1 of 1 1/30/07 3:31 PM

The Ecology and Oceanography of Harmful Algal Blooms

A National Research Agenda

Preface

For many years, the United States has struggled to manage fisheries resources and marine ecosystems 

impacted by an expanding array of toxic and harmful algae. Our understanding of the fundamental

ecological, toxicological, and oceano graphic issues underlying these phenomena, however, is woefully

inadequate. In recognition of this shortcoming, the Na tional Science Foundation (NSF) and the

National Oceanic and Atmospheric Administration (NOAA) co-sponsored a work shop on the Ecology

and Oceanography of Harmful Algal Blooms at the Snow Mountain Ranch Conference Center, CO 

from 23-28 August 1994. This research agenda is the result of those deliberations. The forty workshop

participants (Appendix A) included academic and government scientists as well as program managers

and officials representing the NSF, NOAA Coastal Ocean Program, Sea Grant, and the National Marine

Fisheries Service. The scientists attending the workshop were selected from among nationally

recognized leaders in fields spanning both the biological and physical sciences. The diverse composi

tion of the group (Appendix A) reflects the interdisciplinary nature of this subject as well as the need to 

solicit recommenda tions from the oceanographic community at large.

Position papers were prepared and distributed prior to the workshop so all participants would be 

familiar with the issues and questions associated with HABs. Selected participants were asked to

present summaries of issues reflecting their area of expertise and geographical focus. Specific theme

topics fell under the general categories of: Physiology, Biochemistry and Genetics; 

Food-web/Community Interactions; Nutrients and Eutrophication in the Coastal Environment ;

Physical/Biological Interactions; and, Emerging Technologies. Following these presentations and 

extensive plenary discussions, participants were divided into working groups and charged with

identifying research priorities, approaches and essential technologies in three theme areas: The 

Organisms, Environmental Regulation of Blooms , and Food-Web/Community Interactions. Alternating 

be tween working group sessions and plenary discussions, research issues and priorities were refined

for each of these program elements .

This national research agenda is being widely circulated to individual scientists, agency personnel, 

government officials and science administrators. Feedback is welcome at all stages and on all aspects of

this planning process.

Acknowledgements. The workshop was sponsored by the Division of Ocean Sciences of the National 

Science Foundation, and by the Coastal Ocean Program of the National Oceanic and Atmospheric

Administration. Maine and Texas Sea Grant Programs provided support for several participants, and the

Southeast Fisheries Science Center of the National Marine Fish eries Service in Charleston SC provided

staff support to help facilitate travel. Special thanks to Debbie Braddock and Ethel Le Fave for

administrative support, to C. R. Tomas, T.J. Smayda, and P.J.S. Franks for serving as working group 

chairs, and to P. Donaghy, G. J. Doucette, D.L. Garrison, R. A. Horner, J.J. Cullen, and F.G. Plumley

for their efforts as the Editorial Committee for this report.

Donald M. Anderson, Workshop Chair
1 of 5 1/30/07 3:31 PM

The Ecology and Oceanography of Harmful Algal Blooms

A National Research Agenda

Executive Summary

Over the last several decades, the United States has experienced an escalating and worrisome trend in 

the incidence of problems associated with harmful and toxic algae. Impacts of these phenomena include

mass mortalities of wild and farmed fish and shellfish, human illness and death from contaminated

shellfish or fish, death of marine mammals, seabirds, and other animals, and alteration of marine habitats

or trophic structure through shading, overgrowth, or adverse effects on life history stages of fish and

other marine organisms. Formerly only a few regions were affected by harmful algal blooms (HABs) in

scattered locations, but now virtually every coastal state is threatened, in many cases over large 

geographic areas and by more than one harmful or toxic species.

It is still a matter of debate as to the causes behind this expansion, with possible explanations ranging 

from natural mechanisms of species dispersal to a host of human-related phenomena such as nutrient

enrichment, climatic shifts, or transport of algal species via ship ballast water. Whatever the reasons,

virtually all coastal regions of the U.S. are now subject to an unprecedented variety and frequency of

HAB events. The U.S. is not alone in this respect, as nations throughout the world are faced with a

bewildering array of toxic or harmful species and impacts and disturbing trends of increasing inci dence.

HAB events are characterized by the proliferation and occasional dominance of particular species of 

toxic or harmful algae. As with most phytoplankton blooms, this proliferation results from a

combination of physical, chemical, and biological mechanisms and interactions that are, for the most

part, poorly understood. Some HABs are unique, however, due to their production of toxins and the

manner in which they affect co-occurring organisms and alter food-web function. As identified in

Marine Biotoxins and Harmful Algae: A National Plan (Anderson et al., 1993), focused research into

these ecological and oceanographic mechanisms is urgently needed. To achieve these ends, a workshop

was co-sponsored by NSF and NOAA to develop a national research agenda to guide activities in the

specific area of HAB ecology and oceanography.

The resulting program, called ECOHAB (ECology and Oceanography of Harmful Algal Blooms) 

provides a scientific framework designed to increase our understanding of the fundamental processes 

underlying the impacts and population dynamics of HABs. This involves a recognition of the many

factors at the organismal level that determine how HAB species respond to, and potentially alter their

environment, the manner in which HAB species affect or are affected by food-web and community

interactions, and how the distribution, abundance, and impact of HAB species are regulated by the 

environment.

In its simplest form, the goal of the ECOHAB program is:

To develop an understanding of the population dynamics and trophic impacts of harmful algal 

species which can be used as a basis for minimizing their adverse effects on the economy, public

health, and marine ecosystems.
2 of 5 1/30/07 3:31 PM

scientifically based management of fisheries resources, public health, and ecosystem health in

regions threatened by toxic and harmful algae.

ECOHAB is thus a scientific program that addresses important societal issues through advances in 

fundamental or basic research. The research priorities identified at the workshop fell naturally into three

main themes that represent the individual program elements of ECOHAB. The rationales, goals, and

specific objectives and activities of each program element are listed below.

Program Element # 1

The Organisms

Rationale: The negative impacts of HABs reflect not only the growth and metabolism of individual 

algal cells, but the ecological selection of those cells within a diverse phytoplankton assemblage. Studies

at the organismal level are essential if we are to understand the population dynamics of HABs and their

toxic and/or harmful effects.

Goal: To determine the physiological, biochemical, genetic, and behavioral features and mechanisms of 

harmful algal species that influence their bloom dynamics, general ecology, and negative impacts.

Specific objectives: 

· Develop methods to rapidly and accurately identify, enumerate, and physically separate HAB species

from mixed phy toplankton assemblages.

· Identify the life history stages of major HAB species, determine what factors control transitions

between those stages, and establish the role of the stages in bloom dynamics.

· Characterize the physiological responses and tolerances of HAB species to differing environmental

conditions.

· Develop methods to permit in situ measurements of species-specific rates of growth, photosynthesis,

and nutrient uptake,

and to assess the physiological condition of cells at different times and locations.

· Characterize the nutritional requirements, uptake and nutrient assimilatory characteristics of HAB

species.

· Determine the functional role of toxins and/or exudates produced by HAB species.

· Define the genetic basis of toxin production, elucidate toxin biosynthetic pathways, and determine how

toxin accumulation in cells is regulated.

· Investigate the mechanisms and importance of motility and other behaviors of HAB species.

Program Element # 2

Environmental Regulation of Blooms

Rationale: Concurrent with escalating influences of human activities on coastal ecosystems, the 

environmental and eco nomic impacts of HABs have increased over recent decades. It is therefore
3 of 5 1/30/07 3:31 PM

complex topic is environmental regulation, that is, the influence of environmental factors on the

population dynamics of harmful algal species and their competitors.

Goals: 1) Determine and parameterize the environmental factors that govern the initiation, growth, 

maintenance, dissipa tion and impacts of HABs; and 2) Formulate principles that explain similarities

between ecosystems during HABs and under stand how those systems are unique with respect to the

types of blooms that occur.

Specific objectives:

· Determine the extent to which HAB events reflect increases in growth rate versus physical transport,

immigration, and accumulation. Determine whether there is a specific suite of physical factors with

which known HABs are associated.

· Investigate physical and ecological processes that control the partitioning of nutrients within a system

and the relationship between nutrient inputs and population dynamics of HAB species.

· Investigate whether there are specific physical, chemical, and biological regimes or processes that are

associated with HAB events.

· Determine whether some ecosystems are more susceptible to HABs than others. If so, determine what

makes them unique and whether they share characteristics that can be used to anticipate HAB events in

other systems.

· Characterize HAB population dynamics, including the rate processes required in predictive models of

bloom incidence.

Program Element # 3

Food-Webs and 

Community Interactions

Rationale: The negative impacts of HABs are the result of complex interactions that begin at the 

phytoplankton community level and extend to upper trophic level compartments. Habitat physics, life

cycles, community structures, growth and grazing processes all combine to regulate the dynamics of the

HAB event. Therefore, studies on the impacts of trophic interactions in the selection and dynamics of

HABs, and conversely, the impacts of HAB events on trophic structure, processes and interac tions are

essential if we are to understand the ecology and oceanography of harmful algal blooms .

Goals: 1) Determine the impacts of trophic interactions on selection for, and dynamics of, HABs; and 

2) determine the impacts of HABs on trophic structure, processes and interactions.

Specific objectives:

· Determine the extent to which bloom formation results from a breakdown of grazing or from harmful 

species outcompeting other phytoplankton for limiting resources.

· Determine whether biological controls (e.g., grazers, allelopathy, pathogens) are the cause of bloom 

termination.

· Investigate how HAB effects on the food-web are controlled by toxin dynamics, food-web routing of 

toxins, and the differential susceptibility of species at higher trophic levels. Determine whether chronic,
4 of 5 1/30/07 3:31 PM

blooms and critical life cycle stages of target species.

· Determine whether high biomass (non-toxic) HABs adversely impact the food-web directly through

reduced food quality, or indirectly through environmental effects.

Program Implementation

The diverse nature of HAB phenomena and the hydrodynamic and geographic variability associated 

with different out breaks throughout the U.S. pose a significant constraint to the development of a

coordinated research initiative. Where other multi-investigator oceanographic research programs can

concentrate field activities on one specific area of the ocean (e.g., GLOBEC on Georges Bank), no

single ECOHAB study site could be identified that would permit all of the major biological and physical

features that underly HAB phenomena to be investigated. Given this diversity, the ECOHAB program 

will rely on comparisons among large-scale, regional field programs, on laboratory and mesocosm

studies by individual investigators or small groups, and on theoretical studies using new and existing

models to provide realistic and testable simulations of HAB dynamics in different oceanographic

systems. An integration of physical, chemical, and biological components is essential to all of these

approaches.

The ECOHAB Research Agenda outlines research priorities that are intended to guide agencies in the 

efficient allocation of resources targeted to HAB issues, and to help them formulate new,

multi-disciplinary HAB initiatives. The rate and extent of future progress will depend upon how the

recommendations in this report are received and implemented. State and federal agencies should use this

document to identify topics that they can support, and individual scientists should shape their specific

research programs to meet the perceived needs of the HAB community.

Despite the focus on ecology and oceanography and the exclusion of many other aspects of HAB 

phenomena, the scope of the issues to be addressed by ECOHAB exceed the resources of any one

agency or program. ECOHAB will be succesful only if a nationally coordinated interagency effort can

be implemented to focus research personnel, facilities, and financial resources to the common goals

outlined in this comprehensive national strategy. Nowhere else do the missions and goals of so many

government agencies intersect and interact as in the coastal zone where HAB phenomena are prominent. 

Every effort must be made to keep the program flexible, efficient and responsive to the needs of the

agencies that become partners in this endeavor. As soon as the participating agencies and programs are

identified, a Steering Committee will be appointed to oversee program implementation. Where

necessary, small working groups or sub-committees will be convened to address specific program

needs. Once ECOHAB is underway and research programs begin to accumulate results, regional and 

national workshops will be convened to identify common mechanisms and processes underlying the

diverse array of HAB phenomena and their impacts. One of the strengths of ECOHAB lies in this

"comparative approach," but resources must be allocated to facilitate the scientific communication that is

required for successful implementation.

Rationale and Benefits

The significant economic, public health and ecosystem impacts of HAB outbreaks are strong, practical 

motivations for a research program such as ECOHAB, made all the more pressing by the apparently

escalating trend in their incidence. The direct benefits to society from a research program of this kind are

many, and include management issues such as bloom detection and prediction, control or mitigation

strategies, site selection criteria for aquaculture, and assessment of impacts from altered nutrient loading,

dredging or other coastal zone activities. There are indirect benefits as well. For example, support of

multidisciplinary field HAB programs can address specific, practical problems while providing new 

techniques and basic scientific information relevant to plankton ecology and oceanography in general. In
5 of 5 1/30/07 3:31 PM

instruments. Methods are needed to "tag" target species with molecular probes and then enumerate cells 

or separate them from co-occurring organisms, and techniques must be developed to estimate in situ

growth rates or cell physiology. These are but a few examples of the areas where new technologies

developed to meet the objectives of ECOHAB can benefit all of oceanography.
1 of 4 1/30/07 3:31 PM

The Ecology and Oceanography of Harmful Algal Blooms

A National Research Agenda

1. Introduction

1.1 The Nature of Harmful Algal 

Bloom Phenomena

Among the thousands of species of microscopic algae at the base of the marine food chain are a few 

dozen which produce potent toxins. These species make their presence known in many ways, ranging

from massive "red tides" or blooms of cells that discolor the water, to dilute, inconspicuous

concentrations of cells noticed only because of the harm caused by their highly potent toxins. Blooms of

non-toxic micro- and macroalgae (seaweeds) also cause harm due either to indirect effects of biomass

accumulation (such as anoxia or habitat alteration) or to physical features (such as spines which lodge in 

fish gill tissue). Impacts of HAB phenomena include mass mortalities of wild and farmed fish and

shellfish, human illness and death from contaminated shellfish or fish, death of marine mammals,

seabirds, and other animals, and alteration of marine habitats or trophic structure.

The term "red tide" has been used to describe some of these phenomena, since in certain cases, 

microalgal species increase in abundance until they dominate the planktonic community and discolor the

water with their pigments. The term is mislead ing, however, since non-toxic species can also bloom and

harmlessly discolor the water or conversely, adverse effects can occur when algal cell concentrations are

low and the water is clear. Furthermore, blooms of benthic or planktonic macroalgae can have major

ecological impacts such as the displacement of indigenous species, habitat destruction, oxygen depletion, 

and even alteration of biogeochemical cycles. The causes and effects of macroalgal blooms are thus

similar in many ways to those associated with harmful microscopic phytoplankton species. The

scientific community now employs the term "harmful algal bloom" (HAB) to describe this diverse array

of bloom phenomena.

1.2 HAB Impacts

1.2.1 Public Health and Ecosystem Effects

One major category of public health impact from HABs occurs when toxic phytoplankton are filtered 

from the water by shellfish such as clams, mussels, oysters, or scallops, which then accumulate the algal

toxins to levels that are potentially lethal to humans or other consumers (Shumway, 1990). These

poisoning syndromes are named paralytic, diarrhetic, neuro toxic, and amnesic shellfish poisoning

(PSP, DSP, NSP, and ASP). Except for ASP, an alarming new syndrome that results in permanent

short-term memory loss in victims, all are caused by biotoxins synthesized by a group of marine algae 

called dinoflagellates. The ASP toxin is produced by diatoms, a group of phytoplankton that until

recently was considered free of toxins and generally harmless (Bates et al., 1989). A fifth human illness,

ciguatera fish poisoning (CFP), is caused by biotoxins produced by epibenthic dinoflagellates attached

to surfaces in many coral reef communities (reviewed in Anderson and Lobel, 1987). Ciguatera toxins

are transferred through the food chain from herbivorous reef fishes to larger carnivorous, commer cially

valuable finfish. In a similar manner, the viscera of commercially important fish such as herring, 
2 of 4 1/30/07 3:31 PM

Anderson and White, 1992). All of these poisoning syndromes occur within the U.S. and its territories.

Another HAB impact occurs when marine fauna are killed by microalgal species that release toxins and 

other compounds into the water (Box 1.2.1), or that kill without toxins by physically damaging gills or

by creating low oxygen conditions as bloom biomass decays. These impacts frequently occur at

aquaculture sites where caged fish cannot escape the harmful blooms. Farmed fish mortalities from

HABs have increased considerably in recent years, and are now a major concern to fish farmers and

their insurance companies. Wild fish, however, may also be affected. The list of finfish, shellfish and 

wildlife affected by microalgal toxins is long and diverse (Table 1) and accentuates the magnitude and

complexity of this one manifes tation of HAB phenomena. It does not, however, adequately document

the true scale of that impact.

We are only now beginning to recognize that there can be impacts from toxic blooms in virtually 

all compartments of the marine food-web due to adverse effects on viability, growth, fecundity,

and recruitment. As reviewed by Smayda (1992), toxins can move through ecosystems in a manner 

analagous to the flow of carbon or energy, and the impacts can thus be far-reaching and significant (Box

3.3.1). In this expanded context, it is evident that our present knowledge base is inad equate even to

define the scale and complexity of many HAB phenomena.

Blooms of macroalgae (seaweeds) can also be harmful, especially to seagrass and coral reef ecosystems 

and the food-webs dependent on those habitats. Nuisance seaweed species replace indigenous

macroalgae in the benthos and microscopic phytoplankton in the water column. They thus modify

benthic habitats, affect microbial and macrofaunal foodwebs, and alter key biogeochemical features of

coastal ecosystems. Because seaweeds are generally benthic organisms and inhabit inshore coastal

waters that mark the interface between land and sea, they are often the first primary pro ducers to be

impacted by nutrient inputs from land. Indeed, increased nutrient supply seems to be implicated in 

virtually all harmful seaweed blooms. A dramatic example of the impact of macroalgal blooms was seen

in Bermuda, where the green macroalga Cladophora prolifera formed widespread blooms of drifting, 

filamentous balls that overgrew seagrasses and corals in response to N and P enrich ment from

groundwater (LaPointe and O'Connell 1989). This bloom, which many consider to be the most dramatic 

ecological change in the recent history of Bermuda's waters, led to a dramatic decline in benthic species

diversity, including the commer cially-valuable calico clam.

1.2.2 Economic Impacts

The range of the economic impacts from HAB outbreaks and the magnitude of those costs have 

expanded with increasing public awareness, coastal development, and the growth of mariculture.

Shellfish quarantines, wild or farmed fish mortalities, and frightened consumers who avoid seafood

(including products which are totally safe) are well-known impacts of major blooms of harmful algae

(Ahmed, 1991). Adverse health effects and lost sales of fish and shellfish products are direct costs, but

constrained development or investment decisions in coastal aquaculture due to the potential for 

outbreaks of toxic algae are examples of indirect or hidden costs. Lost marine recreational opportunities

are also important indirect costs of harmful algal bloom incidents. Unfortunately, no national estimate of

the combined economic costs of HAB phenomena is available. Estimates from isolated, individual

events provide some indication of the scale of the problem:

· A single PSP outbreak cost the state of Maine an estimated $7 million in 1980 (Shumway et al., 1988).

PSP outbreaks are annual events in Maine, and several have been more severe than the 1980 event.

· An NSP outbreak in 1987-88 closed more than 400 km of North Carolina coastline for shellfishing

during the peak harvest ing season, causing economic losses estimated at $25 million (Tester et al.,

1991)
3 of 4 1/30/07 3:31 PM

ecosystem and economic impacts. At this writing, legislation is under consideration to have parts of

Long Island declared Disaster Areas as a result of a massive 1995 outbreak.

· In 1987, phytoplankton blooms of the diatom Chaetoceros convolutus were linked to the mortality of 

250,000 Atlantic salmon valued at over $500,000 (Rensel et al., 1989). In other years, blooms of the

flagellate Heterosigma carterae have caused farmed-fish mortalities in British Columbia and 

Washington state costing the industry $4-5 million per year (Horner et al., 1991).

· PSP was detected in the rich shellfish beds of Georges Bank in 1989, forcing the closure of those

offshore resources. The Georges Bank surf clam fishery alone, closed now for five successive years,

has an estimated annual value of $3 million (New England Fisheries Development Association).

· In 1917, the shellfish industry in Alaska produced 5 million pounds of product. Today, except for

aquaculture, the state's commercial shellfish industry is virtually non-existent as a direct result of

persistent product contamination by PSP (Neve and Reichardt, 1984). The value of the sustainable, but

presently unexploited, shellfish resource in Alaska is estimated to be $50 million per year.

· The Gulf coast of Florida experiences frequent red tides, often accompanied by dead fish washed up

on beaches, NSP -contaminated shellfish, and human respiratory problems due to toxins aerosolized by

the surf. Habas and Gilbert (1974) estimated a loss of $20 million per event, including losses to the

tourist industry, hotel/motel suppliers, commercial fisheries, and local governments for the expense of

beach cleanup.

· Domoic acid in razor clams and Dungeness crabs in Washington and Oregon in 1991 caused economic

losses estimated at $15-20 million (T. Nosho, pers. comm.). Losses included reduced tourist trade,

unemployment, reduced or delayed sales, lower prices, and bankruptcy for some commercial

processors. Commercial oyster growers experienced declines in both sales and prices during the peak

holiday period, although the oysters never contained detectable levels of domoic acid. Some losses

continue as razor clam seasons are shortened or closed due to the continued presence of domoic acid in 

some areas.

· The states of Maine, New Hampshire, Massachusetts, Rhode Island, Connecticut, Florida, California,

Oregon, Washington, and Alaska maintain annual shellfish monitoring programs to detect algal toxins in

shellfish. The total cost of these programs exceeds $1 million per year.

1.3 Recent Trends

The nature of the HAB problem in the United States has changed considerably over the last two decades 

(Box 1.3.1). Where formerly a few regions were affected in scattered locations, now virtually 

every coastal state is threatened, in many cases over large geographic areas and by more than

one harmful or toxic microalgal species. Few would argue that the number of toxic blooms, the 

economic losses from them, the types of resources affected, and the number of toxins and toxic species

have all increased dramatically in recent years in the United States and around the world (Anderson, 

1989; Smayda, 1990; Hallegraeff, 1993). Disagreement only arises with respect to the reasons for this

expansion. Possible explanations include: a) species dispersal through currents, storms, or other natural

mechanisms; b) nutrient enrichment of coastal waters by human activities, leading to a selection for, and

proliferation of, harmful algae; c) increased aquaculture operations which can enrich surrounding waters

and stimulate algal growth; d) introduction of fisheries resources (through aquaculture development)

which then reveal the presence of indigenous harmful algae; e) transport and dispersal of exotic HAB 

species via ship ballast water or shellfish seeding activities; f) long-term climatic trends in temperature,

wind speed, or insolation; g) increased scien tific and regulatory scrutiny of coastal waters and fisheries

products; and h) improved chemical analytical capabilities that lead to the discovery of new toxins and
4 of 4 1/30/07 3:31 PM

the benthos of shallow water bodies is an increasingly common phenomenon along virtually all of the

world's shorelines. Human activities, including deforestation, agriculture, and generation of domestic

and industrial wastewaters are increasing the concentrations and fluxes of nitrogen and phosphorus in

coastal waters that in turn enhance seaweed productivity leading to high biomass levels (see Box 1.3.2).

As with microalgal blooms, these trends are difficult to document statistically due to a lack of long-term

datasets, the number of species involved, and the lack of a simple measure of population size or harmful 

impact that can be tabulated for all outbreaks. Nevertheless, workers in the field are united in their

opinion that the problems are worse and the trends disturbing.
1 of 4 1/30/07 3:31 PM

The Ecology and Oceanography of Harmful Algal Blooms

A National Research Agenda

2. The ECOHAB Program

2.1 Why a National Program on HABs is Needed

If we accept that HAB problems are expanding and that they have multiple causes, both natural and 

human-assisted, what can be done about them in a practical sense? What information is needed to

efficiently manage affected marine resources, protect public and ecosystem health, encourage and

support aquaculture development, and contribute to policy decisions on coastal zone issues such as

waste or sewage disposal, aquaculture development, or dredging? If human activities are making the

HAB problem worse, how can that be verified, and what steps should be taken to minimize further 

impacts? These are important practical questions, and the apparent trends in HAB incidence make them

even more pressing. The need for applied, practical research on HAB bloom phenomena is clear.

However, the problems are complex, and will require a compre hensive research program that includes

basic and fundamental studies of HAB species, their environment, and the organisms that interact with

them or their toxins. The ECOHAB program has been designed to address these issues.

2.2 What is ECOHAB?

ECOHAB (ECology and Oceanography of Harmful Algal Blooms) is a scientific program designed to 

increase our under standing of the fundamental processes underlying the impacts and population

dynamics of HABs. This program addresses the many factors at the organismal level that determine

how HAB species respond to, and potentially alter their environment, the manner in which HAB species

affect or are affected by food-web and community interactions, and how the distribution, abundance,

and impact of HAB species are regulated by the environment.

In its simplest form, the goal of the ECOHAB program is to develop an understanding of the 

population dynamics and trophic impacts of harmful algal species which can be used as a basis

for minimizing adverse effects on the economy, public health, and marine ecosystems.

2.3 Evolution of the ECOHAB 

Initiative

The U.S. is not alone in its struggle with the expanding HAB problem. Nations throughout the world 

are faced with a diverse array of toxic or harmful species and impacts, and many of these countries are

poorly prepared for the threat posed to their coastal economies and ecosystems. As a result, international

agencies or organizations such as the Intergovernmental Oceanographic Commission (IOC) of

UNESCO, the International Council for Exploration of the Seas (ICES), the Scientific Committee for

Oceanic Research (SCOR), the European Union (EU) and the Asia Pacific Economic Cooperation 

Program (APEC) have all established programs or working groups focused specifically on HABs and

their impacts.

The IOC's HAB program is assuming a leadership role in the international arena. A series of workshops 
2 of 4 1/30/07 3:31 PM

From the outset, the IOC HAB program was intended to be a coalescence of national and international 

programs. On the international side, ICES established a working group on the Dynamics of Harmful

Algal Blooms which has planned several major field programs or pilot studies targeting key HAB

phenomena. However, due to the regional nature of many HAB problems, it is evident that these field

studies will involve individual countries or groups of neighboring countries, and not large multi-national

teams of investigators, as is often the case in international programs. At the national level, however, it

became clear that many countries did not have a national program or plan to attack HAB issues. In the 

U.S., this was true despite an array of problems associated with harmful algae and a long history of

HAB research. In order to rectify this lack of coordination of HAB problems in the U.S., a workshop

was convened in 1992 at the National Marine Fisheries Service laboratory in Charleston, SC. That

meeting produced the report " Marine Biotoxins and Harmful Algae: A National Plan "(Anderson et al., 

1993), which identified numerous impediments to progress in the HAB field and made specific 

recommen dations to address those impediments. In addition to identifying areas for future research, the

National Plan structured proposed HAB activities in a framework that helped agencies identify their

roles in the overall program.

A prominent gap in U.S. attempt to deal with HAB issues was immediately apparent - that dealing with 

the ecology and oceanography of the blooms. The National Plan identified this as an important area for

research, but a detailed scientific agenda was lacking and no agencies were actively supporting such

research. NSF and NOAA then co-sponsored a workshop at Snow Mountain Ranch Conference Center

in Colorado, involving participants representing an array of scientific disci plines, geographic regions,

and agencies. The goal was to integrate field, laboratory, and theoretical studies into a focused effort to

understand the fundamental issues underlying HABs and their impacts. The resulting ECOHAB 

program addresses these national needs, but it also represents a U.S. component of the international

HAB programs of IOC and ICES.

2.4 The ECOHAB Strategy

The objective of the ECOHAB program is to combine field, laboratory and modeling studies in a 

coordinated effort to characterize the physical, chemical and biological processes governing the growth,

distribution and impacts of HAB species.

Three program elements have been identified: The Organisms; Environmental Regulation of Blooms; 

and Food-web/Community Interactions. One challenge has been to design a program that could 

accomodate the wide array of HAB species, their impacts, and oceanographic regimes without being so

broad or diffuse that implementation would be impossible. Given this diversity, ECOHAB will rely on

coordinated, multi-investigator programs as well as projects by individual investigators or small groups.

The program will require at least three types of research, all of which will involve an integration of 

physical, chemical and biological components.

Laboratory or Mesocosm Studies. Carefully controlled studies of HAB species and their food chain 

interactions are needed, focusing on genetic, biochemical, behavioral and life history processes that are

important factors in the dynamics and impacts of blooms. These experimental studies will range from

the organismal to the ecosystem level.

Field Investigations. Multi-investigator, multi-disciplinary field studies of HAB species are needed to 

document the distri bution and dynamics of key elements of HAB ecosystems, emphasizing the complex

interactions between biotic and physical or chemical factors. Since no single field program could

possibly address the wide array of HAB phenomena, a series of regional field studies is envisioned, in

the expectation that this comparative approach will reveal differences and commonali ties when both

hydrographic regimes and ecosystems are compared. An underlying challenge in all of these studies will 
3 of 4 1/30/07 3:31 PM

incorporate field and labora tory measurements into realistic and testable simulations of HAB dynamics

in different oceanographic systems. Models will include conceptual studies in idealized flows that

examine how circulation patterns affect biological processes at the level of the individual, population,

community and ecosystem, as well as site-specific models that address mechanistic interactions of the

physics and biology within a particular oceanographic regime.

2.5 Rationale and Benefits

The significant economic, public health and ecosystem impacts of HAB outbreaks are strong, practical 

motivations for a research program such as ECOHAB, made all the more pressing by the apparently

escalating trend in their incidence. The direct benefits to society from a program of this kind are many,

and include management issues such as bloom detection and prediction, control or mitigation strategies,

site selection criteria for aquaculture, and assessment of impacts from altered nutrient loading, dredging

or other coastal zone developments. There are indirect benefits as well. For example, many of the

mechanisms underlying bloom formation by harmful algal species are the same as those responsible for 

blooms of other phytoplankton in the ocean. Multidisciplinary field HAB programs address a practical

problem while also providing basic scientific information relevant to plankton ecology and

oceanography in general.

Another compelling aspect of the ECOHAB program stems from the need to study individual HAB 

species, rather than mixed planktonic assemblages. New autecological techniques must be developed,

such as remote detection of bloom popula tions using swimming robots or moored instruments.

Methods are needed to "tag" target species with molecular probes and then enumerate or separate them

from co-occurring organisms, and techniques to estimate in situ growth rates or to deter mine the

physiological status of a species must be developed. These are but a few examples of the areas where 

new technolo gies developed to meet the objectives of ECOHAB can benefit all of oceanography.

2.6 ECOHAB Implementation

To address the many scientific issues outlined in this report, federal agencies must break away from the 

parochial view that has often dominated HAB research in the past. A comprehensive understanding of

the present status of coastal waters, and the manner in which those waters and their ecosystems will

respond to changes, both natural and human-assisted, cannot be achieved without effective interagency

cooperation, coordination and collaboration. Nowhere else do the missions and goals of so many

government agencies intersect and overlap as in the coastal zone where HAB phenomena are prominent. 

ECOHAB will be succesful only if a nationally coordinated interagency effort can be 

implemented to direct research personnel, facilities, and financial resources to the common goals

outlined in this comprehensive national strategy .

Thus far, the planning of the ECOHAB program has involved the NSF Division of Ocean Sciences, 

and several agencies or programs within NOAA, including the National Marine Fisheries Service, Sea

Grant, and the Coastal Ocean Program. As the science plan evolves, more state and federal agencies are

expected to join the program. The research agenda outlined herein is intended to guide these agencies in

the efficient allocation of resources targeted to HAB issues, and to help them formulate new,

multi-investigator, multi-disciplinary HAB initiatives as well. Joint interagency announcements of 

opportunity for re search support as well as interagency cooperation on the provision of needed

resources and facilities are thus possible. However, an additional feature of the ECOHAB program will

be a reliance on proposals submitted by individual investigators or small groups, in recognition of the

diversity of causative organisms, impacts, and oceanographic systems associated with HABs.

A Steering Committee has not yet been established, as that awaits a final indication of the agencies that 

will participate in ECOHAB. Once those issues are resolved, a committee will be selected to oversee
4 of 4 1/30/07 3:31 PM

identify common mechanisms and processes underlying the diverse array of HAB phenomena and their 

impacts. One of the strengths of ECOHAB lies in this "comparative approach" but resources must be

allocated to facilitate the requisite scientific communication.
1 of 23 1/30/07 3:32 PM

The Ecology and Oceanography of Harmful Algal Blooms

A National Research Agenda

3. ECOHAB Program Elements

Program Element #1

3.1 The Organisms

3.1.1 Introduction

Rationale: The negative impacts of HABs reflect not only the growth and metabolism of 

individual algal cells, but the ecological selection of those cells within a diverse phytoplankton

assemblage. Studies at the organismal level are essen tial if we are to understand the population

dynamics of HABs. 

The impact of harmful algal blooms (HABs) is a function of the growth and metabolism of individual 

algal cells ecologically selected from a diverse phytoplankton assemblage. Growth is a general term

reflecting photosynthesis, nutrient uptake and assimilation, and numerous other metabolic processes

within cells. The inherent growth characteristics of species are geneti cally determined, but the realization

of growth potential is often controlled by external environmental factors.

There is considerable diversity among HAB species with respect to strategies for growth and bloom 

formation in natural systems. Some cause harm at relatively low cell concentrations (e.g., DSP can occur

with only a few hundred Dinophysis cells per liter), but in other cases, population growth of HAB 

species results in a monospecific bloom at high concentrations (e. g., a red tide). There are numerous

explanations for that type of growth and accumulation, and many are rooted in the unique physiology of

the organisms involved. For example, it has long been argued that production of toxins or other 

exudates allows some species to outcompete co-occurring organisms (e.g., Pratt, 1966) or to deter

grazing (Huntley, 1982; Huntley et al., 1986; Ives, 1987). Practical demonstrations of these mechanisms

are few, however.

Another survival and growth strategy involves the benthic resting stages of many HAB species. These 

cysts or spores provide a recurrent "seed" source or inoculum for planktonic populations, and this

characteristic may be a critical factor in determining not only the geographic distribution of species, but

possibly their eventual abundance as well (Anderson and Wall, 1978; Anderson et al., 1983). Some

HAB species are motile, and under certain environmental conditions their swimming behavior may

result in formation of high-density patches (e.g., Kamykowski, 1974; Cullen and Horrigan, 1981; 

Franks, 1992). Diel vertical movement by motile cells in a stratified environment undoubtedly has

functional significance, for example, maximizing encounter frequencies for sexual reproduction,

minimizing grazing losses, and allowing cells to obtain nutrients at depth and light at the surface.

These diverse issues can be incorporated into the following goal for the Organisms program element of 

ECOHAB:
2 of 23 1/30/07 3:32 PM

3.1.2 Research Agenda

The following issues are considered high priorities in organismal research within ECOHAB:

Issue:

There is a need to rapidly and accurately identify, enumerate, and physically separate HAB 

species from mixed phytoplankton assemblages.

Positive identification and enumeration of specific algal species in discrete field samples collected over 

large temporal and spatial scales is a labor intensive, but necessary process for the characterization of

HABs. A common problem in research and monitoring programs focused on HAB species occurs

when the species of interest is only a minor component of the planktonic assemblage. Many potentially

useful measurements are simply not feasible because of the co-occurrence of other organisms and

detritus. Studies must thus rely on tedious microscope counts to enumerate the target species, and 

measurements of toxicity or other physiological parameters are generally not possible for just the species

of interest. Another constraint arises from the difficulties in adequately identifying and distinguishing

between species or strains which are morphologically simi lar. (see Box 3.1.2) Considerable time and

effort are often required to identify a particular species when its distinguishing characteristics are

difficult to discern under the light microscope. Such fine levels of discrimination are not generally 

feasible in monitoring programs or other studies which generate large numbers of samples for cell

enumeration.

At present, the time lag between sample collection and the identification and counting of specific 

organisms severely limits our ability to follow the population dynamics of HAB species in real-time. As

a consequence, we are limited in our ability to predict when potentially harmful organisms may develop

in areas where they might pose a threat to public health or wildlife. Once species identification is

automated and/or greatly accelerated, population data can be collected that is compatible with

high-frequency measurements of chemical and physical oceanographic features.

We need to:

1. Collect, isolate, and maintain a wide range of HAB species in unialgal and/or axenic cultures.

2. Characterize key species using standard microscopic methods (e.g, light, epifluorescence, and

electron microscopy as appropriate).

3. Characterize key species using molecular genetic methods (e.g., RFLP, RAPD, gene

sequencing).

4. Develop molecular probes and application strategies for use in field and laboratory settings,

and make these tools broadly available.

5. Detect and quantify toxins produced by HAB species using bioassays, HPLC, immunoassays,

and receptor binding assays; refine those techniques for routine use on field and culture

samples.

6. Develop optical sensors able to distinguish taxon-specific features such as pigments.

Approach and Technology. The problem of uncertain and slow identification can be addressed by 

cross-disciplinary investigations that utilize a spectrum of techniques to distinguish between species,
3 of 23 1/30/07 3:32 PM

multiple probe types. (see Box 3.1.2) These new technologies should be actively pursued, but traditional

systematic or morphological investigations using standard microscopy or biochemistry should also be 

supported. The tradi tional methods are well-established, but considerable effort is needed to develop the

species-specific probes and the methods to use them in a rapid and precise manner. Results from this

aspect of the program will greatly accelerate progress in several other ECOHAB activities, especially

those involving large-scale field programs.

Probe technologies can also be used to detect the toxins (rather than the cells) in environmental samples 

(see Box 3.1.3). This type of application has the potential to provide rapid and accurate information on

toxin levels and distribution that can be highly useful to resource managers.

Issue:

There is a need to identify the life history stages of HAB species, to determine what factors 

control transitions between those stages, and to establish the role of each stage in bloom

dynamics.

Many marine phytoplankton species produce cysts or spores during their life histories, and these resting 

stages can have a significant impact on many aspects of HAB phenomena (Anderson and Wall, 1978;

Anderson et al., 1983). Cyst or spore germination provides the inoculum for many blooms, and the

transformation back to the resting state can remove substantial numbers of vegetative cells from the

population and be a major factor in bloom decline. Cysts are important mechanisms for population

dispersal, they permit a species to survive through adverse conditions, and since sexuality is typically 

required for their formation, they facilitate genetic recombination (Wall, 1971). They can even be

important sources of toxin to shellfish and other benthic animals. Clearly, all investigations of the

ecology and bloom dynamics of HAB organisms must be based on a thorough understanding of an

organism's life history, as well as the factors that regulate the transitions between dormancy and a

vegetative existence.

Unfortunately, the state of knowledge about resting stages and life histories is neither complete nor 

uniform for the many HAB species. For several (e.g., Alexandrium spp., Heterosigma carterae, 

Pfiesteria piscicida ), the existence of resting cysts has been documented. For many others, however, no

life history information is available. The prevalence of life-cycle stages among other HAB species is not

well known, and factors triggering transitions are poorly defined. Recognizing and determin ing the role

of these stages in bloom initiation, growth and termination is critical to our understanding of HAB 

phenomena.

We need to:

1. Develop culture techniques which simulate in situ growth conditions sufficiently well that life

history transitions can be induced and characterized.

2. Isolate and culture many HAB species, and support the maintenance of HAB culture

collections. The importance of maintaining multiple isolates of individual species must be

emphasized here, given the genetic diversity observed in regional populations of HAB "species."

3. Develop molecular probes that can assist in the identification of life history stages in natural

samples.

4. Incorporate studies of resting cyst or spore distribution, abundance, and dynamics into field

investigations of HAB bloom dynamics.
4 of 23 1/30/07 3:32 PM

required given the diversity of species represented by HAB organisms. Some technique development

effort is needed, such as in the design and application of probes to identify life history stages of a target

organism and refinement of culture techniques to permit full-cycle life history transformations to occur

in the laboratory. Otherwise, methodologies are in-hand for these studies.

Issue:

It is essential to understand the physiological responses of HAB species to differing 

environmental conditons.

The manner in which HAB species respond to a changing environment determines their survival and 

growth. These re sponses are governed by the physiological requirements and tolerances of each species

for environmental variables such as nutrients, light, temperature, and salinity. All HAB species must be

characterized with respect to these tolerances if we are to understand and predict their distribution and

occurrence in natural waters. For example, an extraordinary bloom referred to as "the Texas brown tide"

has persisted in the Laguna Madre for five years (Buskey and Stockwell, 1993). There are multiple

potential explanations for this dominance, one of which is that the causative species out-competes other 

phytoplankton for essential resources. In addition to possible selection on the basis of temperature or

salinity tolerances, the brown tide alga cannot use nitrate as a nitrogen source. This unique nutritional

strategy may be fundamental to the success of the species in that system, but further experimental

studies are clearly needed to document how this might be occur ring.

The brown tide in Texas is but one example of the need for information on physiological responses of 

individual HAB species to their chemical and physical environments. The same can be said for virtually

all important HAB species. Why are Alexandrium blooms in the southwestern Gulf of Maine tightly 

linked to a coastal current of low salinity water (Franks and Anderson, 1992a)? Do the cells grow faster

in that water mass due to its unique macro- or micro-nutrients? How is Gymnodinium breve, a red tide 

dinoflagellate from the Gulf of Mexico, able to survive during transport for 1000 km or more around the

Florida peninsula and up the southeastern coast of the U.S. to North Carolina via the Gulf Stream 

(Tester et al., 1991)?

Experimental approaches to organismal physiology must include the following:

1. Establish new clones of key HAB species representing their entire geographical range.

2. For multiple toxic and non-toxic clones of HAB species, determine tolerance ranges and

optima for growth and toxin production in response to a suite of environmental variables.

3. Conduct classical steady-state analyses of nutrient requirements and uptake rates for key

HAB species.

4. Compare laboratory results with data from mesocosm and field investigations.

Approach and Technology. Species-specific physiological data can be most easily derived from 

experiments with unialgal cultures under controlled conditions. However, clones of a single species

typically exhibit marked variation in numerous characteristics, including growth and toxin production

(Maranda et al., 1985; Bomber, et al., 1989; Cembella et al., 1987; Hayhome et al., 1989; Anderson et

al., 1994). Since no single isolate can be considered to be representative of a regional population, growth

studies are needed for multiple strains to define the extent of genetic variability and environmental

plasticity. Several laboratories in the United States have initiated "syndrome-based" culture collections 

of harmful marine microalgae, and these collections should be supported and exploited in this respect.

As discussed below, techniques for some of the above physiological studies are not uniformly accepted.
5 of 23 1/30/07 3:32 PM

Issue:

In situ measurements of the rates of photosynthesis, growth, and nutrient uptake are essential 

for understanding the dynamics of HABs, as are assessments of the physiologial condition of

cells at different times and locations. 

This issue epitomizes a unique and challenging feature of HAB studies that separates them from more 

traditional process -oriented oceanographic investigations. Many techniques are available to assess the

biological rate processes and biomass of planktonic communities (e.g., 14C-fixation, chlorophyll), but

there are few methods suitable for determining growth or uptake rates or physiological condition of an

individual species when it occurs in a mixed population and does not dominate the phytoplankton

assemblage. Considerable methods development is thus required to fully address this autecological 

characteris tic of ECOHAB.

Effort is needed in the following areas:

1. Investigate the physiology, biochemistry, and molecular biology of specific processes to

identify "diagnostic indica tors" for physiological condition.

2. Develop methods to estimate in situ rates of growth, photosynthesis, and nutrient uptake for

HAB species.

3. Calibrate these methods carefully, and then apply them aggressively to field populations.

Approach and Technology. The necessary studies can build on molecular and biochemical techniques 

developed to assess growth rate (Dortch et al., 1983; Chang and Carpenter, 1991; Lin et al., 1994) and a

suite of physiological processes within cells such as nitrogen fixation (e.g., Currin et al., 1990), nutrient

uptake or limitation (Berdalet and Estrada, 1994; see Box 3.1.3) and photosynthetic activity (Orellana

and Perry, 1992). The objective of these studies will be to develop analytical methods and diagnostic

indicators that can be applied to individual cells. The more traditional bulk analyses work on commu

nities rather than species. For some HAB organisms, it will be necessary to couple the above methods 

with identification probes and flow cytometry or cell imaging techniques to measure species-specific

characteristics.

Although recent technological advances are encouraging in these fields, there is a clear need for an initial 

methods devel opment and calibration effort within the ECOHAB framework. The ultimate goal is to

apply these techniques in ecological studies.

Issue:

It is essential to know the nutrient requirements, uptake, and assimilation characteristics of 

HAB species.

Nutrient limitation of phytoplankton growth is a fundamental factor that places a limit on the 

accumulation of biomass and may determine the outcome of competition among species in mixed

assemblages. It is often suggested that increasing inci dences of harmful algal blooms in coastal waters

are related to changes in nutrient loading from human activities (e.g., Smayda, 1990), so verification of

this linkage would have important societal implications. These nutrients can stimulate or enhance the

impact of toxic or harmful species in several ways. At the simplest level, toxic phytoplankton may 

increase in abundance due to nutrient enrichment but remain as the same relative fraction of the total

phytoplankton biomass (i.e. all phytoplankton species are affected equally by the enrichment).

Alternatively, there may be a selective stimulation of HAB species by pollution. This view is based on 
6 of 23 1/30/07 3:32 PM

vast majority of which are harmless, require silicon in their cell walls, whereas other phytoplankton do

not. Since silicon is not abundant in sewage effluent but nitrogen and phosphorus are, the N:Si or P:Si

ratios in coastal waters have increased through time over the last several decades. Diatom growth in

these waters ceases when silicon supplies are depleted, but other phytoplankton classes (which include

most of the known toxic species) can proliferate using the "excess" nitrogen and phosphorus.

This concept is controversial, but is not without supporting data. A 23-year time series off the German 

coast documents the general enrichment of coastal waters with nitrogen and phosphorus, as well as a

four-fold increase in the N:Si and P:Si ratios (Radach et al., 1990). This was accompanied by a striking

change in the composition of the phytoplankton community, as diatoms decreased and flagellates

increased more than ten-fold. As coastal communities and countries struggle with pollution and

eutrophication issues, the implications of these concepts are profound and clearly deserve further 

investigation.

A few measurements of nutrient uptake kinetics and cell nutrient quotas of HAB species (e.g., 

dinoflagellates and raphidophytes) suggest that they have high nutrient requirements, indicating that they

would be able to proliferate only in high nutrient environments (e.g., Eppley et al., 1969; Caperon and

Meyer, 1972). Relatively few HAB species have been investigated in this context, however. Nutrient

uptake and growth rate kinetics and nutrient quotas for HAB species must thus be determined to predict

their growth response relative to other species. In addition, some supposedly autotrophic phy toplankton

species appear to utilize dissolved organic nutrients (Cembella et al., 1984; Taylor and Pollingher, 1987) 

while others rely on mixotrophy to supplement their carbon requirements (Sanders and Porter, 1988). If

confirmed in HAB species, these nutritional strategies may confer a competitive advantage over other

phytoplankton.

Nutrient studies within ECOHAB should focus on the following:

1. Determine nutrient uptake and growth kinetics for HAB species under a range of

environmental conditions. Depend ing on the species, this information is needed for N, P, Si, Se

and Fe at least, but other micronutrients may need to be considered.

2. Assess the prevalence among HAB species of unique nutritional strategies such as

osmotrophy and mixotrophy.

3. Develop and optimize culture techniques for fastidious HAB species.

Approach and Technology. The hypotheses that changing nutrient ratios can influence competition 

dynamics and that HAB species have nutrient requirements different from other phytoplankton species

can be assessed using a combination of nutrient kinetics and manipulative experiments with cultures and

natural populations. Several approaches have been used to derive nutrient kinetic parameters, and there

is the need to standardize experimental protocols before embarking on comparative studies among HAB

species. Moreover, there is no general agreement on the merits and limitations of using batch versus

continuous culture methods for nutritional requirement studies. As a result, it may be necessary to 

convene an ECOHAB community working group to address standard experimental approaches.

Issue:

The functional role of toxins and/or exudates produced by HAB species is not known.

Toxin production is a wide-spread, but not universal, characteristic of HAB species. The functional 

roles suggested for toxins are: 1) as deterrents to grazers (Box 3.3.1); 2) as allelopathic compounds that

restrict the growth of co-occurring algal species; and 3) as storage products. It may well be that toxins
7 of 23 1/30/07 3:32 PM

studies are limited to a few species and are only a beginning. They certainly have not addressed the

diversity of grazer-algal relationships necessary to evaluate the role of toxins in natural populations.

We need to:

1. Conduct laboratory and field studies to determine if there is differential grazing on toxic

versus non-toxic species.

2. Determine the effects of toxic algae on ecologically significant grazers.

3. Evaluate the allelopathic activity of exudates and toxins of HAB species.

Approach and Technology. This work will depend upon a supply of appropriate isolates, our ability 

to manipulate them in culture, and the availability of sensitive and reliable methods of toxin analysis. In

general, techniques are available to pursue this important line of investigation, although advances in

3-dimensional video analysis of grazer behavior when presented with HAB species can provide new

and relevant insights.

Issue:

It is essential that we define the genetic basis of toxin production, elucidate toxin biosynthetic 

pathways, and determine how toxin accumulation in cells is regulated.

Toxin production is a distinguishing characteristic of many HAB species. However, the prevalence of 

toxin synthesis among these organisms is continuously being re-evaluated. For some species the toxins

are well described (e.g., saxitoxins, domoic acid, brevetoxins; Hall et al., 1990; Shimizu, 1993;

Falconer, 1993), although non-toxic strains or sub-species have been documented for several such taxa

(e.g., Yentsch et al., 1978; Smith et al., 1990). Other species such as Heterosigma carterae and 

Pfiesteria piscicida are known to produce toxins, but the actual compounds remain uncharacterized (e.g.,

Burkholder et al., 1992; 1995). Still, other species are considered likely to be toxigenic based on an

association with events such as fish kills, but their toxicity has yet to be confirmed. Our lack of

information about this basic trait for many HAB species limits our ability to ascertain the nature and

extent of HAB impacts or to evaluate mechanisms underlying trends in HAB incidence.

While relatively few organisms have been examined, the available data suggest that the amounts and 

forms of toxin con tained in a cell vary with its physiological status. For the saxitoxins, environmental

factors such as nutrient concentration and temperature can influence the expression of individual toxin

derivatives (Hall, 1982; Anderson et al., 1990a,b). This is an important ecological consideration,

because various derivatives can differ markedly in their potencies (Oshima et al., 1989). Production of

algal toxins can also be modulated by co-occurring bacteria (Bates et al., 1995), and in certain cases, 

bacteria themselves represent autonomous sources of phycotoxins (Kodama et al., 1988; Doucette and

Trick, 1995).

Nutrients have a clear and significant influence on the production of toxins by some algae. In species 

from a variety of taxonomic groups producing different toxins, cellular toxin content varies dramatically

during nutrient starvation in culture. For example, the abundance of saxitoxins in Alexandrium species

can vary by more than an order of magnitude depending upon whether phosphorus or nitrogen is

limiting (e.g., Hall, 1982; Boyer et al., 1987; Anderson et al., 1990). Likewise, domoic acid production

in Pseudo-nitzschia species varies with silicate availability (Bates et al., 1991; Bates and Douglas, 

1993), and Chrysochromulina polylepis, the chyrsophyte responsible for massive fish and invertebrate 

mortalities in Sweden and Norway in 1987, has been shown to be more toxic when phosphorus is

limiting (Edvardsen et al., 1990; Granéli et al., 1993).
8 of 23 1/30/07 3:32 PM

the nature of the linkage between nutrients and toxicity, and then only for a few species. Biochemical

and cellular mechanisms remain to be elucidated, as does the extent to which the nutrient limitations that

alter toxicity are actually occurring in natural waters. Without more detailed information about the

physiology of toxin production for a wider range of HAB species, it is very difficult to assess the 

ecological role of toxins in population and community dynamics (see sections 3.2 and 3.3).

The biosynthetic pathways for the production of several toxins have been described to the extent that 

elementary "building blocks" have been identified (Shimizu et al., 1984; Douglas et al., 1992; Box

3.1.4), but in no case have complete pathways, including all intermediates involved, been elucidated.

Isolation of the enzymes involved in toxin synthesis or interconversions is also at a very early stage of

development (Sako et al., 1995). At the most basic level isolation of the genes and enzymes directing the

production of algal toxins remains an important but elusive goal.

Organismal studies of toxin production and its genetic control will need to include the following:

1. Determine the prevalence of toxin production among HAB species in culture and the

time-varying concentrations of toxin at different stages of growth.

2. Determine the linkage between bacteria and toxin production.

3. Isolate and purify poorly characterized or unknown toxins and determine their chemical

structures.

4. Elucidate toxin biosynthetic pathways and characterize the genetics and regulation of toxin

production.

5. Determine the nutrient assimilation and partitioning pathways which permit toxin synthesis,

and determine the factors which influence toxin production at the cellular level.

Approach and Technology. A number of well-established experimental approaches are available and 

appropriate to address patterns of toxin production, typically involving the growth of an HAB species

under a suite of environmental conditions and monitoring the manner in which toxicity varies. The

isolation of toxin genes/enzymes is a critical first-step toward identifying the actual mechanisms

underlying environmentally-induced toxin variability. Additionally, studies at the molecular level will

allow us to evaluate the intracellular trade-offs between toxin production and maintenance of "normal" 

cellular metabolism, ultimately leading to a clearer understanding of "why" it might be ecologically

beneficial for toxigenic organisms to synthesize toxins. Technological strategies for implementing these

studies will include: classical laboratory culture methods, application of toxin probes, assays and

analyses; biosynthetic feeding/label-incorporation experiments; standard chromatographic techniques;

and, methods incorporating mutagenesis and gene expression protocols.

Issue:

We must understand the importance of motility and other behaviors of HAB species.

Some motile HAB species exhibit directed swimming behavior such as vertical migration or orientation 

towards prey, as has been demonstrated for the ambush dinoflagellate, Pfiesteria piscicida which is 

capable of detecting and swimming towards its preferred food. Vertical migration is thought to be a

response to light, salinity, nutrient gradients, and even gravity (e.g., Holmes et al., 1967; Eppley et al.,

1968; Kamykowski, 1974; Cullen and Horrigan, 1981). This mechanism is fundamental to the

population dynamics of many motile HAB species, as it can result in dense concentrations of cells that 

affect grazing losses, light harvesting, nutrient availability, and encounter frequencies for sexuality. The
9 of 23 1/30/07 3:32 PM

We need to:

1. Conduct vertical migration studies at a variety of scales, from tube cultures to mesocosms to

natural populations.

2. Characterize the influence of environmental variables such as salinity, light, and nutrients on

these behaviors.

3. Refine models of swimming behavior and examine how different strategies interact with

physical features such as pycnoclines, fronts, or internal waves.

Approach and Technology. A combination of laboratory and field investigations is necessary to 

address the significance of these behaviors. Much of the technology required for such studies exists, but

new approaches such as fine-scale sampling techniques, (e.g., Donaghay et al., 1992) will be needed to

measure biological, chemical and physical parameters with appropri ate resolution. Rapid detection and

enumeration techniques for HAB species will be required (see Box 3.1.2), and mesocosm strategies will

be important as well.

3.1.3 Summary

The Organism program element of ECOHAB reflects the fundamental importance of physiological, 

genetic, and behavioral studies in an initiative designed to develop an understanding of the population

dynamics and trophic impacts of harmful algal species. We take it as a given that studies of HAB 

blooms require a thorough understanding of genetic variability and regulation, nutritional and

environmental tolerances and responses, behavioral adaptations, life history transforma tions,

toxin physiology and function, and numerous other processes and features that will vary among

HAB species. Given the diverse array of HAB species in the U.S. and the many different environments 

in which they occur, this program element will likely be dominated by small research programs

conducted by individual investigators or small teams. Focused, multi-investigator proposals are also

envisioned on specific issues where coordination and comparisons between organisms would be

beneficial. In many cases, the technology exists for the studies that are proposed, but a focused methods 

develop ment effort will greatly accelerate progress on numerous other ECOHAB elements. For

example, rapid and automated detec tion and enumeration of HAB species using probe technologies

would eliminate a major constraint to field programs namely the time required to process cell count

samples collected at spatial and temporal frequencies similar to those for hydrographic and chemical

parameters. Such techniques would also make cell counts and even the physical separation of HAB

species from co-occurring organisms fast and accurate, permitting measurements that otherwise would 

not be possible. Prioritization within the research issues highlighted above was not attempted, as the list

already reflects an effort by work shop participants to include only the most important and timely

research topics.

3.2.1 Introduction

Rationale: Concurrent with escalating influences of human activities on coastal ecosystems, the 

environmental and economic impacts of HABs have increased in recent decades. It is therefore

imperative to know if present trends of human activities and HABs will lead to unacceptable

consequences, and if the means can be developed to mitigate impacts. The key to this knowledge

is an understanding of the ecology and oceanography of harmful algal blooms. An important

facet of this complex topic is environmental regulation, that is, the influence of environmental 

factors on the population dynamics of harmful algal species and their competitors.

The geographic range, persistence, and intensity of HABs are determined by both physical and 
10 of 23 1/30/07 3:32 PM

from a source region where blooms are already established (e.g., Gymnodinium catenatum in northwest 

Spain; Fraga et al., 1988), or exploitation of unusual climatic or hydrographic conditions (e.g.,

Pyrodinium bahamense and ENSO events in the Indo-West Pacific; Maclean, 1989). Once a population 

has begun growing, its range and biomass are still affected by physical controls and nutrient supply.

Physical controls include long distance transport of populations (e.g., Franks and Anderson, 1992a),

accumulation of biomass in response to water flows and swimming behavior of organisms

(Kamykowski, 1974; Cullen and Horrigan, 1981), and maintenance of suitable environ mental

conditions (including temperature and salinity, stratification, irradiance, and nutrient supply; Whitledge, 

1993). Aspects of nutrient supply include not only the amount of macro- and micronutrients, but also

their ratio and mechanism of supply. Thus, physical forcings, nutrient supply, and behavior of

organisms all interact to determine the timing, location, and ultimate biomass achieved by the bloom, as

well as its impacts. The first goal of the Environmental Regulation program element of ECOHAB is

thus:

Goal: To determine and parameterize the environmental factors that govern the initiation, 

growth, maintenance, dissipation and impacts of HABs.

Physiological responses and life histories of HAB species are varied, as are local and regional physical 

environments where HABs occur. Thus there is considerable variability in the relationship of HABs to

their environment. In spite of this complexity, however, it is usually possible to elucidate the patterns

underlying recurrent blooms in an area. Generalizations to other regions is not usually appropriate,

however. An understanding of the relationship between an HAB species and its physical and biological

environment is critical to predicting environmental and economic impacts and to the formulation of

mitigation strategies to minimize those effects. Since it is impractical to study all of the ecosystems in 

which HABs occur, a second goal is:

Goal: To formulate principles that explain similarities between ecosystems during HABs and to 

understand how these systems are unique with respect to the types of blooms that occur.

3.2.2 Research Agenda

The following section outlines specific issues defining high priority field, modeling and experimental 

studies required in the Environmental Regulation program element of ECOHAB.

Issue:

To what extent do HABs reflect increases in growth rate versus physical transport and 

immigration? Is there a specific suite of physical factors associated with many HABs?

Physical factors in the environment influence HAB population dynamics both directly by moving and 

aggregating cells, and indirectly by influencing the cells' physical and biological environment. Factors

that can influence the population dynamics and physiology of phytoplankton include: nutrients,

temperature; salinity; irradiance; stability of the water column; turbulent mixing; currents; vertical

advection, dispersion or dilution; wind stress; bottom stress and bathymetry. Temperature, salinity and

irradiance directly influence growth rate, physiology, and in some species, behavior (e.g., Watras et al., 

1982; Tyler and Seliger 1981). High shear associated with turbulent mixing may alter growth, behavior,

and in extreme cases induce mortality (e.g., Pollingher and Zemel, 1981; Thomas and Gibson 1990;

Berdalet 1992). Water motions (a complex interaction of most of these factors) determine the losses and

gains from advection as well as losses to dispersion (Kamykowski 1979, 1981). In addition, water

motions determine in large part an alga's ability to exploit light and nutrients. Finally, stratification of the

water column allows weakly swimmming algae to interact with current shear and thereby drastically 

alter immigration rates. The success of individual HAB species is associated with different hierarchies
11 of 23 1/30/07 3:32 PM

regimes and highly stratified river plumes. Among these diverse settings, vertical and horizontal

transport processes play important roles in regulating bloom development, although the physical

mechanisms and rates may vary considerably between environments. Characterizing transport processes

in these stratified and/or spatially non-homogeneous regimes represents a challenging basic research

problem. Our progress in understanding HABs thus requires advances in coastal physical 

oceanography. Some of these unresolved physics problems that have an important bearing on HABs

include:

Turbulence and Vertical Transport. While there are many turbulence closure models that 

parameterize the effects of stratification (e.g., Martin, 1985), such models may not apply across the

range of conditions found in coastal environments. A particularly difficult problem is the mixing in

stratified shear layers removed from boundaries, such as those found at the base of buoyant plumes. The

rate of vertical mixing must be accurately quantified and related to measurable mean properties in order

to interpret observations and develop models of HABs. Vertical transport processes associated with 

upwelling, frontal processes and secondary circulations may be comparable to (or more important than)

vertical mixing. These motions facili tate vertical exchange, but they also play an important role in the

aggregation of plankton.

Horizontal Dispersion Processes. As is the case with parameterizing vertical mixing, the rate of 

horizontal dispersion is difficult to quantify at the scales relevant to HABs. In estuarine environments,

there have been a number of attempts to relate flushing rate to easily measurable physical parameters.

There has been some success in this regard, but there remains consid erable room for improvement in

parameterization of flushing. In coastal settings, Okubo's (1971) mixing diagrams still pro vide the

benchmark for estimation of small-scale horizontal exchange. Dispersion theory has advanced 

considerably with the contributions of Young et al (1982) with respect to shear dispersion and

Zimmerman (1986) for chaotic dispersion. However, there are few observational studies that provide the

requisite measurements of small-scale velocity variation required to turn these theoretical ideas into

estimates of horizontal dispersion. Given recent progress in measurement of small-scale variations of

velocity (e.g., Geyer and Signell, 1992; Prandle 1991), there is great potential to make substantial 

progress on this important research area, and one mechanism for such study would be through

ECOHAB.

Buoyant Plumes. HABs are frequently observed in association with buoyant plumes (Therriault et al., 

1985; Franks and Anderson, 1992a; Tester et al., 1991). While the bulk characteristics of buoyant

plumes are well established, the details of the velocity and density structure and their variability are not

adequately understood to explain the transport, aggregation and dispersion of algal cells within plumes.

The strong vertical and horizontal shears occurring within plumes result in a complex advective regime

that may concentrate cells within the front or disperse them, depending on the interaction between the

relative motion of the organisms and the flow field. Secondary circulations associated with winds, 

planetary rotation and topography also contribute to the complexity of the flow within these

environments. Numerical models simulating theoretical coastal buoyant plumes under surface wind

stress have been formulated (e.g., Chao, 1987), but no one has yet incorporated behavioral or

physiological models of HAB species into such physical models.

Estuarine Circulation. The classic paradigm of two-layer estuarine circulation is a gross 

oversimplification of time-depen dent and three-dimensional motions in estuaries. Wind-driven motions

provide a large perturbation that in many environ ments may dominate the horizontal exchange, and tidal

dispersive effects often control small-scale transport and in some cases regulate the estuary-scale

exchange. Complex, three-dimensional motions due to the interaction of stratification, tides and winds

play an important role in horizontal dispersion and vertical exchange, and they provide critical controls 

on the spatial distribution of plankton cells. These processes and their interactions are certainly complex,

but careful consideration of both physical and biological features can lead to important insights into the
12 of 23 1/30/07 3:32 PM

Each of the physical processes described above is an active area of research in physical oceanography, 

but much of this work is taking place without reference to phytoplankton populations. With respect to

the ECOHAB program, it would be unrealistic to strive for a complete understanding of how each these

processes can drive ecosystem response. There are, however, tractable physical problems that can be

addressed, and large advances in our understanding can be obtained with collaborations between HAB

biologists, physicists, and modelers.

Priority acitivites should be to:

1. Describe and model the dynamics of HABs in relation to their physical environment.

2. Determine how variations in population growth rate and biomass depend on small scale

turbulence through its influence on nutrient uptake, grazing, cell division, accumulation, and

bloom structure.

3. Determine how the vertical distribution of HAB populations regulates bloom development

and dissipation, and how vertical distribution relates to physical (e.g., horizontal and vertical

advection, vertical mixing and stability) and biological processes (e.g., motility, buoyancy

control).

Approach and Technology. To determine the influence of environmental factors on the development 

of HABs, it is essen tial to describe their distributions in time and space, and this will require

coordinated and multidisciplinary studies. Informa tion on the distributions of physical and biological

variables should be synoptic in space (local to regional scales) and highly resolved in time (hours to

days) covering successive bloom periods (interannual variability). This level of coverage would be ideal,

but it is expensive and probably unrealistic in the context of ECOHAB alone, given the many sites 

where HABs occur. Excellent results have been obtained, however, with focused field programs that

involve significant physical components (e.g., Seliger et al., 1970; Tyler and Seliger, 1978,1981; Franks

and Anderson, 1992a). Future collaborative efforts between physical and biological oceanographers

should thus be emphasized and encouraged.

There is considerable potential for the use of moored optical sensors in red tide/toxic algae research and 

monitoring (see Box 3.2.2). When properly designed and calibrated, these sensors measure radiometric

quantities that should be particularly appropriate for long time-series observations in coastal systems.

That is, unlike measurements of chlorophyll, floristics, and stimulated fluorescence, which are

somewhat dependent on equipment and methods, records of irradiance and radiance should be

completely comparable over many years, documenting changes associated with eutrophication or 

remediation, for example. If such observations can be made autonomously and interpreted reliably, they

would be ideal for the detection of HABs in coastal waters, even in remote locations. Because some

harmful species can exert profound negative effects on coastal resources without dominating the

phytoplankton and changing the color of the water, there are limitations to the usefulness of optical

instruments for detecting HAB phenomena. Nonetheless, continuous optical measurements in coastal

waters would be extremely useful for describing bloom dynamics and long-term trends. Furthermore, 

with the development of species-identification technologies described in section 3.1.2, it should become

feasible to use moorings to obtain long-term records of HAB species distributions and associated

environmental variables.

A hierarchy of remote sensing platforms would provide frequent, synoptic, near-surface spatial 

information (see Box 3.2.3). Aircraft-mounted units are needed to provide high-resolution distributions

on local to regional scales (e.g., Millie et al., 1992). Satellite sensors, such as SeaWiFS, will provide

lower temporal and spatial resolution, but over regional to global scales. Calibration and deployment of

these instruments during HAB events is essential to the development of a remote sensing capability for
13 of 23 1/30/07 3:32 PM

direct measurements of rates and standing stocks of key components, but also as a means of relating

component variability to information from moorings and remote platforms. Field programs aimed at

understanding the interactions between HAB species and their physical environment are typically

hampered by the enumeration of HAB individuals in a diverse assemblage of phytoplank ton,

microzooplankton and detritus. Small, low cost profilers are needed that can be rapidly deployed in the 

vicinity of HABs to define their spatial structure and temporal evolution. These profilers can be

deployed with self-contained CTD/fluorom eter/transmissometer/optical backscatter packages for

measurement of key physical parameters that may directly or indi rectly control bloom development.

Analytical and numerical models are important tools for studying physical-biological interactions in the 

ocean. Models have been used for decades to understand how physical forcings influence the

distribution and production of HAB species. New archi tectures for physical models which incorporate

turbulence-closure formulations for the small-scale motions (e.g., Blumberg and Mellor, 1987) now

provide important platforms for the investigation of physical-biological interactions over scales of 

meters to hundreds of kilometers. The incorporation of behavioral and physiological models of HAB

species into these physical models is a necessary and important step in elucidating the couplings

between nonlinear physical flows and time-dependent biological re sponses (see Box 3.1.6). The

formulation of theoretical models investigating the nature of interactions between physical flows and

organism behaviors must be encouraged.

Issue:

How do physical and ecological processes control the partitioning of nutrients within a system 

and the relationship between nutrient inputs and the population dynamics of HAB species?

The availability of nutrients (inorganic and organic) to individual organisms ultimately regulates the 

growth rate and net biomass of blooms. Physical forcings, such as vertical mixing, stratification or

advection can be significant factors in determin ing the availability of those nutrients. It is also clear that

the relationship between nutrient inputs and population dynamics is complex and reflects many other,

interacting processes. One of the explanations given for the increased incidence of HAB outbreaks

worldwide is that these events are a result of increased pollution and nutrient loading of coastal waters. 

Some argue that we are witnessing a fundamental change in the phytoplankton species composition of

coastal marine ecosystems throughout the world due to the changes in nutrient supply ratios from

human activities (Smayda, 1990). There is no doubt that this is true in certain areas where pollution has

increased dramatically. It is perhaps real, but less evident in areas where coastal pollution is more

gradual and unobtrusive. In Tolo Harbor, Hong Kong, human population within the watershed grew 

6-fold between 1976 and 1986, during which time the number of red-tide events increased 8-fold (Lam

and Ho, 1989). The underly ing mechanism is presumed to be increased nutrient loading from pollution

that accompanied human population growth. A similar pattern emerged from a long-term study of the

Inland Sea of Japan, where visible red tides increased steadily from 44 per year in 1965 to over 300 a

decade later, matching the pattern of increased nutrient loading from pollution (Murakawa, 1987).

Japanese authorities instituted effluent controls in the mid-1970's, resulting in a 50% reduction in the 

number of red tides that has persisted to this day.

As coastal communities and countries struggle with pollution and eutrophication issues, the implications 

of the trends in Hong Kong, Japan, and other countries are profound. The public, the press, and

regulatory officials are concerned about whether this is happening in the U.S. as well, and are asking for

predictions and answers about HAB incidence that exceed our present capabilities. Unfortunately, 

competitive outcomes in phytoplankton species selection and succession cannot yet be predicted,

nor can the relative effects of natural versus anthropogenic factors be resolved . A variety of

important issues involving nutrients and the manner in which they are supplied to and utilized by HAB 

species must thus be addressed.
14 of 23 1/30/07 3:32 PM

ecosystems can influence ecological responses, especially those that favor HABs.

2. Determine whether the frequency and duration of harmful algal blooms are increasing in

coastal waters relative to increases in phytoplankton production in general.

3. Investigate the extent to which HABs are indicators of local (point-source) or regional (diffuse

input) increases in nutrient loading.

4. Investigate how climatic variability from local to global scales influences the development and

dispersal of HABs.

5. Learn whether HABs are indicators of environmental or habitat changes induced by nutrient

over-enrichment or other anthropogenic effects (e.g., alterations in freshwater or contaminant

inputs).

Approach and Technology. The potential stimulatory influence of anthropogenic nutrient inputs on 

HAB incidence is certainly one of the more pressing unknowns we face, and will require a focused

commitment of resources and effort greatly in excess of that previously devoted to the topic. Time-series

analysis of existing data bases for phytoplankton communities and of variables such as major nutrients

or pollutants are required. Where such data are lacking, long-term monitoring programs must be initiated

in key regions where anthropogenic changes are anticipated. Moored instrument packages includ ing

optical sensors and other devices to resolve HAB classes or species within the plankton would be 

highly effective in this regard. Laboratory studies of the stimulatory effects of chemicals contained in

effluents or terrestrial runoff are also needed, as are kinetic studies and other experiments that can

quantify the nutritional requirements and uptake capabilities of HAB species (see section 3.1.2 for a

more detailed list of approaches to nutrient issues).

Issue:

Are there specific physical, chemical, and biological regimes or processes that are associated with 

HAB events? Are some ecosystems more susceptible to HABs than others?

Issue:

Population dynamics, including the rate processes required in predictive models of harmful 

blooms, cannot be adequately described or predicted, although this information is of

fundamental importance to effective resource management.

Information on bloom dynamics can be gained through laboratory and field studies that define nutrient 

uptake kinetics, growth rates, loss terms, and life cycle dynamics. While field conditions such as

circulation, meteorology, and water chemistry have long been recognized as critical elements in blooms

of some toxic species, neither the initial boundary conditions, nor the hydrographic regimes within

which harmful blooms occur are clearly understood. The comparative ecosystem approach adopted by

ECOHAB will permit common features to be identified, such as coastal currents, upwelling, and 

nutrient enhance ment of biomass levels. Additional insights will be obtained through numerical

modeling efforts. Despite the fundamental importance of predictive models for harmful algal blooms in

different regions, no such models exist for U.S. problem species (see Box 3.2.4). The ultimate goal is to

couple population dynamics with physical circulation models for a given hydrographic regime, and to

refine physically/biologically coupled models using field bloom observations and toxicity patterns.

We need to:
15 of 23 1/30/07 3:32 PM

2. Determine biological rate processes and initiate studies of coastal hydrography and water

circulation for development of physically/biologically coupled models at temporal and spatial

scales appropriate to harmful algal blooms.

Approach and Technology: Here again, shipboard observations, field programs, satellite remote 

sensing and moored instrument arrays can all provide the level of detail required for the identification of

the mechanisms underlying HAB out breaks. The key is to obtain data at appropriate time and space

scales for the blooms under study, and this will require careful planning and considerable advance study

so that programs are mounted in the proper place at the proper time.

Theoretical and heuristic models that can be used to guide the formulation and testing of hypotheses and 

to evaluate the causes and consequences of variability in nature should be developed as an integral part

of these multidisciplinary field studies. Models are required to represent the broad range of

environmental dependencies that contribute to HABs. Since HABs reflect physical and biological

dynamics over a broad range of time and space scales, a hierarchy of models will be required. On small

scales, models that examine the vertical experience of HAB populations over the diurnal cycle are 

needed to eluci date cell dynamics. On larger scales, models that examine bloom transport and

dispersion are essential. Model dynamics and parameterization must be driven by field and laboratory

data that are sufficiently detailed to allow independent testing and corroboration. Such robust models

may then have predictive capability. Numerous data sets exist that can be used for testing hypotheses

regarding HAB dynamics, but often such data have not been examined in depth nor have they been 

examined in terms of potential interactions among physical, chemical and biological variables as they

relate to HABs. Retrospective analy ses of historical data and information may provide important

insights at a relatively low cost.

Often the main limitation of models is the paucity of data available to formulate, force and test them. As 

discussed above, field programs must be combined with coupled physical-biological models to gain the

most from limited resources and to test hypotheses concerning bloom initiation, transport, and patterns

of accumulation and dispersal. Much can be accomplished with limited data if it is obtained at the right 

places and the right times.

3.2.3 Summary

The Environmental Regulation program element of ECOHAB addresses factors that act on harmful algal 

populations and regulate their distribution, abundance, and impact. Despite the diverse array of HAB

species and the many hydrographic regimes in which they occur, one common characteristic of such

phenomena is that physical oceanographic forcings play a significant role in both bloom dynamics and

the patterns of toxicity or adverse impacts. Furthermore, the interplay or coupling between physical

variables and biological "behaviors", such as swimming, vertical migration, or physiological adaptation,

holds the key for understanding many HAB phenomena. This physical/biological coupling can occur at 

both large and small scales, and includes processes of great interest to both physical and biological

oceanographers.

Understanding the small- and large-scale physics underlying HAB phenomena is a clear priority, but 

this need should not be restrictive. Observational and modeling studies of physical processes need not

be massive in scale, cost, or complexity to provide useful information. Significant insights on HAB

dynamics have been obtained from field programs with modest but focused physical components (e.g.,

Seliger et al., 1970; Tyler and Seliger, 1978; Franks and Anderson, 1992a).

The potential stimulatory influence of anthropogenic nutrient inputs on HAB incidence is a key 

unknown and time-series analyses of existing data bases are required, as are laboratory studies of the

stimulatory effects of chemicals contained in effluents or terrestrial runoff.
16 of 23 1/30/07 3:32 PM

data to be obtained on time and space scales similar to those currently possible with physical and

chemical measurements. This challenge is compounded by the need to focus on individual species rather

than communities.

The issues highlighted in this program element are entirely complementary to those of the Organism 

element, and together they outline a direct path toward the goal of understanding HAB dynamics and

impacts. Managers must recognize the urgent need for better information about how the environment,

and especially how human alterations to the environment, can alter coastal ecosystems and lead to

harmful blooms.

3.3.1 Introduction

Rationale: The negative impacts of HABs are the result of complex interactions that begin at the 

phytoplankton commu nity level and extend to upper trophic level compartments. Habitat

physics, life cycles, community structure, growth and grazing processes all combine to regulate

the dynamics of the HAB event. Therefore, studies on the impacts of trophic interactions in the

selection and dynamics of HABs, and conversely, the impacts of HAB events on trophic 

structure, processes and interactions are essential if we are to understand the ecology and

oceanography of harmful algal blooms.

Phytoplankton blooms develop through a sequence of stages termed initiation, growth, maintenance and 

decline. A key to understanding bloom dynamics is the identification of processes leading to transitions

between these stages; that is, what factors in the biology of harmful algal species and their grazers lead

to changes in growth and loss processes at different phases of the HAB cycle? Of the terms included in

the population growth equation given in Box 3.2.1, we consider in this section only the trophic

interactions. Specifically, it is imperative that we understand how competitive interactions between

harmful algal species and other phytoplankton contribute to the formation of blooms. Likewise, we must 

evaluate how grazing controls, or fails to control, HAB development. These issues define the first goal

of the Food-Web/Community Inter actions program element:

Goal: Determine the impacts of trophic interactions on selection for, and dynamics of, HABs.

Harmful algal blooms involve multiple interactions among predators, competitors and the harmful algal 

species within an ecosystem. Many routes have been demonstrated by which HABs can impact

food-webs (Box 3.3.1), yet little is known about the nature, extent, and ramifications of many of those

pathways. We must therefore determine the relative importance of each of these interactions over

appropriate spatial and temporal scales. Implicit in this task is the elucidation of the pathways and fates

of HAB toxins in the food-web. The mechanisms by which the timing and frequency of HABs (both 

toxic and high -biomass types) affect community and trophic structure also need to be identified.

Progress in these areas is essential to realizing our second goal:

Goal: Determine the impacts of HABs on trophic structure, processes and interactions.

3.3.2 Research Agenda. 

The following section outlines specific issues defining high priority field and experimental studies 

required to establish how trophic interactions regulate HAB species' selection and population dynamics,

and how HAB events, in turn, influence community/trophic structure and trophodynamics.

Issue:

It is essential to know the extent to which bloom formation results from a breakdown of grazing 
17 of 23 1/30/07 3:32 PM

species reduces the capacity of the environment to support one species' requirements from a common

pool of limiting resources (e.g., nutri ents). Species competition coefficients are modified continuously

by changes in growth parameters such as temperature, light and nutrient availability, and are further

altered by changes in grazing pressure, community structure and allelochemical effects. Enhanced

growth or physical accumulation alone does not always explain HABs, as some taxa secrete allelopathic

substances that inhibit or stimulate the growth of competing and co-occurring algal species (e.g., Pratt, 

1966; Gentien and Arzul, 1990) or inhibit grazing (Smayda, 1992).

Grazing control of HABs depends upon both the local abundance of grazers and their ability to ingest 

the harmful algal species (Box 3.3.2). Low grazer abundance can be critical in the early phases of bloom

development by providing times or regions where grazing losses are less than increases from cell

division. Low grazer abundance can result from a variety of external biological factors (e.g., predation

on grazers), or physical factors (e.g.,spatial separation of HAB species from benthic grazers).

Reductions in grazer abundance may also occur in direct response to an HAB event (e.g., avoidance or 

mortality induced by HABs; Fiedler, 1982; Huntley, 1982), or as a result of the effects of past HAB

events on grazer populations. In cases where grazers are abundant, grazing control may still not be

exerted because toxins or small size can reduce the chance that HAB species will be ingested. If harmful

algal species are consumed, grazers may be unaffected, impaired or killed. The response of zooplankton

and benthic grazers to toxic algal occurrence is often species-specific in terms of behavioral responses

and toxin susceptibility.

Grazing control of HABs can also depend on the population density of the harmful alga, as, for 

example, when suppression of grazing occurs above a threshold concentration of the alga, as

demonstrated for the Narragansett Bay brown tide in 1985 (Tracey, 1988). A threshold effect may also

occur if the daily production of new HAB cells becomes large enough to saturate the ingestion response

of the grazers and the ability of grazers to increase their populations. In that case, population growth can 

accelerate dramatically (Donaghay, 1988). A breakdown of grazing control has been implicated in the

brown tides in Narragansett Bay (Tracey, 1988) and in Texas (Buskey and Stockwell, 1993) and

removal/loss of the grazer population has been reported to precede or accompany bloom development

(Montagna et al., 1993). There is, however, little information on how the nature of the grazer response

influences the timing, magnitude and duration of HABs.

In order to address the issue of trophic influences on HAB formation we need to:

1. Determine the role of differential growth rates, nutrients and nutritional strategies in

competitive interactions among phytoplankton species.

2. Determine the nature and extent of allelopathic interactions.

3. Determine the importance of spatial and temporal separation between harmful algal species

and grazers, and the relative contribution of pelagic and benthic grazing.

4. Determine the role of harmful algal species' behavior, toxicity and food quality in reducing or

avoiding grazing controls, as well as the importance of density-dependent processes (e.g.,

grazing thresholds).

5. Determine the effects of mixed (toxic/non-toxic) assemblages on grazing control (e.g., does

breakdown of grazing only occur once harmful algae become a dominant component of the

phytoplankton?).

Approach and Technology. A combination of field, mesocosm and laboratory studies will be required 

to elucidate the nature and extent of species' interactions and grazing regulation in HAB phenomena.
18 of 23 1/30/07 3:32 PM

temporal and spatial variability of an HAB and its potential grazers, are essential for quantifying the role 

of grazers in controlling HAB dynamics. Mesocosm experiments are needed to determine the patterns

and dynamics of interac tions between HAB species and grazers, and the population growth

characteristics of competitors in the presence and absence of harmful algal species. Laboratory

investigations are required to determine interactions between HAB species and individual grazers, to

measure growth and grazing rates on harmful algal species in the presence of "organics" secreted by 

HAB species, and to elucidate allelopathic impacts, mechanisms and pathways involved in HABs.

Development and/or improvement of the following technologies are required to implement the 

approaches described above: species-specific molecular probes for HAB identification; methods for in

situ detection and quantification of HABs during all bloom phases; diagnostic indicators of grazer

physiological status; methods for assessing grazer food quality; video techniques for measuring in situ

grazing and avoidance behavior; high-resolution sampling of fine-scale HAB and grazer distributions;

and suitably scaled microcosm and mesocosm experimental strategies and systems.

Issue:

Are biological controls (e.g., grazers, pathogens) the cause of bloom termination?

The role of biological mechanisms in contributing to bloom termination remains largely unknown. In 

some instances, HAB impacts on grazers are so severe that these organisms may be of little

consequence in the termination of blooms (e.g., Bricelj and Kuenstner, 1989; see Box 3.3.1). The

occurrence of viral particles in cells of a harmful algal species has also been observed (Sieburth et al.,

1988; Milligan and Cosper, 1994), but the efficacy of this mechanism to control natural HABs remains 

to be demonstrated. In addition, it has been suggested that bacteria may play a role in regulating the

population dynamics of HAB species (Doucette, 1995).

Assessing the involvement of biological controls in terminating HABs requires investigation of:

1. The effects of HABs on the grazer community in terms of functional groups and their

concentrations.

2. Alternative biological mechanisms for HAB decline and termination (e.g., pathogens).

Approach and Technology. Several approaches, including field studies and mesocosm and laboratory 

experimentation, are needed to determine how specific biological mechanisms can contribute to the

termination of HABs. The majority of tasks described earlier as essential to defining the influences of

trophic factors on bloom formation are also required here. In addition, the impacts of pathogens such as

viruses and bacteria on HABs need to be assessed in a quantitative fashion in the context of both field

studies and mesocosm manipulations. Sampling schemes must take into account the appropriate tempo

ral/spatial scales relevant to these interactions, as well as environmental factors potentially regulating the 

distribution and abundance of the pathogens. When possible, pathogenic organisms should be isolated

and examined in the laboratory to provide a mechanistic understanding of their effects on HAB taxa.

Strategies for elucidating factors involved in the formation and termination of HABs overlap 

considerably. Most of the technologies required to investigate bloom termination are well established in

the phytoplankton and zooplankton literature. To evaluate the role of pathogens in terminating blooms,

several new techniques must be developed or improved: taxon -specific molecular probes and their

application for identifying and quantifying pathogens in situ; sampling methods for concurrently

resolving HAB and pathogen distributions over a range of temporal/spatial scales; techniques for 

measuring negative impacts of pathogens on HAB species; identifying the underlying mechanisms, and

assessing the taxonomic specific ity of these effects; and appropriately "contained" experimental
19 of 23 1/30/07 3:32 PM

It is essential that we learn the manner in which the effects of HABs on the food-web are 

controlled by toxin dynamics, routing pathways, and the differential susceptibility of species at

higher trophic levels.

The toxins of HAB species may have evolved to release these species from grazing pressure. Similar 

anti-herbivore defenses are well-documented in terrestrial plants, but have received scant attention in

marine systems. Many algal toxins (e.g., PSP and DSP toxins) are endotoxins that affect planktonic and

benthic grazers after consumption. Susceptibility to ingested toxins and, thus, the ability to accumulate

toxins, vary markedly within and among taxa (Twarog et al., 1972), as suggested by reports that finfish

appear to be more sensitive to PSP toxins than crustaceans or molluscs (Robineau et al., 1991). If the 

grazing species are not killed, accumulated toxins may be transferred to other components of the 

food-web and affect other organisms at higher trophic levels. This is an area where our knowledge 

is rudimentary at best, as subtle, ecosystem -level effects are probably pervasive, affecting many

different trophic levels, depending on the toxin involved. Recruitment rates or year-class sizes of

important commercial fish species may well be directly affected by brief exposures of larval or juvenile

stages to toxic algae.

Zooplankton impaired by ingesting harmful algal species may be more susceptible to predation, and thus 

may become an important vector for transferring toxins in the pelagic food-web. Alternatively,

zooplankton killed outright may sediment and allow toxins to enter benthic food-webs. Zooplankton

fecal pellets may also be important sources of toxin to benthic commu nities. Thus, zooplankton can act

as vectors of HAB toxins resulting in events such as fish kills (White, 1981; Smayda, 1992).

Herbivorous fish can also accumulate and transfer toxins, and even cause mass mortalities of the marine 

birds that consume them (Work et al., 1993). Mortality of marine mammals linked to trophic transfer of

HAB toxins has also been reported (Geraci et al., 1989). During their food-web transfers, toxins may be

bioaccumulated, excreted, degraded or structurally modified, as in the case of enzymatic

bio-transformation of PSP toxins in some bivalve molluscs (Cembella et al., 1993).

In order to define the role of toxins in mediating the effects of HABs on food-webs, it is 

necessary to:

1. Identify target species and their life-history stages that are adversely affected by toxic algae,

and those that act as vectors of toxin transmission through the food-web.

2. Determine pathways, transfer rates and mechanisms for bioaccumulation, transformation,

degradation and elimina tion of algal toxins.

3. Characterize modes of action of various phycotoxins (e.g., neurotoxic, cytotoxic, hemolytic) on

marine fauna and determine their differential susceptibility.

Approach and Technology. Field studies as well as supporting laboratory and mesocosm studies 

using algal toxins as tracers are needed to describe changes in toxin concentrations and transformations

of toxins from one trophic level to another. Predictive and heuristic models of food-web transfer of algal

toxins should be developed. These models might be analogous to those formulated for anthropogenic

contaminants (heavy metals, radionuclides, organic pesticides). A comparative, experi mental approach

is also needed to determine dose-dependent behavioral (e.g., swimming avoidance), physiological (e.g.,

grazing inhibition) and cellular (e.g., toxin inactivation, compartmentalization) responses of marine 

organisms to toxic algal species.

In order to carry out the research on toxins associated with HABs outlined above, rapid, standardized 

toxin assays, with detection based on both chemical structure and toxic activity, must be developed to
20 of 23 1/30/07 3:32 PM

Issue:

Are chronic, sublethal impacts of HABs more significant than acute (lethal) impacts in altering 

food-webs or causing trophic dysfunction?

Blooms of harmful algae may be recurrent in some areas (e.g., red tides of PSP-and NSP-producing 

dinoflagellates in the Northeast U.S. and Gulf of Mexico, respectively), episodic (e.g., 1987-88

Gymnodinium breve red tide in North Carolina estuaries) or, more rarely, persistent (e.g., brown tides in 

Laguna Madre, Texas). Chronic, sublethal effects of HABs on marine biota have been documented, as

in the case of brown tide persistence being linked to gradual reductions in eelgrass and shoalgrass

meadows (Dennison et al., 1989). More often, however, it is the effects of brief, but acute blooms that 

have received the most attention because of their immediate impacts on ecosystems or humans (e.g.,

Shumway, 1988; Bates et al., 1989; Smayda, 1992; Burkholder et al., 1992). Episodic HABs are often

associated with acute, lethal effects on adult stages of commercially important species (Tracey, 1988;

Summerson and Peterson, 1990; Burkholder et al., 1992; Taylor, 1993). Re moval of parental stocks

may cause recruitment failure of some natural populations with limited dispersal capabilities (Peterson

and Summerson, 1992). However, it is more likely that HABs adversely affect recruitment success by 

exerting sublethal, chronic impacts on reproduction (e.g., reduced fecundity), growth and behavior

(Bricelj et al., 1987; Buskey and Stockwell, 1993). These chronic effects, which may have long-term

consequences for year-class strength and persistence that are critical in the recovery of natural

populations to pre-bloom levels, have received little attention and merit serious consideration.

Characterizing the relative importance of chronic, sublethal versus acute, lethal impacts of 

HABs on food-webs and their components requires that we:

1. Determine lethal and sublethal effects of HABs on life-history stages of key species in the food

web.

2. Identify mechanisms of recruitment failure, or reduction in affected species.

3. Investigate the extent, time frame and mechanisms of recovery of natural populations

impacted by HABs.

4. Characterize differential effects of episodic, recurrent and chronic HAB events on food-webs.

5. Identify HAB-induced changes in ecosystem energy/nutrient pathways.

Approach and Technology. Field and mesocosm studies, as well as laboratory experimentation, are 

essential for evaluating the impacts of chronic versus acute exposure to HABs on food-web structure

and trophodynamics. This suite of approaches is needed to determine the species-specific effects of

harmful algal species on egg, larval, juvenile and adult stages of target species. Comparisons of HAB

impacts are needed both among different habitats and within the same system where HABs occur with

different frequencies, duration and intensities. We must quantify the effects of recurrent, episodic and 

persistent HAB events on recolonization rates of species from representative trophic levels, which vary

in their life-history strategy, generation time and susceptibility to HABs. We also need to investigate the

impacts of HABs at aquaculture sites, where stocks are concentrated at high densities and are routinely

monitored for growth, mortality and disease incidence.

Several technological advances/improvements are needed to augment those currently employed for 

acquiring the types of information cited above: remote sensing technology and in situ high frequency

optical devices to obtain more rapid, efficient measurements of phytoplankton abundance and
21 of 23 1/30/07 3:32 PM

Issue:

Are HAB impacts are controlled by the degree of temporal and spatial overlap between blooms 

and critical life cycle stages of affected species.

The impacts of HABs on sensitive life cycle stages of affected species higher in the food-web depend 

upon their co -occurrence in time and space, which varies dramatically with the degree of vertical

stratification and exchange with surround ing waters. In some well-mixed estuaries and lagoons, HABs

may be sufficiently persistent and dispersed throughout the system so that all species are equally

exposed, as in the case of brown tides in Laguna Madre, Texas (Buskey and Stockwell, 1993). Such

even exposure greatly simplifies the task of relating observed changes to the effects of HAB 

populations. However, in stratified waters, reduced vertical mixing may allow weakly swimming

plankton, including HABs and potentially affected groups (i.e., microzooplankton, macrozooplankton

and fish larvae) to form highly concentrated layers surrounded by regions of low or undetectable

concentrations of the organisms (Donaghay et al., 1992). In stratified systems exposed to current shear

from winds and tides, the distributions of both HABs and target plankton may also vary dramatically in 

response to lateral advection of layers and interactions between organismal swimming behavior and

current shear. Regardless of the prevalent physical system, however, it is highly unlikely that HAB

impacts can be predicted from average concentrations of HAB and affected species.

In order to assess the extent to which temporal and spatial factors control the impact of HABs 

on other species, we need to:

1. Investigate the temporal and spatial coincidence of susceptible life-history stages of key

species (e.g., grazers) with HABs.

2. Determine the physical processes and biophysical interactions that control bloom

development and grazer responses.

Approach and Technology. Determining the degree to which HAB impacts are regulated by temporal 

and spatial factors requires evaluation of impacts on affected species from actual time-space abundance

measurements. The typical approach has been to estimate responses based on statistically derived

average dispersion and abundance measurements, often on an annual basis. Yearly, and probably even

seasonal means, are, however, inadequate to assess impacts of HAB species, which often form

short-term, high-impact blooms in areas that provide critical spawning/nursery habitat for higher trophic 

levels. Consequently, we need to determine the small-scale, temporal/spatial distribution patterns and

abundances of HAB taxa.

Resolution of co-occurrence effects in stratified waters will require both field and mesocosm studies. 

Field programs must be aimed at quantifying temporal and spatial scales, as well as in situ

concentrations of HAB and co-occurring, affected species. This will require application of high

resolution sampling techniques, both to detect changes in abundance on sub -meter scales, and to link

those changes to physical structure and processes in the system where the HAB occurs. Such field

investigations must be complemented by mesocosm experiments designed to elucidate the underlying 

mechanisms that lead to observed patterns of co-occurrence or avoidance.

Accurate, fine-scale characterization of the temporal/spatial aspects of HAB interactions with affected 

species will depend on: adapting spectral optical and video sensors for deployment on vertical profilers

or towed systems to detect HAB distribu tions in real-time; designing "smart" sampling systems

triggered by these sensors to collect discrete samples for simultaneous identification of and

experimentation on HAB and affected species; developing techniques for measuring in situ swimming 

behavior of motile HAB taxa and affected species; and improving methods for rapid quantification of 
22 of 23 1/30/07 3:32 PM

Do high biomass (non-toxic) HABs adversely impact the food-web directly through reduced 

food quality, or indi rectly through environmental effects?

Harmful effects of algal blooms may occur in the form of anoxic/hypoxic events. Such incidents result 

from increased sedimentation of organic matter coupled with enhanced microbial decomposition of

phytoplankton on the bottom, and/or via transient increases in water column respiratory demands of the

phytoplankton (Box 3.3.3; Falkowski et al., 1980). Mass mortalities of benthic fauna associated with

these events are widespread and affect a broad range of taxa (e.g., Swanson and Sindermann, 1979), but

their connection to HABs is often circumstantial or speculative. High microalgal biomass and result ing

light attenuation are also known to cause marked declines in biomass and distribution of seagrasses. 

Both effects have been noted in eelgrass and shoalgrass communities exposed to picoplanktonic brown

tides in New York and Texas waters. Reductions in irradiance levels may also induce shifts in

macrophytie species' composition toward less desirable forms. Blooms of picoplanktonic microalgae

show enhanced light-scattering properties and are thus particularly likely to cause these light-related

effects, yet the prevalence and magnitude of the problem have not been adequately characterized. 

Because seagrasses provide an important nursery habitat for many commercially valuable shellfish and

finfish species as well as their associated fauna, issues related to these habitats are of special concern.

Nutrient-mediated macroalgal blooms can also lead to the decline of seagrass as well as coral reef 

ecosystems (LaPointe and O'Connell, 1989). In addition, high biomass HABs may limit growth and

recruitment of grazers if the dominant algal species is poorly predated upon due to its unpalatability,

small size and indigestibility, or because of physical impairment of feeding (e.g., Bass et al., 1990).

High algal densities per se may also interfere with food uptake and utilization by many suspension

feeders. Sublethal effects of food quantity/quality, which remain poorly understood (Donaghay, 1985),

are potentially important deter minants of recruitment success in grazer populations.

Evaluating the direct and indirect effects of high biomass HABs on food-webs requires that we:

1. Determine the relative importance of oxygen depletion from HABs in the water column vs.

surface sediments.

2. Understand the extent and ecological consequences of light attenuation from HABs, including

relative effects on phytoplankton, epiphytic algae, seaweeds, seagrasses and their supporting

fauna.

3. Investigate the effects of HABs on food quality available to consumers (e.g., via changes in size

spectra, chemical composition).

4. Define the mechanisms and threshold levels at which high algal biomass interferes with food

capture and utilization by grazers.

5. Understand the controlling mechanisms for restructuring marine communities during

recovery.

Approach and Technology. Elucidation of high biomass HAB impacts on food-webs will require a 

multi-faceted approach, including field studies, experimental mesocosm manipulations and laboratory

investigations. Field work should be aimed at quantifying organic sources and rate processes within the

water column and in sediments to allow development of an oxygen budget. This will involve continuous

monitoring of dissolved oxygen and irradiance levels at spatial and temporal scales relevant to HABs.

Assessment of macrophyte and faunal coverages, as well as seasonal successional patterns, before and 

after bloom events are likewise needed, and should incorporate synoptic aerial mapping of the
23 of 23 1/30/07 3:32 PM

perturbation of target species on food-web structure and processes. Laboratory and mesocosm experi

ments will provide insights into the mechanisms and linkages between high biomass HAB events and 

associated food-web /habitat responses.

Implementing the variety of studies needed to characterize the effects of high biomass HABs on 

food-webs will rely on: remote sensing approaches to aid in determining the occurrence and distribution

of HAB events and high biomass coverage; moored instrumentation for continuous monitoring of

impacted vs. non-impacted sites; techniques for automated, simulta neous sampling of the diel changes

in vertical structure of light, oxygen, phytoplankton (distinguishing HAB taxa from other

phytoplankton) and vertical mixing; regional geographic information system data bases for 

high-biomass blooms; computer ized predictive models for oxygen deficits from HABs, relating

water-column dissolved oxygen, BOD and algal abundance with sediment BOD and algal abundance;

improving available methods for assessing food quality, both biochemically and by comparison to other

known quality foods.

3.3.3 Summary

As algal toxins move through marine food-webs, they can have a broad spectrum of effects on marine 

organisms in inshore, offshore, pelagic, and benthic habitats (Box 3.3.4). The scope of these effects,

resulting from both chronic and acute exposure to the toxins, has become more evident in recent years,

since a wide variety of animals are now known to accumulate biotoxins and act as intermediate vectors

to consumers at higher trophic levels. Algal blooms can also have harmful effects not related to

production of toxins, such as overgrowth and shading by seaweeds, oxygen depletion of the water 

column from high biomass blooms, fish mortalities from over-stimulation of gill mucus production, and

mechanical interference with filter -feeding structures. The Food-Webs/Community Interactions

program element of ECOHAB recognizes the diverse nature of these processes, and highlights key

areas for focused investigation. What is needed is a recognition by managers and regula tory officials

that harmful algal bloom impacts extend far beyond the obvious manifestations of poisonous shellfish 

and dead fish, and include subtle, sub-lethal effects that can alter or even destroy ecosystems through

time. Identifying such impacts and determining their extent and magnitude is a significant challenge for

ECOHAB scientists.

This program element also emphasizes research in the other direction the effects of grazers and other

organisms on the harmful algal blooms, since in many cases, the bloom reflects the supression or

absence of grazing. This again is an area of obvious importance to the dynamics of HABs, but one

which has received only rudimentary study thus far.
1 of 16 1/30/07 3:32 PM

The Ecology and Oceanography of Harmful Algal Blooms

A National Research Agenda

4. Regional HAB Phenomena in the United 

States

4. Regional HAB Phenomena in the United States

The following regional summaries present brief perspectives on specific HABs. Written by workshop 

participants familiar with each region, they review available information and point out deficiencies.

These are provided to document the extensive geographic scale of HAB impacts and to illustrate the

diversity of the phenomena involved. In some cases, the regional summary only reflects one

manifestation of a particular phenomenon, and thus understates the extent of the HAB problem. For 

example, macroalgal blooms in Florida are described, but similar outbreaks occur in coastal waters

throughout the U.S. Similarly, cyanobacterial blooms are highlighted on the U.S. east coast, but occur

on both costs as well as in rivers, lakes and ponds throughout the country.

It is obvious from these summaries that serious information gaps exist in all regions and for all 

organisms, but some deficiencies are similar across multiple regions. The summaries also highlight how

information bases differ among regions, due to different physical regimes, causative organisms, and/or

level of research. This is true even when the organisms are the same or similar (e.g., Alexandrium spp. 

along the Northeast and Pacific coasts).

HAB phenomena are truly diverse, and it is this diversity that must be accomodated in the ECOHAB 

science plan. Clearly, single investigator and multi-investigator, regional projects are required to address

the many identified deficiencies. This approach can address the immediate information needs of each

region, but ECOHAB will derive significant benefit from comparisons among regions and attempts to

highlight common principles or mechanisms underlying many of these phenom ena.

Northeast Region: PSP

The most significant HAB problem in the northeastern U.S. is PSP caused by several closely related 

species in the di noflagellate genus Alexandrium. The affected resources are predominantly shellfish, but 

PSP toxins also affect higher levels of the food-web, including lobsters, fish, and marine mammals.

Paralytic Shellfish Poisoning. PSP is a recurring problem that has affected large areas of the region 

every year for over two decades. Prior to 1972, shellfish toxicity was known only in eastern Maine and

Canadian waters to the north. That year, a massive bloom introduced A. tamarense to southern waters, 

and there have been shellfish harvesting quarantines along large sections of coastline every year since. A

second expansion of the regional PSP problem occurred in 1989, when the rich shellfish beds of

Georges Bank and Nantucket Shoals were found to be contaminated with PSP toxins. The size of the 

offshore area affected, the difficulty in monitoring an area so far from land, and the slow depuration of

toxin from the affected shellfish have necessitated a permanent closure of the surf clam fishery on
2 of 16 1/30/07 3:32 PM

they include a dormant cyst stage in their life histories. Cysts germinate in the spring to inoculate

overlying waters with a "seed" population.

In the southwestern Gulf of Maine, Alexandrium cell distributions are associated with a coastal current

or buoyant plume formed by the outflow from rivers in southern Maine (Franks and Anderson, 1992a).

The southward propagation of this plume and the entrained Alexandrium cells creates an annual 

north-to-south sequence of PSP toxicity, beginning in late May or early June. The plume is influenced

by freshwater flow, wind, and bathymetry, with predictable consequences for the location and timing of

coastal PSP events. Extensive freshwater flow in early May creates a strong, fast plume, while low river

flow may preclude the formation of a coastal plume. Upwelling-favorable winds oppose the propagation 

of the plume, forcing it offshore and arresting its north-to-south motion. This tends to halt the

alongshore propagation of toxicity, leaving the southern regions toxin-free. In contrast,

downwelling-favorable winds force the plume against the coast, and accelerate its alongshore

propagation. Such conditions lead to widespread toxicity, and may account for the recent occurrence of 

PSP on Georges Bank (Franks and Anderson, 1992b). Understanding of the physical forcings that

influence the location and dynamics of the coastal buoyant plume, and information concerning the

abundance of Alexandrium cells within the plume have given us a limited predictive capability of the

location and timing of toxic outbreaks over large (>100 km) scales (Franks and Anderson, 1992b).

Other potential HAB Problems. The general view of the harmful algal bloom problem in New 

England is that PSP is widespread, persistent and expanding, while outbreaks of other harmful species

cause sporadic damage on a smaller scale. A realistic concern is that HAB species already present within

the region are likely to cause problems in the future. For example, an outbreak of Gymnodinium 

mikimotoi caused extensive benthic mortalities in 1988 in Maine, a region of New England that is

rapidly expanding its salmon farming industry. This fish-killing species causes recurrent and significant 

financial losses to the fish farming industries throughout the world. Likewise, Pseudo-nitzschia 

pungens f. multiseries, a diatom responsible for ASP, has been detected in Gulf of Maine waters, and

its toxin (domoic acid) detected in scallops. Over the last several years, DSP has been detected in

Canadian shellfish located just to the north of New England, where DSP is not yet a problem.

Some species, identified in other regions as problem algae, are regular components of the Gulf of Maine 

flora. The prymnesiophyte, Phaeocystis pouchetii, is a regular and sometimes dominant component of 

the spring bloom, but does not reach the high cell densities recorded in western Europe, where foam on

beaches, fouling of fishermen's nets, and other negative impacts are common.

Economic Impacts. The economic impact of these outbreaks is significant, though difficult to estimate 

in total. Shellfish monitoring programs in each of the coastal New England states have minimized

illnesses from PSP-contaminated shellfish and prevented any deaths. This extraordinary level of human

health protection has come at a cost that has never been directly quantified, but must be in the range of

millions of dollars per year, including the annual cost of the state and federal shellfish monitoring

programs (nearshore and offshore), the value of unexploited resources such as surf clams and roe-on 

scallops, and the loss to shellfishermen and retailers from shorter-term quarantines, including "spinoff"

effects on other perfectly safe fisheries products that are rejected by consumers during red tide

outbreaks. Estimates of the losses to shellfishermen and other seafood-related industries are few, but a

single PSP outbreak cost the state of Maine $6 million (Shumway et al., 1988).

Significant unknowns in our understanding of Alexandrium blooms include:

· What are the geographic origins of newly germinated cells that initiate the Alexandrium populations in 

the coastal current and the physical/behavioral mechanisms by which they enter the buoyant plume?

· Is accumulation of cells at small-scale fronts necessary for their entrainment in the buoyant plume?
3 of 16 1/30/07 3:32 PM

the long-distance transport?

· Is the localization of elevated Alexandrium populations within the plume a result of physical

entrainment, or does it reflect an increased growth rate in response to unique chemical properties of

plume waters?

· Are nearshore cells in the coastal current responsible for PSP offshore on Georges Bank?

· What are the hydrodynamic forcings that regulate PSP outbreaks in other areas of the Gulf of Maine?

· What effect does zooplankton grazing have on the Alexandrium populations, and what are the 

ecosystem impacts of toxin transfer through the food-web?

Mid-Atlantic Coastal Region: Brown Tides

Blooms of the small (2-3 μm) chrysophyte Aureococcus anophagefferens, referred to as "brown tide" 

due to the resulting water color, have been confirmed in many locations along the northeast coast of the

United States, especially in. Narragansett Bay, RI, Barnegat Bay, NJ, and the Peconics-Gardiners Bay

estuary and south shores of Long Island, NY (Cosper et al., 1989a). The figure on the next page shows

the widespread distribution of this organism in the northeastern U.S., including many areas with no

previous history of visible or destructive blooms (Anderson et al., 1993).

Brown tides are restricted to shallow, vertically well-mixed waters, and occur during late spring and 

summer at maxi mum concentrations of 3 x 109 cells l-1; bloom duration ranges from one to four

months. The first outbreak occurred concurrently in New York and Rhode Island in 1985, and blooms

have recurred in New York bays in subsequent years, with varying intensity, duration and geographic

spread. An immunofluorescent method is used for the reliable identification and quantification of A. 

anophagefferens.

Severe light attenuation in Long Island bays due to the brown tide caused a significant reduction in the 

depth penetration and leaf biomass of eelgrass (Dennison et al., 1989), which serves as an important

nursery habitat for numerous fish and shellfish. Brown tides also caused severe mortalities, recruitment

failure, and growth inhibition of commercially important, suspension-feeding bivalves, including blue

mussels in RI (Tracey, 1988) and bay scallops in NY (Bricelj and Kuenstner, 1989). Economic losses

from the brown tide for the New York State bay scallop fishery were estimated at $2 million per year

during early outbreaks.

Aureococcus adversely affects feeding of larval and adult bivalves, but only through direct cell contact. 

Although specific cell toxins have not yet been identified, the cell surface of this microalga contains a

bioactive compound that interferes with ciliary beat and thus food capture of bivalves, a response

mimicked by the common neurotransmitter, dopamine. Thus, impaired grazing by zooplankton and

filter-feeding benthos are believed to contribute to bloom occurrence.

The physico-chemical conditions that contribute to the formation of A. anophagefferens blooms are still 

largely unknown. Low annual rainfall, and increased residence time of bay waters that lead to increased 

salinity (> 28 ppt) may favor the development of the brown tide, as does increased water temperature

(Cosper et al., 1989b). Year-to-year persistence of A. anophagefferens in the Long Island region is 

partly attributed to its wide temperature tolerance and thus its ability to survive overwintering conditions.

Mesocosm experiments show that this alga grows well at relatively low concentrations of dissolved

inorganic nitrogen (DIN), and a negative correlation has been described between the abundance of 
4 of 16 1/30/07 3:32 PM

formation. The iron requirement of Aureococcus and its ability to grow in the presence of organic 

nutrients (e.g., glutamic acid) are higher than for many other common phytoplankton species. Viral

particles have been described and isolated from field-collected Aureococcus cells, and viral-lysis of algal 

cells has been attributed a potential role in bloom dissipation (Milligan and Cosper, 1994).

A number of questions need to be answered in order to more fully understand the physical and 

biological mechanisms controlling the population dynamics of A. anophagefferens , and the effects of

brown tides on nearshore marine communi ties.

· What role does micronutrient availability, especially via groundwater, play in controlling bloom

dynamics?

· What climatological-metereological and/or hydrographic events are associated with the regional

occurrence of the brown tide in the northeast?

· To what extent do biological mechanisms (e.g., grazing depression, competitive interactions with other

phytoplankton, and viral lysis) contribute toward the formation of monospecific blooms and subsequent

decline of the brown tide?

· Is microzooplankton grazing negatively impacted by brown tide? What are the toxins/metabolites that

cause species -specific inhibition of suspension-feeding in planktonic and benthic organisms?

· What are the time- and concentration-dependent effects of brown tides on marine fauna, during various

life history stages? What are the effects on submerged aquatic vegetation and its associated community

(secondary as well as primary consumers)? What are the long-term impacts of recurrent brown tides on

community trophic structure?

East Coast Region: Cyanobacterial Blooms

Harmful cyanobacterial blooms (HCBs) are indicative of excessive nutrient loading in oligohaline 

estuarine waters. These blooms represent economic and environmental threats nationally, and have

occurred in several large estuarine systems (e.g., Chesapeake Bay, Albemarle-Pamlico Sound, and

Florida Bay). Cyanobacterial blooms are also serious problems in freshwater systems. Here we 

highlight the east coast of the U.S., but cyanobacterial blooms occur in virtually every state, 

given the existance of toxic species in both freshwater and marine environments.

Bloom taxa include filamentous (Anabaena, Aphanizomenon ) and aggregated coccoid (Microcystis) 

genera, which exhibit severe neuro-, cyto-, and hepato-toxicity to a variety of mammals (including man),

birds, farm animals, fish, and invertebrates (including zooplankton). HCBs accumulate as buoyant

surface-dwelling, high biomass blooms. They impart negative aes thetic values, and cause taste and odor

problems. These blooms rapidly terminate or "crash" in response to sudden physical perturbations (e.g.,

rapid drop in temperature, sudden destratification and water column turnover, or reduced irradiance

associated with poor weather). When crashes occur, excessive oxygen consumption as the biomass 

decays can lead to anoxia. This chain of events has been responsible for major estuarine fish and

shellfish kills and loss of habitat for benthic infauna (Paerl, 1988a, 1990).

Conditions which favor harmful cyanobacterial bloom development and persistence include: 1) 

enhanced P and N loading; 2) increases in water retention time; 3) water column stability; 4) relatively

high dissolved organic matter content; and, 5) for nitrogen-fixing genera, molar N:P input ratios < 15:1.

Typically, blooms develop in oligohaline tributaries experiencing periods of excessive spring N and P
5 of 16 1/30/07 3:32 PM

remain for weeks to months (Paerl, 1988b). Grazing pressure by macrozooplankton has little impact on

either initiating or controlling cyanobacterial blooms. Trophic interactions and ecosystem structure are

often radically altered in response to such blooms (Porter and Orcutt, 1980; Fulton and Paerl, 1987).

While physiological and molecular knowledge of individual HCB species is good, knowledge of

growth, reproductive, and trophic dynamics on the ecosystem level is at best fragmentary.

Informational needs include:

· What trophic alterations (e.g., community changes and food transfer) are attributable to HCBs?

· What are the dynamics of akinete (cyst) dispersion, activation, and bloom initiation?

· To what extent can known and novel HCBs (e.g., Synechococcus spp. in Florida Bay; Nodularia, 

Schizothrix , and Lyngbya in reefs and intertidal environments) disperse into nutrient-enriched 

mesohaline/euhaline waters?

· What are the genetic and physiological potentials for such species dispersal?

· How does the ability to fix atmospheric nitrogen (N 2), facilitate expansion into N-limited estuaries or

freshwater systems?

East Coast Region: Fish Kills

In 1991, an ichthyotoxic dinoflagellate with "ambush predator" behavior and a complex life cycle was 

discovered at a fish kill in the Pamlico River, a large estuary in the Southeast (Burkholder et al., 1992,

1995). The organism, Pfiesteria piscicida (Steidinger et al., submitted; 1995), represents a new family, 

genus, and species of armored dinoflagellates. Its cryptic or "phantom-like" behavior was observed

several years earlier when it appeared as a contaminant of unknown origin in aquarium fish cultures

(Burkholder et al., 1992; Smith et al., 1989).

Unknown substances freshly secreted by finfish and shellfish stimulate P. piscicida to transform from 

benthic cysts or amoebae, or non-toxic flagellated stages to toxic zoospores. Highly lipophilic

exotoxin(s) are released to the water and travel as micelles that narcotize finfish, slough fish epidermis,

and cause formation of open bleeding sores (see photo below), while also damaging osmoregulatory

function (Noga et al., in press). In some species, (e.g., striped bass), extensive hemorrhaging also

occurs. This dinoflagellate has proven lethal to every fish species tested, including more than 20 native 

and exotic species (Burkholder et al., in press). At sublethal densities, Pfiesteria-like dinoflagellates 

likely cause significant chronic impacts to fish populations, affecting recruitment, reproduction, and

disease resistance. Clinical research recently demonstrated that P. piscicida is the causative agent of the 

disease known as ulcerative "mycosis" in Atlantic menhaden (Noga et al., in press). The Pamlico is

known for high incidence of fish ulcerations and up to 98% of all fish sampled in this estuary have 

manifested large, open, bleeding sores during warmer months.

The dinoflagellates consume bits of epidermal tissue and blood cells from affected fish while also 

engulfing bacteria, phytoplankton, and other microfauna. In addition, they produce gametes that

complete sexual fusion in the presence of dying fish. Upon fish death, toxic zoospores and planozygotes

form non-toxic amoeboid stages that feed on the fish remains, or without abundant food resources, the

toxic stages encyst. In the absence of live fish, gametes and toxic zoospores revert to non-toxic

zoospores that remain highly active in phosphate-enriched waters, especially when flagellated algal prey 

are abun dant (Burkholder and Glasgow, 1995). Surprisingly, most of the 19 known life cycle stages
6 of 16 1/30/07 3:32 PM

In enclosed laboratory conditions, human exposure to aerosols from toxic cultures with live fish has 

been linked to a variety of short- and long-term symptoms, including narcosis, respiratory distress with

asthma-like symptoms, severe stom ach cramping, nausea, vomiting, and eye irritation. Other autonomic

nervous system dysfunction such as high, localized perspiring and erratic heart beat may last for weeks.

Central nervous system dysfunction, including sudden rages and other erratic behavior can last hours to

days, and reversible cognitive impairment for weeks; chronic effects such as sustained asthma-like

symptoms and suppressed immune system may last for months to years (Glasgow et al., in press).

The extent of P. piscicida's involvement in fish kills likely has been underestimated because of difficulty 

in reaching many kills when toxic zoospores are still present. Most Pfiesteria-associated field kills have 

occurred in quiet, upper estuarine tributaries with poor flushing rates, where both fish secreta and toxins

can accumulate and be more readily detected. During the past three years, P. piscicida has been 

implicated as the causative agent of ca. 50% of the major fish kills in large estuaries of the

Albemarle-Pamlico system, the only region where rigorous sampling protocols have been established 

(Burkholder et al., in press).

About two-thirds of the Pfiesteria-caused fish kills in North Carolina have occurred in the 

phosphate-rich Pamlico, and laboratory bioassays have shown that some life cycle stages are stimulated

by organic phosphate sources. Field surveys documented significantly higher abundance of zoospores at

sewage outfall sites relative to unpolluted sites. P. piscicida is euryhaline and eurythermal, with optimal 

growth at 15 psu and 26 oC, but with toxic activity from 2-35 psu and 10-33 oC (Burkholder et al., in

press). Some stages can remain active down to 5 oC. The wide salinity/temperature tolerance of P.

piscicida suggests that this species and its close relatives are probably widespread, at least in warm 

temperate/subtropical regions, acting as significant but often undetected sources of fish mortality and

disease. This species has been documented in sediments or water from the mid-Atlantic to the St. Johns

estuary in Florida. Recently, a second, apparently more subtropical, Pfiesteria-like species was identified 

(Landsberg et al., 1995).

Critical questions that need to be answered include:

· What is the geographic range of Pfiesteria -like dinoflagellates? Do they occur only in warm

temperate/subtropical areas or do they occur in colder regions as well?

· Can molecular probes be developed to facilitate detection of the various life cycle stages and/or the

toxins they produce?

· What are the toxins? What is their chemical structure?

· How do organic and inorganic nutrients control life cycle stages and/or toxicity?

· What chronic effects does Pfiesteria and its relatives have on fish recruitment, disease resistance, and

survival?

· What is the role of dinoflagellates in estuarine microbial food-webs in light of the discovery of

multiple, benthic amoeboid stages in Pfiesteria? Might these also be found in the life cycles of other 

dinoflagellates?

Southeast and Gulf of Mexico Regions: NSP

The toxic dinoflagellate Gymnodinium breve has a distribution from the Gulf of Mexico
7 of 16 1/30/07 3:32 PM

months; they impact fishing and tourist industries and alter population levels or recruitment potential of

affected marine animals. These recurrent bloom events cause an economic loss of approximately $18-24

million per episode (Steidinger and Vargo, 1988; Tester et al., 1991). Associated with this economic 

impact is an unquantifiable "halo" effect that results in reduced sales of all seafood products within the

region of the bloom and even outside the region.

The most likely scenario for the development of G. breve blooms in the Gulf of Mexico and South 

Atlantic Bight is the following. The source of the blooms appears to be on the west Florida shelf in the

eastern gulf where the Loop Current may entrain bloom patches and transport them into the South

Atlantic Bight via Loop Current filaments/eddies and the Gulf Stream system (Steidinger and Vargo,

1988; Tester et al., 1991, 1993). Eddies can also transport entrained blooms to the western gulf. Blooms

are initiated in association with Loop Current intrusions accompanied by upwelling on the west Florida

shelf. These blooms develop on the leading edge of the Loop Current front where the boundary layer is 

ideal for near -monospecific growth of G. breve. Typically the cyanobacterium Trichodesmium precedes 

or co-occurs with G. breve at bloom initiation and its presence may condition the water mass and

enhance G. breve growth as well as reduce grazing pressure. Bloom initiation is followed by population

growth in excess of predation, natural mortality, and advective loss, then by sustained growth

(maintenance), and finally by dissipation by advection or mixing of water masses. The physical integrity 

of the water mass appears to be the key factor controlling growth and maintenance of G. breve blooms. 

Offshore populations of G. breve can be transported shoreward with winds and inoculate inshore 

waters. Nutrient availability in the nearshore waters then contributes to the duration and intensity of

blooms. Although G. breve is more concentrated in surface waters, it is distributed throughout the water

column down to >50 m depths.

A conceptual framework for understanding G. breve blooms thus exists, but there are a number of

questions that need to be answered:

· In the life cycle of G. breve, does sexual reproduction only occur in the zone of initiation, and are 

resting cells such as cysts or zygotes present in sediments or at pycnoclines?

· Are there "hot spots" within the zone of initiation on the west Florida shelf that retain resting stages?

· Can molecular probes be used to detect toxins in seawater or identify different strains of G. breve?

· Is zooplankton grazing inhibited at moderate to high G. breve cell concentrations when brevetoxins or 

other substances are released? Does G. breve regulate plankton community structure?

· Are there multiple hydrographic features that are requisite for bloom initiation that can be detected

using moored instru ment arrays and remote sensing?

· Does Trichodesmium condition the water prior to G. breve blooms?

· What are the roles of macro- and micronutrients in the initial growth phase of blooms and how does

the situation change over time with bloom development?

Tropical Regions (Florida, Puerto Rico, U.S. Virgin Islands, 

Hawaii): Ciguatera

Ciguatera fish poisoning (CFP) is the most frequently reported non-bacterial illness associated with 

eating fish in the United States and its territories. The actual number of cases is, however, estimated to
8 of 16 1/30/07 3:32 PM

50% of the adults have been poisoned at least once. Many CFP intoxications have been reported from

temperate "inland" locations in the U.S., resulting from the commercial distribution of sub-tropical and 

tropical fish species.

Gambierdiscus toxicus, an epibenthic dinoflagellate, is the organism primarily responsible for ciguatera 

fish poisoning (Yasumoto et al., 1977). G. toxicus produces ciguatoxin precursors and analogues that 

are biotransformed during food-web transfers into ciguatoxin, the causative neurotoxin (Lewis and

Holmes, 1993). The ciguatera toxins are transported through herbivorous fish to carnivorous species,

where they accumulate and persist over extended periods. Fish exposed to ciguatoxin exhibit impaired

swimming behavior, and as a result may be subject to increased predation. Other toxic dinoflagellates,

including species of Prorocentrum, Ostreopsis and Coolia, share the same epiphytic habitat and entry 

routes into the food chain as G. toxicus, but remain only circumstantially linked to CFP since their 

toxins are not known to occur in fish at levels that can affect humans.

G. toxicus does not form pelagic blooms of motile cells, but is most prolific in shallow waters (3-15 m) 

primarily as an epiphyte on red and brown macroalgae associated with coral reefs and protected

embayments. Field and laboratory studies have established the temperature and salinity ranges of G. 

toxicus as 20-34 oC and 25-40 psu, respectively. Ciguatera endemic areas in both the Caribbean and

Pacific are characterized by oceanic salinities and are primarily associated with island land masses; CFP

is essentially absent along continental perimeters. In Florida, most cases of ciguatera are contracted in 

the summer, which is consistent with the elevated G. toxicus abundance observed during this period. By

comparison, in the Virgin Islands neither the number of CFP incidents nor G. toxicus abundance exhibit 

notable fluctuations. Overall, the spatio -temporal variability of CFP in a local area corresponds largely

to the patchiness of G. toxicus populations; however, it is difficult to explain the often rapid, localized 

changes in the concentration of this species based on a response to any one environmental factor (e.g.,

temperature, salinity, nutrients, etc.). The variable, localized occurrence of ciguatoxic dinoflagel lates

within a region may also be related to their rafting on drift algae, which is considered to be a primary 

means of dispersal.

Phenotypic variation in toxicity observed between clones from distinct geographical areas are stable in 

acclimated cultures and thus are indicative of genetic differences. For CFP cases occurring in the

Caribbean and eastern Atlantic, gastrointestinal symptoms occur first, while the characteristic

neurological manifestations of ciguatera develop later and may persist for weeks to months or even

years, producing chronic disabilities. Conversely, in the Pacific, neurological symptoms are exhibited

first, while gastrointestinal symptoms are minor or absent. These patterns in symptomology may reflect 

different geographic distributions of individual CFP toxin(s).

Presently, no coordinated, systematic monitoring progams exist for CFP in the U.S. and its territories. 

This poisoning syndrome has a significant impact on commercial and recreational fishing activities in the

U.S. and throughout the world.

Questions for future research include:

· Are there environmental factors that promote G. toxicus blooms or cause increases in the toxicity of 

this dinoflagellate? and, if so, can they be incorporated into predictive indices of CFP events?

· Can human activities such as reef destruction or pollution increase the scale of the problem?

· What roles do toxic species of Prorocentrum, Ostreopsis and Coolia play in CFP?

· Where and how are ciguatoxin precursors and analogues biotransformed in herbivorous and/or

carnivorous fish? How do ciguatera toxins affect food-web function?
9 of 16 1/30/07 3:32 PM

Southeast Region: Macroalgae

Macroalgae cause problems throughout the coastal waters of the U.S. This summary for southern 

Florida provides one example of the nature and scale of the problem.

Over the past several decades blooms of macroalgae (seaweeds) have been increasing along many of the 

world's develop ing coastlines in response to nutrient enrichment associated with coastal eutrophication.

In southern Florida, a diverse group of opportunistic macroalgal species outcompete, overgrow, and

replace seagrass and coral reef ecosystems that are adapted to stable, oligotrophic conditions. Moreover,

once they are established, the macroalgal blooms may remain in an environment for years to decades

until the nutrient supply decreases. This is in contrast to phytoplankton blooms that are usually relatively

short-lived (days to weeks).

The negative effects of eutrophication include nuisance blooms of macroalgae and attached filamentous 

epiphytes that reduce light availability to seagrasses (Sand-Jensen, 1977; Twilley et al., 1985; Silberstein

et al., 1986). This results in lower seagrass productivity, habitat loss from hypoxia/anoxia, and eventual

die-off of sensitive species (LaPointe et al., 1994).

Nutrient enrichment of Florida Bay and the Florida Reef Tract results from multiple nutrient sources and 

supply mecha nisms, including: 1) advection of phosphorus-rich water from the eastern Gulf of Mexico

into Florida Bay; 2) nitrogen-rich inputs from land-based agricultural activities that enter coastal waters

through the Everglades via groundwater discharge and surface runoff; and 3) nitrogen and

phosphorus-rich domestic wastewater generated in the Florida Keys that enters coastal waters via

groundwater discharge (septic tanks, cesspits, and injection wells) and surface water outfalls. This 

cumulative nutrient enrichment can cause high biomass algal blooms, which include the red algae

Laurencia intricata and Spyridia filamentosa, the brown algae Dictyota sp. and Sargassum filipendula, 

and the green algae Enteromorpha sp., Codium isthmocladum , and Halimeda sp.

Macroalgal blooms in South Florida, as well as other factors, have contributed to the marked decline in 

extent and vigor of seagrass ecosystems that provide a vital nursery habitat for pink shrimp, spiny

lobster, and finfish. These commercially -valuable marine species support multi-million dollar

recreational and commercial fisheries that have undergone drastic de clines over the past decade. The

Florida Reef Tract, the third largest coral reef in the world and the only coral reef system in North

America, supports the largest recreational dive industry in the world. This valuable reef system is being 

overgrown by macroalgal species. The trend could lead to ecological collapse of the Florida Reef Tract,

with subsequent economic losses in the tourist-related industries that support the most visited coral reef

and largest marine sanctuary in the world.

Questions for future research include:

· What are the physiological and ecological mechanisms that regulate the ability of macroalgae to alter the

patterns of nutrient storage and primary production by reducing the role of benthic macrophytes

(seagrasses) and increasing the importance of pelagic phytoplankton communities?

· How does increased macroalgal biomass accelerate nutrient release from sediment pore waters

underlying seagrass com munities, and how does this lead ultimately to seagrass die-off?

· What are the mechanisms for benthic-pelagic coupling of nutrients and primary production? How does

increased nutrient availability mediate a shift in primary production from reef corals to macroalgal

HABs?
10 of 16 1/30/07 3:32 PM

Gulf of Mexico Region (Texas): Brown Tide

For over 5 years, regions of the South Texas coast centered around the Laguna Madre have experienced 

a continuous, dense algal bloom referred to as the "brown tide." The nearly monospecific bloom has

been caused by high densities (1-5 x 10 9 cells/L) of a small (4-5 μm diameter) chrysophyte similar to

Aureococcus anophagefferens that causes brown tides on the U.S. northeast coast. Brown tide blooms

occur in shallow (1-2 m depth) embayments and lagoons that have minimal advective transport and/or

dispersion. The onset of the bloom was preceded by a drought (that increased the salinity) and severe 

freezes during periods of extremely low tides (Whitledge, 1993). Declines in invertebrate populations

and widespread fish kills were associated with these conditions. High ambient concentrations of

nutrients, especially nitrogen in the form of ammonium, resulted from the decaying fish. Ammonium is

important because the Texas brown tide species cannot utilize nitrate (DeYoe and Suttle, 1994).

Although bloom initiation depended on the increased ammonium, its persistence was facilitated by 

severe declines in grazer populations and continued low rates of advection and physical dispersion

(Buskey and Stockwell, 1993). However, generalizations about nutrient effects, flushing, and trophic

antagonism are not sufficient to predict the occurrence, persistence, or long term effects of the brown

tide.

The environmental and economic impact of the Texas brown tide stems from effects on several 

components of the food -web. Zooplankton and larval fish do not eat the brown tide alga, but more

importantly, after a threshold cell density is reached, their mortality increases. Eggs of important

estuarine fish species (e.g., red and black drum, spotted seatrout) have reduced hatching and the young

larvae rapidly die from lack of food. Large declines in the abundance of benthic filter feeders have also

been observed. Exudate(s) from the brown tide organisms are thought to be responsible for these 

effects, but specific inhibitory compounds have not yet been identified. Another harmful effect of dense

brown tides is a decline in the abundance of seagrasses due to light absorption by the microalgae. Severe

long-term ecological changes thus result from the combination of loss of seagrass habitat and the

reduced abundance of secondary consumers in the water and sediments. The economic losses to tourism

and recreational fishing caused by the Texas brown tide are estimated to be several million dollars

annually.

Important questions for future research include:

· To what extent do external nutrient sources and their elemental composition moderate brown tide

blooms?

· What external or internal factors besides nutrient availability lead to the decline or dissipation of a

brown tide bloom?

· To what extent do brown tide organisms modify environmental conditions so as to enhance their

survival?

· What is the nature of the growth and feeding inhibition associated with brown tide blooms? Are toxins

involved?

Pacific Coast Region (California and Oregon): PSP, ASP

Paralytic Shellfish Poisoning (PSP). Paralytic shellfish poisoning has a long history on the U.S. west 
11 of 16 1/30/07 3:32 PM

field surveys focused on this species. What little is known has been gleaned from shellfish -toxin

monitoring programs (Price et al., 1991). In California, blooms of A. catenella cause toxicity nearly 

every year. PSP toxins are usually highest during July and August with most toxic events occurring

from May to October. PSP is known to accumulate in numerous benthic filter feeders, and there is

considerable variability among species with respect to toxin retention (Price et al., 1991).

Hydrographic mechanisms underlying the PSP problems along the west coast are poorly understood. A 

good case can be made that PSP outbreaks in some areas of California occur following the relaxation of

seasonal upwelling. This moves offshore waters and their established dinoflagellate populations rapidly

to the coast, causing increases in toxicity far faster than can be attributed to in situ growth alone. A

similar mechanism linking shellfish toxicity to changes in upwelling condi tions has been reported for

the northwest coast of Spain (Fraga et al., 1988), where hydrographic conditions resemble those along

the northern California coast.

A number of questions underlying California and west coast PSP outbreaks remain to be resolved:

· Where are the source populations for the coastal blooms? If cysts are involved, where are the seedbeds

located? Do blooms spread from one or a few points of origin or do isolated blooms develop

simultaneously in several locations in response to similar hydrographic conditions? Do blooms originate

in offshore waters, to be advected onshore with changes in meteoro logical conditions?

· What are the important meteorological or hydrographic forcings underlying toxicity in the different

regions along the coast?

· If outbreaks are tied closely to transport of offshore waters and cells to coastal sites, can those events

be detected and predicted using moored instruments and weather forecasts?

· What effect do recurrent blooms of toxic dinoflagellates have on west coast ecosystems, at all levels

from zooplankton to fish and marine mammals?

Domoic acid-producing diatom blooms. Domoic acid poisoning (DAP) , associated with ASP in 

humans, first became a concern along the west coast of North America in September, 1991 when more

than 100 brown pelicans and cormorants were found dead or suffering from unusual neurological

symptoms in Monterey Bay, CA (Fritz et al., 1992; Work et al., 1993). This event was attributed to a

bloom of the pennate diatom, Pseudo-nitzschia australis (Buck et al., 1992; Garrison et al.. 1992). At

the peak of the 1991 bloom, domoic acid levels were >10 μg/L and P. australis reached over 106 

cells/L. Since the 1991 autumn bloom, domoic acid has been detected in both autumn and spring

plankton assemblages in Monterey Bay, but with domoic acid concentrations usually < 1-5 μg/L, and P. 

australis densities of 104 -105 cells/L. Blooms during the 1991-1994 period often have been comprised

of two or three potentially toxic species (i.e., P. australis, P. pungens f. multiseries, and P. 

pseudodelicatissima); however, P. australis is believed to be the main source of the toxin. Domoic acid

production from locally-isolated clones has only been confirmed for P. australis (Garrison et al., 1992) 

and P. pungens f. multiseries (Villac et al., 1993).

Monitoring studies in Monterey Bay suggest blooms of P. australis are most common and persist 

longer during the summer to autumn months (Buck et al., 1992; Walz et al., 1994). Hydrographic

conditions during this period are characterized by warmer sea-surface temperatures, thermal

stratification, and lower concentrations of organic nutrients. In contrast, P. australis blooms in southern 

California appear to be most common in the late spring to early summer months, and may be associ ated

with upwelling pulses (Lange et al., 1994).

The 1991 domoic acid producing bloom in Monterey Bay was somewhat unusual because toxin was 
12 of 16 1/30/07 3:32 PM

Haywood and Silver, 1994). With the exception of seabirds, nothing is known of the effects or impact

of domoic acid on the pelagic food-web.

It is difficult to assess the costs associated with the domoic acid blooms. In California, much of the cost 

of the domoic acid blooms is associated with the monitoring program conducted by the California

Department of Health Services (Langlois et al., 1993) and U.S. Food and Drug Administration (FDA).

The California Department of Health Services presently monitors domoic acid in conjunction with its

established PSP monitoring program, using intertidal mussels as "sentinel" organisms. This strategy

may prove to be inadequate because mussel monitoring is apparently not able to detect domoic acid 

when it is present in planktonic assemblages in low concentration (Walz et al., 1994). Mussel, rock crab,

and razor clam harvesting is a small sport fishing activity in California and their monetary losses from

blooms are difficult to assess.

Domoic acid-producing blooms are a relatively new phenomena in U.S. waters. Unanswered questions 

about these blooms include:

· What are the sources of domoic acid in West Coast waters? How many species of Pseudo-nitzschia are 

toxic? Are there other sources?.

· How is domoic acid production related to bacteria?

· Is domoic acid production in natural populations triggered by nutrient stress?

· How is domoic acid transported in marine food-webs? Are there effects on consumers at all trophic

levels?

Other Potential HAB Problems. Dinoflagellate species (e.g., Dinophysis spp.) associated with 

diarrhetic shellfish poison ing (DSP), noxious bloom- forming species such as Phaeocystis pouchetii, 

and setose diatom species (e.g., Chaetoceros convolutus and C. concavicornis ), that damage gills of

pen-raised finfish (see below) are found throughout the California Current region. Red-tides, apparently

all caused by non-toxic species, are common during the summer months.

Questions related to potential HAB problems include:

· What are the effects of high-density, monospecific blooms of non-toxic "red tide" forming species on

food-web structure?

· What are the occurrences and distributions of the potentially harmful species in California coastal

waters?

· How are HAB species dynamics related to hydrographic events on short-term, seasonal, and

interannual time scales?

· What is the importance of meso-scale features and short-term events on bloom dynamics?

· How do the life cycles of the HAB species influence their distribution and population cycles?

Pacific Coast Region (Washington): PSP, ASP, Finfish 

Mortalities
13 of 16 1/30/07 3:32 PM

Paralytic Shellfish Poisoning. Following the deaths of three people and mass mortalities of seabirds in 

1942, the Washing ton coast from Dungeness Spit on the Strait of Juan de Fuca to the mouth of the

Columbia River is closed each year from 1 April through 31 October for the harvest of bivalve

molluscs. PSP was not a problem in Puget Sound until 1978, but since then, it has apparently spread

southward with some closures now happening every year in central Puget Sound. The first closure in

southern Puget Sound occurred in 1988 and in northern Hood Canal in 1991.

The causative organisms are members of the dinoflagellate genus Alexandrium. Species known from the 

area are A. catenella, A. acatenella, and A. tamarense . Two other potentially toxic species, A. ostenfeldii 

and A. hiranoi have been identified recently in British Columbia (Taylor and Horner, 1994).

Hydrographic mechanisms underlying the PSP problem in western Washington are poorly understood. 

There have been no sustained field programs, so bloom dynamics and physical forcings remain

significant and important unknowns. PSP along the ocean coast and in coastal bays appears to be caused

by blooms originating offshore. In Puget Sound, blooms originate in situ and toxicity may be

widespread or very localized (Nishitani and Chew, 1988). A combination of physical factors and

nutrient supply may explain why PSP has not been a problem in central and southern Hood Canal 

(Rensel, 1993). Some PSP outbreaks have been correlated with El Niño events (Erickson and Nishitani,

1985).

Economic impacts include the costs of shellfish and phytoplankton monitoring by state health officials, 

the closure of many beaches to the recreational harvest of shellfish during the summer months, and lost

tourist trade. Commercial sales may be affected if the public thinks shellfish are contaminated. Recently,

the harvest of non-traditional shellfish, such as predatory snails, has become a problem (Matter, 1994).

Important questions concerning PSP outbreaks in western Washington include:

· Where are the source populations for the blooms? Are cysts involved? If so, where are the seed beds?

· What meteorological or hydrographical forcings affect toxicity? Are outbreaks related to upwelling

events or other transport of offshore waters and cells to coastal areas? Can those events be

detected/predicted? What hydrographic conditions are necessary for blooms in inland waters?

· Do nutrients regulate/limit blooms in some areas?

Amnesic Shellfish Poisoning. Domoic acid was first found in razor clams on the Oregon/Washington 

coasts in late October 1991, and both commercial and recreational harvests of razor clams were halted.

Other bivalves, including comercially grown oysters and mussels were tested and did not contain the

toxin. However, domoic acid was also present in the viscera of Dungeness crabs and their commercial

harvest was closed for a short time. Since 1991, the fall and spring recreational seasons for razor clams

have been delayed, shortened, or not opened due to domoic acid. Furthermore, depuration of domoic 

acid from razor clams is apparently slow (Drum et al., 1993; Horner et al., 1993). In November 1994,

domoic acid was found for the first time in mussels from southern Hood Canal.

The causative organisms have not been identified with certainty, but it has been assumed that species of 

the diatom genus Pseudo-nitzschia are to blame. Known toxin-producing species present in Washington 

waters include P. australis, P. pungens f. multiseries , and P. pseudodelicatissima. Both P pungens f. 

pungens and P. pungens f. multiseries were present in the bloom in Hood Canal when domoic acid was

found in mussels.

As with PSP, hydrographic conditions related to domoic acid occurrence are not known. 
14 of 16 1/30/07 3:32 PM

occurred, extending from California to Alaska, linked to unusually warm weather conditions associated 

with an ENSO event in 1991.

The 1991 domoic acid incident caused an estimated $15 - $20 million in damages to the 

Oregon/Washington coastal economy. Losses included health effects, lost and/or delayed sales, lower

prices, lost jobs, bankruptcies, and lost recreational opportunities and tourist trade. No estimate is

available for losses since 1991.

Unanswered questions with regard to domoic acid and ASP include:

· What are the causative organisms? Are Pseudo-nitzschia spp. the only ones involved or are other 

diatoms and/or macroalgae also culprits?

· What is the source of the organisms? Is there an offshore bloom that is advected to inshore localities?

In Puget Sound, are there local seed populations in some areas?

· What is the life cycle of the Pseudo-nitzschia spp.?

· What environmental conditions are needed for domoic acid production by the cells?

· How do the razor clams and Dungeness crabs obtain domoic acid? How long does it take them to

depurate domoic acid? Under what conditions?

· Has the Washington incident been one event with slow depuration or is there continual reintoxication?

Finfish Mortalities. Catastrophic losses of cultured and wild fish sometimes occur due to species of 

phytoplankton that do not cause illnesses in humans. Blooms of the raphidophyte flagellate

Heterosigma carterae (sometimes called H. akashiwo or, erroneously, Olisthodiscus luteus ) have

occurred in British Columbia every year since the early 1960s and fish kills have been reported most

years since 1986; in Washington, fish kills occurred in pen-reared fish in 1989 and 1990, and wild fish 

in 1994. Losses to the fish growers are about $4-5 million per year when blooms occur. The way

Heterosigma kills is not known, but superoxide radicals may be involved because fish can be protected 

with the addition of superoxide dismutase (Yang et al., 1993). This organism is a vertical migrator,

usually occurring in surface waters during the day and at depth during the night. Vertical stability of the

water column is probably an important factor in maintaining blooms.

The harmful diatom species Chaetoceros concavicornis , C. convolutus, and perhaps C. danicus have

long setae armed with short secondary spines and may kill at fairly low concentrations (<10 4 cells/L).

Chains of cells apparently become lodged between secondary lamellae in the fish gills and cause blood

hypoxia as a result of mucus production. These diatoms may be restricted to near-surface waters or

mixed throughout the water column depending on local hydrographic conditions. Most fish growers

have their own phytoplankton monitors who sample at the pen sites on a daily basis from April through 

Septem ber. They also rely on reports from other phytoplankton monitoring programs. Economic losses

are about $0.5 million per event.

Unanswered questions here include:

· What environmental conditions cause blooms of Heterosigma?

· Does Heterosigma produce a toxin? If so, what is it? How does it kill the fish? What environmental 

conditions are needed for toxin production?
15 of 16 1/30/07 3:32 PM

any species with second ary spines (e.g., C. danicus) or capilli (long, hairlike siliceous spines, e.g., C. 

radicans) on the setae kill fish?

· Can harmful Chaetoceros species and/or other harmful phytoplankton species influence the 

distribution and abundance of finfish in inland waters of Washington State?

· What environmental factors affect the timing and magnitude of harmful Chaetoceros blooms in inland 

waters?

· Are phytoplankton associated with summer mortality of finfish? If so, which species?

Other HAB problems. Ceratium fusus and Gymnodinium sanguineum have been linked to mortality 

of oyster larvae and adults (Cardwell et al., 1977, 1979) and spot prawns (Rensel and Prentice, 1980) in

southern Puget Sound. There is no indication of a chemical toxin and mortality may be due to

mechanical means or oxygen stress when blooms decay.

The major questions for these species are:

· How do they cause mortality?

· How often do they cause shellfish mortality? Could these dinoflagellates, or other phytoplankton

species, be implicated in summer mortality of oysters?

Pacific Coast Region (Alaska): PSP, ASP, Bitter Crab Disease

Alaska, with 54% of the U.S. coastline, has a significant problem managing the impacts of HABs. 

Although some baseline information is available, virtually all studies have been either of short duration

and/or restricted to small geographic areas. No studies have critically and specifically evaluated HABs

on a broad geographic scale.

Paralytic Shellfish Poisoning. PSP is the most significant HAB problem in Alaska. Numerous 

beaches, bays, and coves in the southeast and east are periodically or perpetually plagued with high

levels of saxitoxins in blue mussels, butter, little necks, and horse clams, geoduck, oysters, and cockles.

Commercially valuable crabs are also affected. The causative species is apparently Alexandrium 

catenella, but other toxin-producing species may also be present. Toxic blooms have been reported in 

almost every month of the year, making it difficult to ascribe bloom conditions to any particular

environmental or hydrographical condition. One frequently reported trend is that shellfish from

headwaters of estuaries have more toxin than those collected near the mouths, perhaps suggesting that

blooms originate or grow better near the headwaters. It is certainly possible that the rising tide or certain

wind patterns may push toxic algae into shallow areas, but there is a growing perception that blooms 

originate offshore and move inland. Despite the prevalence of PSP, large areas of the coast remain

relatively free of toxins.

In 1917, 5 million pounds of shellfish products were harvested from Alaskan waters, but today the 

state's commercial bivalve industry is virtually nonexistent. The destruction of the clam industry,

estimated at 25-50 million pounds of bivalves per year, is in large part a result of product contamination

by PSP (Neve and Reichardt, 1984). Other commercially valuable species, such as Dungeness crabs,

are also affected by PSP, presumably from consumption of tainted bivalves. Other economi cally

valuable crustaceans have not tested positive for PSP.
16 of 16 1/30/07 3:32 PM

their swimming patterns, satellite imagery to identify and track blooms, and a citizen monitoring

program with an 800 number for reporting PSP illnesses, discolored water, fish kills, unusual behavior

of seabirds or mammals, etc. This program needs to be coupled with physical, chemical, and biological 

oceano graphic studies being conducted on the coast to provide insights into bloom formation, spread,

and collapse.

Questions that need to be answered with regard to PSP in Alaska include:

· What algal species are involved?

· What are their seasonal and geographic distributions?

· What hydrographic and environmental factors contribute to blooms?

· What information is needed to guide the development of a shellfish industry in a region with extensive

PSP problems?

Domoic Acid. Alaska does not have a severe problem with domoic acid, but low levels have been 

found in razor clams and Pseudo-nitzschia pungens and P. australis have been found in Alaskan

waters. Whether they produce domoic acid is not known.

While domoic acid is not yet a problem in Alaska, some questions are still pertinent:

· Do blooms of Pseudo-nitzschia occur in Alaskan waters? Are any of the populations toxic?

· What are the seasonal and geographic distributions of Pseudo-nitzschia spp., and what controls their 

abundance and toxic ity?

Other potential HAB Problems. Phaeocystis blooms occur occasionally in Alaska, and under 

conditions that are not well understood. This alga can be a major component of the spring bloom or

form a second, smaller bloom later. It produces both acrylic acid and DMSP, but the ecological and

environmental impacts of these compounds are not known. Southeastern Alaska shares with

Washington State the presence of several potentially harmful diatoms, e.g., Chaetoceros convolutus and 

C. concavicornis , however no problems have been associated with these species, since fish farming is

not yet a major industry..

A parasitic dinoflagellate, Hematodinium sp., has been of increasing concern since 1985 because it 

causes "bitter crab" disease. The parasite infects crabs during their molt (Love et al., 1993; Meyers et al.,

1987). Once established, it is 100% lethal and the crab meat becomes unmarketable before the crabs die.

Questions with regard to Phaeocystis and Hematodinium include:

· How extensive are the blooms, and what hydrographic/environmental factors favor them?

· What are the economical/societal costs of Phaeocystis blooms?

· What oceanographic conditions favor growth and survival of the parasitic Hematodinium sp. during its 

life cycle when it is not within the host Tanner crab? What natural controls are there to Hematodinium

abundance?
1 of 12 1/30/07 3:32 PM

The Ecology and Oceanography of Harmful Algal Blooms

A National Research Agenda

5. Literature Cited

Ahmed, F.E. (Ed). 1991. Seafood Safety. National Academy Press, Wash. D.C. 432 pp.

Anderson, D.M. 1995. Toxic red tides and harmful algal blooms: a practical challenge in coastal 

oceanography. Rev. Geophysics, Suppl. U.S. National Report to the Int. Union of Geodesy and

Geophysics 1991-1994. pp. 1189-1200.

Anderson, D.M. 1989. Toxic algal blooms and red tides: a global perspective. In: T. Okaichi, D.M. 

Anderson, and T. Nemoto (eds.), Red Tides: Biology, Environmental Science and Toxicology. Elsevier,

New York. pp. 11-16.

Anderson, D.M. and A.W.White. 1992. Marine biotoxins at the top of the food chain. Oceanus 

35:55-61.

Anderson, D.M. and B.A. Keafer. 1987. An endogenous annual clock in the toxic marine dinoflagellate 

Gonyaulax tamarensis. Nature 325:616 -617.

Anderson, D.M. and B.A. Keafer. 1992. Paralytic Shellfish Poisoning on Georges Bank: in situ growth 

or advection of established dinoflagellate populations. In: J. Wiggen and C.N.K. Mooers

(eds.).Proceedings of the Gulf of Maine Scientific Workshop, Urban Harbors Institute, Univ. Mass.

Boston. pp. 217-224.

Anderson, D.M., Keafer, B.A., Kulis, D.M., Waters, R.M., Nuzzi, R. 1993. An immunofluorescent 

survey of the brown tide chrysophyte Aureococcus anophagefferens along the northeast coast of the 

United States. J. Plankton. Res. 15: 563-580.

Anderson, D.M. and P.S. Lobel. 1987. The continuing enigma of ciguatera. Biol. Bull. 172:89-107.

Anderson, D.M. and K.D. Stolzenbach. 1985. Selective retention of two dinoflagellates in a well-mixed 

estuarine embayment: the importance of diel vertical migration and surface avoidance. Mar. Ecol. Prog.

Ser. 25:39-50.

Anderson, D.M. and D.Wall. 1978. Potential importance of benthic cysts of Gonyaulax tamarensis and 

G. excavata in initiating toxic dinoflagel late blooms. J. Phycol. 14:224-234.

Anderson, D.M., D.M. Kulis,, J.J. Sullivan, S. Hall, and C. Lee. 1990a Dynamics and physiology of 

saxitoxin production by the dinoflagellates Alexandrium spp. Mar. Biol. 104:511-524.

Anderson, D.M., D.M. Kulis, J.J.Sullivan, and S. Hall. 1990b. Toxin composition variations in one 

isolate of the dinoflagellate Alexandrium fundyense. Toxicon 28:885-893.
2 of 12 1/30/07 3:32 PM

Anderson, D.M., S.B. Galloway, and J.D. Joseph. 1993. Marine Biotoxins and Harmful Algae: A 

National Plan. Woods Hole Oceanographic Institution Tech. Rep. WHOI-93-02. 59 pp.

Anderson, D.M., S.W. Chisholm, and C.J. Watras. 1983. Importance of life cycle event in the 

population dynamics of Gonyaulax tamarensis. Mar. Biol. 76:179-189.

Bass, A.E., R.E. Malouf, and S.E. Shumway, 1990. Growth of northern quahogs (Mercenaria 

mercenaria [Linnaeus, 1758]) fed on picoplankton. J. Shellfish Res. 9:299-307.

Bates, S.S., Leger, C., Keafer, B.A., Anderson, D.M. (1993). Discrimination between 

domoic-acid-producing and non-toxic forms of the diatom Pseudonitzschia pungens using 

immunofluorescence. Mar. Ecol. Prog. Ser. 100:185-195.

Bates, S.S., C.J. Bird, A.S.W. deFreitas, R. Foxall, M. Gilgan, L.A. Hanic, G.R. Johnson, A.W. 

McCulloch, P. Odense, R. Pocklington, M.A. Quilliam, P.G. Sim, J.C. Smith, D.V. Subba Rao, E.C.D.

Todd, J.A. Walter, and J.L.C. Wright. 1989. Pennate diatom Nitzschia pungens as the primary source of 

domoic acid, a toxin in shellfish from eastern Prince Edward Island, Canada. Can. J. Fish. Aquat. Sci. 

46:1203-1215.

Bates, S.S., A.S.W. deFreitas, J.E. Milley, R. Pocklington, M.A. Quilliam, J.C. Smith, and J. Worms. 

1991. Controls on domoic acid production by the diatom Nitzschia pungens f. multiseries in culture:

nutrients and irradiance. Can. J. Fish. Aquat. Sci. 48:1136-1144.

Bates, S.S. and D.J. Douglas. 1993. Laboratory studies of domoic acid production by Pseudonitzschia 

pungens. Harmful Algae News 6:6-7.

Bates, S.S., D.J. Douglas, G.J. Doucette, and C. Léger. 1995. Effects of reintroducing bacteria on

domoic acid production by axenic cultures of the diatom Pseudonitzschia pungens f. multiseries . In: P.

Lassus, G. Arzul, E. Erard-Le Denn, P. Gentien, and C. Marcaillou-Le Baut (eds.), Harmful Marine

Algal Blooms. Lavoisier Publishing, Paris. pp. 401-406.

Berdalet, E. 1992. Effects of turbulence on the marine dinoflagellate Gymnodinium nelsonii. J. Phycol. 

28:267-272.

Berdalet, E. and M. Estrada. 1994. Effects of nitrogen and phosphorous starvation on nucleic acid and 

protein content of Heterocapsa sp. J. Plankton Res. 16:303-316.

Blumberg, A.F. and G.L. Mellor. 1987. A description of a three-dimensional coastal ocean circulation 

mode. In: Three-Dimensional Coastal Ocean Models, N.S. Heaps, ed. Coastal and

Bomber, J.W., D.R. Tindall, and D.M. Miller. 1989. Genetic variability in toxin production among 

seventeen clones of Gambierdiscus toxicus (Dinophyceae). J. Phycol. 25:617-625.

Boyer, G.L., J.J. Sullivan, R.J. Andersen, P.J. Harrison, and F.J.R.Taylor. 1987. Effects of nutrient 

limitation on toxin production and composi tion in the marine dinoflagellate Protogonyaulax tamarensis

. Mar. Biol. 96:123-128.

Bricelj, V.M. and S.H. Kuenstner. 1989. Effects of the "brown tide" on the feeding physiology and 

growth of bay scallops and mussels. In: E.M. Cosper, V.M. Bricelj and E.J. Carpenter (eds.), Novel

Phytoplankton Blooms: Causes and Impacts of Recurrent Brown Tides and Other Unusual Blooms.

Coastal and Estuarine Studies, Vol. 35. Springer-Verlag, Berlin. pp. 491-509.
3 of 12 1/30/07 3:32 PM

Buck, K.R., L. Uttal-Cooke, C.H. Pilskaln, D.L. Roelke, M.C. Villac, G.A. Fryxell, L. Cifuentes, and 

F.P. Chavez. 1992. Autecology of Pseudonitzschia australis Frenguelli, a suspected domoic acid 

producer, from Monterey Bay, California. Mar. Ecol. Prog. Ser. 84:293-302.

Burkholder, J.M. and H.B. Glasgow, Jr. 1995. Response of the toxic estuarine dinoflagellate, Pfiesteria 

piscicida to N and P from organic and inorganic sources. In: Abstracts, Annual Meeting, American

Society of Limnology and Oceanography, June 11-15, Reno, Nevada.

Burkholder, J.M., H.B. Glasgow, Jr., and C.W. Hobbs. In press. Distribution and environmental 

conditions for fish kills linked to a toxic ambush-predator dinoflagellate. Mar. Ecol. Prog. Ser.

Burkholder, J.M., H.B. Glasgow, Jr., and K.A. Steidinger. 1995. Stage transformations in the complex 

life cycle of an ichthyotoxic "ambush -predator" dinoflagellate. In: P. Lassus, G. Arzul, E. Erard-Le

Denn, P. Gentien, C. Marcaillou-Le Baut (eds.), Harmful Marine Algal Blooms. Lavoisier Publishing,

Paris. pp. 567-572.

Burkholder, J.M., E.J. Noga, C.H. Hobbs, and H.B. Glasgow, Jr. 1992. New 'phantom' dinoflagellate 

is the causative agent of major estuarine fish kills. Nature 358:407-410.

Buskey, E.J. and D.A. Stockwell. 1993. Effects of a persistent "brown tide" on zooplankton 

populations in the Laguna Madre of South Texas. In: T.J. Smayda. and Y. Shimizu (eds.), Toxic

Phytoplankton Blooms in the Sea. Elsevier Science Publ. B.V., Amsterdam. pp. 659-666.

Caperon, J. and J. Meyer. 1972. Nitrogen-limited growth of marine phytoplankton. II. Uptake kinetics 

and their role in nutrient-limited growth of phytoplankton. Deep-Sea Res. 19:619-632.

Cardwell, R.D., S. Olsen, M.I. Carr, and E.W. Sanborn. 1979. Causes of oyster larvae mortality in 

southern Puget Sound. NOAA Tech. Mem. ERL MESA-39. 73 pp.

Cardwell, R.D., C.E. Woelke, M.I. Carr, and E.W. Sanborn. 1977. Evaluation of water quality of Puget 

Sound and Hood Canal in 1976. NOAA Tech. Mem. ERL MESA-21. 36 pp.

Carlsson, P., E. Granéli, and P. Olsson. Grazer elimination through poisoning: One of the mechanisms

behind Chrysochromulina polylepis blooms. In: Graneli, E., B. Sundstrom, L. Edler, and D.M. 

Anderson (Eds.),Toxic Marine Phytoplankton , , Elsevier, New York. pp. 116-122.

Cembella, A.D., N.J. Antia, and P.J. Harrison. 1984. The utilization of inorganic and organic 

phosphorus compounds as nutrients by eukaryotic microalgae: a multidisciplinary perspective. Part. 1.

CRC Crit. Rev. Microbiol. 10:317-391.

Cembella, D., S.E. Shumway, and N.I. Lewis, 1993. Anatomical distribution and spatio-temporal 

variation in paralytic shellfish toxin composi tion in two bivalve species from the Gulf of Maine. J.

Shellfish Res. 12:389-403.

Cembella, A.D., J.J. Sullivan, G.I. Boyer, F.J.R. Taylor, and R.J. Andersen. 1987. Variation in 

paralytic shellfish toxin composition within the Protogonyaulax tamarensis/catenella species complex: 

red tide dinoflagellates. Biochem. System. Ecol. 15:171-186.

Chang, J. and E.J. Carpenter. 1991. Species specific phytoplankton growth rates via diel DNA 

synthesis cycles. V. Application to natural populations in Long Island Sound. Mar. Ecol. Prog. Ser.

78:115-122.
4 of 12 1/30/07 3:32 PM

and Effects of Recurrent Brown Tides and Other Unusual Blooms. Coastal and Estuarine Studies, Vol.

35. Springer-Verlag, Berlin. 799 pp.

Cosper, E.M. W. Dennison, A. Milligan, E.J. Carpenter, C. Lee, J. Holzapfel, and L. Milanese. 1989b. 

An examination of the environmental factors important to initiating and sustaining "brown tide" blooms.

In: E.M. Cosper, V.M. Bricelj, and E.J. Carpenter (eds.), Novel Phy toplankton Blooms: Causes and

Effects of Recurrent Brown Tides and Other Unusual Blooms. Coastal and Estuarine Studies, Vol. 35.

Springer-Verlag, Berlin. pp. 317-340.

Cullen, J.J. and S.G. Horrigan. 1981. Effects of nitrate on the diurnal vertical migration, carbon to 

nitrogen ratio, and the photosynethetic capacity of the dinoflagellate, Gymnodinium splendens . Mar.

Biol. 62:81-89.

Currin, C.A., H.W. Paerl, G.K. Suba, and R.S. Alberte. 1990. Immunofluorescence detection and 

characterization of N 2 -fixing microorganisms from aquatic environments. Limnol. Oceanogr.

35:59-71.

DeLong, E. F., G. S. Wickham, N. R. Pace. 1989. Phylogenetic stains: ribosomal RNA-based probes 

for the identification of single cells. Science 243: 1360-1364.

Dennison, W.C., G.J. Marshall, and C. Wigand. 1989. Effect of 'brown tide' shading on eelgrass (

Zostera marina L.) distributions. In: E.M. Cosper, V.M. Bricelj, and E.J. Carpenter (eds.), Novel 

Phytoplankton Blooms: Causes and Impacts of Recurrent Brown Tides and Other Unusual Blooms.

Coastal and Estuarine Studies, Vol. 35. Springer-Verlag, Berlin. pp. 675-692.

DeYoe, H.R. and C.A. Suttle. 1994. The inability of the Texas "brown tide" alga to use nitrate and the 

role of nitrogen in the initiation of a persistent bloom of this organism. J. Phycol. 30:800-806.

Donaghay, P.L. 1985. An experimental test of the relative significance of food quality and past feeding 

history to the limitation of egg produc tion of the estuarine copepod Acartia tonsa. Arch. Hydrobiol. 

Beih. Ergebn. Limnol. 21:235-245.

Donaghay, P.L. 1988. The role of temporal scales of acclimation, food quality and trophic dominance in 

controlling the evolution of copepod feeding behavior. Bull. Mar. Sci. 43:469-485.

Donaghay, P.L., H.M. Rines and J.M. Sieburth. 1992. Simultaneous sampling of fine scale biological, 

chemical and physical structure in stratified waters. Arch. Hydrobiol. Beih. Ergeb. Limnol. 36:97-108.

Dortch, Q., T.L. Roberts, J.R. Clayton, Jr., and S.I. Ahmed. l983. RNA/DNA ratios and DNA 

concentrations as indicators of growth rate and biomass in planktonic marine organisms. Mar. Ecol.

Prog. Series. l3:6l-7l.

Doucette, G.J. 1995. Interactions between bacteria and harmful algae: a review. Natural Toxins 3:65-74.

Doucette, G.J. and C.G. Trick. 1995. Characterization of bacteria associated with different isolates of 

Alexandrium tamarense. In: P. Lassus, G. Arzul, E. Erard-Le Denn, P. Gentien, C. Marcaillou-Le Baut

(eds.), Harmful Marine Algal Blooms. Lavoisier Publishing, Paris. pp. 33-38.

Douglas, D.J., U.P. Ramsey, J.A. Walter, and J.L.C. Wright. 1992. Biosynthesis of the neurotoxin 

domoic acid by the marine diatom Nitzschia pungens forma multiseries, determined with[ 13C]-labelled

precursors and nuclear magnetic resonance. J. Chem. Soc. Chem. Commun. 1992:714-716.
5 of 12 1/30/07 3:32 PM

Edvardsen, B., F. Moy, and E. Paasche. 1990. Hemolytic activity in extracts of Chrysochromulina 

polylepis grown at different levels of selenite and phosphate. In: E. Granéli, B. Sundström, L. Edler and

D.M. Anderson (eds.), Toxic Marine Phytoplankton. Elsevier Science Publ., New York. pp. 284-289.

Eppley, R.W., O. Holm-Hansen, and J.D.H. Strickland. 1968. Some observations on the vertical 

migration of dinoflagellates. J. Phycol. 4:333 -340.

Eppley, R.W., J.N. Rogers, and J.J. McCarthy. 1969. Half-saturation constants for uptake of nitrate and 

ammonium by marine phytoplankton. Limnol. Oceanogr. 14:912-920.

Erickson, G.M. and L. Nishitani. 1985. The possible relationship of El Niño/Southern Oscillation

events to interannual variation in Gonyaulax populations as shown by records of shellfish toxicity,. In: 

W.S. Wooster and D.L. Fluharty (eds.), El Niño North. Niño Effects in the Eastern Subarctic Pacific

Ocean. Washington Sea Grant Program, University of Washington, Seattle. pp. 283-290.

Falconer, I.R. (ed.) 1993. Algal Toxins in Seafood and Drinking Water. Academic Press, London. 224 

pp.

Falkowski, P.G., T.S. Hopkins, and J.J. Walsh, 1980. An analysis of factors affecting oxygen depletion 

in the New York Bight. J. Mar. Res. 38:479 -506.

Fiedler, P.C. 1982. Zooplankton avoidance and reduced grazing responses to Gymnodinium splendens

(Dinophyceae). Limnol. Oceanogr. 27:961-965.

Fraga, S., D.M. Anderson, I. Bravo, B. Reguera, K.A. Steidinger, and C.M. Yentsch. 1988. Influence 

of upwelling relaxation on dinoflagellates and shellfish toxicity in Ria de Vigo, Spain. Estuar. Coast.

Shelf Sci. 27:349-361.

Franks, P.J.S. 1992. Sink or swim: accumulation of biomass at fronts. Mar. Ecol. Prog. Ser. 82:1-12.

Franks, P.J.S. and D.M. Anderson. 1992a. Alongshore transport of a toxic phytoplankton bloom in a 

buoyancy current: Alexandrium tamarense in the Gulf of Maine. Mar. Biol. 112:153-164.

Franks, P.J.S. and D.M. Anderson. 1992b. Toxic phytoplankton blooms in the southwestern Gulf of 

Maine: testing hypotheses of physical control using historical data. Mar. Biol. 112:165-174.

Fritz L., M.A. Quilliam, J.A. Walter, J.C.L. Wright, A.M. Beale, and T.M. Work. 1992. An outbreak of 

domoic acid poisoning attributed to the pennate diatom Pseudonitzschia australis. J. 

Phycol.28:439-442.

Fulton, R.S. and H.W. Paerl. 1987. Toxic and inhibitory effects of the blue-green alga Microcystis 

aeruginosa on herbivorous zooplankton. J. Plankton Res. 9: 837-855.

Garrison D.L., S.M. Conrad, P.P. Eilers, and E.M. Waldron. 1992. Confirmation of domoic acid 

production by Pseudonitzschia australis (Bacillariophyceae) cultures. J. Phycol. 28:604-607.

Gentien, P. and G. Arzul. 1990. Exotoxin production by Gyrodinium cf. aureolum (Dinophyceae). J. 

Mar. Biol. Ass. U.K. 70:571-581.

Geraci, J.R., D.M. Anderson, R.J. Timperi, D.J. St. Aubin, G.A. Early, J.H. Prescott, and C.A. Mayo. 

1989. Humpback whales ( Megaptera novaeangliae) fatally poisoned by dinoflagellate toxin. Can. J. 

Fish. Aquat. Sci. 46:1895-1898.
6 of 12 1/30/07 3:32 PM

Glasgow, H.B., Jr., J.M. Burkholder, D.E. Schmechel, P.A. Tester, and P.A. Rublee. In press. 

Insidious effects of a toxic dinoflagellate on fish survival and human health. J. Toxicol. Environ. Health.

Granéli, E., E. Paasche, and S.Y. Maestrini. 1993. Three years after the Chrysochromulina polylepis 

bloom in Scandinavian waters in 1988: some conclusions of recent research and monitoring. In: T.J.

Smayda and Y. Shimizu (eds.), Toxic Phytoplankton Blooms in the Sea. Elsevier Science Publ. B.V.,

Amsterdam. pp. 23-32.

Habas, E.J. and C.K. Gilbert. 1974. The economic effects of the 1971 Florida red tide and the damage it 

presages for future occurrences. Environ. Letters 6:139-147.

Hall, S. l982. Toxins and toxicity of Protogonyaulax from the northeast Pacific. Ph.D. Thesis, Univ. of

Alaska, Fairbanks. 196 pp.

Hall, S., G. Strichartz, E. Moczydlowski, A. Ravindran, and P.B. Reichardt. 1990. The saxitoxins: 

sources, chemistry, and pharmacology. In: S. Hall and G. Strichartz (eds.), Marine Toxins: Origin,

Structure, and Molecular Pharmacology. American Chemical Society Symposium Series No. 418.

Washington, D.C. pp. 29-65.

Hallegraeff, G.M. 1993. A review of harmful algal blooms and their apparent global increase. 

Phycologia 32:79-99.

Hayhome, B.A., D.M. Anderson, D.M. Kulis, and D.J. Whitten. 1989. Variation among congeneric 

dinoflagellates from the northeastern United States and Canada. I. Enzyme electrophoresis. Mar. Biol.

101:427-435.

Haywood, G.J., and M.W. Silver. 1994. The concentration of domoic acid by zooplankton. Abstract. 

EOS 75:89.

Holmes, R.W., P.M. Williams, and R.W. Eppley. 1967. Red water in La Jolla bay, 1964-l966. Limnol. 

Oceanogr. 12:503-512.

Horner R.A., J.R. Postel, and J.E. Rensel. 1991. Noxious phytoplankton blooms and marine salmon 

culture in Puget Sound, Washington. In: J.R. Forbes (ed.), Pacific Coast Research on Toxic Marine

Algae. Can. Tech. Rep. Hydrogr. Ocean Sci. 135:59-61.

Horner, R.A., M.B. Kusske, B.P. Moynihan, R.N. Skinner, and J.C. Wekell. 1993. Retention of 

domoic acid by Pacific razor clams, Sliqua patula (Dixon, 1789): preliminary study. J. Shellfish Res. 

12:451-456.

Huntley, M. 1982. Yellow water in La Jolla Bay, California, July 1980. II. Suppression of zooplankton 

grazing. J. Exp. Mar. Biol. Ecol. 63:81-91.

Huntley, M., P. Sykes, S. Rohan, and V. Marin. 1986. Chemically-mediated rejection of prey by the 

copepods Calanus pacificus and Paracalanus parvus : mechanism, occurrence and significance. Mar.

Ecol. Prog. Ser. 28:105-120.

Kahn, J. and M. Rochel. 1988. Measuring the economic effects of brown tides. J. Shellfish Res. 

7:677-682.

Kamykowski, D. 1974. Possible interactions between phytoplankton and semidiurnal internal tides. J. 

Mar. Res. 32:67-89.
7 of 12 1/30/07 3:32 PM

Kamykowski, D. 1981. The simulation of a southern California red tide using characteristics of a 

simultaneously-measured internal wave field. Ecol. Model. 12:253-265.

Kamykowski, D. 1995. Trajectories of autotrophic marine dinoflagellates. Journal of Phycology 

31:200-208.

Keafer, B.A., and D.M. Anderson. 1993. Use of remotely-sensed sea surface temperatures in studies of 

Alexandrium tamarense bloom dynamics. In: T.J. Smayda and Y. Shimizu (eds.), Toxic Phytoplankton 

Blooms in the Sea. Elsevier Science Publ. B.V., Amsterdam. pp. 763-768.

Kodama, M., T. Ogata, and S. Sato. 1988. Bacterial production of saxitoxin. Agric. Biol. Chem. 

52:1075-1077.

Lam, C.W.Y and K.C. Ho. 1989. Red tides in Tolo Harbour, Hong Kong. In: T. Okaichi, D.M. 

Anderson, and T. Nemoto (eds.), Red Tides: Biology, Environmental Science and Toxicology. Elsevier,

New York. pp. 49-52.

Landsberg, J.H., K.A. Steidinger, and B.A. Blakesley. 1995. Fish-killing dinoflagellates in a tropical 

marine aquarium. In: P. Lassus, G. Arzul, E. Erard-Le Denn, P. Gentien, C. Marcaillou-Le Baut (eds.),

Harmful Marine Algal Blooms. Lavoisier Publishing, Paris. pp. 65-70.

Lange, C.B., F.M.H. Reid, and M. Vernet. 1994. Temporal distributions of the potentially toxic diatom 

Pseudonitzschia australis at a coastal site in southern California. Mar. Ecol. Prog. Ser. 104:309-312.

Langlois, G.W., K.W. Kizer, P. Smith, K. Hansgen, and R. Howell. 1993. Preliminary results of the 

California phytoplankton monitoring pro gram. In: Abstracts, Sixth International Conference on Toxic

Marine Phytoplankton, Nantes, France, October 18-22, 1993. p. 119.

LaPointe, B.E. and J.D. O'Connell. 1989. Nutrient-enhanced growth of Cladophora prolifera in 

Harrington Sound, Bermuda: eutrophication of a confined, phosphorus-limited marine ecosystem.

Estuar. Coast. Shelf Sci. 28:347-360.

LaPointe, B.E., D.A. Tomasko, and W.R. Matzie. 1994. Eutrophication and trophic state classification 

of seagrass communities in the Florida Keys. Bull. Mar. Sci. 54:696-717.

Lewis, R.J. and M.J. Holmes. 1993. Origin and transfer of toxins involved in ciguatera. Comp. 

Biochem. Physiol. 106C:615-628.

Lin, S., Chang, J. and E. J. Carpenter. 1994. Detection of proliferating cell nuclear antigen analog in 

four species of marine phytoplankton . J.Phycol.30: 449-456.

Love, D.C., S.D. Rice, D.A. Moles, and W.D. Eaton. 1993. Seasonal prevalence and intensity of bitter 

crab dinoflagellate infection and host mortality in Alaskan Tanner crabs Chionoecetes bairdi from Auke

Bay, Alaska, USA. Dis. Aquat. Org. 15:1-7.

Maclean, J.L. 1989. Indo-Pacific red tides, 1985-1988. Marine Pollution Bulletin 20:304-310.

Maranda, L., D.M. Anderson, and Y. Shimizu. 1985. Comparison of toxicity between populations of 

Gonyaulax tamarensis of eastern North American waters. Estuar. Coast. Shelf Sci. 21:401-410.

Martin, P. 1985. Simulation of the mixed layer at OWS November and Papa with several models. J. 

Geophys. Res. 90:903-916.
8 of 12 1/30/07 3:32 PM

Meyers, T.R., T.M. Koeneman, C. Botelho, and S. Short. 1987. Bitter crab disease: a fatal dinoflagellate 

infection and marketing problem for Alaskan Tanner crabs, Chionoecetes bairdi. Dis. Aquat. Org. 

3:195-216.

Millie, D.F., Baker, M.C., Tucker, C.S., Vinyard, B.T. and Dionigi, C.P. 1992. High resolution, 

airborne remote-sensing of bloom forming phytoplankton. J. Phycol. 28:281-290.

Milligan, K.L.D.and Cosper, E.M. 1994. Isolation of virus capable of lysing the brown tide microalga, 

Aureococcus anophagefferens. Science 266:805-807.

Montagna, P.A., D.A. Stockwell, and R.D. Kalke. 1993. Dwarf surfclam Mulinia lateralis (Say, 1822) 

populations and feeding during the Texas brown tide event. J. Shellfish Research 12:433-442.

Morejohn G.V., J.T. Harvey, and L.T. Krasnow. 1978. The importance of Loligo opalescens in the 

food-web of marine invertebrates in Monterey Bay, California. Calif. Dept. Fish Game, Fish. Bulletin.

169:67-98.

Murakawa, M. 1987. Marine Pollution and countermeasures in Japan. Oceanus 30:55-60.

Neve, R.A. and P.B. Reichardt. 1984. Alaska's shellfish industry,. In: E.P. Ragelis (ed.) Seafood 

Toxins. American Chemical Society Symposium Series 262. Washington, D.C. pp. 53-58.

Nishitani, L. and K. Chew. 1988. PSP toxins in the Pacific coastal states: monitoring programs and 

effects on bivalve industries. J. Shellfish Res. 7:653-669.

Noga, E.J., L. Khoo, J.B. Stevens, Z. Fan, and J.M. Burkholder. In press. Novel toxic dinoflagellate 

causes epidemic disease in estuarine fish. Mar. Poll. Bull.

Okaichi, T. 1989. Red tide problems in the Seto Inland Sea, Japan. In: T. Okaichi, D.M. Anderson, and 

T. Nemoto (eds.), Red Tides: Biology, Environmental Science, and Toxicology. Elsevier, New York.

pp. 137-142.

Okubo, A. 1971. Oceanic diffusion diagrams. Deep-Sea Res. 18:789-802.

Orellana, M.V. and M.J. Perry. 1992. An immunoprobe to measure Rubisco concentrations and 

maximal photosynthetic rates of individual phytoplankton cells. Limnol.Oceanogr. 37:478-490.

Oshima, Y., Sugino, K., Yasumoto, T. 1989. Latest advances in HPLC analysis of paralytic shellfish 

toxins. In: S. Natori, K. Hashimoto,and Y. Ueno (eds.) Mycotoxins and Phycotoxins. Elsevier,

Amsterdam. pp. 319-326

Paerl, H.W. 1988a. Nuisance phytoplankton blooms in coastal, estuarine and inland waters. Limnol. 

Oceanogr. 33:823-847.

Paerl, H.W. 1988b. Growth and reproductive strategies of freshwater blue- green algae 

(Cyanobacteria),. In: C.D. Sandgren (ed.), Growth and Reproductive Strategies of Freshwater

Phytoplankton. Cambridge University Press, Cambridge. pp. 261-315.

Paerl, H.W. 1990. Physiological ecology and regulation of N 2 fixation in natural waters. Adv.

Microbial Ecol. 11:305-344.

Peterson, C.H. and H.C. Summerson. 1992. Basin-scale coherence of population dynamics of an 
9 of 12 1/30/07 3:32 PM

Pollingher, U. and E. Zemel. 1981. In situ and experimental evidence of the influence of turbulence on

cell division processes of Peridinium cinctum forma westii (Lemm.) Lefevre. Br. Phycol. J. 16:281-287.

Porter, K.G. and J.D. Orcutt Jr. 1980. Nutritional adequacy, manageability, and toxicity as factors that 

determine food quality of green and blue -green algae for Daphnia. In W.E. Kerfoot (ed.), Evolution of 

Zooplankton Communities. University Press of New England, Hanover. pp. 268 -281.

Prandle, D. 1991. A new view of near-shore dynamics based on observations from HF radar. Prog. 

Oceanogr. 27:403-438.

Pratt, D.M. 1966. Competition between Skeletonema costatum and Olisthodiscus luteus in Narragansett 

Bay and in culture. Limnol. Oceanogr.11:447 -455.

Price, D.W., K.W. Kizer, and K.H Hansgen. 1991. California's paralytic shellfish poisoning prevention 

program, 1927-89. J. Shellfish Res. 10:119 -145.

Radach, G., J. Berg, and E. Hagmeier. 1990. Long-term changes of the annual cycles of meteorological, 

hydrographic, nutrient and phytoplank ton time series at Helgoland and at LV ELBE 1 in the German

Bight. Cont. Shelf Res. 10:305-328.

Rensel, J.E. 1993. Factors controlling paralytic shellfish poisoning (PSP) in Puget Sound, Washington. 

J. Shellfish Res. 12:371-376.

Rensel, J.E. and E.F. Prentice. 1980. Factors controlling growth and survival of cultured spot prawn, 

Pandalus platyceros, in Puget Sound, Washington. Fish. Bull. 78:781-788.

Rensel, J.E., R.A. Horner, and J.R. Postel. 1989. Effects of phytoplankton blooms on salmon 

aquaculture in Puget Sound, Washington: initial research. Northw. Environ. J. 5:53-69.

Reynolds, C.S. and A.E. Walsby. 1975. Water blooms. Biol. Rev. 50:437- 481.

Robineau, B., G.L. Fortier and A.D. Cembella. 1991. Potential impact of a toxic dinoflagellate (

Alexandrium excavatum) bloom on survival of fish and crustacean larvae. Mar. Biol. 198:293-301.

Sako, Y., N. Naya, T. Yoshida, C.H. Kim, A. Uchida, and Y. Ishida. 1995. Studies on stability and 

heredity of PSP toxin composition in the toxic dinoflagellate Alexandrium. In: P. Lassus, G. Arzul, E. 

Erard-Le Denn, P. Gentien, and C. Marcaillou-Le Baut (eds.), Harmful Marine Algal Blooms. Lavoisier

Publishing, Paris. pp. 401-406.

Sand-Jensen, K. 1977. Effect of epiphytes on eelgrass photosynthesis. Aquat. Bot. 3:55-63.

Sanders, R.W. and K. G. Porter. 1988. Phagotrophic phytoflagellates. In: K. Marshall (ed.), Advances 

in Microbial Ecology 10. Plenum Press, New York. pp. 167-192.

Seliger, H. H., J. H. Carpenter, M. Loftus, and W. D. McElroy. l970. Mechanism for the accumulations 

of high concentrations of dinoflagellates in a bioluminescent bay. Limnol. Oceanogr. l5: 234-245.

Shimizu, Y. 1993. Microalgal metabolites. Chemical Reviews. 93: 1685-1698.

Shimizu, Y., Norte, M., Hori, A., Genenah, A., and Kobayashi, M. 1984. Biosynthesis of saxitoxin 

analogues: the unexpected pathway. J. Am. Chem. Soc. 106: 6433-6434.
10 of 12 1/30/07 3:32 PM

Shumway, S.E. 1990. A review of the effects of algal blooms on shellfish and aquaculture. J. World 

Aquacult. Soc. 21:65-104.

Shumway, S., S. Sherman-Caswell, and J. Hurst. 1988. Paralytic shellfish poisoning in Maine: 

monitoring a monster. J. Shellfish Res. 7:643-652.

Sieburth, J. M., P.W. Johnson and P.E. Hargraves. 1988. Ultrastructure and ecology of Aureococcus 

anophagefferens gen. et sp. nov. (Chrysophyceae): the dominant picoplankter during a bloom in 

Narragansett Bay, Rhode Island, summer 1985. J. Phycol. 24:416-425.

Silberstein, K., A.W. Chiffings, and A.J. McComb. 1986. The loss of seagrass in Cockburn Sound, 

Western Australia. III. The effect of epiphytes on productivity of Posidonia australis Hook. F. Aquat. 

Bot. 24:355-371.

Smayda, T.J. 1990. Novel and nuisance phytoplankton blooms in the sea: evidence for a global 

epidemic. In: E. Granéli, B. Sundström, L. Edler, and D.M. Anderson.(eds.), Toxic Marine

Phytoplankton. Elsevier, New York. pp. 29-40.

Smayda, T.J. 1992. Global epidemic of noxious phytoplankton blooms and food chain consequences in 

large ecosystems. In: K. Sherman, L.M. Alexander, and B.D. Gold (eds.), Food Chains, Models and

Management of Large Marine Ecosystems. Westview Press, San Francisco. pp. 275 -307.

Smith, J.C., P. Odense, R Angus, S. Bates, C.J. Bird, P. Cormier, A.S.W. deFreitas, C. Léger, D.

O'Neil, K. Pauley, and J. Worms. 1990. Variation in domoic acid levels in Nitzschia species: 

implications for monitoring programs. Bull Aquacult. Ass. Can. 90:27-31.

Smith, S.A., E.J. Noga, and R.A. Bullis. 1989. Mortality in Tilapia aurea due to a toxic dinoflagellate 

bloom. Proc. 3rd Int. Colloquium Path. Mar. Aquaculture 167-168.

Steidinger, K.A. and G.A. Vargo. 1988. Marine dinoflagellate blooms: dynamics and impacts. In C.A. 

Lembi and J. R. Waaland (eds.), Algae and Human Affairs. Cambridge University Press, New York.

pp. 373-401.

Steidinger, K.A., E.W. Truby, J.K. Garrett, and J.M. Burkholder. 1995. The morphology and cytology 

of a newly discovered toxic dinoflagellate. In: P. Lassus, G. Arzul, E. Erard-De Denn, P. Gentien, C.

Marcaillou-Le Baut (eds.), Harmful Marine Algal Blooms. Lavoisier Publishing, Paris. pp. 83-88.

Steidinger, K.A., J.M. Burkholder, H.B. Glasgow, Jr., C.W. Hobbs, J.K. Garrett, E.W. Truby, E.J. 

Noga, and S.A. Smith. Submitted. Pfiesteria piscicida, gen. et sp. nov. (Pfiesteriaceae, fam. nov.), a 

new toxic dinoflagellate with a complex life cycle and behavior. J. Phycol.

Summerson, H.C. and C.H. Peterson. 1990. Recruitment failure of the bay scallop, Argopecten 

irradians concentricus, during the first red tide, Ptychodiscus brevis, outbreak recorded in North 

Carolina. Estuaries 13:322-331.

Swanson, R.I. and C.J. Sindermann (eds.). 1979. Oxygen depletion and associated benthic mortalities in 

New York Bight, 1976. NOAA Profes sional Paper 11. Rockville, MD. 345 pp.

Sykes, P. A. and M. E. Huntley. 1987. Acute physiological reactions of Calanus pacificus to selected 

dinoflagellates: direct observations. Mar. Biol. 94:19-24.

Taylor, F.J.R. 1993. Current problems with harmful phytoplankton blooms in British Columbia waters. 
11 of 12 1/30/07 3:32 PM

Taylor, F.J.R. and R.A. Horner. 1994. Red tides and other problems with harmful algal blooms in 

Pacific Northwest coastal waters. In: R.C.H. Wilson, R.J. Beamish, F. Aitkens, and J. Bell (eds.),

Review of the marine environment and biota of Strait of Georgia, Puget Sound, and Juan de Fuca Strait:

Proceedings of the BC/Washington Symposium on the Marine Environment, Jan 13 & 14, 1994. Can. 

Tech. Rep. Fish. Aquat. Sci. 1948:175-185.

Taylor, F.J.R. and U. Pollingher. 1987. Ecology of Dinoflagellates. In: F.J.R. Taylor (ed.), The Biology 

of Dinoflagellates. Blackwell Scientific Publ., Oxford. pp. 398-529.

Tester, P.A., M.E. Geesey, and F.M. Vukovich. 1993. Gymnodinium breve and global warming: What 

are the possibilities? In T.J. Smayda and Y. Shimizu (eds.), Toxic Phytoplankton Blooms in the Sea.

Elsevier Science Publ. B. V., Amsterdam. pp. 67-72.

Tester, P.A., R.P. Stumpf, F.M. Vukovich, P.K. Fowler, and J.T. Turner. 1991. An expatriate red tide 

bloom: transport, distribution, and persis tence. Limnol. Oceanogr. 36:1053-1061.

Therriault, J.C., J. Painchaud, and M. Levasseur. 1985. ontrolling the occurrence of Protogonyaulax 

tamarensis and shellfish toxicity in the St. Lawrence estuary: Freshwater runoff and the stability of the

water column. pp. 141-146 In: D. M. Anderson, A.W. White and D. G. Baden (eds.) Toxic 

Dinoflagellates, Elsevier, New York.

Thomas, W.H. and C.H. Gibson. 1990. Quantified small-scale turbulence inhibits a red tide 

dinoflagellate Gonyaulax polyedra Stein. Deep-Sea Res. 37:1583-1593.

Tomas, C. R. 1980. Olisthodiscus luteus (Chrysophyceae). V. Its occurrence, abundance and dynamics 

in Narragansett Bay, Rhode Island. J. Phycol. 16:157-166.

Tracey, G.A. 1988. Feeding reduction, reproductive failure, and mortality in Mytilus edulis during the 

1985 "brown tide" in Narragansett Bay, Rhode Island. Mar. Ecol. Prog. Ser. 50:73-81.

Trainer, V. L. and Baden, D. G. 1991. An enzyme immunoassay for the detection of Florida red tide 

brevetoxins. Toxicon 29:1387-1394.

Twarog, B.M., T. Hidaka, and H. Yamaguchi. 1972. Resistance of tetrodotoxin and saxitoxin in nerves 

of bivalve molluscs. Toxicon 10:273-278.

Twilley, R.R., W.M. Kemp, K.W. Staver, J.C. Stevenson, and W.R. Boynton. 1985. Nutrient 

enrichment of estuarine submerged vascular plant communities: 1. Algal growth and effects on

production of plants and associated communities. Mar. Ecol. Prog. Ser. 23:179-191.

Tyler, M. A. and H. H. Seliger. l978. Annual subsurface transport of a red tide dinoflagellate to its 

bloom area: water circulation patterns and organism distributions in the Chesapeake Bay. Limnol.

Oceanogr. 23: 227-246.

Tyler, M.A. and H.H. Seliger. 1981. Selection for a red tide organism: physiological responses to the 

physical environment. Limnol. Oceanogr. 26:310-324.

Villac, M.C., D.L. Roelke, F.P. Chavez, L.A. Cifuentes, and G.A. Fryxell. 1993. Pseudonitzschia 

australis Frenguelli and related species from the west coast of the U.S.A.: occurrence and domoic acid

production. J. Shellfish Res. 12:457-465.

Wall, D. l97l. Biological problems concerning fossilizable dinoflagellates. Geoscience and Man. 3:l-l5.
12 of 12 1/30/07 3:32 PM

Watras, C.J., S.W. Chisholm, and D.M. Anderson. 1982. Regulation of growth in an estuarine clone of 

Gonyaulax tamarensis Lebour: salinity-dependent temperature responses. J. Exp.. Mar. Biol. Ecol. 

62:25-37.

White, A.W. 1981. Marine zooplankton can accumulate and retain dinoflagellate toxins and cause fish 

kills. Limnol. Oceanogr. 26:103-109.

Whitledge, T.E. 1993. The nutrient and hydrographic conditions prevailing in Laguna Madre, Texas 

before and during a brown tide bloom. In: T.J. Smayda and Y. Shimizu (eds.), Toxic Phytoplankton

Blooms in the Sea, Elsevier Science Publ. B. V., Amsterdam. pp. 711-716.

Work, T.M., A.M. Beale, L. Fritz, M.A. Quilliam, M.W. Silver, K.R. Buck, and J.L.C. Wright. 1993. 

Domoic acid intoxication of brown pelicans and cormorants in Santa Cruz, California. In: T.J. Smayda

and Y. Shimizu (eds), Toxic Phytoplankton Blooms in the Sea. Elsevier Science Publ. B.V.,

Amsterdam. pp. 643-649.

Yang, C.Z., A.M. Yousif, T. Perkins, and L.J. Albright. 1993. The mode of action of the toxic 

phytoplankter, Heterosigma akashiwo on juvenile sockeye salmon ( Oncorhynchus nerka). In: 

Abstracts, Sixth International Conference on Toxic Marine Phytoplankton, Nantes, France, October

18-22, 1993. p. 277.

Yasumoto, T., I. Nakajima, E. Chunque, and R. Adachi. 1977. Finding of a dinoflagellate as a likely 

culprit of ciguatera. Bull. Jpn. Soc. Sci. Fish. 43:1021-1026.

Yentsch, C.M., B. Dale, and J.W. Hurst. 1978. Coexistence of toxic and non-toxic dinoflagellates 

resembling Gonyaulax tamarensis in New England coastal waters (N.W. Atlantic). J. Phycol. 

14:330-332.

Young, W.R., P.B. Rhines, and C.J.R. Garrett. 1982. Shear-flow dispersion, internal waves and 

horizontal mixing in the ocean. J. Phys. Oceanogr. 12:515-527.

Zimmerman, J.T.F., 1986. The tidal whirlpool: A review of horizontal dispersion by tidal and residual 

currents. Netherlands J. Sea Res. 20:133 -154.