthropogenic disturbance can 

shape genetic diversity of coral populations. 

Susan J. Roberts became the director of the National Research 

Council’s Ocean Studies Board in 2004. She received her Ph.D. 

in marine biology from the Scripps Institution of Oceanography, 

where she studied the biochemistry of fish muscle and discovered a 

symbiotic bacterium in the gills of the deep sea bivalve Xylophaga 

washingtona. She was a postdoctoral fellow at UC Berkeley in developmental biology and then moved east to take a position at the 

National Cancer Institute. In 1998 Susan joined the staff of the 

Ocean Studies Board, where she has directed a variety of ocean 

policy studies on topics such as marine protected areas, fisheries 

science and management, and coastal processes. She is a past president of the Washington, D.C. chapter of the Association for Women 

in Science and a fellow of the Washington Academy of Science.

Laura Rogers-Bennett received her B.A. from the University of 

New Hampshire after conducting subtidal research with Dr. Larry 

Harris. She completed an M.S. at the University of Massachusetts 

Boston by working with green sea urchins in nearshore kelp beds. 

After moving to California, she completed her Ph.D. in ecology 

at the University of California (UC), Davis, and two postdoctoral 

fellowships, one at the UC Santa Cruz Institute of Marine Science 

and the other at the University of Washington Friday Harbor Laboratories. Laura is a senior biologist with the California Department of Fish and Game and a research associate at UC Davis at the 

Bodega Marine Lab. The work in her lab focuses on processes that 

impact marine populations and communities and how to apply 

findings to resource assessment, fishery management, and marine 

conservation. Laura has been an active research diver for more 

than 30 years, co-teaches the research dive classes at UCD, and is 

chair of the UCD diving control board.

Russell J. Schmitt is a professor of ecology in the Department of 

Ecology, Evolution, and Marine Biology at the University of California, Santa Barbara. Russ is the lead principal investigator of the 

NSF Moorea Coral Reef Long Term Ecological Research (LTER) 

site and is an associate investigator on the Santa Barbara Coastal 

LTER. Russ directs the Coastal Research Center of UC Santa Barbara’s Marine Science Institute, is a scientific advisor to the California Coastal Commission on mitigating effects of the San Onofre 

Nuclear Generating Station on marine resources, and founded the 

UC-wide graduate training program in coastal toxicology. His 

research interests bridge population and community ecology. He 

explores the dynamics and regulation of subtidal reef populations 

as well as the interplay between direct and indirect species interactions in shaping the structure and dynamics of reef communities. 

All of Russ’s field research has involved scientific diving.

Kenneth P. Sebens is currently director of the University of 

Washington’s (UW) Friday Harbor Laboratories (since 2005) 

and A. O. Dennis Willows Director’s Endowed Professor of biology in the UW Department of Biology in Seattle. Ken received 

his B.A. from the University of Connecticut in 1972 and his 

Ph.D. from the University of Washington in 1977. He was previously at Harvard University, Northeastern University, University 

of Massachusetts Boston, and the University of Maryland. He 

conducts research on marine subtidal benthic populations and 

communities in both temperate and tropical locations. One ongoing project is an investigation of community and population 

dynamics and long-term change in rocky subtidal habitats in 

Massachusetts. He has authored more than 80 peer-reviewed

publications. Support for Ken’s research includes continuous 

funding from the National Science Foundation (since 1979) and 

facilities support from the National Oceanic and Atmospheric 

Administration and the Smithsonian Institution.

Diana L. Steller is a research biologist, lecturer, diving safety officer at Moss Landing Marine Laboratories and member of the 

board of directors of the American Academy of Underwater Sciences. Diana holds a B.A. in aquatic ecology from the University 

of California, Santa Barbara (1988), an M.S. in marine biology 

from Moss Landing Marine Laboratories (1993), and a Ph.D. in 

ecology and evolutionary biology from the University of California, Santa Cruz (2003). She has been working and teaching in the 

Gulf of California for the past twenty years. Her research interests include the ecology of temperate reefs and subtropical carbonate rhodolith beds with an emphasis on macroalgal ecology, 

algal physiology, and species interactions. Diana is particularly 

interested in the role that macroalgae play as a substrate and 

food resource in subtidal communities and in how algal dynamics influence community dynamics. 

Robert S. Steneck is a professor in the School of Marine Sciences 

at the University of Maine Darling Marine Center. He received a 

B.Sc. in biology/geology from Baldwin-Wallace College in 1973, 

an M.S. in botany and plant pathology from the University of 

Maine in 1978, and a Ph.D. in earth and planetary sciences from 

the Johns Hopkins University in 1982. Bob received a Pew Fellowship in marine conservation in 1998 and is a fellow of the 

American Association for the Advancement of Science. The focus 
258 • smithsonian contributions to the marine sciences

of Bob’s research is in situ ecology. His research interests are the 

structure and function of coastal marine ecosystems in the Gulf 

of Maine and the Caribbean. With his students Bob has explored 

kelp forest ecosystems, studying lobsters, sea urchins, and fish 

stocks. He has also worked extensively throughout the Caribbean and tropical Pacific studying coral reefs from biological and 

geological perspectives.

Tanya L. Streeter is a ten-time world record freediver, television 

presenter, and environmentalist. Born and raised in Grand Cayman and educated at Brighton University in England, Tanya’s 

10 freediving world records span six years and seven disciplines, 

including five absolute and two current world records. In 2003 

Sports Illustrated called her “The World’s Most Perfect Athlete.” 

In her quest to change the global misperception of her sport, 

Tanya has subjected herself to clinical physiological studies before, during, and after dives to facilitate a better understanding 

of freediving and safety. Her collaborations as an adventure and 

wildlife television presenter include series with the BBC, Animal 

Planet, and National Geographic. Tanya is a spokesperson for 

The Whale and Dolphin Conservation Society, The Coral Reef 

Alliance, Bite-Back (shark protection), and World Society for the 

Protection of Animals (WSPA); she is also patron to the Scuba 

Trust (a disabled diver charity). 

Phillip R. Taylor is the University of Southern California’s executive director of research advancement and federal relations 

and the former head of the Ocean Section in the National Science Foundation’s (NSF) Ocean Sciences Division. He received 

a Ph.D. from the University of California, Irvine, in ecology and 

evolutionary biology based on research on California coastal 

systems pertaining to the biological interactions and physical 

processes controlling the composition of species assemblages on 

shorelines. Following time in the professorate at the University of 

the Virgin Islands, a term as a visiting scientist at the Smithsonian’s National Museum of Natural History, and further research 

on the role of grazers in the control of community structure in 

Caribbean coral reef and mangrove ecosystems, Phil joined the 

NSF as a rotator in biological oceanography in 1985 and became 

director of the Biological Oceanography Program in 1988.

Karen B. Van Hoesen became a certified diver at age 17 and a 

diving instructor with the National Association of Underwater 

Instructors in 1983 while teaching diving at University of California, Davis. Her interest in diving physiology and medicine 

prompted her to attend Duke University Medical School and 

subsequently to collaborate with the Divers Alert Network and 

Duke Hyperbaric Center. She was the recipient of the Our World 

Underwater Scholarship in 1988. Karen is currently a clinical 

professor of medicine in emergency medicine at the University 

of California, San Diego (UCSD), and is board certified in both 

emergency medicine and undersea and hyperbaric medicine. She 

is also the director of the UCSD Diving Medicine Center and 

UCSD Undersea and Hyperbaric Medicine Fellowship. Karen is 

recognized as one of the world’s leading authorities on diving 

medicine. She loves opening up the underwater world to others 

and teaching all aspects of diving medicine, safety, and appreciation of the underwater environment.

Steve V. Vollmer received his Ph.D. from Harvard University in 

evolutionary biology. His research group at Northeastern University’s Marine Science Center in Massachusetts studies the evolutionary ecology of marine organisms, especially reef-building 

corals. Steve’s research has focused on how evolution shapes the 

genetic architecture of coral populations and species. The current focus of his lab is on the genetic bases of innate immunity, 

pathogen recognition, and host resistance in reef corals. Steve has 

a long-standing relationship with the Smithsonian Institution; 

his coral research is based at the Smithsonian Tropical Research 

Institute in Panama, where he worked as a Smithsonian Marine 

Science Network and Hoch Fellow from 2004 through 2010. 

James M. Watanabe received his Ph.D. in zoology from University of California, Berkeley. His background and research interests lie in the fields of invertebrate zoology and marine ecology, 

with particular emphasis on kelp forests and rocky intertidal 

communities. Jim has conducted research on the distribution 

and abundance of kelp forest invertebrates, the dynamics of sea 

urchin-mediated deforestations, and the physiological ecology of 

kelp (Macrocystis pyrifera and Pterygophora californica). These 

studies have focused on predator–prey interactions, interspecific 

competition, and the effects of disturbance on marine organisms. He is also interested in the statistical problems of detecting changes in natural populations through time. Jim’s primary 

responsibility at Stanford University’s Hopkins Marine Station 

is undergraduate teaching. During winter, spring, and summer 

quarters he teaches subjects ranging from introductory biology 

and invertebrate zoology to kelp forest ecology, experimental 

design, and statistics. His courses attempt to nurture an appreciation for the natural world through accumulation of detailed 

knowledge and hands-on experience.

Jon D. Witman grew up near the broad horizon of the ocean, 

which sparked his interest in large-scale marine ecology. Jon’s 

exposure to marine ecology began at Sandy Hook Marine Lab, 

New Jersey, where he studied the impacts of sewage dumping 

on marine life. After an independent study (University of Otago, 

New Zealand) he took two years off from university to explore 

the relatively pristine coral reefs of Fiji and the New Hebrides 

Islands. These contrasting early experiences shaped Jon’s present 

view of anthropogenic impacts in the oceans and the need for 

conservation. Jon conducted a Ph.D. in subtidal ecology in the 

Gulf of Maine (University of New Hampshire, 1984). A postdoc 

at Northeastern University’s Marine Science Center led to an assistant professorship there. Jon is currently a professor of biology 

at Brown University. His research interests include the effects of 

large-scale processes on local communities, benthic–pelagic coupling, biodiversity, and supply-sided and trophic ecology. 
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use the parentheses system for volume(number):pagination 

[e.g., “10(2):5–9”]. Do not use “et al.”; all authors/editors 

should be included in reference citations. In titles, capitalize 

first word, last word, first word after colon, and all other 

words except articles, conjunctions, and prepositions. Examples of the most common types of citations are provided in the 

SISP Manuscript Preparation and Author Style Guide. 

For questions regarding the guidelines, please email SISP at 

schol.press@si.edu. 

requirements for smithsonian series publication