Ecohab the ecology and oceanography of harmful algal blooms : a national research agenda

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ECOHAB

THE ECOLOGY AND OCEANOGRAPHY OFHARMFUL ALGAL BLOOMS

A National Research Agenda

Property of CSC Library

DECEMBER 1995 US Department of Commerce
NOAA Coastal Services Center Library,
2234 South Hobson Avenue
Charleston, SC 29405-2413

This document was published and distributed by the Woods Hole Oceanographic Institution,
with support from the Division of Ocean Sciences of the National Science Foundation and
the National Oceanic and Atmospheric Administration's Coastal Ocean Program.
Copies can be obtained from:

Donald M. Anderson
Biology Department, MS#32, Woods Hole Oceanographic Institution
Woods Hole, MA 02543-1049
Tel: 508-289-2351 * Fax: 508-457-2134
e-mail: [email protected]

Cover photo: A massive "red tide" of the dinoflagellate Noctilaca stretching more than 20 miles along the
Southern California coast. Blooms such as this one can be harmless, or they can have devastating impacts on
human health, coastal economies, and marine ecosystems. Photo by P.J.S. Franks.

Inside cover: Dead fish and discolored water during a Florida red tide. Photo courtesy of Florida Department of
Environmental Protection.

CONTENTS

E C 0 H'A B

THEECOLOGY AND OCEANOGRAPHY OFHARMFULALGALBLOOMS

A National Research Agenda

Preface ........................... ...................................... ............................ .....................................................................................................................2

Executive Summary ......................................................................................................I...................................................................-...........3

1. Introduction
1.1 The Nature of Harmful Algal Bloom Phenomena... ......... .............................. .......................... ..........................7
1.2 HAB Impacts ........ ..................................... ....................................................... ........................................ ................. .....................7
1.2.1 Public Health and Ecosystem Effects ....................... ......... .........................................-................... ..................7
1.2.2 Economic Impacts ............................................................................................. ....................................................... ....... 10
1.3 Recent Trends .... ........................... ............ ........................................ ................................................................................ ........... 11

2. The ECOHAB Program
2.1 Why a National Program on HABs is Needed ............................. ......................................................................... 13
2.2 What is ECOHAB? ..................... .......... ............................... ........... ............................................................ . ............................. 13
2.3 Evolution of the ECOHAB Initiative ............. ................. .............................. .............................-....................... 13
2.4 The ECOHAB Strategy ......................... ........................................ ....................... 11 .............I............................. 14
2.5 Rationale and Benefits ..................................... ..................................................................... ........................... ............ 14
2.6 ECOHAB Implementation ......................................................................................... .................... ........... ........................... 15

3. ECOHAB Program Elements
3.1 The Organisms. ....... _ .............-........... .......... .......... _....... .......... __ ................ ............ ......... 16
3.1.1 Introduction ......................................_.................. ............................................................ ........................ ................... 16
3.1.2 Research Agenda ................... ............................. .................. .... ......*............- .............. .... ...*.. .................... 17
3.1.3 Summary .......................................................................... ......................... ............................................................................. 24
3.2 Environmental Regulation of Blooms ............................................ .............................. ................................ ............. 26
3.2.1 Introduction ........................... ............................................................................................................................................... 26
3.2.2 Research Agenda ............... .................................................... ............................................................... ........................... 26
3.2.3 Summary ............................................................................... ............................................ ............................................ ........ 33
3.3 Food-web and Community Interactions ........................................................................................ ............................ 34
3.3.1 Introduction ...................................... ............................................................................................... ................................ _. 34
3.3.2 Research Agenda ........................... ........................................ ........................................................................................ _ 34
3.3.3 Summary .................. ..................................................................................................................................... __ ...................... 41

4. Regional HAB Phenomena in the United States .............. ............................... ............................... ............................. 42

5. Literature Cited .......................... ............................................................................................................................................................. 59

Appendix: List of Workshop Participants ..........................I.................................................. ........................................... 65

PREFACE

For many years, the United States has the Coastal Environment; PhysicallBiological In-
struggled to manage fisheries resources and teractions; and, Emerging Technologies. Follow-
marine ecosystems impacted by an expanding ing these presentations and extensive plenary
array of toxic and harmful algae. Our under- discussions, participants were divided into
standing of the fundamental ecological, toxi- working groups and charged with identifying
cological, and oceanographic issues underly- research priorities, approaches and essential
ing these phenomena, however, is woefully technologies in three theme areas: The Organ-
inadequate. In recognition of this shortcom- isms, Environmental Regulation of Blooms, and
ing, the National Science Foundation (NSF) and Food-WeblCommunity Interactions. Alternating
the National Oceanic and Atmospheric Admin- between working group sessions and plenary
istration (NOAA) co-sponsored a workshop on discussions, research issues and priorities were
the Ecology and Oceanography of Harmful Al- refined for each of these program elements .
gal Blooms at the Snow Mountain Ranch Con- This national research agenda is being
ference Center, CO from 23-28 August 1994. widely circulated to individual scientists,
This research agenda is the result of those de- agency personnel, government officials and sci-
liberations. The forty workshop participants ence administrators. Feedback is welcome at
(Appendix A) included academic and govern- all stages and on all aspects of this planning
ment scientists as well as program managers process.
and officials representing the NSF, NOAA
Coastal Ocean Program, Sea Grant, and the Na- Acknowledgements. The workshop was
tional Marine Fisheries Service. The scientists sponsored by the Division of Ocean Sciences
attending the workshop were selected from of the National Science Foundation, and by the
among nationally recognized leaders in fields Co 'astal Ocean Program of the National Oce-
spanning both the biological and physical sci- anic and Atmospheric Administration. Maine
ences. The diverse composition of the group and Texas Sea Grant Programs provided sup-
(Appendix A) reflects the interdisciplinary na- port for several participants, and the South-
ture of this subject as well as the need to so- east Fisheries Science Center of the National
licit recommendations from the oceanographic Marine Fisheries Service in Charleston SC pro-
community at large. vided staff support to help facilitate travel. Spe-
Position papers were prepared and distrib- cial thanks to Debbie Braddock and Ethel Le
uted prior to the workshop so all participants Fave for administrative support, to C. R. Tomas,
would be familiar with the issues and ques- T.J. Smayda, and P.J.S. Franks for serving as
tions associated with HABs. Selected partici- working group chairs, and to P. Donaghy, G. J.
pants were asked to present summaries of is- Doucette, D.L. Garrison, R. A. Horner, J.J.
sues reflecting their area of expertise and Cullen, and F.G. Plumley for their efforts as
geographical focus. Specific theme topics fell the Editorial Committee for this report.
under the general categories of: Physiology, Bio- Donald M. Anderson
chemistry and Genetics; Food-weblCommunity Workshop Chair
Interactions; Nutrients and Eutrophication in

EXECUTIVE SUMMARY

Over the last several decades, the United achieve these ends, a workshop was co-spon-
States has experienced an escalating and wor- sored by NSF and NOAA to develop a national
risome trend in the incidence of problems as- research agenda to guide activities in the spe-
sociated with harmful and toxic algae. Impacts cific area of HAB ecology and oceanography.
of these phenomena include mass mortalities The resulting program, called ECOHAB
of wild and farmed fish and shellfish, human (ECology and Oceanography of Harmful Algal
illness and death from contaminated shellfish Blooms) provides a scientific framework de-
or fish, death of marine mammals, seabirds, signed to increase our understanding of the
and other animals, and alteration of marine fundamental processes underlying the impacts
habitats or trophic structure through shading, and population dynamics of HABs. This in-
overgrowth, or adverse effects on life history volves a recognition of the many factors at the
stages of fish and other marine organisms. For- organismal level that determine how HAB spe-
merly only a few regions were affected by cies respond to, and potentially alter their en-
harmful algal blooms (HABs) in scattered lo- vironment, the manner in which HAB species
cations, but now virtually every coastal state affect or are affected by food-web and com-
is threatened, in many cases over large geo- munity interactions, and how the distribution,
graphic areas and by more than one harmful abundance, and impact of HAB species are
or toxic species. regulated by the environment.
It is still a matter of debate as to the causes In its simplest form, the goal of the ECOHAB
behind this expansion, with possible explana- program is:
tions ranging from natural mechanisms of spe-
cies dispersal to a host of human-related phe- To develop an understanding of the
nomena such as nutrient enrichment ' climatic population dynamics and trophic im-
shifts, or transport of algal species via ship pacts of harmful algal species which
ballast water. Whatever the reasons, virtually can be used as a basis for minimizing
all coastal regions of the U.S. are now subject their adverse effects on the economy,
to an unprecedented variety and frequency of public health, and marine ecosystems.
HAB events. The U.S. is not alone in this re-
spect, as nations throughout the world are The objective of the ECOHAB program is:
faced with a bewildering array of toxic or harm-
ful species and impacts and disturbing trends To investigate fundamental physical,
of increasing incidence. biological, and chemical oceanographic
HAB events are characterized by the prolif- questions critical to scientifically based
eration and occasional dominance of particu- management of fisheries resources,
lar species of toxic or harmful algae. As with public health, and ecosystem health in
most phytoplankton blooms, this proliferation regions threatened by toxic and harm-
results from a combination of physical, chemi- ful algae.
cal, and biological mechanisms and interac-
tions that are, for the most part, poorly under- ECOHAB is thus a scientific program that
stood. Some HABs are unique, however, due addresses important societal issues through
to their production of toxins and the manner advances in fundamental or basic research. The
in which they affect co-occurring organisms research priorities identified at the workshop
and alter food-web function. As identified in fell naturally into three main themes that rep-
Marine Biotoxins and Harmful Algae: A Na- resent the individual program elements of
tional Plan (Anderson et al., 1993), focused ECO14AB. The rationales, goals, and specific
research into these ecological and oceano- objectives and activities of each program ele-
graphic mechanisms is urgently needed. To ment are listed below.

ExECUTIVE SUMMARY
41

Program Element # I Program Element # 2
The Organisms Environmental Regulation of Blooms

Rationale: The negative impacts of HABs Rationale: Concurrent with escalating in-
reflect not only the growth and metabolism fluences of human activities on coastal eco-
of individual algal cells, but the ecological se- systems, the environmental and economic im-
lection of those cells within a diverse phy- pacts of HABs have increased over recent
toplankton assemblage. Studies at the decades. It is therefore imperative to know if
organismal level are essential if we are to present trends of human activities and HABs
understand the population dynamics of HABs will lead to unacceptable consequences, and
and their toxic and/or harmful effects. if the means can be developed to mitigate nega-
tive impacts. The key to this knowledge is an
Goal: To determine the physiological, bio- understanding of the ecology and oceanogra-
chemical, genetic, and behavioral features and phy of HABs. An important facet of this com-
mechanisms of harmful algal species that in- plex topic is environmental regulation, that is,
fluence their bloom dynamics, general ecol- the influence of environmental factors on the
ogy, and negative impacts. population dynamics of harmful algal species
and their competitors.
Specific objectives:
� Develop methods to rapidly and accurately Goals: 1) Determine and parameterize the
identify, enumerate, and physically separate environmental factors that govern the initia-
HAB species from mixed phytoplankton as- tion, growth, maintenance, dissipation and
semblages. impacts of HABs; and 2) Formulate principles
� Identify the life history stages of major HAB that explain similarities between ecosystems
species, determine what factors control tran- during HABs and understand how those sys-
sitions between those stages, and establish tems are unique with respect to the types of
the role of the stages in bloorn dynamics. blooms that occur.
� Characterize the physiological responses
and tolerances of HAB species to differing Specific objectives:
environmental conditions. Determine the extent to which HAB events
� Develop methods to permit in situ measure- reflect increases in growth rate versus physi-
ments of species-specific rates of growth, cal transport, immigration, and accumula-
photosynthesis, and nutrient uptake, and to tion. Determine whether there is a specific
assess the physiological condition of cells suite of physical factors with which known
at different times and locations. HABs are associated.
� Characterize the nutritional requirements, Investigate physical and ecological processes
uptake and nutrient assimilatory character- that control the partitioning of nutrients
istics of HAB species. within a system and the relationship be-
� Determine the functional role of toxins and/ tween nutrient inputs and population dy-
or exudates produced by HAB species. namics of HAB species.
� Define the genetic basis of toxin production, * Investigate whether there are specific physi-
elucidate toxin biosynthetic pathways, and cal, chemical, and biological regimes or pro-
determine how toxin accumulation in cells cesses that are associated with HAB events.
is regulated. * Determine whether some ecosystems are
� Investigate the mechanisms and impor- more susceptible to HABs than others. If so,
tance of motility and other behaviors of determine what makes them unique and
HAB species. whether they share characteristics that can
be used to anticipate HAB events in other
systems.
9 Characterize HAB population dynamics, in-
cluding the rate processes required in pre-
dictive models of bloom incidence.

ExECUTIVE SUMMARY
5

Program Element # 3 t
rograin ripIemieht "' n
Food-Webs and
Community Interactions The diverse nature of HAB phenomena and
the hydrodynamic and geographic variability
Rationale: The negative impacts of HABs associated with different outbreaks through-
are the result of complex interactions that be- out the U.S. pose a significant constraint to
gin at the phytoplankton community level and the development of a coordinated research ini-
extend to upper trophic level compartments. tiative. Where other multi-investigator oceano-
Habitat physics, life cycles, community struc- graphic research programs can concentrate
tures, growth and grazing processes all com- field activities on one specific area of the ocean
bine to regulate the dynamics of the HAB event. (e.g., GLOBEC on Georges Bank), no single
Therefore, studies on the impacts of trophic ECOHAB study site could be identified that
interactions in the selection and dynamics of would permit all of the major biological and
HABs, and conversely, the impacts of HAB physical features that underly HAB phenom-
events on trophic structure, processes and in- ena to be investigated. Given this diversity, the
teractions are essential if we are to understand ECOHAB program will rely on comparisons
the ecology and oceanography of harmful al- among large-scale, regional field programs, on
gal blooms. laboratory and mesocosm studies by individual
investigators or small groups, and on theoreti-
Goals: 1) Determine the impacts of trophic cal studies using new and existing models to
interactions on selection for, and dynamics of, provide realistic and testable simulations of
HABs; and 2) determine the impacts of HABs HAB dynamics in different oceanographic sys-
on trophic structure, processes and interac- tems. An integration of physical, chemical, and
tions. biological components is essential to all of
these approaches.
Specific objectives: The ECOHAB Research Agenda outlines re-
� Determine the extent to which bloom for- search priorities that are intended to guide
mation results from a breakdown of graz- agencies in the efficient allocation of resources
ing or from harmful species outcompeting targeted to HAB issues, and to help them for-
other phytoplankton for limiting resources. mulate new, multi-disciplinary HAB initiatives.
� Determine whether biological controls (e.g., The rate and extent of future progress will de-
grazers, allelopathy, pathogens) are the pend upon how the recommendations in this
cause of bloom termination. report are received and implemented. State and
� Investigate how HAB effects on the food- federal agencies should use this document to
web are controlled by toxin dynamics, food- identify topics that they can support, and indi-
web routing of toxins, and the differential vidual scientists should shape their specific
susceptibility of species at higher trophic lev- research programs to meet the perceived needs
els. Determine whether chronic, sublethal of the HAB community.
impacts of HABs are more significant than Despite the focus on ecology and oceanog-
acute (lethal) impacts. raphy and the exclusion of many other aspects
� Determine if HAB impacts are controlled by of HAB phenomena, the scope of the issues to
the degree of temporal and spatial overlap be addressed by ECOHAB exceed the resources
between blooms and critical life cycle stages of any one agency or program. ECOHAB will
of target species. be succesful only if a nationally coordinated
� Determine whether high biomass (non- interagency effort can be implemented to fo-
toxic) HABs adversely impact the food-web cus research personnel, facilities, and finan-
directly through reduced food quality, or in- cial resources to the common goals outlined
directly through environimental effects. in this comprehensive national strategy. No-
where else do the missions and goals of so
many government agencies intersect and in-
teract as in the coastal zone where HAB phe-
nomena 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

EXECUTIVE SUMMARY
61

identified, a Steering Committee will be ap-
pointed to oversee program implementation.
J Where necessary, small working groups or sub-
ittees will be convened to address spe-
Comm
cific program needs. Once ECOHAB is under
1- 4w- w
ay and research programs begin to
A!., accumulate results, regional and national work-
shops will be convened to identify common
mechanisms and processes underlying the di-
N
verse array of HAB phenomena and their im-
pacts. 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.

tionale and Benefits
Ra
J!
The significant economic, public health and
Y; 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 aquacul-
ture, 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
@i problems while providing new techniques and
basic scientific information relevant to plank-
ton ecology and oceanography in general. In
this respect, one compelling aspect of the
ECOHAB program derives from the need to
A nutritious meal of mussels can cause illness and even death when algal study individual HAB species, rather than
toxins are present. mixed planktonic assemblages. New auteco-
logical techniques must be developed, such as
remote detection of bloom populations using
satellites, swimming robots or moored instru-
ments. Methods are needed to "tag" target spe-
cies with molecular probes and then enumer-
ate cells or separate them from co-occurring
organisms, and techniques must be developed
to estimate in situ growth rates or cell physiol-
ogy. These are but a few examples of the areas
where new technologies developed to meet the
objectives of ECOHAB can benefit all of ocean-
ography.

1. INTRODUCTION

adverse effects can occur when algal cell con-
centrations are low and the water is clear. Fur-
thermore, blooms of benthic or planktonic
macroalgae can have major ecological impacts
Among the thousands of species of micro- such as the displacement of indigenous spe-
scopic algae at the base of the marine food cies, habitat destruction, oxygen depletion, and
chain are a few dozen which produce potent even alteration of biogeochernical cycles. The
toxins. These species make their presence causes and effects of macroalgal blooms are
known in many ways, ranging from massive thus similar in many ways to those associated
11 red tides" or blooms of cells that discolor the with harmful microscopic phytoplankton spe-
water, to dilute, inconspicuous concentrations cies. The scientific community now employs
of cells noticed only because of the harm the term "harmful algal bloom" (HAB) to de-
caused by their highly potent toxins. Blooms scribe this diverse array of bloom phenomena.
of non-toxic micro- and macroalgae (seaweeds)
also cause harm due either to indirect effects
of biomass accumulation (such as anoxia or "ITHMIN@iPAC
habitat alteration) or to physical features (such
as spines which lodge in fish gill tissue). Im- 1.2.1 Public Health and Ecosystem Effects
pacts of HAB phenomena include mass mor- One major category of public health impact
talities of wild and farmed fish and shellfish, from HABs occurs when toxic phytoplankton
human illness and death from contaminated are filtered from the water by shellfish such as
shellfish or fish, death of marine mammals, clams, mussels, oysters, or scallops, which then
seabirds, and other animals, and alteration of accumulate the algal toxins to levels that are
marine habitats or trophic structure. potentially lethal to humans or other consum-
The term "red tide" has been used to de- ers (Shurnway, 1990). These poisoning syn-
scribe some of these phenomena, since in cer- dromes are named paralytic, diarrhetic, neu-
tain cases, microalgal species increase in abun- rotoxic, and amnesic shellfish poisoning (PSP,
dance until they dominate the planktonic DSP, NSP, and ASP). Except for ASP, an alarm-
community and discolor the water with their ing new syndrome that results in permanent
pigments. The term is misleading, however, short-term memory loss in victims, all are
since non-toxic species can also bloom and caused by biotoxins synthesized by a group of
harmlessly discolor the water or conversely, marine algae called dinoflagellates. The ASP
toxin is produced by diatoms, a group of phy-
toplankton 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 pro-
duced by epibenthic dinoflagellates attached
to surfaces in many coral reef communities (re-
viewed in Anderson and Lobel, 1987).
Ciguatera toxins are transferred through the
food chain from herbivorous reef fishes to
larger carnivorous, commercially valuable fin-
DANGER fish. In a similar manner, the viscera of com-
mercially important fish such as herring, mack-
erel, or sardines are known to accumulate PSP
Area Closed toxins, endangering human health following
consumption of whole fish. Whales, porpoises,
Shellfish (oysters, clams, mussels, and other seabirds and other animals can be victims as
bivalve molluscs) in the area described below well, receiving PSP toxins through the food
contain paralytic toxins and are not safe chain via contaminated zooplankton or fish
f or use as food. (Geraci et al., 1989; Anderson and White,
1992). All of these poisoning syndromes oc-

1. INTRODUCTION
81

cur within the U.S. and its territories. food-web due to adverse effects on viability,
Another HAB impact occurs when marine growth, fecundity, and recruitment. As re-
fauna are killed by microalgal species that re- viewed by Smayda (1992), toxins can move
lease toxins and other compounds into the through ecosystems in a manner analagous to
water (Box 1.2.1), or that kill without toxins the flow of carbon or energy, and the impacts
by physically damaging gills or by creating low can thus be far-reaching and significant (Box
oxygen conditions as bloom biomass decays. 3.3.1). In this expanded context, it is evident
These impacts frequently occur at aquaculture that our present knowledge base is inadequate
sites where caged fish cannot escape the harm- even to define the scale and complexity of
ful blooms. Farmed fish mortalities from HABs many HAB phenomena.
have increased considerably in recent years, Blooms of macroalgae (seaweeds) can also
and are now a major concern to fish farmers be harmful, especially to seagrass and coral
and their insurance companies. Wild fish, how- reef ecosystems and the food-webs dependent
ever, may also be affected. The list of finfish, on those habitats. Nuisance seaweed species
shellfish and wildlife affected by microalgal replace indigenous macroalgae in the benthos
toxins is long and diverse (Table 1) and accen- and microscopic phytoplankton in the water
tuates the magnitude and complexity of this column. They thus modify benthic habitats,
one manifestation of HAB phenomena. It does affect microbial and macrofaunal foodwebs,
not, however, adequately document the true and alter key biogeochernical features of coastal
scale of that impact. ecosystems. Because seaweeds are generally
We are only now beginning to recognize benthic organisms and inhabit inshore coastal
that there can be impacts from toxic blooms waters that mark the interface between land
in virtually all compartments of the marine and sea, they are often the first primary pro-

Whether toxic or noxious algal species dominate a
bloom or alternatively, occur at low but- harmful levels
within a phytoplankton' community, their presence of-
ten affects other trophic levels, resulting in mass eco-
system dysfunction, public health risk, and enormous
economic losses. The devastating effects of HABs are
frequently seen on the west coast of Florida where the
proliferation of the toxic dinoflagellateGymnodinium
breve can result in massive fish kills, closure of shell-
fish beds due to NSP, and skin and respiratory irritation
to humans at the seashore. These blooms are respon-
sible for the loss of millions of dollars to the commer- hazard as they rot and decay, and birds such as peli-
cial and recreational fisheries and tourist industries. cans, seagulls, cormorants and possibly marine mam-
Pictured here are fish killed by red tide blooms, washed mals can become intoxicated by eating dead or dying
ashore either to accumulate on beaches or in small quiet fish. Photos courtesy of Florida Department of Environ-
coves near residential homes. These fish pose a health mental Protection.

1. INTRODUCTION
19

(Adapted from Anderson et al. 1993)

Harmful Algal Species Geographic Area Affected Organisms*

Alexandrium spp. (PSP) Northern Atlantic Mussels, surfclams, softshell clams,
and Pacific Coast sea scallops, butterclams, ocean quahogs
of North America oysters, gastropods, lobsters, crabs
Herring, salmon, menhaden, sandlance,
mackerel and possibly other fish species.
Whales, sea lions+, sea -otters+, sea birds
Squid, zooplankton, and other
benthic invertebrates

Alexandrium monilata Gulf of Mexico Oysters, coquinas, mussels, gastropods, fish

Pseudo-nitzschia Gulf of Maine; Puget Sound WA Mussels
pungens f. multiseries (ASP)

P. australis (ASP) California Anchovies, sea birds

R australis (ASP) Washington, Oregon Razorclams', Dungeness crabs'

Unidentified (ASP) Massachusetts and Maine Bay scallops+, Sea scallops'

Prorocentrum spp. Long Island Sound Northern quahogs, bay scallops

Gyrodinium aureolum Northern New England Mussels, softshell clams+

Aureococcus anophagefferens New York, Rhode Island, Bay scallops, mussels
New Jersey Anchoa sp., cladocerans

Gymnodinium breve (NSP) Gulf of Mexico, Bay scallops, surfclams, oysters,
South Atlantic Bight southern quahogs, coquinas.

Timicates

Many commercial and recreational
species of fish. Sea birds + , sea turtles,
manatees+, dolphins+

Chaetoceros spp. Pacific northwest Salmon aquaculture

Heterosigma carterae Pacific northwest Salmon aquaculture
Narragansett Bay wild fish,zooplankton

Unnamed gonyaulacoid Mid-Atlantic region Striped bass, flounder, croaker,
mullet, menhaden, pinfish, sea trout,
blue crabs, bay scallops

Gambierdiscus toxicus South Florida, Florida Keys, Grouper, snapper, mackerel,
Prorocentrum lima + Puerto Rico, U.S. Virgin Islands, jack, barracuda, parrot fish,
P. concavum + Hawaii, Guam tang, goat fish, and other finfish
P. hoffinannianum +
Ostreopsis lenticularis + Gastropods
0. siamensis

Found to contain algal toxins, or be adversely affected by toxic or harmful marine algae
+ Causative algae implicated, not confirmed.

1. INTRODUCTION
10@

ducers to be impacted by nutrient inputs from from groundwater (LaPointe and O'Connell
land. Indeed, increased nutrient supply seems 1989). This bloom, which many consider to be
to be implicated in virtually all harmful sea- the most dramatic ecological change in the re-
weed blooms. A dramatic example of the im- cent history of Bermuda's waters, led to a dra-
pact of macroalgal blooms was seen in Ber- matic decline in benthic species diversity, in-
muda, where the green macroalga Cladophora cluding the commercially-valuable calico clam.
prolifera formed widespread blooms of drift-
ing, filamentous balls that overgrew seagrasses 1.2.2 Economic Impacts
and corals in response to N and P enrichment 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,
Long Island bays, Now York wild or farmed fish mortalities, and frightened
1.0. Aureococcus anophageffemns consumers who avoid seafood (including prod-
0.9. blooms ucts which are totally safe) are well-known
impacts of major blooms of harmful algae
0.8
(Ahmed, 1991). Adverse health effects and lost
Z'0 0.7- sales of fish and shellfish products are direct
C I
00.6 costs, but constrained development or invest-
CL
0-6 0.5 ment decisions in coastal aquaculture due to
_J go
_J c 0.4 potential for outbreaks of toxic algae are
4 0 the
0- A A@
0 _@ 0.3 examples of indirect or hidden costs. Lost
S
C0.2 V marine recreational opportunities are also im-
0.1 VV portant indirect costs of harmful algal bloom
0 incidents. Unfortunately, no national estimate
1940 1950 1960 1970 1980 1990 of the combined economic costs of HAB phe-
YEAR nomena is available. Estimates from isolated,
individual events provide some indication of
700- North Carolina sounds the scale of the problem:
600- GYMnodinium bmve bloom A single PSP outbreak cost the state of Maine
an estimated $7 million in 1980 (Shurnway
et al., 1988). PSP outbreaks are annual
Z -0 500-
C
events in Maine, and several have been more
z 0
J !@ 400- severe than the 1980 event.
0. 0 An NSP outbreak in 1987-88 closed more
00
-A " 300- than 400 km of North Carolina coastline for
_J C,
shellfishing during the peak harvesting sea-
00 200- son, causing economic losses estimated at
$25 million (Tester et al., 1991)
10 Brown tide outbreaks in 1985 and several
succeeding years devastated the New York
i9G5 1970 1975 1980 1985 1990
66 -71 -76 -al -86 -91 state bay scallop industry. Economic losses
VEINTER HARVEST SEASON for the fishery were estimated at $2 million
per year (Kahn and Rochel, 1988). The
HAB outbreaks can have devastating effects on fisheries that brown tide has recurred on Long Island most
can extend years after the initial bloom episode. In these fig- years since 1985, and continues to have
ures, the clear effects of harmful algae are seen on two differ- major ecosystem and economic impacts. At
ent bay scallop fisheries, one as a result of recurrent blooms of this writing, legislation is under consider-
the brown tide alga Aureococcus anophagefferens in New York ation to have parts of Long Island declared
beginning in 1985 (top panel), and the other in response to a Disaster Areas as a result of a massive 1995
single bloom of Gymnodinium breve in North Carolina in 1987 outbreak.
(bottom). In both cases, the scallop landings were reduced to In 1987, phytoplankton blooms of the dia-
tom Chaetoceros convolutus were linked to
levels far below those of the recent past, resulting in economic the mortality of 250,000 Atlantic salmon val-
losses of millions of dollars per year. Figures courtesy of MY.M. ued at over $500,000 (Rensel et al., 1989).
Bricelj and C.H. Peterson. In other years, blooms of the flagellate

1. INTRODUCTION

mated annual value of $3 million (New
WE I "M 6 I'm "Mm M WW F MIF W %0 England Fisheries Development Associa-
UNITED STATES OVER THE PAST Two DECADES. tion).
In 1917, the shellfish industry in Alaska pro-
duced 5 million pounds of product. Today,
Pre-1 972 except for aquaculture, the state's commer-
cial shellfish industry is virtually non-exis-
tent as a direct result of persistent product
0 NSP contamination by PSP (Neve and Reichardt,
0 PSP 1984). The value of the sustainable, but pres-
* Fish kills ently unexploited, shellfish resource in
* Ciguatera Alaska is estimated to be $50 million per
Occasional anoxia year.
The Gulf coast of Florida experiences fre-
quent red tides, often accompanied by dead
fish washed up on beaches, NSP-contami-
nated shellfish, and human respiratory prob-
lems due to toxins aerosolized by the surf.
0 HI E PR Habas and Gilbert (1974) estimated a loss
of $20 million per event, including losses to
the tourist industry, hotel/motel suppliers,
Post-1 972 commercial fisheries, and local governments
for the expense of beach cleanup.
0 NSP E Ciguatera Domoic acid in razor clams and Dungeness
0 PSP A Brown tide crabs in Washington and Oregon in 1991
0 Fish kills A ASP caused economic losses estimated at $IS-
Occasional anoxia 20 million (T. Nosho, pers. comm.). Losses
DSP (scattered, unconfirmed) included reduced tourist trade, unemploy-
Atlantic dolphin mortalities? ment, reduced or delayed sales, lower prices,
Whale mortalities (PSP in mackeral) 0
Noxious blooms (aesthetics) and bankruptcy for some commercial pro-
cessors. Commercial oyster growers experi-
enced declines in both sales and prices dur-
ing the peak holiday period, although the
0 Hl oysters never contained detectable levels of
0 PR domoic acid. Some losses continue as razor
clam seasons are shortened or closed due
to the continued presence of domoic acid
These maps depict the HAB outbreaks known before (top) in some areas.
and after (bottom) 1972. This is not meant to be an exhaustive The states of Maine, New Hampshire, Mas-
compilation of all events, but rather an indication of major or sachusetts, Rhode Island, Connecticut,
recurrent HAB episodes. In addition to the toxic impacts shown, Florida, California, Oregon, Washington,
harmful micro- and macroalgal species have caused whale and and Alaska maintain annual shellfish moni-
other marine mammal or animal mortalities, occasional anoxia, toring programs to detect algal toxins in
habitat destruction, and a general decline in coastal aesthetics shellfish. The total cost of these programs
in many coastal areas during the last 20 years. Neurotoxic shell- exceeds $1 million per year.
fish poisoning = NSP, paralytic shellfish poisoning = PSP, and
amnesic shellfish poisoning = ASP. From Anderson, 1995.
TREM"RRM!
3 K en s
Heterosigma carterae have caused farmed-
fish mortalities in British Columbia and The nature of the HAB problem in the United
Washington state costing the industry $4-5 States has changed considerably over the last
N TSl
P

million per year (Horner et al., 1991). two decades (Box 1.3.1). Where formerly a
PSP was detected in the rich shellfish beds few regions were affected in scattered loca-
of Georges Bank in 1989, forcing the clo- tions, now virtually every coastal state is
sure of those offshore resources. The threatened, in many cases over large geo-
Georges Bank surf clam fishery alone, closed graphic areas and by more than one harmful
now for five successive years, has an esti- or toxic microalgal species. Few would argue

1. INTRODUCTION
121

that the number of toxic blooms, the economic
losses from them, the types of resources af-
fected, and the number of toxins and toxic spe-
cies 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 ex-
planations 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
Z@
proliferation of, harmful algae; c) increased
aquaculture operations which can enrich sur-
rounding 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 ac-
Blooms of seaweeds can cause significant ecosystem and tivities; f) long-term climatic trends in tempera-
economic impacts. Overgrowth of coral, indigenous macroalgae, ture,. wind speed, or insolation; g) increased
and general destruction of benthic habitat are only part of the scientific and regulatory scrutiny of coastal
significant problem posed by nuisance seaweeds, many of which waters and fisheries products; and h) improved
are thriving in areas subject to nutrient enrichment from pollu- chemical analytical capabilities that lead to the
tion. This photograph shows sponges and corals being smoth- discovery of new toxins and toxic events.
ered by the opportunistic green seaweed Codium isthmocladum The trends are equally disturbing for
on fringing reefs off southeast Florida. Photo courtesy of B. macroalgae. The development of dense cano-
LaPointe. pies of macroalgae in the benthos of shallow
water bodies is an increasingly common phe-
nomenon along virtually all of the world's
shorelines. Human activities, including defor-
estation, agriculture, and generation of domes-
tic and industrial wastewaters are increasing
the concentrations and fluxes of nitrogen and
phosphorus in coastal waters that in turn en-
hance 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 prob-
lems are worse and the trends disturbing.

113

2. THE ECOHAB PROGRAM

ona rogram 2. 3 EV6 lution of the ECOHAB
1, a NA'ti '' ' `VP on
HABs is Needed Initiative

If we accept that HAB problems are expand- The U.S. is not alone in its struggle with the
ing and that they have multiple causes, both expanding HAB problem. Nations throughout
natural and human-assisted, what can be done the world are faced with a diverse array of toxic
about them in a practical sense? What infor- or harmful species and impacts, and many of
mation is needed to efficiently manage affected these countries are poorly prepared for the
marine resources, protect public and ecosys- threat posed to their coastal economies and
tem health, encourage and support aquacul- ecosystems. As a result, international agencies
ture development, and contribute to policy or organizations such as the Intergovernmen-
decisions on coastal zone issues such as waste tal Oceanographic Commission (IOQ of
or sewage disposal, aquaculture development, UNESCO, the International Council for Explo-
or dredging? If human activities are making ration of the Seas (ICES), the Scientific Com-
the HAB problem worse, how can that be veri- mittee for Oceanic Research (SCOR), the Eu-
fied, and what steps should be taken to mini- ropean Union (EU) and the Asia Pacific
mize further impacts? These are important Economic Cooperation Program (APEC) have
practical questions, and the apparent trends all established programs or working groups fo-
in HAB incidence make them even more press- cused specifically on HABs and their impacts.
ing. The need for applied, practical research The IOC's HAB program is assuming a lead-
on HAB bloom phenomena is clear. However, ership role in the international arena. A series
the problems are complex, and will require a of workshops was convened beginning in 1987,
comprehensive research program that includes leading to the creation of a science plan which
basic and fundamental studies of HAB species, separates the IOC HAB program into three di-
their environment, and the organisms that in- visions - scientific, educational and operational.
teract with them or their toxins. The ECOHAB The scientific program has three branches: ecol-
program has been designed to address these ogy and oceanography; taxonomy and genet-
issues. ics; and toxicology and toxin chemistry.
From the outset, the IOC HAB program was
intended to be a coalescence of national and
------ - international programs. On the international
ECOHAB (ECology and Oceanography of side, ICES established a working group on the
Harmful Algal Blooms) is a scientific program Dynamics of Harmful Algal Blooms which has
designed to increase our understanding of the planned several major field programs or pilot
fundamental processes underlying the impacts studies targeting key HAB phenomena. How-
and population dynamics of HABs. This pro- ever, due to the regional nature of many HAB
gram addresses the many factors at the problems, it is evident that these field studies
organismal level that determine how HAB spe- will involve individual countries or groups of
cies respond to, and potentially alter their en- neighboring countries, and not large multi-
vironment, the manner in which HAB species national teams of investigators, as is often the
affect or are affected by food-web and com- case in international programs. At the national
munity interactions, and how the distribution, level, however, it became clear that many coun-
abundance, and impact of HAB species are tries did not have a national program or plan
regulated by the environment. to attack HAB issues. In the U.S., this was true
In its simplest form, the goal of the despite an array of problems associated with
ECOHAB program is to develop an under- harmful algae and a long history of HAB re-
standing of the population dynamics and search. In order to rectify this lack of coordi-
trophic impacts of harmful algal species nation of HAB problems in the U.S., a work-
which can be used as a basis for minimizing shop was convened in 1992 at the National
adverse effects on the economy, public Marine Fisheries Service laboratory in Charles-
health, and marine ecosystems. ton, SC. That meeting produced the report "Ma-
rine Biotoxins and Harmful Algae: A National

2. THE ECOHAB PROGRAM
141

Plan "(Anderson et al., 1993), which identi- on genetic, biochemical, behavioral and life
fied numerous impediments to progress in the history processes that are important factors in
HAB field and made specific recommendations the dynamics and impacts of blooms. These
to address those impediments. In addition to experimental studies will range from the
identifying areas for future research, the Na- organismal to the ecosystem level.
tional Plan structured proposed HAB activities
in a framework that helped agencies identify Field Investigations. Multi-investigator,
their roles in the overall program. multi-disciplinary field studies of HAB species
A prominent gap in U.S. attempt to deal are needed to document the distribution and
with HAB issues was immediately apparent - dynamics of key elements of HAB ecosystems,.
that dealing with the ecology and oceanogra- emphasizing the complex interactions between
phy of the blooms. The National Plan identi- biotic and physical or chemical factors. Since
fied this as an important area for research, no single field program could possibly address
but a detailed scientific agenda was lacking the wide array of HAB phenomena, a series of
and no agencies were actively supporting such regional field studies is envisioned, in the ex-
research. NSF and NOAA then co-sponsored pectation that this comparative approach will
a workshop at Snow Mountain Ranch Con- reveal differences and commonalities when
ference Center in Colorado, involving partici- both hydrographic regimes and ecosystems are
pants representing an array of scientific disci- compared. An underlying challenge in all of
plines, geographic regions, and agencies. The these studies will be the need to obtain spe-
goal was to integrate field, laboratory, and cies-specific or autecological information from
theoretical studies into a focused effort to un- natural populations.
derstand the fundarriental issues underlying
HABs and their impacts. The resulting Theoretical Studies. Existing models will
ECOHAB program addresses these national be applied, and new approaches developed,
needs, but it also represents a U.S. compo- which incorporate field and laboratory mea-
nent of the international HAB programs of IOC surements into realistic and testable simula-
andICES. tions of HAB dynamics in different oceano-
graphic systems. Models will include
WRINIMM, @PFR conceptual studies in idealized flows that ex-
amine how circulation patterns affect biologi-
cal processes at the level of the individual,
The objective of the ECOHAB program is to population, community and ecosystem, as well
combine field, laboratory and modeling stud- as site-specific models that address mechanis-
ies in a coordinated effort to characterize the tic interactions of the physics and biology
physical, chemical and biological processes within a particular oceanographic regime.
governing the growth, distribution and impacts
of HAB species.
id Rene ltmsw""
rTKIT =ft i o nUtme Wan
Three program elements have been identi- '15' Rdtioha md'76"e"n
fied: The Organisms; Environmental Regulation
of Blooms; and Food-weblCommunity Interac- The significant economic, public health and
tions. One challenge has been to design a pro- ecosystem impacts of HAB outbreaks are
gram that could accomodate the wide array of strong, practical motivations for a research
HAB species, their impacts, and oceanographic program such as ECOHAB, made all the more
regimes without being so broad or diffuse that pressing by the apparently escalating trend in
implementation would be impossible. Given their incidence. The direct benefits to society
this diversity, ECOHAB will rely on coordi- from a program of this kind are many, and in-
nated, multi-investigator programs as well as clude management issues such as bloom de-
projects by individual investigators or small tection and prediction, control or mitigation
groups. The program will require at least three strategies, site selection criteria for aquacul-
types of research, all of which will involve an ture, and assessment of impacts from altered
integration of physical, chemical and biologi- nutrient loading, dredging or other coastal zone
cal components. developments. There are indirect benefits as
well. For example, many of the mechanisms
Laboratory or Mesocosm. Studies. Carefully underlying bloom formation by harmful algal
controlled studies of HAB species and their species are the same as those responsible for
food chain interactions are needed, focusing blooms of other phytoplankton in the ocean.

2. THE ECOHAB PROGRAM
115

77f, cannot be achieved without effective inter-
agency cooperation, coordination and collabo-
ration. Nowhere else do the missions and goals
of so many government agencies intersect and
o
erlap as in the coastal zone where HAB phe-
v
nt. ECOHAB will be
04 nomena are promine
succesful only if a nationally coordinated in-

IRV
teragency effort can be implemented to di-
rect research personnel, facilities, and finan-
cial resources to the common goals outlined
in this comprehensive national strategy.
Thus far, the planning of the ECOHAB pro-
gram 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 out-
lined herein is intended to guide these agen-
cies in the efficient allocation of resources tar-
geted to HAB issues, and to help them
formulate new, multi-investigator, multi-disci-
plinary HAB initiatives as well. Joint inter-
agency announcements of opportunity for re-
Some algal Multidisciplinary field HAB programs address search support as well as interagency
blooms are non- a practical problem while also providing basic cooperation on the provision of needed re-
toxic but aestheti- scientific information relevant to plankton ecol- sources and facilities are thus possible. How-
cally unpleasant ogy and oceanography in general. ever, an additional feature of the ECOHAB pro-
or noxious. Another compelling aspect of the ECOHAB gram will be a reliance on proposals submitted
program stems from the need to study indi- by individual investigators or small groups, in
vidual HAB species, rather than mixed plank- recognition of the diversity of causative organ-
tonic assemblages. New autecological tech- isms, impacts, and oceanographic systems as-
niques must be developed, such as remote sociated with HABs.
detection of bloom populations using swim- A Steering Committee has not yet been es-
ming robots or moored instruments. Methods tablished, as that awaits a final indication of
are needed to "tag" target species with mo- the agencies that will participate in ECOHAB.
lecular probes and then enumerate or sepa- Once those issues are resolved, a committee
rate them from co-occurring organisms, and will be selected to oversee implementation of
techniques to estimate in situ growth rates or ECOHAB at the national level. Where neces-
to determine the physiological status of a spe- sary, small working groups or sub-committees
cies must be developed. These are but a few will be convened to address specific program
examples of the areas where new technologies needs. Once ECOHAB is underway and research
developed to meet the objectives of ECOHAB programs begin to accumulate results, regional
can benefit all of oceanography. and national workshops will be convened to
identify common mechanisms and processes
underlying the diverse array of HAB phenom-
21" -- CID 6fifellialtibit ena and their impacts. One of the strengths of
ECOHAB lies in this "comparative approach"
To address the many scientific issues out- but resources must be allocated to facilitate the
lined in this report, federal agencies must break requisite scientific communication.
away from the parochial view that has often
dominated HAB research in the past. A com-
prehensive understanding of the present sta-
tus of coastal waters, and the manner in which
those waters and their ecosystems will respond
to changes, both natural and human-assisted,

161

3. ECOHAB Program Elements

growth potential is often controlled by exter-
M
f KT',,,W,,Wpr
I I 41WRIE, 5"" ill
04
nal environmental factors.
n
3.1 Th e Organisms Th 'ere is considerable diversity among HAB
species with respect to strategies for growth
and bloom formation in natural systems. Some
3.1.1 Introduction cause harm at relatively low cell concentra-
Rationale: The negative impacts of HABs tions (e.g., DSP can occur with only a few hun-
reflect not only the growth and metabolism dred Dinophysis cells per liter), but in other
of individual algal cells, but the ecological cases, population growth of HAB species re-
selection of those cells within a diverse phy- sults in a monospecific bloom at high concen-
toplankton assemblage. Studies at the trations (e. g., a red tide). There are numerous
organismal level are essential if we are to explanations for that type of growth and accu-
understand the population dynamics of mulation, and many are rooted in the unique
HABs. physiology of the organisms involved. For ex-
The impact of harmful algal blooms (HABs) ample, it has long been argued that produc-
is a function of the growth and metabolism of tion of toxins or other exudates allows some
individual algal cells ecologically selected from species to outcompete co-occurring organisms
a diverse phytoplankton assemblage. Growth (e.g., Pratt, 1966) or to deter grazing (Huntley,
is a general term reflecting photosynthesis, nu- 1982; Huntley et al., 1986; Ives, 1987). Practi-
trient uptake and assimilation, and numerous cal demonstrations of these mechanisms are
other metabolic processes within cells. The in- few, however.
herent growth characteristics of species are Another survival and growth strategy in-
genetically determined, but the realization of volves the benthic resting stages of many HAB
species. These cysts or spores provide a recur-
r
ent "seed" source or inoculum for planktonic
ARMFOUL`AL'G,@L SOECIES.
populations, and this characteristic may be a
critical factor in determining not only the geo-
graphic 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 en-
vironmental conditions their swimming behav-
ior may result in formation of high-density
patches (e.g., Kamykowski, 1974; Cullen and
Horrigan, 1981; Franks, 1992). Diel vertical
Only a few dozen of the movement by motile cells in a stratified envi-
many thousands of species of ronment undoubtedly has functional signifi-
microscopic and macroscopic cance, for example, maximizing encounter fre-
algae are repeatedly associated quencies for sexual reproduction, minimizing
with toxic or harmful blooms. grazing losses, and allowing cells to obtain
Some species, such as the di- nutrients at depth and light at the surface.
noflagellates Alexandrium These diverse issues can be incorporated
tarnarense (top left) and the into the following goal for the Organisms pro-
diatom Pseudo-nitzschia australis (bottom) produce potent tox- gram element of ECOHAB:
ins which are liberated when the algae are eaten. other species
kill'Without toxins, like this Chaetoceros species (top right) which Goal: To determin e the physiological, bio-
has spines with serrated edges which can lodge in fish gill tis- chemical, genetic, and behavioral features
sues, causing irritation, over-production of mucous, and even- and mechanisms of harmful algal species
tual death. Each of these species, and many others, need care- that influence their bloom dynamics, gen-
ful study at the organismal level if we are to understand the eral ecology, and impacts.
population dynamics and trophic impacts of HABs throughout
the U.S. Photos by D. Wall, J. Rines, and R. Horner.

3. ECOHAB PROGRAM ELEMENTS
117
Box 3.1.2 MOLECULAR PROBES 3.1.2 Research Agenda
The following issues are considered high
priorities in organismal research within
ECOHAB:
71

Issue:
There is a need to rapidly and accu-
far
rately identify, enumerate, and physi-
cally separate HAB species from mixed
phytoplankton assemblages.
Positive identification and enumeration of
specific algal species in discrete field samples
ed over large temporal and spatial scales
collect
is a labor intensive, but necessary process for
the characterization of HABs. A common prob-
lem in research and monitoring programs fo-
cused on HAB species occurs when the spe-
cies 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 organ-
isms and detritus. Studies must thus rely on
tedious microscope counts to enumerate the
target species, and measurements of toxicity
or other physiological parameters are gener-
ally not possible for just the species of inter-
est. Another constraint arises from the diffi
culties in adequately identifying and
distinguishing between species or strains which
are morphologically similar. (see Box 3.1.2)
Considerable time and effort are often required
to identify a particular species when its distin-
guishing characteristics are difficult to discern
under the light microscope. Such fine levels of
discrimination are not generally feasible in
Antibodies and nucleic acid probes are sensitive tools that monitoring programs or other studies which
can enhance the identification and enumeration of HAB spe- generate large numbers of samples for cell
cies. In this example, a ribosomal RNA-targeted oligonucleotide enumeration.
specific for Pseuto-nitzschia pungens f. multiseries was applied At present, the time lag between sample
to a natural sample collected from Monterey Bay, California. collection and the identification and counting
Material was fixed and processed as described by DeLong et of specific organisms severely limits our abil-
al., (1989). A transmitted light micrograph of this material is ity to follow the population dynamics of HAB
shown in the top photo. A chain of needle-like diatoms which species in real-time. As a consequence, we are
could be either R pungens f. pungens (non-toxic) or R pungens limited in our ability to predict when poten-
f. multiseTies (toxic) is seen, in addition to other non-toxic plank- tially harmful organisms may develop in areas
ton. The two forms of P. pungens are indistinguishable using where they might pose a threat to public health
transmitted light microscopy. However, when the same frame or wildlife, Once species identification is auto-
is viewed using epifluorescence microscopy (bottom photo) the mated and/or greatly accelerated, population
fluorescein-labeled rRNA probe (green) is visible, identifying data can be collected that is compatible with
the Pseudo-nitzschia chain as a R pungens f. multiseries - the high-frequency measurements of chemical and
toxic variety linked to amnesic shellfish poisoning. Note how physical oceanographic features.
other cells visible in the transmitted light image do not retain
the probe. Antibody probes are also capable of making such We need to:
distinctions between closely related species or strains of phy- I .Collect, isolate, and maintain a wide range
toplankton (e.g., Bates et al., 1993). Photos by C. Scholin and of HAB species in unialgal and/or axenic
K. Buck. cultures.
2. Characterize key species using standard

3. ECOHAB PROcRAm ELEMENTS
181

microscopic methods (e.g, light, duce cysts or spores during their life histories,
epifluorescence, -and electron microscopy and these resting stages can have a significant
as appropriate). impact on many aspects of HAB phenomena
3. Characterize key species using molecular (Anderson and Wall, 1978; Anderson et al.,
genetic methods (e.g., RFLP, RAPD, gene 1983). Cyst or spore germination provides the
sequencing). inoculum for many blooms, and the transfor-
4. Develop molecular probes and application mation back to the resting state can remove
strategies for use in field and laboratory substantial numbers of vegetative cells from
settings, and make these tools broadly the population and be a major factor in bloom
available. decline. Cysts are important mechanisms for
5. Detect and quantify toxins produced by population dispersal, they permit a species to
HAB species using bioassays, HPLC, im.- survive through adverse conditions, and since
munoassays, and receptor binding assays; sexuality is typically required for their forma-
refine those techniques for routine use on tion, they facilitate genetic recombination
field and culture samples. (Wall, 1971). They can even be important
6. Develop optical sensors able to distinguish sources of toxin to shellfish and other benthic
taxon-specific features such as pigments. animals. Clearly, all investigations of the ecol-
ogy and bloom dynamics of HAB organisms
Approach and Technology. The problem must be based on a thorough understanding
of uncertain and slow identification can be of an organism's life history, as well as the
addressed by cross-disciplinary investigations factors that regulate,the transitions between
that utilize a spectrum of techniques to distin- dormancy and a vegetative existence.
guish between species, strains of single spe- Unfortunately, the state of knowledge about
cies, and toxic and non-toxic forms. Culture resting stages and life histories is neither com-
collections, especially those including multiple plete nor uniform for the many HAB species.
strains of key species, are essential to this ef- For several (e.g., Alexandrium spp.,
fort. A variety.of identification techniques Heterosigma carterae, Pflesteria piscicida ), the
should be supported, as future applications of existence of resting cysts has been documented.
rapid detection methods for HAB species will For many others, however, no life history in-
likely employ multiple probe types. (see Box formation is available. The prevalence of life-
3.1.2) These new technologies should be ac- cycle stages among other HAB species is not
tively pursued, but traditional systematic or well known, and factors triggering transitions
morphological investigations using standard are poorly defined. Recognizing and determin-
microscopy or biochemistry should also be sup- ing the role of these stages in bloom initiation,
ported. The traditional methods are well-es- growth and termination is critical to our un-
tablished, but considerable effort is needed to derstanding of HAB phenomena.
develop the species-specific probes and the
methods to use them in a rapid and precise We need to:
manner. Results from this aspect of the pro- I .Develop culture techniques which simu-
gram will greatly accelerate progress in sev- late in situ growth conditions sufficiently
eral other ECOHAB activities, especially those well that life history transitions can be
involving large-scale field programs. induced and characterized.
Probe technologies can also be used to de- 2. Isolate and culture many HAB species, and
tect the toxins (rather than the cells) in envi- support the maintenance of HAB culture
ronmental samples (see Box 3.1.3). This type collections. The importance of maintain-
of application has the potential to provide rapid ing multiple isolates of individual species
and accurate information on toxin levels and must be emphasized here, given the ge-
distribution that can be highly useful to re- netic diversity observed in regional popu-
source managers. lations of HAB "species."
3. Develop molecular probes that can assist
Issue: in the identification of life history stages
There is a need to identify the life his- in natural samples.
tory stages of HAB species, to determine 4. Incorporate studies of resting cyst or
what factors control transitions be- spore distribution, abundance, and dy-
tween those stages, and to establish the namics into field investigations of HAB
role of each stage in bloom dynamics. bloom dynamics.
Many marine phytoplankton species pro-

3. ECOHAB PROGRAM ELEMENTS
19

ther experimental studies are clearly needed to
document how this might be occurring.
W The brown tide in Texas is but one example
0
f the need for information on physiological
ses of individual HAB species to their
respon
jt"
chemical and physical environments. The same
can be said for virtually all important HAB spe-
ies. Why are Alexandrium blooms in the
c

S
outhwestern 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-nu
"V trients? How is Gymnodinium breve,
a red tide dinoflagellate from the Gulf of
Germination of Approach and Technology. A combination Mexico, able to survive during transport for
dormant cysts in of laboratory and field studies is required to 1000 km or more around the Florida penin-
bottom sediments determine the complete life histories of HAB sula and up the southeastern coast of the U.S.
provide the inocu- species and to elucidate the factors that regu- to North Carolina via the Gulf Stream (Tester
lurn for many late transitions between life stages. Here again, et al., 1991)?
HABs. Photo by culture collections of multiple HAB species are
D. Wall necessary, and multiple studies are required Experimental approaches to organismal
given the diversity of species represented by physiology must include the following:
HAB organisms. Some technique development 1. Establish new clones of key HAB species
effort is needed, such as in the design and representing their entire geographical
application of probes to identify life history range.
stages of a target organism and refinement of 2. For multiple toxic and non-toxic clones
culture techniques to permit full-cycle life his- of HAB species, determine tolerance
tory transformations to occur in the labora- ranges and optima for growth and toxin
tory. Otherwise, methodologies are in-hand for production in response to a suite of envi-
these studies. ronmental variables.
3. Conduct classical steady-state analyses of
Issue: nutrient requirements and uptake rates
It is essential to understand the physi- for key HAB species.
ological responses of HAB species to 4. Compare laboratory results with data from
differing environmental conditons. mesocosm and field investigations.
The manner in which HAB species respond
to a changing environment determines their Approach and Technology. Species-specific
survival and growth. These responses are gov- physiological data can be most easily derived
erned by the physiological requirements and tol- from experiments with unialgal cultures un-
erances of each species for environmental vari- der controlled conditions. However, clones of
ables such as nutrients, light, temperature, and a single species'typically exhibit marked varia-
salinity. All HAB species must be characterized tion in numerous characteristics, including
with respect to these tolerances if We are to un- growth and toxin production (Maranda et al.,
derstand and predict their distribution and oc- 1985; Bomber, et al., 1989; Cembella et al.,
currence in natural waters. For example, an 1987; Hayhome et al., 1989; Anderson et al.,
extraordinary bloom referred to as "the Texas 1994). Since no single isolate can be consid-
brown tide" has persisted in the Laguna Madre ered to be representative of a regional popula-
for five years (Buskey and Stockwell, 1993). tion, growth studies are needed for multiple
There are multiple potential explanations for strains to define the extent of genetic variabil-
this dominance, one of which is that the caus- ity and environmental plasticity. Several labo-
ative species out-competes other phytoplank- ratories in the United States have initiated "syn-
ton for essential resources. In addition to pos- drome-based" culture collections of harmful
sible selection on the basis of temperature or marine microalgae, and these collections
salinity tolerances, the brown tide alga cannot should be supported and exploited in this re-
use nitrate as a nitrogen source. This unique spect. As discussed below, techniques for some
nutritional strategy may be fundamental to the of the above physiological studies are not uni-
success of the species in that system, but fur- formly accepted. It may be necessary to con-

3. ECOHAB PROGRAm ELFMENTS
201

The detection of initial (small) HAB populations is
LONGITUDE W
hampered by our inability to discern low concentrations MW 87.00 Mm W.00 84.w w.w 82.00 elm WM
of toxic species which can then proliferate to form ma-
j or blooms. In part, this is due to the time and difficulty
in using traditional microscopic methods to identify and MOO
enumerate cells in low abundance. One new approach
to this problem is based on the principle that toxic cells "M
produce potent chemical markers which can be detected
by immunological methods at extremely low levels. A 28M 2&00
recent enzyme-linked immunosorbent assay (ELISA) for Z Z
brevetoxins (Trainer and Baden, 1991), developed pri- D nw V.W Z)
a 0
a600
marily for laboratory use, was modified and adapted for
J 1000 _J
testing natural waters of the West Florida shelf. in this 2&00 5000 20M
example, the immunoassay for the toxins was used on 7000
numerous surface water samples from the shelf, result- 25.00- 25M
ing in a highly informative map of toxin concentrations
(Tomas, unpub. data). This sensitive detection system,
24.W- BREVETOXIN pg/LITER CP92-3 24.W
although presently not in a routine format, illustrates 27 Ju I - 7 A, g 92
. C. T.- FOEP/FMR]
the value of developing new methods Which are rapid, 23.. J 21..
accurate and sensitive, and which complement the tra- .!W 85M a4.w W.00 .2@W S1.00 M
LONGITUDE W
ditional microscopic approach to population studies.

vene a small working group to standardize ap- of growth, photosynthesis, and nutrient
proaches and protocols for these investigations. uptake for HAB species.
3. Calibrate these methods carefully, and
Issue: then apply them aggressively to field
In situ measurements of the rates of populations.
photosynthesis, growth, and nutrient
uptake are essential for understanding Approach and Technology. The necessary
the dynamics of HABs, as are assess- studies can build on molecular and biochemi-
ments of the physiologial condition of cal techniques developed to assess growth rate
jcells at different times and locations. (Dortch et al., 1983; Chang and Carpenter,
This issue epitomizes a unique and challeng- 1991; Lin et al., 1994) and a suite of physi-
ing feature of HAB studies that separates them ological processes within cells such as nitro-
from more traditional process-oriented oceano- gen fixation (e.g., Currin et al., 1990), nutri-
graphic investigations. Many techniques are ent uptake or limitation (Berdalet and Estrada,
available to assess the biological rate processes 1994; see Box 3.1.3) and photosynthetic activ-
and biomass of planktonic communities (e.g., ity (Orellana and Perry, 1992). The objective
"C-fixation, chlorophyll), but there are few of these studies will be to develop analytical
methods suitable for determining growth or methods and diagnostic indicators that can be
uptake rates or physiological condition of an applied to individual cells. The more traditional
individual species when it occurs in a mixed bulk analyses work on communities rather than
population and does not dominate the phy- species. For some HAB organisms, it will be
toplankton assemblage. Considerable methods necessary to couple the above methods with
development is thus required to fully address identification probes and flow cytometry or cell
this autecological characteristic of ECOHAB. imaging techniques to measure species-specific
characteristics.
Effort is needed in the following areas: Although recent technological advances are
I .Investigate the physiology, biochemistry, encouraging in these fields, there is a clear need
and molecular biology of specific pro- for an initial methods development and cali-
cesses to identify "diagnostic indicators" bration effort within the ECOHAB framework.
for physiological condition. The ultimate goal is to apply these techniques
2. Develop methods to estimate in situ rates in ecological studies.

3. ECOHAB PROGRAM ELEMENTS
121

Issue: ity of specific nutrients, and that human ac-
It is essential to know the nutrient re- tivities have altered these nutrient supply ra-
quirements, uptake, and assimilation tios in ways that favor toxic or harmful forms.
characteristics of HAB species. For example, diatoms, the vast majority of
Nutrient limitation of phytoplankton growth which are harmless, require silicon in their cell
is a fundamental factor that places a limit on walls, whereas other phytoplankton do not.
the accumulation of biomass and may deter- Since silicon is not abundant in sewage efflu-
mine the outcome of competition among spe- ent but nitrogen and phosphorus are, the N:Si
cies in mixed assemblages. It is often suggested or P:Si ratios in coastal waters have increased
that increasing incidences of harmful algal through time over the last several decades. Dia-
blooms in coastal waters are related to changes tom growth in these waters ceases when sili-
in nutrient loading from human activities (e.g., con supplies are depleted, but other phy-
Smayda, 1990), so verification of this linkage toplankton classes (which include most of the
would have important societal implications. known toxic species) can proliferate using the
These nutrients can stimulate or enhance the excess" nitrogen and phosphorus.
impact of toxic or harmful species in several This concept is controversial, but is not with-
ways. At the simplest level, toxic phytoplank- out supporting data. A 23-year time series off
ton may increase in abundance due to nutrient the German coast documents the general en-
enrichment but remain as the same relative frac- richment of coastal waters with nitrogen and
tion of the total phytoplankton biomass (i.e. phosphorus, as well as a four-fold increase in
all phytoplankton species are affected equally the N:Si and P:Si ratios (Radach et al., 1990).
by the enrichment). Alternatively, there may This was accompanied by a striking change in
be a selective stimulation of HAB species by the composition of the phytoplankton commu-
pollution. This view is based on the nutrient nity, as diatoms decreased and flagellates in-
ratio hypothesis (Smayda 1990) which argues creased more than ten-fold. As coastal com-
that environmental selection of phytoplankton munities and countries struggle with pollution
species is associated with the relative availabil- and eutrophication issues, the implications of

F StOLOGI'@iL CONDITION
RS PHY C
`B& 3 1.4"DI Ai&NiN03TIC IND' I'C"A'T'O' '6

Key enzymes are often indicators of physiological state transcripts as indicators of algal physiological status. The
in phytoplankton. The specific activity of alkaline phos- left photograph is a light migrograph of a diatom culture
phatase, nitrate reductase, glutamine synthetase, and showing many cells which appear morphologically simi-
other enzymes has tradionally been used to indicate the lar. The right photograph shows the same cells after they
ability of individual species to assimilate and utilize nu- were treated with an antibody specific for the nitrate re-
trient substrates. These biochemical measurements are ducing enzyme, nitrate reductase (NR). Cells having
time consuming, require specialized equipment and re- strong NR activity are brightly colored (rose color), while
agents, and cannot be applied to individual species in a those with little or no activity appear as ghosts. This
mixed plankton assemblage. Recently, through molecu- type of antibody probe-based visualization is one example
lar technology involving antibody recognition of active of several new technologies that will be used in ECOHAB
sites and /or application of DNA probes, it has becdrne to determine the physiological status of HAB species in
possible to assess the abundance of key enzymes or gene natural waters. Photos courtesy of J. Coyer and R. Alberte.

3. ECOHAB PROGRAM ELEMENTS
221

these concepts are profound and clearly de- Issue:
serve further investigation. The functional role of toxins and/or
A few measurements of nutrient uptake ki- exudates produced by HAB species is
netics and cell nutrient quotas of HAB species not known.
(e.g., dinoflagellates and raphidophytes) sug- Toxin production is a wide-spread, but not
gest that they have high nutrient requirements, universal, characteristic of HAB species. The
indicating that they would be able to prolifer- functional roles suggested for toxins are: 1) as
ate only in high nutrient environments (e.g., deterrents to grazers (Box 3.3.1); 2) as allelo-
Eppley et al., 1969; Caperon and Meyer, 1972). pathic compounds that restrict the growth of
Relatively few HAB species have been investi- co-occurring algal species; and 3) as storage
gated in this context, however. Nutrient up- products. It may well be that toxins are sec-
take and growth rate kinetics and nutrient quo- ondary metabolites with no physiological func-
tas for HAB species must thus be determined tion. Field observations suggest that some fish
to predict their growth response relative to and zooplankton avoid dense concentrations
other species. In addition, some supposedly of HAB species (Huntley, 1982) and labora-
autotrophic phytoplankton species appear to tory studies indicate that toxic species can be
utilize dissolved organic nutrients (Cembella rejected by grazers (Sykes and Huntley, 1987;
et al., 1984; Taylor and Pollingher, 1987) while Ives, 1987). These studies are limited to a few
others rely on mixotrophy to supplement their species and are only a beginning. They cer-
carbon requirements (Sanders and Porter, tainly have not addressed the diversity of
1988). If confirmed in HAB species, these nu- grazer-algal relationships necessary to evalu-
tritional strategies may @confer a competitive ate the role of toxins in natural populations.
advantage over other phytoplankton.
We need to:
Nutrient studies within ECOHAB should 1. Conduct laboratory and field studies to de-
focus on the following: termine if there is differential grazing on
1 .Determine nutrient uptake and growth ki- toxic versus non-toxic species.
netics for HAB species under a range of 2. Determine the effects of toxic algae on eco-
environmental conditions. Depending on logically significant grazers.
the species, this information is needed for 3. Evaluate the allelopathic activity of exu-
N, P, Si, Se and Fe at least, but other mi- dates and toxins of HAB species.
cronutrients may need to be considered.
2. Assess the prevalence among HAB spe- Approach and Technology. This work will
cies of unique nutritional strategies such depend upon a supply of appropriate isolates,
as osmotrophy and mixotrophy. our ability to manipulate them in culture, and
3. Develop and optimize culture techniques the availability of sensitive and reliable meth-
for fastidious HAB species. ods of toxin analysis. In general, techniques
are available to pursue this important line of
Approach and Technology. The hypotheses investigation, although advances in 3-dimen-
that changing nutrient ratios can influence com- sional video analysis of grazer behavior when
petition dynamics and that HAB species have presented with HAB species can provide new
nutrient requirements different from other phy- and relevant insights.
toplankton species can be assessed using a com-
bination of nutrient kinetics and manipulative Issue:
expenments with cultures and natural popula- It is essential that we define the genetic
tions. Several approaches have been used to basis of toxin production, elucidate
derive nutrient kinetic parameters, and there toxin biosynthetic pathways, and de-
is the need to standardize experimental proto- termine how toxin accumulation in
cols before embarking on comparative studies cells is regulated.
among HAB species. Moreover, there is no gen- Toxin production is a distinguishing char-
eral agreement on the merits and limitations of acteristic of many HAB species. However, the
using batch versus continuous culture meth- prevalence of toxin synthesis among these or-
ods for nutritional requirement studies. As a ganisms is continuously being re-evaluated. For
result, it may be necessary to convene an some species the toxins are well described (e.g.,
ECOHAB community working group to address saxitoxins, domoic acid, brevetoxins; Hall et
standard experimental approaches. al., 1990; Shimizu, 1993; Falconer, 1993), al-
though non-toxic strains or sub-species have

3. ECOHAB PROGRAm ELEMENTS
123

been documented for several such taxa (e.g., itoxins, environmental factors such as nutrient
Yentsch et al., 1978; Smith et al., 1990). Other concentration and temperature can influence
species such as Heterosigma carterae and the expression of individual toxin derivatives
Pfiesteria piscicida are known to produce tox- (Hall, 1982; Anderson et al., 1990a,b). This is
ins, but the actual compounds remain an important ecological consideration, because
uncharacterized (e.g., Burkholder et al., 1992; various derivatives can differ markedly in their
1995). Still, other species are considered likely potencies (Oshima et al., 1989). Production of
to be toxigenic based on an association with algal toxins can also be modulated by co-oc-
events such as fish kills, but their toxicity has cutting bacteria (Bates et al., 1995), and in
yet to be confirmed. Our lack of information certain cases, bacteria themselves represent au-
about this basic trait for many HAB species tonomous sources of phycotoxins (Kodama et
limits our ability to ascertain the nature and al., 1988; Doucette and Trick, 1995).
extent of HAB impacts or to evaluate mecha- Nutrients have a clear and significant influ-
nisms underlying trends in HAB incidence. ence on the production of toxins by some al-
While relatively few organisms have been gae. in species from a variety of taxonomic
examined, the available data suggest that the groups producing different toxins, cellular toxin
amounts and forms of toxin contained in a cell content varies dramatically during nutrient star-
vary with its physiological status. For the sax- vation in culture. For example, the abundance
of saxitoxins in Alexandrium species can vary
by m
@41MWTi@ ore than an order of magnitude depending
CS 0 ON upon whether phosphorus or nitrogen is limit-
T7MT7X-M MNE@Tl@ F OXIN
ing (e.g., Hall, 1982; Boyer et al., 1987; Ander-
MET-ADENOSINE son et al., 1990). Likewise, domoic acid pro-
S-ADENOSYL S duction in Pseudo-nitzschia species varies with
METHIONINE &, silicate availability (Bates et al., 1991; Bates and
CH3 Douglas, 1993), and Chrysochromulina
CELLULAR ACETATE I N
METABOLITES - -(E-Y@)n polylepis, the chyrsophyte responsible for mas-
DOC sive fish and invertebrate mortalities in Swe-
ARGININE H N% den and Norway in 1987, has been shown to
SAXITOXIN be more toxic when phosphorus is limiting
H2N N Toxin
rnRNAe (Edvardsen et al., 1990; Gran6li et al., 1993).
PAR nnRNAs I These and other demonstrations of the ef-
Toxin fects of nutrient availability on toxicity have
[Nitrogen] rnRNAs SAXITOXIN
DERIVATIVES major implications with respect to our efforts
NudeuWNwleoid to understand the manner in which HABs are
[Phosphoms] influenced by, and impact their environment.
There are many unknowns remaining, how-
Ternperature SAXITOXIN BICISYNTHETIC PATHWAY ever, as studies to date have only demonstrated
(AFTER Y. SHIMIZU)FGF the nature of the linkage between nutrients and
The biosynthetic pathway for saxitoxins that are responsible toxicity, and then only for a few species. Bio-
for PSP involves a unique series of reactions (Shimizu et al., chemical and cellular mechanisms remain to
1984). Arginine, acetate and the methyl group of s- be elucidated, as does the extent to which the
adenosylmethionine are incorporated into saxitoxin, as revealed nutrient limitations that alter toxicity are actu-
by feeding studies involving radioactive substrates. The pre- ally occurring in natural waters. Without more
cise sequence of enzymatic steps is unknown, as is the number detailed information about the physiology of
of enzymes involved. The parent compound saxitoxin can be toxin production for a wider range of HAB spe-
enzymatically modified to form several derivatives, each with cies, it is very difficult to assess the ecological
a different toxicity. Genetic studies have shown that the genes role of toxins in population and community
responsible for this derivitization are encoded in the nucleus of dynamics (see sections 3.2 and 3.3).
saxitoxin-producing dinoflagellates, and preliminary data sug- The biosynthetic pathways for the produc-
gest that those genes may be linked closely on one chromo- tion of several toxins have been described to
some. An important goal is to isolate and characterize the sax- the extent that elementary "building blocks"
itoxin genes as a first step toward determining how have been identified (Shimizu et al., 1984; Dou-
environmental conditions, such as low phosphate or low tem- glas et al., 1992; Box 3.1.4), but in no case
perature enhance the expression of saxitoxin genes and the have complete pathways, including all inter-
accumulation of toxin, mediates involved, been elucidated. Isolation
of the enzymes involved in toxin synthesis or

3. ECOHAB PROGRAM ELEMENTS
241

interconversions is also at a very early stage of Some motile HAB species exhibit directed
development (Sako et al., 1995). At the most swimming behavior such as vertical migration
basic level isolation of the genes and enzymes or orientation towards prey, as has been dem-
directing the production of algal toxins remains onstrated for the ambush dinoflagellate,
an important but elusive goal. Pfiesteria piscicida which is capable of detect-
ing and swimming towards its preferred food.
Organismal studies of toxin production Vertical migration is thought to be a response
and its genetic control will need to include to light, salinity, nutrient gradients, and even
the following: gravity (e.g., Holmes et al., 1967; Eppley et al.,
I .Determine the prevalence of toxin produc- 1968; Kamykowski, 1974; Cullen and Horrigan,
tion among HAB species in culture and 1981). This mechanism is fundamental to the
the time-varying concentrations of toxin population dynamics of many motile HAB spe-
at different stages of growth. cies, as it can result in dense concentrations of
2. Determine the linkage between bacteria cells that affect grazing losses, light harvest-
and toxin production. ing, nutrient availability, and encounter fre-
3. isolate and purify poorly characterized or quencies for sexuality. The aggregation of cells
unknown toxins and determine their is also directly related to the scale of the ad-
chemical structures. verse impact from the blooms. Non-motile al-
4. Elucidate toxin biosynthetic pathways and gae are also capable of orienting themselves
characterize the genetics and regulation vertically by changing their relative buoyancy.
of toxin production.
5. Determine the nutrient assimilation and We need to:
partitioning pathways which permit toxin I .Conduct vertical migrationstudies at a va-
synthesis, and determine the factors riety of scales, from tube cultures to
which influence toxin production at the mesocosms to natural populations.
cellular level. 2. Characterize the influence of environmen-
tal variables such as salinity, light, and
Approach and Technology. A number of nutrients on these behaviors.
well-established experimental approaches are 3. Refine models of swimming behavior and
available and appropriate to address patterns examine how different strategies interact
of toxin production, typically involving the with physical features such as
growth of an HAB species under a suite of en- pycnoclines, fronts, or internal waves.
vironmental conditions and monitoring the
manner in which toxicity varies. The isolation Approach and Technology. A combination
of toxin genes/enzymes is a critical first-step of laboratory and field investigations is neces-
toward identifying the actual mechanisms un- sary to address the significance of these behav-
dertying environmentally-induced toxin vari- iors. Much of the technology required for such
ability. Additionally, studies at the molecular studies exists, but new approaches such as fine-
level will allow us to evaluate the intracellular scale sampling techniques, (e.g., Donaghay et
trade-offs between toxin production and main- al., 1992) will be needed to measure biological,
tenance of "normal" cellular metabolism, ulti- chemical and physical parameters with appro-
mately leading to a clearer understanding of priate resolution. Rapid detection and enumera-
11 why" it might be ecologically beneficial for tion techniques for HAB species will be required
toxigenic organisms to synthesize toxins. Tech- (see Box 3.1.2), and mesocosm strategies will
nological strategies for implementing these be important as well.
studies will include: classical laboratory cul-
ture methods, application of toxin probes, as- 3.1.3 Summary
says and analyses; biosynthetic feeding/label- The Organism program element of ECOHAB
incorporation experiments; standard reflects the fundamental importance of physi-
chromatographic techniques; and, methods in- ological, genetic, and behavioral studies in an
corporating mutagenesis and gene expression initiative designed to develop an understand-
protocols. ing of the population dynamics and trophic im-
pacts of harmful algal species. We take it as a
Issue: given that studies of HAB blooms require a
We must understand the importance of thorough understanding of genetic variabil-
motility and other behaviors of HAB ity and regulation, nutritional and environ-
species. mental tolerances and responses, behavioral

3. ECOHAB PROGRAM ELEMENTS
125

adaptations, life history transformations, automated detection and enumeration of HAB
toxin physiology and function, and numer- species using probe technologies would elimi-
ous other processes and features that will nate a major constraint to field programs -
vary among HAB species. Given the diverse namely the time required to process cell count
array of HAB species in the U.S. and the many samples collected at spatial and temporal fre-
different environments in which they occur, quencies similar to those for hydrographic and
this program element will likely be dominated chemical parameters. Such techniques would
by small research programs conducted by in- also make cell counts and even the physical
dividual investigators or small teams. Focused, separation of HAB species from co-occurring
multi-investigator proposals are also envi- organisms fast and accurate, permitting mea-
sioned on specific issues where coordination surements that otherwise would not be pos-
and comparisons between organisms would sible. Prioritization within the research issues
be beneficial. In many cases, the technology highlighted above was not attempted, as the
exists for the studies that are proposed, but a list already reflects an effort by workshop par-
focused methods development effort will ticipants to include only the most important
greatly accelerate progress on numerous other and timely research topics.
ECOHAB elements. For example, rapid and

WTV

TIME (hr)

0 2 4 6 8 10 12 14 16 18 20 22 24

-2

-4 X X

-6

-8

LU -10

-12

-14

-16

-18

Most HAB species move relative to the surrounding tion, and decline. This figure shows the vertical migra-
water. Some non-flagellated species are more dense than tion patterns of 10 different dinoflagellate species in a
water and sink; other species are less dense than water water column forced by a 3 m/sec wind. Sunset occurs
and float. Flagellated species exhibit a broad range of at 0 hrs., and sunrise at 12 hrs. The data are computer
swimming capabilities that in more extreme cases can generated, but the behavioral model is based on a sum-
support daily vertical movement of 10 to 20 m. The sig- mary of observations reported in the literature. Clearly,
nificance of motility for HAB initiation, growth, mainte- each species responds in a unique manner with respect
nance and dissipation is not well known. However the to respiration/photosynthesis rates, depth of penetration,
vertical trajectories of individual cells based on the corri- and timing of ascent and descent. These factors will have
bined effect of directed motility and vertical water mo- a profound effect on the timing, location, and magnitude
tion in principle can influence HAB initiation, accumula- of individual HAB events. Data from Kamykowski (1995).

3. ECOHAB PROGRAM ELEMENTS
261
@1 ag WMAWN
3.2 Environmental Regulation of Blooms

3.2.1 Introduction ronmental Regulation program element of
Rationale: Concurrent with escalating in- ECOHAB is thus:
fluences of human activities on coastal eco- Goal: To determine and parameterize the
systems, the environmental and economic environmental factors that govern the ini-
impacts of HABs have increased in recent tiation, growth, maintenance, dissipation
decades. It is therefore imperative to know and impacts of HABs.
if present trends of human activities and
HABs will lead to unacceptable conse- Physiological responses and life histories of
quences, and if the means can be developed HAB species are varied, as are local and re-
to mitigate impacts. The key to this knowl- gional physical environments where HABs oc-
edge is an understanding of the ecology and cur. Thus there is considerable variability in
oceanography of harmful algal blooms. An the relationship of HABs to their environment.
important facet of this complex topic is en- In spite of this complexity, however, it is usu-
vironmental regulation, that is, the influence ally possible to elucidate the patterns under-
of environmental factors on the population lying recurrent blooms in an area. Generali-
dynamics of harmful algal species and their zations to other regions is not usually
competitors. appropriate, however. An understanding of the
The geographic range, persistence, and in- relationship between an HAB species and its
tensity of HABs are determined by both physi- physical and biological environment is criti-
cal and biological factors. For example, the cal to predicting environmental and economic
initiation of a bloom requires successful re- impacts and to the formulation of mitigation
cruitment of a population into a water mass. strategies to minimize those effects. Since it is
This may result from excystment of resting impractical to study all of the ecosystems in
cells during a restricted set of suitable condi- which HABs occur, a second goal is:
tions (e.g., Alexandrium in the Gulf of Maine; Goal: To formulate principles that explain
Anderson and Keafer, 1987), transport of cells similarities between ecosystems during
from a source region where blooms are al- HABs and to understand how these systems
ready established (e.g., Gyrnnodiniurn are unique with respect to the types of
catenaturn in northwest Spain; Fraga et al., blooms that occur.
1988), or exploitation of unusual climatic or
hydrographic conditions (e.g., Pyrodinium 3.2.2 Research Agenda
bahamense and ENSO events in the Indo-West The following section outlines specific is-
Pacific; Maclean, 1989). Once a population sues defining high priority field, modeling and
has begun growing, its range and biomass are experimental studies required in the Environ-
still affected by physical controls and nutri- mental Regulation program element of
ent supply. Physical controls include long dis- ECOHAB.
tance transport of populations (e.g., Franks
and Anderson, 1992a), accumulation of bio- Issue:
mass in response to water flows and swim- To what extent do HABs reflect in-
ming behavior of organisms (Kamykowski, creases in growth rate versus physical
1974; Cullen and Horrigan, 1981), and main- transport and immigration? Is there a
tenance of suitable environmental conditions specific suite of physical factors asso-
(including temperature and salinity, stratifi- ciated with many HABs?
cation, irradiance, and nutrient supply; Physical factors in the environment influ-
Whitledge, 1993). Aspects of nutrient supply ence HAB population dynamics both directly
include not only the amount of macro- and by moving and aggregating cells, and indirectly
micronutrients, but also their ratio and mecha- by influencing the cells' physical and biologi-
nism of supply. Thus, physical forcings, nu- cal environment. Factors that can influence the
trient supply, and behavior of organisms all population dynamics and physiology of phy-
interact to determine the timing, location, and toplankton include: nutrients, temperature;
ultimate biomass achieved by the bloom, as salinity; irradiance; stability of the water col-
well as its impacts. The first goal of the Envi- umn; turbulent mixing; currents; vertical ad-

3. ECOHAB PROGRAm ELEMENTS
127

p
B&`3.!.-1'HA8-POPULATION DYNAMICS

Achievement of the goals of ECOHAB will require forcings, nutrient supply and ecological processes to de-
multidisciplinary field studies, supported by long-term scribe how they foster HABs. The primary problem is
environmental observations and broad-based research on that the observed changes in the abundance of harmful
the fundamental processes that form the links between algae at a given location are a function not only of bio-
organismal physiology, environmental forcing, commu- logical processes such as organismal growth and trophic
nity interactions, and the development of HABs. The first interactions, but also of physical transport, physical dis-
steps are to identify the factors that might influence eco- persion, and the interactions of swimming and sinking
system structure in general, and harmful algal species in behavior with these physical processes. Although some
particular, then to determine which factors dominate in of these terms may be minimized by local hydrography
particular systems. We know the physical and nutritional (e.g., reduction of advection losses in coastal lagoons)
factors that can influence the population dynamics of or local biology (e.g., reduction of grazing losses in toxic
phytoplankton, and we have some information on how blooms), in most cases one cannot a priori determine
nutrients and light might modify harmful characteristics the cause of an HAB without assessing the relative mag-
of some species (e.g. Boyer et al., 1987). However, we nitudes of all the specific rate terms in the population
cannot yet parameterize the interplay between physical dynamics conservation equation:
where: (I/N) (dN/dT) = KO + Ki - K 9- KM_K a - Kd
(I/N) (dN/dT) is the specific rate of increase in population numbers;
KO is the specific rate of growth of the organism (cell division rate);
Ki is the specific rate of immigration (usually resulting from swimming or sinking behavior interacting with
advection and mixing);
K 9is the specific rate of grazer induced mortality
KM is the specific rate of mortality from all other causes
Ka's the specific rate of loss due to advection (e.g., velocity in three components); and
Kd is the specific rate of loss due to dispersion by small scale mixing. (e.g., turbulent advective flux).

This equation is exact and concise, and is the basis for development of both idealized and realistic models.
However, it is difficult to apply to natural populations for four reasons:
i) There is insufficient knowledge of all the processes which affect the different terms;
ii) it is difficult to measure or parameterize the advective and turbulent transport;
iii) There is extreme spatial complexity and temporal variability of the biological quantities;
iv) The problem of describing biological rate processes under the influence of environmental variability is daunting.

These difficulties are offset by two advantages. The model:
i) Represents a quantitative basis for assessing the relative roles of physical vs biological processes; and
ii) Is a logical framework for comparison among different systems.

vection, dispersion or dilution; wind stress; motions determine in large part an alga's abil-
bottom stress and bathymetry. Temperature, ity to exploit light and nutrients. Finally, strati-
salinity and irradiance directly influence fication of the water column allows weakly
growth rate, physiology, and in some species, swimmming algae to interact with current
behavior (e.g., Watras et al., 1982; Tyler and shear and thereby drastically alter immigration
Seliger 1981). High shear associated with tur- rates. The success of individual HAB species
bulent mixing may alter growth, behavior, and is associated with different hierarchies of these
in extreme cases induce mortality (e.g., influences, and we expect these associations
Pollingher and Zemel, 1981; Thomas and to vary among ecosystems.
Gibson 1990; Berdalet 1992). Water motions There are a wide variety of flow regimes in
(a complex interaction of most of these fac- which HABs occur, from well-mixed estuaries
tors) determine the losses and gains from ad- to upwelling regimes and highly stratified river
vection as well as losses to dispersion plumes. Among these diverse settings, verti-
(Kamykowski 1979, 1981). In addition, water cal and horizontal transport processes play

3. ECOHAB PROGRAM ELEMENTS
281

important roles in regulating bloom develop- is the mixing in stratified shear layers removed
ment, although the physical mechanisms and from boundaries, such as those found at the
rates may vary considerably between environ- base of buoyant plumes. The rate of vertical
ments. Characterizing transport processes in mixing must be accurately quantified and re-
these stratified and/or spatially non-homoge- lated to measurable mean properties in order
neous regimes represents a challenging basic to interpret observations and develop models
research problem. Our progress in under- of HABs. Vertical transport processes associ-
standing HABs thus requires advances in ated with upwelling, frontal processes and sec-
coastal physical oceanography. Some of these ondary circulations may be comparable to (or
unresolved physics problems that have an im- more important than) vertical mixing. These
portant bearing on HABs include: motions facilitate vertical exchange, but they
also play an important role in the aggregation
Turbulence and Vertical Transport. While of plankton.
there are many turbulence closure models that
parameterize the effects of stratification (e.g., Horizontal Dispersion Processes. As is the
Martin, 1985), such models may not apply case with parameterizing vertical mixing, the
across the range of conditions found in coastal rate of horizontal dispersion is difficult to quan-
environments. A particularly difficult problem tify at the scales relevant to HABs. In estua-
rine 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
0.006 - remains considerable room for improvement
Diatom Bloom in parameterization of flushing. In coastal set-
7
0.005 - 45 nm offshore tings, Okubo's (1971) mixing diagrams still
provide the benchmark for estimation of small-
--------- 75 nm offshore scale horizontal exchange. Dispersion theory
C) 0.004 -
0) has advanced considerably with the contribu-
tions of Young et al (1982) with respect to shear
70 0.003 -
LU dispersion and Zimmerman (1986) for chaotic
dispersion. However, there are few observa-
0.002 tional studies that provide the requisite mea-
V.
surements of small-scale velocity variation re-
quired to turn these theoretical ideas into
0.001
estimates of horizontal dispersion. Given re-
0.000 cent progress in measurement of small-scale
400 500 600 700 variations of velocity (e.g., Geyer and Signell,
1992; Prandle 1991), there is great potential to
Wavelength (nm) make substantial progress on this important
research area, and one mechanism for such
This figure shows variations in ocean color in coastal waters study would be through ECOHAB.
off Oregon (September, 1994). Measurements of upwelling spec-
tral radiance (Lu(k); @LW cm-1 nyffl sr-1) and downwelling irra- Buoyant Plurnes. HABs are frequently ob-
diance at 490 nm (Ed(490); gW cm-1 nm-1) were recorded at I served in association with buoyant plumes
Hz with a Tethered Spectral Radiometer Buoy (TSRB) during (Therriault et al., 1985; Franks and Anderson,
deployments of up to several hours. The ratio of Lu (k) /Ed (490) 1992a; Tester et al., 1991). While the bulk char-
(units of sr-1, � s.d.) is a measure of reflectance. The sensor acteristics of buoyant plumes are well estab-
system, with five spectral bands comparable to the SeaWiFS lished, the details of the velocity and density
ocean color satellite, and two more to characterize the fluores- structure and their variability are not ad-
cence of chlorophyll, easily distinguishes different water types. equately understood to explain the transport,
The buoy does not have the spatial coverage of a satellite, but it aggregation and dispersion of algal cells within
does work under cloud cover, and it measures brightness with- plumes. The strong vertical and horizontal
out uncerta *inties about atmospheric corrections. Such a sys- shears occurring within plumes result in a com-
tem is well suited for characterizing the frequency and dura- plex advective regime that may concentrate
tion of HABs in surface waters. Unpublished data of J.J. Cullen, cells within the front or disperse them, depend-
M. Ciotti, M.R. Lewis, and S. McLean. ing on the interaction between the relative
motion of the organisms and the flow field.

3. ECOHAB PRoGRAm ELEMENTS
129

Estuarine Circulation. T e c assic para igm
Bo)@ 3.23 REMOTE gi'N`@@7 of two-layer estuarine circulation is a gross
oversimplification of time-dependent and three-
dimensional motions in estuaries. Wind-driven
motions provide a large perturbation that in
many environments may dominate the hori-
zontal 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
Al interaction of stratification, tides and winds
play an important role in horizontal dispersion
re
and vertical exchange, and they provide criti-
cal controls on the spatial distribution of plank-
ton cells. These processes and their interac-
tions are certainly complex, but careful
consideration of both physical and biological
features can lead to important insights into the
opulation dynamics of phytoplankton in an
Ao@ p
area. The work of Seliger et al., (1970) and
Tyler and Seliger (19 78) are noteworthy in this
Remote sensing has long been considered an ideal tool for regard.
detection of algal blooms, but satellite images of the chloro- Each of the physical processes described
phyll distributions have typically been of little use to HAB sci- above is an active area of research in physical
entists. This is because the pigment signature is a bulk mea- oceanography, but much of this work is tak-
surement that includes all the phytoplankton that. are present, ing place without reference to phytoplankton
and HAB species are often only a minor component of the total populations. With respect to the ECOHAB pro-
assemblage. In addition, many motile HAB species accumulate gram, it would be unrealistic to strive for a
in subsurface layers that are not detected with satellite sensors complete understanding of how each these
that mainly register pigments in surface waters. In contrast, processes can drive ecosystem response. There
sea surface temperature, detected with infrared sensors on sat- are, however, tractable physical problems that
ellites, has proven to be far more useful, as it can delineate can be addressed, and large advances in our
water masses that contain the algal blooms. Above is an AVHRR understanding can be obtained with collabo-
satellite infrared image depicting sea-surface temperature off rations between HAB biologists, physicists, and
the coast of North Carolina in late October, 1987. This advanced, modelers.
very high resolution radiometer (AVHRR) photo shows a blue Priority acitivites should be to:
filament of Gulf Stream water (24-25 OC) near Cape Lookout 1. Describe and model the dynamics of HABs
that is now known to have transported toxic Gymnodinium in relation to their physical environment.
breve cells from the Gulf Stream (deep blue), into the colder 2. Determine how variations in population
(yellow) coastal waters. The filament remained detectable in growth rate and biomass depend on small
satellite images for three weeks. Similar applications of remotely scale turbulence through its influence on
sensed sea surface temperature have led to significant insights nutrient uptake, grazing, cell division, ac-
into the alongshore transport of PSP-producing dinoflagellates cumulation, and bloom structure.
in the northeast U.S. Photo courtesy of T. Leming. 3. Determine how the vertical distribution
of HAB populations regulates bloom de-
velopment and dissipation, and how ver-
Secondary circulations associated with winds, tical distribution relates to physical (e.g.,
planetary rotation and topography also con- horizontal and vertical advection, vertical
tribute to the complexity of the flow within mixing and stability) and biological pro-
these environments. Numerical models simu- cesses (e.g., motility, buoyancy control).
lating theoretical coastal buoyant plumes un-
der surface wind stress have been formulated Approach and Technology. To determine
(e.g., Chao, 1987), but no one has yet incor- the influence of environmental factors on the
porated behavioral or physiological models of development of HABs, it is essential to describe
HAB species into such physical models. their distributions in time and space, and this
will require coordinated and multidisciplinary

3. ECOHAB PROGRAM ELEMENTS
301

Chain-forming eutrophication or remediation, for example. If
dinoflagellates such observations can be made autonomously
like this Alexan- and interpreted reliably, they would be ideal
drium species
for the detection of HABs in coastal waters,
thrive in well- even in remote locations. Because some harm-
mixed environ- ful species can exert profound negative effects
.ments where on coastal resources without dominating the
solitary cells do
phytoplankton and changing the color of the
poorly, The cou-
pling between water, there are limitations to the usefulness
physics and biol- of optical instruments for detecting HAB phe-
ogy is clear, but nomena. Nonetheless, continuous optical mea-
the mechanisms surements in coastal waters would be ex
are poorly under- tremely useful for describing bloom dynamics
stood. Photo by
and long-term trends. Furthermore, with the
Y.Fukoyo
-identification technolo-
development of species
gies described in section 3.1.2, it should be-
come 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-reso-
lution distributions on local to regional scales
(e.g., Millie et al., 1992). Satellite sensors, such
as SeaWiFS, will provide lower temporal and
#4 spatial resolution, but over regional to global
studies. Information on the distributions of scales. Calibration and deployment of these
physical and biological variables should be syn- instruments during HAB events is essential to
optic in space (local to regional scales) and the development of a remote sensing capabil-
highly resolved in time (hours to days) cover- ity for such phytoplankton blooms.
ing successive bloom periods (interannual vari- Shipboard research programs are also es-
ability). This level of coverage would be ideal, sential to the elucidation of HAB dynamics,
but it is expensive and probably unrealistic in not only to obtain direct measurements of rates
the context of ECOHAB alone, given the many and standing stocks of key components, but
sites where HABs occur. Excellent results have also as a means of relating component vari-
been obtained, however, with focused field ability to information from moorings and re-
programs that involve significant physical com- mote platforms. Field programs aimed at un-
derstanding the interactions between HAB
ponents (e.g., Seliger et al., 1970; Tyler and
Selig Ier, 1978,1981; Franks and Anderson, species and their physical environment are typi-
1992a). Future collaborative efforts between cally hampered by the enumeration of HAB
physical and biological oceanographers should individuals in a diverse assemblage of phy-
thus be emphasized and encouraged. toplankton, microzooplankton and detritus.
There is considerable potential for the use Small, low cost profilers are needed that can
of moored optical sensors in red tide/toxic al- be rapidly deployed in the vicinity of HABs to
gae research and monitoring (see Box 3.2.2). define their spatial structure and temporal evo-
When properly designed and calibrated, these lution. These profilers can be deployed with
sensors measure radiometric quantities that self-contained CTD/fluorometer/transmissom-
should be particularly appropriate for long eter/optical backscatter packages for measure-
time-series observations in coastal systems. ment of key physical parameters that may di-
That is, unlike measurements of chlorophyll, rectly or indirectly control bloom development.
floristics, and stimulated fluorescence, which Analytical and numerical models are impor-
are somewhat dependent on equipment and tant tools for studying physical-biological inter-
methods, records of irradiance and radiance actions in the ocean. Models have been used for
should be completely comparable over many decades to understand how physical forcings
years, documenting changes associated with influence the distribution and production of HAB
species. New architectures for physical models

3. ECOHAB PROGRAm ELEMENTS
131

which incorporate turbulence-closure formula- 1987). Japanese authorities instituted effluent
tions for the small-scale motions (e.g., Blumberg controls in the mid-1970's, resulting in a 50%
and Mellor, 1987) now provide important plat- reduction in the number of red tides that has
forms for the investigation of physical-biologi- persisted to this day.
cal interactions over scales of meters to hundreds
of kilometers. The incorporation of behavioral As coastal communities and countries
and physiological models of HAB species into struggle with pollution and eutrophication is-
these physical models is a necessary and impor- sues, the implications of the trends in Hong
tant step in elucidating the couplings between Kong, Japan, and other countries are profound.
nonlinear physical flows and time-dependent bio- The public, the press, and regulatory officials
logical responses (see Box 3.1.6). The formula- are concerned about whether this is happen-
tion of theoretical models investigating the na- ing in the U.S. as well, and are asking for pre-
ture of interactions between physical flows and dictions and answers about FIAB incidence that
organism behaviors must be encouraged. exceed our present capabilities. Unfortunately,
competitive outcomes in phytoplankton spe-
Issue: cies selection and succession cannot yet be
How do physical and ecological pro- predicted, nor can the relative effects of natu-
cesses control the partitioning of nutri- ral versus anthropogenic factors be resolved.
ents within a system and the relation- A variety of important issues involving nutri-
ship between nutrient inputs and the ents and the manner in which they are sup-
population dynamics of HAB species? plied to and utilized by HAB species must thus
The availability of nutrients (inorganic and be addressed.
organic) to individual organisms ultimately
regulates the growth rate and net biomass of We need to:
blooms. Physical forcings, such as vertical mix- 1. Determine how changes in the magnitude
ing, stratification or advection can be signifi- and elemental ratios of nutrient inputs to
cant factors in determining the availability of coastal ecosystems can influence ecologi-
those nutrients. It is also clear that the rela- cal responses, especially those that favor
tionship between nutrient inputs and popula- HABs.
tion dynamics is complex and reflects many 2. Determine whether the frequency and du-
other, interacting processes. One of the expla- ration of harmful algal blooms are increas-
nations given for the increased incidence of ing in coastal waters relative to increases
HAB outbreaks worldwide is that these events in phytoplankton production in general.
are a result of increased pollution and nutrient 3. Investigate the extent to which HABs are
loading of coastal waters. Some argue that we indicators of local (point-source) or re-
are witnessing a fundamental change in the gional (diffuse input) increases in nutri-
phytoplankton species composition of coastal entloading.
marine ecosystems throughout the world due 4. Investigate how climatic variability from
to the changes in nutrient supply ratios from local to global scales influences the de-
human activities (Smayda, 1990). There is no velopment and dispersal of HABs.
doubt that this is true in certain areas where 5. Learn whether HABs are indicators of en-
pollution has increased dramatically. It is per- vironmental or habitat changes induced
haps real, but less evident in areas where by nutrient over-enrichment or other an-
coastal pollution is more gradual and unob- thropogenic effects (e.g., alterations in
trusive, In Tolo Harbor, Hong Kong, human freshwater or contaminant inputs).
population within the watershed grew 6-fold
between 1976 and 1986, during which time Approach and Technology. The potential
the number of red-tide events increased 8-fold stimulatory influence of anthropogenic nutri-
(Lam and Ho, 1989). The underlying mecha- ent inputs on HAB incidence is certainly one
nism is presumed to be increased nutrient load- of the more pressing unknowns we face, and
ing from pollution that accompanied human will require a focused commitment of resources
population growth. A similar pattern emerged and effort greatly in excess of that previously
from a long-term study of the Inland Sea of devoted to the topic. Time-series analysis of
Japan, where visible red tides increased existing data bases for phytoplankton commu-
steadily from 44 per year in 1965 to over 300 a nities and of variables such as major nutrients
decade later, matching the pattern of increased or pollutants are required. Where such data
nutrient loading from pollution (Murakawa, are lacking, long-term monitoring programs

3. ECOHAB PROGRAM ELEMENTS
321

must be initiated in key regions where anthro- loss terms, and life cycle dynamics. While field
pogenic changes are anticipated. Moored in- conditions such as circulation, meteorology,
strument packages including optical sensors and water chemistry have long been recognized
and other devices to resolve HAB classes or as critical elements in blooms of some toxic
species within the plankton would be highly species, neither the initial boundary conditions,
effective in this regard. Laboratory studies of nor the hydrographic regimes within which
the stimulatory effects of chemicals contained harmful blooms occur are clearly understood.
in effluents or terrestrial runoff are also needed, The comparative ecosystem approach adopted
as are kinetic studies and other experiments by ECOHAB will permit common features to
that can quantify the nutritional requirements be identified, such as coastal currents, up-
and uptake capabilities of HAB species (see welling, and nutrient enhancement of biom-
section 3.1.2 for a more detailed list of ap- ass levels. Additional insights will be obtained
proaches to nutrient issues). through numerical modeling efforts. Despite
the fundamental importance of predictive mod-
Issue: els for harmful algal blooms in different re-
Are there specific physical, chemical, gions, no such models exist for U.S. problem
and biological regimes or processes that species (see Box 3.2.4). The ultimate goal is to
are associated with HAB events? Are couple population dynamics with physical cir-
some ecosystems more susceptible to culation models for a given hydrographic re-
HABs than others? gime, and to refine physically/biologically
coupled models using field bloom observations
Issue: and toxicity patterns.
Population dynamics, including the
rate processes required in predictive We need to:
models of harmful blooms, cannot be 1. Identify environmental and biological
adequately described or predicted, al- cues or characteristics that can be mea-
though this information is of funda- sured and used to predict the onset and
mental importance to effective resource magnitude of HABs for the purposes of
management. research and management.
Information on bloom dynamics can be 2. Determine biological rate processes and
gained through laboratory and field studies that initiate studies of coastal hydrography and
define nutrient uptake kinetics, growth rates, water circulation for development of
physically/biologically coupled models at
i_w -
temporal and spatial scales appropriate to
harmful algal blooms.

Approach and Technology: Here again,
shipboard observations, field programs, satel-
lite remote sensing and moored instrument
arrays can all provide the level of detail re-
quired for the identification of the mechanisms
underlying HAB outbreaks. The key is to ob-
Ak
tain data at appropriate time and space scales
for the blooms under study, and this will re-
quire careful planning and considerable ad-
vance 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
Studies of benthic be developed as an integral part of these
processes and
multidisciplinary field studies. Models are re-
cyst dynamics are
quired to represent the broad range of envi-
needed for many
ronmental dependencies that contribute to
HAB species.
HABs. Since HABs reflect physical and biologi-
Photo by
"'M Rib
cal dynamics over a broad range of time and
D. Anderson.

3. ECOHAB PROGRAm EUMENTS
133

on harmful algal populations and regulate their
distribution, abundance, and impact. Despite
the diverse array of HAB species and the many
Prediction of HABs is an important goal of HAB research, hydrographic regimes in which they occur, one
yet predictive capability can only come from a detailed under- common characteristic of such phenomena is
standing of the factors controlling bloom dynamics. A feature that physical oceanographic forcings play a sig-
common to most HABs is a strong association with physical nificant role in both bloom dynamics and the
dynamics. Physical processes have quantifiable responses to patterns of toxicity or adverse impacts. Fur-
their forcings - in particular meteorological forcings such as thermore, the interplay or coupling between
wind stress, insolation, and precipitation. The links between physical -variables and biological "behaviors ",
meteorological forcings and HABs, mediated through ocean such as swimming, vertical migration, or physi-
physics and cell physiology, implies that our predictive capa- ological adaptation, holds the key for under-
bility for HABs should strive for, but can never exceed, the standing many HAR phenomena. This physi-
accuracy of weather predictions. There are, however, other forms cal/biological coupling can occur at both large
of prediction that can also be useful, such as delineating loca- and small scales, and includes processes of
tions that are susceptible to HABs, estimating the long-term great interest to both physical and biological
effects of pollution discharges or other human activities, or sim- oceanographers.
ply determining the most likely time interval for HAB outbreaks. Understanding the small- and large-scale
One of the goals of ECOHAB is to develop the information base physics underlying HAB phenomena is a clear
needed to support these types of predictions for a variety of priority, but this need should not be restric-
species and regions. tive. Observational and modeling studies of
physical processes need not be massive in
scale, cost, or complexity to provide useful
space scales, a hierarchy of models will be re- information. Significant insights on HAB dy-
quired. On small scales, models that examine namics have been obtained from field pro-
the vertical experience of HAB populations over grams with modest but focused physical com-
the diurnal cycle are needed to elucidate cell ponents (e.g., Seliger et al., 1970; Tyler and
dynamics. On larger scales, models that ex- Seliger, 1978; Franks and Anderson, 1992a).
amine bloom transport and dispersion are es- The potential stimulatory influence of an-
sential. Model dynamics and parameterization thropogenic nutrient inputs on HAB incidence
must be driven by field and laboratory data is a key unknown and time-series analyses of
that are sufficiently detailed to allow indepen- existing data bases are required, as are labo-
dent testing and corroboration. Such robust ratory studies of the stimulatory effects of
models may then have predictive capability. chemicals contained in effluents or terrestrial
Numerous data sets exist that can be used for runoff.
testing hypotheses regarding HAB dynamics, This program element will require investi-
but often such data have not been examined gations spanning the spectrum from large-scale
in depth nor have they been examined in terms field studies to mesocosm and laboratory ex-
of potential interactions among physical, periments. Modeling has a major role to play
chemical and biological variables as they re- as well. In many cases, the technology exists
late to HABs. Retrospective analyses of histori- to address the questions that are asked, but
cal data and information may provide impor- development is needed to permit biological
tant insights at a relatively low cost. data to be obtained on time and space scales
Often the main limitation of models is the similar to those currently possible with physi-
paucity of data available to formulate, force cal and chemical measurements. This challenge
and test them. As discussed above, field pro- is compounded by the need to focus on indi-
grams must be combined with coupled physi- vidual species rather than communities.
cal-biological models to gain the most from lim- The issues highlighted in this program ele-
ited resources and to test hypotheses ment are entirely complementary to those of
concerning bloom initiation, transport, and pat- the Organism element, and together they out-
terns of accumulation and dispersal. Much can line a direct path toward the goal of under-
be accomplished with limited data if it is ob- standing HAB dynamics and impacts. Manag-
tained at the right places and the right times. ers must recognize the urgent need for better
information about how the environment, and
3.2.3 Summary especially how human alterations to the envi-
The Environmental Regulation program el- ronment, can alter coastal ecosystems and lead
ement of ECOHAB addresses factors that act to harmful blooms.

3. ECOHAB PROGRAM ELEMENTS
341

I t
3T 6 0M n y eractions

3.3.1 Introduction Phytoplankton blooms develop through a
Rationale: The negative impacts of HABs sequence of stages termed initiation, growth,
are the result of complex interactions that maintenance and decline. A key to understand-
begin at the phytoplankton community level ing bloom dynamics is the identification of
and extend to upper trophic level compart- processes leading to transitions between these
ments. Habitat physics, life cycles, commu- stages; that is, what factors in the biology of
nity structure, growth and grazing processes harmful algal species and their grazers lead to
all combine to regulate the dynamics of the changes in growth and loss processes at dif-
HAB event. Therefore, studies on the impacts ferent phases of the HAB cycle? Of the terms
of trophic interactions in the selection and included in the population growth equation
dynamics of HABs, and conversely, the im- given in Box 3.2. 1, we consider in this section
pacts of HAB events on trophic structure, only the trophic interactions. Specifically, it is
processes and interactions are essential if we imperative that we understand how competi-
are to understand the ecology and oceanog- tive interactions between harmful algal spe-
raphy of harmful algal blooms. cies and other phytoplankton contribute to the
formation of blooms. Likewise, we must evalu-
ate how grazing controls, or fails to control,
@,:@@M M
RR : MW HAB development. These issues define the first
7@777
HAA spl,,cms ANn'THEIR lk"6SYS' oal of the Food-Web/Community Interactions
TEMS. 9
------- program element:
Goal: Determine the impacts of trophic in-
NIARM IIIAMAIAM teractions on selection for, and dynamics of,
HABs.
PISCrVOROUS FISH Harmful algal blooms involve multiple in-
teractions among predators, competitors and
the harmful algal species within an ecosystem.
PLANKTIVOROUSH 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
HERBIVOROUS ZOOPLANKTONT MICROBIAL FOODWEB ramifications of many of those pathways. We
must therefore determine the relative impor-
tance of each of these interactions over appro-
171911LARNAE SOLUTION FISH priate spatial and temporal scales. Implicit in
this task is the elucidation of the pathways and
BENTWC LARVAL fates of HAB toxins in the food-web. The
CUMNIS. MUSSELS, SCAUDPS, mechanisms by which the timing and fre-
quency of HABs (both toxic and high-biomass
types) affect community and trophic structure
ORILLS,W GROU SH also need to be identified. Progress in these
areas is essential to realizing our second goal:
Goal: Determine the impacts of HABs on
MACROPHYTES trophic structure, processes and interactions.
t
3.3.2 Research Agenda.
The following section outlines specific is-
sues defining high priority field and experimen-
@1..Vn.R.U@ S.

DEMONSTRATED ROUTE tal studies required to establish how trophic
interactions regulate HAB species' selection
POTENTIAL ROUTE and population dynamics, and how HAB
This conceptual model illustrates direct and vectored routings events, in turn, influence community/trophic
through which toxins and anoxia/hypoxia impact many differ- structure and trophodynamics.
ent trophic compartments. (From Smayda, 1992).

3. ECOHAB PROGRAM ELEMENTS
135

Issue: hibit grazing (Smayda, 1992).
It is essential to know the extent to Grazing control of HABs depends upon both
which bloom formation results from a the local abundance of grazers and their abil-
breakdown of grazing or from harmful ity to ingest the harmful algal species (Box
species outcompeting other phy- 3.3.2). Low grazer abundance can be critical
toplankton for limiting resources. in the early phases of bloom development by
Interspecific competition influences HAB providing times or regions where grazing losses
dynamics. The presence of co-occurring phy- are less than increases from cell division. Low
toplankton species reduces the capacity of the grazer. abundance can result from a variety of
environment to support one species' require- external biological factors (e.g., predation on
ments from a common pool of limiting re- grazers), or physical factors (e.g.,spatial sepa-
sources (e.g., nutrients). Species competition ration of HAB species from benthic grazers).
coefficients are modified continuously by Reductions in grazer abundance may also oc-
changes in growth parameters such as tem- cur in direct response to an HAB event (e.g.,
perature, light and nutrient availability, and avoidance or mortality induced by HABs;
are further altered by changes in grazing pres- Fiedler, 1982; Huntley, 1982), or as a result of
sure, community structure and allelochernical the effects of past HAB events on grazer popu-
effects. Enhanced growth or physical accumu- lations. In cases where grazers are abundant,
lation alone does not always explain HABs, grazing control may still not be exerted because
as some taxa secrete allelopathic substances toxins or small size can reduce the chance that
that inhibit or stimulate the growth of com- HAB species will be ingested. If harmful algal
peting and co-occurring algal species (e.g., species are consumed, grazers may be unaf-
Pratt, 1966; Gentien and Arzul, 1990) or in- fected, impaired or killed. The response of zoop-
lankton and benthic grazers to toxic algal oc-
WIN currence is often species-specific in terms of
I M1=NWM"WWWW
%1T.W4 0@1_ Niffi.PTT behavioral responses and toxin susceptibility.
MECHANISMS WHICH STIMULATE OR SUPPRESS HABs. Grazing control of HABs can also depend on
the population density of the harmful alga, as,
for example, when suppression of grazing oc-
FOOD WEB EFFECTS ON HARMFUL ALGAL BLOOM DYNAMICS curs above a threshold concentration of the alga,
as demonstrated for the Narragansett Bay brown
HARMFUL
ALGAL tide in 1985 (Tracey, 1988). A threshold effect
SPECIES may also occur if the daily production of new
HAB cells becomes large enough to saturate the
ingestion response of the grazers and the abil-
IF HAB IF HAB
TOXIC NON TOXIC ity of grazers to increase their populations. In
that case, population growth can accelerate dra-
matically (Donaghay, 1988). A breakdown of
grazing control has been implicated in the
IF GRAZERS IFGRAZERS
IFGRAZERS CONSUME HAB
AVOID HAB CONSUME HAB brown tides in Narragansett Bay (Tracey, 1988)
and in Texas (Buskey and Stockwell, 1993) and
removal/loss of the grazer population has been
GRAZERS GRAZERS GRAZERS GRAZERS
UNAFFECTED IMPAIRED DEAD INCREASE reported to precede or accompany bloom de-
l X @ I velopment (Montagna et al., 1993). There is,
INCREASED REDUCED INCREASED however, little information on how the nature
GRAZING PRESSURE GRAZING GRAZING PRESSURE of the grazer response influences the timing,
ON HAB COMPETITORS LOSIES ON HAB &OR magnitude and duration of HABs.
COMPETITORS
In order to address the issue of trophic
INCREASED HAB INCREASED NET influences on HAB formation we need to:
POPULATION HAS POPULATION
GROWTH GROWTH RATE 1. Determine the role of differential growth
RELATIVE TO rates, nutrients and nutritional strategies
COMPETITORS
f in competitive interactions among phy-
STIMULATE SUPRESS toplankton species.
HARMFUL ALGAL HARMFUL ALGAL 2. Determine the nature and extent of allelo-
BLOOM BLOOM
pathic interactions.
3. Determine the importance of spatial and
temporal separation between harmful algal

3. ECOHAB PROGRAM ELEMENTS
361

species and grazers, and the relative con- Issue:
tribution of pelagic and benthic grazing. Are biological controls (e.g., grazers,
4. Determine the role of harmful algal spe- pathogens) the cause of bloom
cies' behavior, toxicity and food quality in termination?
reducing or avoiding grazing controls, as The role of biological mechanisms in con-
well as the importance of density-depen- tributing to bloom termination remains largely
dent processes (e.g., grazing thresholds). unknown. In some instances, HAB impacts on
5. Determine the effects of mixed (toxic/non- grazers are so severe that these organisms may
toxic) assemblages on grazing control be of little consequence in the termination of
(e.g., does breakdown of grazing only oc- blooms (e.g., Bricelj and Kuenstner, 1989; see
cur once harmful algae become a domi- Box 3.3.1). The occurrence of viral particles in
nant component of the phytoplankton?). cells of a harmful algal species has also been
observed (Sieburth et al., 1988; Milligan and
Approach and Technology. A combination Cosper, 1994), but the efficacy of this mecha-
of field, mesocosm and laboratory studies will nism to control natural HABs remains to be
be required to elucidate the nature and extent demonstrated. In addition, it has been sug-
of species' interactions and grazing regulation gested that bacteria may play a role in regulat-
in HAB phenomena. Quantitative data for ing the population dynamics of HAB species
growth rates and grazing-related mortality rates (Doucette, 1995).
of harmful algal species are needed, as are
measurements of population recruitment rates Assessing the involvement of biological
for both HAB taxa and their grazers. In situ controls in terminating HABs requires inves-
estimates of growth and grazing rates, obtained tigation of:
in the context of sampling programs that de- 1. The effects of HABs on the grazer com-
fine the temporal and spatial variability of an munity in terms of functional groups and
HAB and its potential grazers, are essential for their concentrations.
quantifying the role of grazers in controlling 2. Alternative biological mechanisms for
HAB dynamics. Mesocosm experiments are HAB decline and termination (e.g., patho-
needed to determine the patterns and dynam- gens)
ics of interactions between HA13 species and
grazers, and the population growth character- Approach and Technology. Several ap-
istics of competitors in the presence and ab- proaches, including field studies and
sence of harmful algal species. Laboratory in- mesocosm and laboratory experimentation, are
vestigations are required to determine needed to determine how specific biological
interactions between HAB species and indi- mechanisms can contribute to the termination
vidual grazers, to measure growth and graz- of HABs. The majority of tasks described ear-
ing rates on harmful algal species in the pres- lier as essential to defining the influences of
ence of "organics" secreted by HAB species, trophic factors on bloom formation are also
and to elucidate allelopathic impacts, mecha- required here. In addition, the impacts of patho-
nisms and pathways involved in HABs. gens such as viruses and bacteria on HABs
Development and/or improvement of the need to be assessed in a quantitative fashion
following technologies are required to imple- in the context of both field studies and
ment the approaches described above: species- mesocosm manipulations. Sampling schemes
specific molecular probes for HAB identifica- must take into account the appropriate tem-
tion; methods for in situ detection and poral/spatial scales relevant to these interac-
quantification of HABs during all bloom tions, as well as environmental factors poten-
phases; diagnostic indicators of grazer physi- tially regulating the distribution and abundance
ological status; methods for assessing grazer of the pathogens. When possible, pathogenic
food quality; video techniques for measuring organisms should be isolated and examined in
in situ grazing and avoidance behavior; high- the laboratory to provide a mechanistic under-
resolution sampling of fine-scale HAB and standing of their effects on HAB taxa.
grazer distributions; and suitably scaled mi- Strategies for elucidating factors involved in
crocosm and mesocosm experimental strate- the formation and termination of HABs over-
gies and systems. lap considerably. Most of the technologies re-
quired to investigate bloom termination are
well established in the phytoplankton and
zooplankton literature. To evaluate the role of

3. ECOHAB PROGRAM ELEMENTS
137

pathogens in terminating blooms, several new 1992). Herbivorous fish can also accumulate
techniques must be developed or improved: and transfer toxins, and even cause mass mor-
taxon-specific molecular probes and their ap- talities of the marine birds that consume them
plication for identifying and quantifying patho- (Work et al., 1993). Mortality of marine mam-
gens in situ; sampling methods for concurrently mals linked to trophic transfer of HAB toxins
resolving HAB and pathogen distributions over has also been reported (Geraci et al., 1989).
a range of temporal/spatial scales; techniques During their food-web transfers, toxins may
for measuring negative impacts of pathogens be bioaccumulated, excreted, degraded or
on HAB species; identifying the underlying structurally modified, as in the case of enzy-
mechanisms, and assessing the taxonomic matic bio-transformation of PSP toxins in some
specificity of these effects; and appropriately bivalve molluscs (Cembella et al., 1993).
11 contained" experimental microcosm and
mesocosm systems. In order to define the role of toxins in me-
diating the effects of HABs on food-webs, it
Issue: is necessary to:
It is essential that we learn the man- 1. Identify target species and their life-his-
ner in which the effects of HABs on the tory stages that are adversely affected by
food-web are controlled by toxin dy- toxic algae, and those that act as vectors
namics, routing pathways, and the dif- of toxin transmission through the food-
ferential susceptibility of species at web.
higher trophic levels. - 2. Determine pathways, transfer rates and
The toxins of HAB species may have evolved mechanisms for bioaccumulation, trans-
to release these species from grazing pressure. formation, degradation and elimination of
Similar anti-herbivore defenses are well-docu- algal toxins.
mented in terrestrial plants, but have received 3. Characterize modes of action of various
scant attention in marine systems. Many algal phycotoxins (e.g., neurotoxic, cytotoxic,
toxins (e.g., PSP and DSP toxins) are endotox- hemolytic) on marine fauna and deter-
ins that affect planktonic and benthic grazers mine their differential susceptibility.
after consumption. Susceptibility to ingested
toxins and, thus, the ability to accumulate tox- Approach and Technology. Field studies as
ins, vary markedly within and among taxa well. as supporting laboratory and mesocosm
(Twarog et al., 1972), as suggested by reports studies using algal toxins as tracers are needed
that finfish appear to be more sensitive to PSP to describe changes in toxin concentrations and
toxins than crustaceans or molluscs (Robineau transformations of toxins from one trophic level
et al., 1991). If the grazing species are not to another. Predictive and heuristic models of
killed, accumulated toxins may be trans- food-web transfer of algal toxins should be
ferred to other components of the food-web developed. These models might be analogous
and affect other organisms at higher trophic to those formulated for anthropogenic contami-
levels. This is an area where our knowledge is nants (heavy metals, radionuclides, organic
rudimentary at best, as subtle, ecosystem-level pesticides). A comparative, experimental ap-
effects are probably pervasive, affecting many proach is also needed to determine dose-de-
different trophic levels, depending on the toxin pendent behavioral (e.g., swimming avoid-
involved. Recruitment rates or year-class sizes ance), physiological (e.g., grazing inhibition)
of important commercial fish species may well and cellular (e.g., toxin inactivation, compart-
be directly affected by brief exposures of lar- mentalization) responses of marine organisms
val or juvenile stages to toxic algae. to toxic algal species.
Zooplankton impaired by ingesting harm- In order to carry out the research on toxins
ful algal species may be more susceptible to associated with HABs outlined above, rapid,
predation, and thus may become an impor- standardized toxin assays, with detection based
tant vector for transferring toxins in the pe- on both chemical structure and toxic activity,
lagic food-web. Alternatively, zooplankton must be developed to elucidate toxin pathways.
killed outright may sediment and allow toxins Toxin probes (e.g., antibodies specific for indi-
to enter benthic food-webs. Zooplankton fecal vidual forms of a toxin), employed in conjunc-
pellets may also be important sources of toxin tion with these assays, may be required to
to benthic communities. Thus, zooplankton quantify and localize toxin derivatives in tar-
can act as vectors of HAB toxins resulting in get organisms.
events such as fish kills (White, 1981; Smayda,

3. ECOHAB PROGRAM ELEMENTS
381

Issue: 5. Identify HAB-induced changes in ecosys-
Are chronic, sublethal impacts of HABs tem energy/nutrient pathways.
more significant than acute (lethal)
impacts in altering food-webs or caus- Approach and Technology. Field and
ing trophic dysfunction? mesocosm studies, as well as laboratory experi-
Blooms of harmful algae may be recurrent mentation, are essential for evaluating the im-
in some areas (e.g., red tides of PSP-and NSP- pacts of chronic versus acute exposure to HABs
producing dinoflagellates in the Northeast U.S. on food-web structure and trophodynamics.
and Gulf of Mexico, respectively), episodic This suite of approaches is needed to deter-
(e.g., 1987-88 Gymnodinium breve red tide in mine the species-specific effects of harmful al-
North Carolina estuaries) or, more rarely, per- gal species on egg, larval, juvenile and adult
sistent (e.g., brown tides in Laguna Madre, stages of target species. Comparisons of HAB
Texas). Chronic, sublethal effects of HABs on impacts are needed both among different habi-
marine biota have been documented, as in the tats and within the same system where HABs
case of brown tide persistence being linked to occur with different frequencies, duration and
gradual reductions in eelgrass and shoalgrass intensities. We must quantify the effects of re-
meadows (Dennison et al., 1989). More@ often, current, episodic and persistent HAB events on
however, it is the effects of brief, but acute recolonization rates of species from represen-
blooms that have received the most attention tative trophic levels, which vary in their life-
because of their immediate impacts on eco- history strategy, generation time and suscepti-
systems or humans (e.g., Shuinway, 1988; bility to HABs. We also need to investigate the
Bates et al., 1989; Smayda, 1992; Burkholder impacts of HABs at aquaculture sites, where
et al., 1992). Episodic HABs are often associ- stocks are concentrated at high densities and
ated with acute, lethal effects on adult stages are routinely monitored for growth, mortality
of commercially important species (Tracey, and disease incidence.
1988; Surnmerson and Peterson, 1990; Several technological advances/ improve-
Burkholder et al., 1992; Taylor, 1993). Removal ments are needed to augment those currently
of parental stocks may cause recruitment fail- employed for acquiring the types of informa-
ure of some natural populations with limited tion cited above: remote sensing technology
dispersal capabilities (Peterson and and in situ high frequency optical devices to
Surnmerson, 1992). However, it is more likely obtain more rapid, efficient measurements of
that HABs adversely affect recruitment success phytoplankton abundance and composition;
by exerting sublethal, chronic impacts on re- computerized motion analysis to study behav-
production (e.g., reduced fecundity), growth ioral effects; toxin assays and probes, includ-
and behavior (Bricelj et al., 1987; Buskey and ing applications development, for quantifying
Stockwell, 1993). These chronic effects, which and localizing toxins in target species.
may have long-term consequences for year-
class strength and persistence that are critical Issue:
in the recovery of natural populations to pre- Are HAB impacts are controlled by the
bloom levels, have received little attention and degree of temporal and spatial overlap
merit serious consideration. between blooms and critical life cycle
stages of affected species.
Characterizing the relative importance of The impacts of HABs on sensitive life cycle
chronic, sublethal versus acute, lethal im- stages of affected species higher in the food-
pacts of HABs on food-webs and their com- web depend upon their co-occurrence in time
ponents requires that we: and space, which varies dramatically with the
1. Determine lethal and sublethal effects of degree of vertical stratification and exchange
HABs on life-history stages of key species with surrounding waters. In some well-mixed
in the food web. estuaries and lagoons, HABs may be suffi-
2. Identify mechanisms of recruitment fail- ciently persistent and dispersed throughout the
ure, or reduction in affected species. system so that all species are equally exposed,
3. Investigate the extent, time frame and as in the case of brown tides in Laguna Madre,
mechanisms of recovery of natural popu- Texas (Buskey and Stockwell, 1993). Such even
lations impacted by HABs. exposure greatly simplifies the task of relating
4. Characterize differential effects of epi- observed changes to the effects of HAB popu-
sodic, recurrent and chronic HAB events lations. However, in stratified waters, reduced
on food-webs. vertical mixing may allow weakly swimming

3. ECOHAB PRoc;RAm ELEMENTS
139

a 4

Just as human consumers of seafood contaminated itoxin in mackerel that they had consumed. Likewise, these
with biotoxins of algal origin are at risk, many animals at emaciated loons that were washed ashore in North Caro-
higher levels of the marine food-web are impacted by lina may have been victims of algal toxins in their food.
HABs. Some toxins are fat-soluble and bioaccumulate in Exposures that are not initially lethal may still cause mor-
higher trophic levels. Others still transfer through succes- tality in wildfowl, during or after stresses such as migra-
sive stages, sometimes having lethal impacts where they tion. Because ecosystem impacts from HABs can be subtle
are least expected, such as with this humpback whale, and difficult to document, their true extent or significance
one of 14 that died in a one-month period due to sax- is not known. Photos courtesy of G. Early and P. Spitzer.

plankton, including HABs and potentially af- sponses based ori statistically derived average
fected groups (i.e., microzooplankton, dispersion and abundance measurements, of-
macrozooplankton and fish larvae) to form ten on an annual basis. Yearly, and probably
highly concentrated layers surrounded by re- even seasonal means, are, however, inadequate
gions of low or undetectable concentrations of to assess impacts of HAB species, which often
the organisms (Donaghay et al., 1992). In strati- form short-term, high-impact blooms in areas
fied systems exposed to current shear from that provide critical spawning/nursery habitat
winds and tides, the distributions of both HABs for higher trophic levels. Consequently, we
and target plankton may also vary dramatically need to determine the small-scale, temporal/
in response to lateral advection of layers and spatial distribution patterns and abundances
interactions between organismal swimming of HAB taxa.
behavior and current shear. Regardless of the Resolution of co-otcurrence effects in strati-
prevalent physical system, however, it is highly fied waters will require both field and
unlikely that HAB impacts can be predicted mesocosm studies. Field programs must be
from average concentrations of HAB and af- aimed at quantifying temporal and spatial
fected species. scales, as well as in situ concentrations of HAB
and co-occurring, affected species. This will
In order to assess the extent to which tem- require application of high resolution sampling
poral and spatial factors control the impact of techniques, both to detect changes in abun-
HABs on other species, we need to: dance on sub-meter scales, and to link those
I .Investigate the temporal and spatial coin- changes to physical structure and processes in
cidence of susceptible life-history stages the system where the HAB occurs. Such field
of key species (e.g., grazers) with HABs. investigations must be complemented by
2. Determine the physical processes and bio- mesocosm experiments designed to elucidate
physical interactions that control bloom the underlying mechanisms that lead to ob-
development and grazer responses. served patterns of co-occurrence or avoidance.
Accurate, fine-scale characterization of the
Approach and Technology. Determining temporal/spatial aspects of HAB interactions
the degree to which HAB impacts are regu- with affected species will depend on: adapt-
lated by temporal and spatial factors requires ing spectral optical and video sensors for de-
evaluation of impacts on affected species from ployment on vertical profilers or towed sys-
actual time-space abundance measurements. tems to detect HAB distributions in real-time;
The typical approach has been to estimate re- designing "smart" sampling systems triggered

3. ECOHAB PROGRAm ELEMENTS
401

by these sensors to collect discrete samples for hanced light-scattering properties and are thus
simultaneous identification of and experimen- particularly likely to cause these light-related
tation on HAB and affected species; develop- effects, yet the prevalence and magnitude of
ing techniques for measuring in situ swimming the problem have not been adequately charac-
behavior of motile HAB taxa and affected spe- terized. Because seagrasses provide an impor-
cies; and improving methods for rapid quanti- tant nursery habitat for many commercially
fication of HAB toxin concentrations. valuable shellfish and finfish species as well
as their associated fauna, issues related to these
Issue: habitats are of special concern.
Do high biomass (non-toxic) HABs ad- Nutrient-mediated macroalgal blooms can
versely impact the food-web directly also lead to the decline of seagrass as well as
through reduced food quality, or indi- coral reef ecosystems (LaPointe and O'Connell,
rectly through environmental effects? 1989). In addition, high biomass HABs may limit
Harmful effects of algal blooms may occur growth and recruitment of grazers if the domi-
in the form of anoxic/hypoxic events. Such nant algal species is poorly predated upon due
incidents result from increased sedimentation to its unpalatability, small size and indigestibil-
of organic matter coupled with enhanced mi- ity, or because of physical impairment of feed-
crobial decomposition of phytoplankton on the ing (e.g., Bass et al., 1990). High algal densities
bottom, and/or via transient increases in wa- per se may also interfere with food uptake and
ter column respiratory demands of the phy- utilization by many suspension feeders. Suble-
toplankton (Box 3.3.3; Falkowski et al., 1980). thal effects of food quantity/quality, which re-
Mass mortalities of benthic fauna associated main poorly understood (Donaghay, 1985), are
with these events are widespread and affect a potentially important determinants of recruit-
broad range of taxa (e.g., Swanson and ment success in grazer populations.
Sindermann, 1979), but their connection to
HABs is often circumstantial or speculative.. Evaluating the direct and indirect effects
High microalgal biomass and resulting light of high biomass HABs on food-webs requires
attenuation are also known to cause marked that we:
declines,in biomass and distribution of 1. Determine the relative importance of oxy-
seagrasses. Both effects have been noted in gen depletion from HABs in the water col-
eelgrass and shoalgrass communities exposed umn vs. surface sediments.
to picoplanktonic brown tides in New York and 2. Understand the extent and ecological con-
Texas waters. Reductions in irradiance levels sequences of light attenuation from HABs,
may also induce shifts in macrophytie species' including relative effects on phytoplank-
composition toward less desirable forms. ton, epiphytic algae, seaweeds, seagrasses
Blooms of picoplanktonic microalgae show en- and their supporting fauna.
3. Investigate the effects of HABs on food
quality available to consumers (e.g., via
changes in size spectra, chemical compo-
--- sition).
TROPHIC EFFECTS OF HARMFUL ALGAL BLOOMS 4. Define the mechanisms and threshold lev-
HAS els at which high algal biomass interferes
with food capture and utilization by graz-
IF TOXIC HAB IF HIGH SIOMAS
HAB ers.
5. Understand the controlling mechanisms
IF GRAZERS IFGRAZERS INCREASE INCREASE INCREASE for restructuring marine communities
AVOID HAB CONSUME HAB LIGHT MASS PLANKTONIC
ATTENUATION SEDIMENTATION OMEN REDUCE INCREASE during recovery.
PRODUCTIO. FOOD FOOD
DEMAND DUALITY QUANITY
REDUM INCREASE
UNAFFECTED IFIMPAIRED DEAD SEA GRASS BENTHIC I I I Approach and Technology. Elucidation of
PRIMARY omm PLANKTON GFL42ERS
PRODUCTION DEMAND HYPOXIA UINAFFECTED high biomass HAB impacts on food-webs will
I GRAZERS CRENFANCED
BENTHIC require a multi-faceted approach, including field
HYPOXIA DEATW studies, experimental mesocosm manipulations
SEA G 1ANQI1A IMPAIRMENT and laboratory investigations. Field work
HABI PASS
TAT
LOSS should be aimed at quantifying organic sources
ASE I@NC
E
REASE @1..=.'C
PLAN

(-HIGHER ECOSYSTEM ATIVE and rate processes within the water column and
I T@HIC I PERTURBATION EFFECTS in sediments to allow development of an oxy-
gen budget. This will involve continuous moni-

3. ECOHAB PROGRAM ELEMENTS
41

ing approaches to aid in determining the oc-
%"J, W'a i'@ @@ IN-i HIM TIONS. HOW, W",
currence and distribution of HAB events and
HAB SPECIES AND GRAZERS high biomass coverage; moored instrumenta-
tion for continuous monitoring of impacted vs.
non-impacted sites; techniques for automated,
simultaneous sampling of the diel changes in
vertical structure of light, oxygen, phytoplank-
ton (distinguishing HAB taxa from other phy-
toplankton) and vertical mixing; regional geo-
graphic information system data bases for
high-biomass blooms; computerized predictive
models for oxygen deficits from HABs, relat-
ing water-column dissolved oxygen, BOD and
algal abundance with sediment BOD and algal
abundance; improving available methods for
Copepods and other macrozooplankton reduce their grazing assessing food quality, both biochemically and
rates when they encounter dense blooms of some toxic di- by comparison to other known quality foods.
noflagellates, perhaps as a result of impaired motor control and 3.3.3 Summary
elevated heart rates (Fiedler, 1982; Huntley, 1982; Huntley et As algal toxins move through marine food-
al., 1986; Sykes and Huntley, 1987). Heterosigma carterae is webs, they can have a broad spectrum of ef-
avoided by zooplankton predators including rotifers, copepods, fects on marine organisms in inshore, offshore,
pilchard larvae, and juvenile menhaden, but the underlying pelagic, and benthic habitats (Box 3.3.4). The
mechanism in unknown. The tintirmid Favella taraikaensis scope of these effects, resulting from both
avoids Heterosigma, even when starved, and reverses the beat chronic and acute exposure to the toxins, has
of its adoral membranelle to reject cells. Further, Heterosigma become more evident in recent years, since a
is a poor food for mussels, clams, and oysters (Tomas, 1980). wide variety of animals are now known to ac-
Chrysochromalinapolylepis negatively affects both feeding and cumulate biotoxins and act as intermediate
growth rate of the tintinnid Favella ehrenbergii Carlsson et al., vectors to consumers at higher trophic levels.
1989). These are but a few examples of how zooplankton can Algal blooms can also have harmful effects not
avoid or reject certain HAB species, and how they can be physi- relatIed to production of toxins, such as over-
ologically impaired once they have consumed the toxic algae. growth and shading by seaweeds, oxygen
Studies of the nature and extent of this type of trophic interac- depletion of the water column from high bio-
tion are important element's of ECOHAB. mass blooms, fish mortalities from over-stimu-
lation of gill mucus production, and mechani-
toring of dissolved oxygen and irradiance lev- cal interference with filter-feeding structures.
els at spatial and temporal scales relevant to The Food-Webs/Community Interactions pro-
HABs. Assessment of macrophyte and faunal gram element of ECOHAB recognizes the di-
coverages, as well as seasonal successional pat- verse nature of these processes, and highlights
terns, before and after bloom events are like- key areas for focused investigation. What is
wise needed, and should incorporate synoptic needed is a recognition by managers and regu-
aerial mapping of the macrophyte communi- latory officials that harmful algal bloom im-
ties. The effects of changes in food quantity pacts extend far beyond the obvious manifes-
and quality must be evaluated in field and tations of poisonous shellfish and dead fish,
mesocosm experiments to determine their im- and include subtle, sub-lethal effects that can
pacts on ingestion, growth and reproduction alter or even destroy ecosystems through time.
for critical life stages of target species. Identifying such impacts and determining their
Mesocosm studies are required to assess the extent and magnitude is a significant challenge
consequences of removal or perturbation of for ECOHAB scientists.
target species on food-web structure and pro- This program element also emphasizes re-
cesses. Laboratory and mesocosm experiments search in the other direction - the effects of
will provide insights into the mechanisms and grazers and other organisms on the harmful
linkages between high biomass HAB events and algal blooms, since in many cases, the bloom
associated food-web/habitat responses. reflects the supression or absence of grazing.
Implementing the variety of studies needed This again is an area of obvious importance to
to characterize the effects of high biomass the dynamics of HABs, but one which has re-
HABs on food-webs will rely on: remote sens- ceived only rudimentary study thus far.

421
4. REGIONAL HAB PHENOMENA IN THE U01 I ion,'

The following regional summaries present similar across multiple regions. The sum-
brief perspectives on specific HABs. Written by maries also highlight how information bases
workshop participants familiar with each region, differ among regions, due to different physi-
they review available information and point out cal regimes, causative organisms, and/or
deficiencies. These are provided to document level of research. This is true even when
the extensive geographic scale of HAB impacts the organisms are the same or similar (e.g.,
and to illustrate the diversity of the phenom- Alexandrium spp. along the Northeast and
ena involved. In some cases, the regional sum- Pacific coasts).
mary only reflects one manifestation of a par- HAB phenomena are truly diverse, and
ticular phenomenon, and thus understates the it is this diversity that must be accomodated
extent of the HAB problem. For example, in the ECOHAB science plan. Clearly, single
macroalgal blooms in Florida are described, but investigator and multi-investigator, regional
similar outbreaks occur in coastal waters projects are required to address the many
throughout the U.S. Similarly, cyanobacterial identified deficiencies. This approach can
blooms are highlighted on the U.S. east coast, address the immediate information needs
but occur on both costs as well as in rivers, of each region, but ECOHAB will derive sig-
lakes and ponds throughout the country. nificant benefit from comparisons among re-
It is obvious from these summaries that se- gions and attempts to highlight common
rious information gaps exist in all regions and principles or mechanisms underlying many
for all organisms, but some deficiencies are of these phenomena.

PSP
11NUMHEAst RE"GION: "`7

The most significant PSP toxins. The size of the offshore area af-
HAB problem in the fected, the difficulty in monitoring an area so
northeastern U.S. is far from land, and the slow depuration of toxin
PSP caused by sev- from the affected shellfish have necessitated a
eral closely related permanent closure of the surf clam fishery on
species in the di- Georges Bank for the past five years.
noflagellate genus One key feature of the ecology and bloom
Alexandrium. The dynamics of toxic Alexandrium species in the
affected resources are northeast is that they include a dormant cyst
pRli@ predominantly shellfish, stage in their life histories. Cysts germinate in
but PSP toxins also affect the spring to inoculate overlying waters with
higher levels of the food-web, in- a "seed" population.
I ding lobsters, fish, and marine In the southwestern Gulf of Maine,
]9@ c u
mammals. Alexandrium cell distributions are associated
Paralytic Shellfish Poison- with a coastal current or buoyant plume formed
NMI,
ing. PSP is a recurring prob- by the outflow from rivers in southern Maine
lern that has affected large ar- (Franks and Anderson, 1992a). The southward
eas of the region every year for over two propagation of this plume and the entrained
decades. Prior to 1972, shellfish toxicity was Alexand7ium cells creates an annual north-to-
known only in eastern Maine and Canadian south sequence of PSP toxicity, beginning in
waters to the north. That year, a massive bloom late May or early June. The plume is influenced
introduced A. tamarense to southern waters, by freshwater flow, wind, and bathymetry, with
and there have been shellfish harvesting quar- predictable consequences for the location and
antines along large sections of coastline every timing of coastal PSP events. Extensive fresh-
year since. A second expansion of the regional water flow in early May creates a strong, fast
PSP problem occurred in 1989, when the rich plume, while low river flow may preclude the
shellfish beds of Georges Bank and Nantucket formation of a coastal plume. Upwelling-favor-
Shoals were found to be contaminated with able winds oppose the propagation of the

4. REGIONAL HAB PHENOMENA IN THE UNI TED STATES
143

plume, forcing it off- times dominant component of the spring
THE COMMONWEALTH OF MASSACHUSETTS shore and arresting bloom, but does not reach the high cell densi-
DEPARTMENT OF its north-to-south ties recorded in western Europe, where foam
ENVIRONMENTAL QUALITY ENGINEERING motion. This tends on beaches, fouling of fishermen's nets, and
to halt the along- other negative impacts are common.
shore propagation Economic Impacts. The economic impact
of toxicity, leaving of these outbreaks is significant, though diffi-
the southern re- cult to estimate in total. Shellfish monitoring
gions toxin-free. In programs in each of the coastal New England
WARNING c o n t r a s t , states have minimized illnesses from PSP-con-
Taking of Shellfish Prohibited downwelling-favor- taminated shellfish and prevented any deaths.
ACTING UNDER CH. 130, SEC. 74A able winds force the This extraordinary level of human health pro-
THE MASSACHUSETTS DEPARTMENT OF plume against the tection has come at a co 'st that has never been
coast, and acceler- directly quantified, but must be in the range of
ENVIRONMENTAL QUALITY ENGINEERING ate its alongshore millions of dollars per year, including the an-
HAS DETERMINED THAT SHELLFISH IN THIS propagation. Such nual cost of the state and federal shellfish moni-
AREA ARE CONTAMINATED WITH PARALYTIC conditions lead to toring programs (nearshore and offshore), the
SHELLFISH POISON. THIS AREA IS widespread toxicity, value of unexploited resources such as surf
CLOSED TO THE TAKING OF SHELLFISH and may account clams and roe-on scallops, and the loss to
AS OF AND UNTIL FURTHER for the recent occur- shellfishermen and retailers from shorter-term
NOTICE, rence of PSP on quarantines, including "spinoff " effects on other
Georges Bank perfectly safe fisheries products that are rejected
(Franks and Ander- by consumers during red tide outbreaks. Esti-
son, 1992b). Understanding of the physical mates of the losses to shellfishermen and other
forcings that influence the location and dynam- seafood-related industries are few, but a single
ics of the coastal buoyant plume, and informa- PSP outbreak cost the state of Maine $6 mil-
tion concerning the abundance of Alexandrium lion (Shurnway et al., 1988).
cells within the plume have given us a limited Significant unknowns in our understanding
predictive capability of the location and timing of Alexand7lum blooms include:
of toxic outbreaks over large I(> 100 km) scales What are the geographic origins of newly
(Franks and Anderson, 1992b). germinated cells that initiate the
Other potential HAB Problems. The gen- Alexandriurn populations in the coastal cur-
eral view of the harmful algal bloom problem rent and the physical/behavioral mechanisms
in New England is that PSP is widespread, per- by which they enter the buoyant plume?
sistent and expanding, while outbreaks of other 9 Is accumulation of cells at small-scale fronts
harmful species cause sporadic damage on a necessary for their entrainment in the buoy-
smaller scale. A realistic concern is that HAB ant plume? What other physical-biological
species already present within the region are interactions are important to bloom dynam-
likely to cause problems in the future. For ex- ics on small (< 10 m) scales?
ample, an outbreak of Gymnodinium * What is the nutrient physiology of the cells,
mikimotoi caused extensive benthic mortali- their requirements, uptake rates and nutri-
ties in 1988 in Maine, a region of New England ent status during the long-distance transport?
that is rapidly expanding its salmon farming o Is the localization of elevated ALexandrium
industry. This fish-killing species causes recur- populations within the plume a result of
rent and significant financial losses to the fish physical entrainment, or does it reflect an
farming industries throughout the world. Like- increased growth rate in response to unique
wise, Pseudo-nitzschia pungens f. multiseries, chemical properties of plume waters?
a diatom responsible for ASP, has been detected e Are nearshore cells in the coastal current
in Gulf of Maine waters, and its toxin (domoic responsible for PSP offshore on Georges
acid) detected in scallops. Over the last sev- Bank?
eral years, DSP has been detected in Canadian * What are the hydrodynamic forcings that
shellfish located just to the north of New En- regulate PSP outbreaks in other areas of the
gland, where DSP is not yet a problem. Gulf of Maine?
Some species, identified in other regions as 9 What effect does zooplankton grazing have
problem algae, are regular components of the on the Alexandrium populations, and what
Gulf of Maine flora. The prymnesiophyte, are the ecosystem- impacts of toxin transfer
Phaeocystis pouchetii, is a regular and some- through the food-web?

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
441
It'', :NTIC,@ digfAL RIOT 77
1%, =Nwk@

Blooms of the small (2-3 @Lrn) chrysophyte to contribute to bloom occurrence.
Aureococcus anophagefferens, referred to as The physico-chernical conditions that con-
"brown tide" due to the resulting water color, tribute to the formation of A. anophagefferens
have been confirmed in many locations along blooms are still largely unknown. Low annual
the northeast coast of the United States, espe- rainfall, and increased residence time of bay
cially in. Narragansett Bay, RI, Barnegat Bay, waters that lead to increased salinity (> 28
NJ, and the Peconics-Gardiners Bay estuary ppt) may favor the development of the brown
and south shores of Long Is- tide, as does increased water temperature
land, NY (Cosper et al., (Cosper et al., 1989b). Year-to-year persistence
1989a). The figure on the of A. anophagefferens in the Long Island re-
next page shows the gion is partly attributed to its wide tempera-
widespread distribution ture tolerance and thus its ability to survive
b -,.h of this organism in the overwintering conditions. Mesocosm experi-
northeastern U.S., includ- ments show that this alga grows well at rela-
Ing ma
ny areas with no previous his- tively low concentrations of dissolved inor-
tory of visible or destructive blooms ganic nitrogen (DIN), and a negative
(Anderson et al., 1993). correlation has been described between the
Brown tides are restricted to shallow, ver- abundance of Aureococcus and mean DIN con-
tically well-mixed waters, and occur during centrations experienced during blooms. There-
late spring and summer at maximum concen- fore, macronutrient loading of bays does not
trations of 3 x 101 cells 1-1; bloom duration appear to be the direct cause of brown tide,
ranges from one to four months. The first out- but micronutrients, including trace metals
break occurred concurrently in New York and such as iron and selenium, and certain chela-
Rhode Island in 1985, and blooms have re- tors, have been implicated as growth promot-
curred in New York bays in subsequent years, ers in its formation. The iron requirement of
with varying intensity, duration and geo- Aureococcus and its ability to grow in the pres-
graphic spread. An immunofluorescent ence of organic nutrients (e.g., glutamic acid)
method is used for the reliable identification are higher than for many other common phy-
and quantification of A. anophagefferens. toplankton species. Viral particles have been
Severe light attenuation in Long Island bays described and isolated from field-collected
due to the brown tide caused a significant re- Aureococcus cells, and viral-lysis of algal cells
duction in the depth penetration and leaf bio- has been attributed a potential role in bloom
mass of eelgrass (Dennison et al., 1989), dissipation (Milligan and Cosper, 1994).
which serves as an important nursery habitat A number of questions need to be answered
for numerous fish and shellfish. Brown tides in order to -more fully understand the physi-
also caused severe mortalities, recruitment cal and biological mechanisms controlling the
failure, and growth inhibition of commercially population dynamics of A. anophagefferens,
important, suspension-feeding bivalves, in- and the effects of brown tides on nearshore
cluding blue mussels in RI (Tracey, 1988) and marine communities.
bay scallops in NY (BriceIj and Kuenstner, 9 What role does micyonutrient availability,
1989). Economic losses from the brown tide especially via groundwater, play in control-
for the New York State bay scallop fishery were ling bloom dynamics?
estimated at $2 million per year during early * What climatological-metereological and/or
outbreaks. hydrographic events are associated with the
Aureococcus adversely affects feeding of lar- regional occurrence of the brown tide in
val and adult bivalves, but only through di- the northeast?
rect cell contact. Although specific cell toxins 9 To what extent do biological mechanisms
have not yet been identified, the cell surface (e.g., grazing depression, competitive in-
of this microalga contains a bioactive com- teractions with other phytoplankton, and
pound that interferes with ciliary beat and viral lysis) contribute toward the formation
thus food capture of bivalves, a response mim- of monospecific blooms and subsequent
icked by the common neuro transmitter, decline of the brown tide?
dopamine. Thus, impaired grazing by zoop- Is microzooplankton grazing negatively im-
lankton and filter-feeding benthos are believed pacted by brown tide? What are the tox-

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
145

ins/metabolites that cause species-specific What are the effects on submerged
inhibition of suspension-feeding in plank- aquatic vegetation and its associated
tonic and benthic organisms? community (secondary as well as pri-
9 What are the time- and concentration-de- mary consumers)? What are the long-
pendent effects of brown tides on marine term impacts of recurrent brown tides
fauna, during various life history stages? on community trophic structure?

M E

N
NH 2 3

MA 8
5

7 6
CT
NY
30

------------
MD 11 51
S7 1153 52 50
1
D. 58 1 54
IDE
II--- 55 Distribution of the brown tide alga
65 '3 Aureococcus anophageffecens. Dark circles
64 . 59 56 denote positive identification of the species.
VA 63 6 Clearly this harmful species is much more
widely distributed that its major blooms
60 thus far would suggest. (see below)
61

RHODE
ISLAND
0

01
140 Long ,land Sound I Narragan ett Bay

Peconic Bays

Great South Say

NEW YORK BIGHT

Documented high
density brown Barnegat
tide blooms of Bay
Aureococcus itde Egg Harbor
anophageffecens Great Bay
since 1985.

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
461

H a r In f u I column stability; 4) relatively high dissolved
cyanobacterial organic matter content; and, 5) for nitrogen-
blooms (HCBs) fixing genera, molar N:P input ratios < 15:1.
are indicative of Typically, blooms develop in oligohaline tribu
Uxuessive nutri- taries experiencing periods of excessive spring
ent loading in N and P loading (via runoff, wastewater dis
oligohaline estua- charge, etc.), followed by decreased flushing,
Tine waters. These persistent vertical stratification, and surface
blooms represent water temperatures >20*C (Reynolds and

.....................
economic and en Walsby, 1975). Buoyant noxious species have
vironmental threats photoprotective pigments that allow them to
nationally, and have oc- survive at the water surface where they can
curred in several large es- remain for weeks to months (Paerl, 1988b).
tuarine systems (e.g., Grazing pressure-by macrozooplankton has
Chesapeake Bay, Albemarle- little impact on either initiating or controlling
Pamlico Sound, and Florida cyanobacterial blooms. Trophic interactions
Bay). Cyanobacterial blooms and ecosystem structure are often radically al-
are also serious problems in tered in response to such blooms (Porter and
freshwater systems. Here Orcutt, 1980; Fulton and Paerl, 1987). While
we highlight the east coast physiological and molecular knowledge of in-
of the U.S., but cyanobac- dividual HCB species is good, knowledge of
terial blooms occur in vir- growth, reproductive, and trophic dynamics on
tually every state, given the the ecosystem level is at best fragmentary.
existance of toxic species in Informational needs include:
both freshwater and marine envi- What trophic alterations (e.g., community
ronments. changes and food transfer) are attributable
Bloom taxa include filamentous to HCBs?
(Anabaena, Aphanizomenon) and aggre- What are the dynamics of akinete (cyst) dis-
gated coccoid (Microcystis) genera, which persion, activation, and bloom initiation?
exhibit severe neuro-, cyto-, and hepato- To what extent can known and novel HCBs
toxicity to a variety of mammals (in- (e.g., Synechococcus spp. in Florida Bay;
cluding man), birds, farm animals, Nodularia, Schizothrix, dnd Lyngbya in reefs
fish, and invertebrates (including and intertidal environments) disperse into nu-
zooplankton). HCBs accumulate as trient-enriched mesohaline/euhaline waters?
buoyant surface-dwelling, high bio- * What are the genetic and physiological po-
mass blooms. They impart nega- tentials for such species dispersal?
tive aesthetic values, and cause * How does the ability to fix atmospheric ni-
o;-' taste and odor problems. These trogen (N), facilitate expansion into N-lim-
blooms rapidly terminate or "crash" in re- ited estuaries or freshwater systems?
sponse to sudden physical perturbations (e.g.,
rapid drop in temperature, sudden
destratification and water column turnover, or
@k ilk
reduced irradiance associated with poor
weather). When crashes occur, excessive oxy-
gen consumption as the biomass decays can
lead to anoxia. This chain of events has been
responsible for major estuarine fish and shell-
fish kills and loss of habitat for benthic infauna
(Paerl, 1988a, 1990).
Conditions which favor harmful
cyanobacterial bloom development and persis
tence include: 1) enhanced P and N loading; Cyanobacterial toxins often kill cattle and other
2) increases in water retention time; 3) water animals. Photo by Wayne Carmichael.

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
47

T t -io- F8 AAL9,

In 1991, an ichthyotoxic toxic amoeboid stages that feed on the fish re-
dinoflagellate with "am- mains, or without abundant food resources,
bush predator" behavior the toxic stages encyst. In the absence of live
and a complex life cycle fish, gametes and toxic zoospores revert to non-
was discovered at a fish toxic zoospores that remain highly active in
kill in the Pamlico River, phosphate-enriched waters, especially when
a large estuary in the flagellated algal prey are abundant (Burkholder
Southeast (Burkholder and Glasgow, 1995). Surprisingly, most of the
et al., 1992, 1995). The or- 19 known life cycle stages are amoebae that
ganism, Pflesteria piscicida range in length from 5-250 gm. Under certain
(Steidinger et al., submitted; conditions (e.g., cold temperatures) some
199S), represents a new family, amoeboid stages become ichthyotoxic.
genus, and species of armored di- In enclosed laboratory conditions, human
noflagellates. Its cryptic or "phantom- exposure to aerosols from toxic cultures with
like" behavior was observed several live fish has been linked to a variety of short-
years earlier when it appeared as a con- and long-term symptoms, including narcosis,
taminant of unknown origin in respiratory distress with asthma-like symp-
aquarium fish cultures (Burkholder toms, severe stomach cramping, nausea, vom-
et al., 1992; Smith et al., 1989). iting, and eye irritation. Other autonomic ner-
Unknown substances freshly vous system dysfunction such as high,
secreted by finfish and shellfish localized perspiring and erratic heart beat may
stimulate P. piscicida to trans- last for weeks. Central nervous system dysfunc-
form from benthic cysts or tion, including sudden rages and other erratic
amoebae, or non-toxic flagel- behavior can last hours to days, and reversible
lated stages to toxic zoospores. cognitive impairment for weeks; chronic effects
Highly lipophilic exotoxin(s) are released to the such as sustained asthma-like symptoms and
water and travel as micelles that narcotize fin- suppressed immune system may last for
fish, slough fish epidermis, and cause forma- months to years (Glasgow et al., in press).
tion of open bleeding sores (see photo below), . The extent of R piscicida's involvement in
while also damaging osmoregulatory function fish kills likely has been underestimated be-
(Noga et al., in press). In some species, (e.g., cause of difficulty in reaching many kills when
striped bass), extensive hemorrhaging also oc- toxic zoospores are still present. Most
curs. This dinoflagellate has proven lethal to Pfiesteria-associated field kills have occurred
every fish species tested, including more than in quiet, upper estuarine tributaries with poor
20 native and exotic species (Burkholder et al., flushing rates, where both fish secreta and tox-
in press). At sublethal densities, Pflesteria-like ins can accumulate and. be more readily de-
dinoflagellates likely cause significant chronic tected. During the past three years, P. piscicida
impacts to fish populations, affecting recruit- has been implicated as the causative agent of
ment, reproduction, and disease resistance. ca. 50% of the major fish kills in large estuar-
Clinical research recently demonstrated that R ies of the Albemarle-Pamlico system, the only
piscicida is the causative agent of the disease region where rigorous sampling protocols have
known as ulcerative "mycosis" in Atlantic men- been established (Burkholder et al., in press).
haden (Noga et al., in press). The Pamlico is About two-thirds of the Pfiesteria-caused
known for high incidence of fish ulcerations fish kills in North Carolina have occurred in
and up to 98 % of all fish sampled in this estu- the phosphate-rich Pamlico, and laboratory
ary have manifested large, open, bleeding sores bioassays have shown that some life cycle
during warmer months. stages are stimulated by organic phosphate
The dinoflagellates consume bits of epider- sources. Field surveys documented signifi-
mal tissue and blood cells from affected fish cantly higher abundance of zoospores at sew-
while also engulfing bacteria, phytoplankton, age outfall sites relative to unpolluted sites. R
and other microfauna. In addition, they pro- piscicida is euryhaline and eurythermal, with
duce gametes that complete sexual fusion in optimal growth at IS psu and @! 26 OC, but with
the presence of dying fish. qpon fish death, toxic activity from 2-35 psu and 10-33 OC
toxic zoospores and planozygotes form non- (Burkholder et al., in press). Some stages can

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
481

remain active down to 5 OC. The wide salin- they occur in colder regions as well?
ity/temperature tolerance of R piscicida sug- 9 Can molecular probes be developed to fa-
gests that this species and its close relatives cilitate detection of the various life cycle
are probably widespread, at least in warm tem- stages and/or the toxins they produce?
perate/subtropical regions, acting as significant * What are the toxins? What is their chemi-
but often undetected sources of fish mortality cal structure?
and disease. This species has been documented * How do organic and inorganic nutrients con-
in sediments or water from the mid-Atlantic to trol life cycle stages and/or toxicity?
the St. Johns estuary in Florida. Recently, a * What chronic effects does Pflesteria and its
second, apparently more subtropical, Pflesteria- relatives have on fish recruitment, disease
like species was identified (Landsberg et al., resistance, and survival?
1995). 9 What is the role of dinoflagellates in estua-
Critical questions that need to be answered rine microbial food-webs in light of the dis-
include: covery of multiple, benthic amoeboid stages
What is the geographic range of Pflesteria- in Pflesteria? Might these also be found in
like dinoflagellates? Do they occur only in the life cycles of other dinoflagellates?
warm temperate/subtropical areas or do

X
@44

A"
'S. -

Lesions on menhaden caused by the dinoflagellate Pflesteria. Photo by J. Burkholder.

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
149

The toxic di- west Florida shelf. These blooms develop on
n o f I a g e I I a t e the leading edge of the Loop Current front
Gymnodinium breve where the boundary layer is ideal for near-
has a distribution from monospecific growth of G. breve. Typically the
the Gulf of Mexico cyanobacterium7hchodesrnium precedes or co-
(Mexico-Florida) to the occurs with G. breve at bloom initiation and
South Atlantic Bight. its presence may condition the water mass and
This fragile species pro- enhance G. breve growth as well as reduce graz-
duces neurotoxins and ing pressure. Bloom initiation is followed by
hemolytic substances that can cause mass population growth in excess of predation, natu-
mortalities of marine animals, neurotoxic ral mortality, and advective loss, then by sus-
shellfish poisoning (NSP), and human respi- tained growth (maintenance), and finally by
ratory irritation. Blooms are usually seasonal, dissipation by advection or mixing of water
starting in late summer/fall and lasting 3-4 masses. The physical integrity of the water
months; they impact fishing and tourist in- mass appears to be the key factor controlling
dustries and alter population levels or recruit- growth and maintenance of G. breve blooms.
ment potential of affected marine animals. Offshore populations of G. breve can be trans-
These recurrent bloom events cause an eco- ported shoreward with winds and inoculate
nomic loss of approximately $18-24 million inshore waters. Nutrient availability in the
per episode (Steidinger and Vargo, 1988; Tester nearshore waters then contributes to the dura-
et al., 1991). Associated with this economic tion and intensity of blooms. Although G. breve
impact is an unquantifiable "halo" effect that is more concentrated in surface waters, it is
results in reduced sales of all seafood prod- distributed throughout the water column down
ucts within the region of the bloom and even to > 50 In depths.
outside the region. A conceptual framework for understanding
The most likely scenario for the develop- G. breve blooms thus exists, but there are a
ment of G. breve blooms in the Gulf of Mexico number of questions that need to be answered:
and South Atlantic In the life cycle of G. breve, does sexual re-
Bight is the follow- production only occur in the zone of initia-
ing. The source of tion, and are resting cells such as cysts or
the blooms appears zygotes present in sediments or at
to be on the west pyenoclines?
Florida shelf in the Are there "hot spots" within the zone of
eastern gulf where initiation on the west Florida shelf that re-
the Loop Current tain resting stages?
71 may entrain bloom Can molecular probes be used to detect tox-
patches and trans- ins in seawater or identify different strains
port them into the of G. breve?
South Atlantic Bight Is zooplankton grazing inhibited at moder-
N
via Loop Current ate to high G. breve cell concentrations when
filaments/eddies brevetoxins or other substances are re-
and the Gulf Stream leased? Does G. breve regulate plankton
system (Steidinger community structure?
and Vargo, 1988; Are there multiple hydrographic features
Tester et al., 1991, that are requisite for bloom initiation that
1993). Eddies can can be detected using moored instrument
also transport en- arrays and remote sensing?
trained blooms to Does T@ichodesmium condition the water
h@
the
_@@g
(M,
S0
Tj
dl.

!77 the western gulf. prior to G. breve blooms?
Blooms are initiated What are the roles of macro- and micronu-
f in association with trients in the initial growth phase of blooms
L Loop Current intru- and how does the situation change over time
7-i sions accompanied with bloom development?
Dead fish from a Texas red tide. Photo by Brazosports. by upwelling on the

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
501

Ciguatera fish poisoning (CFP) is the parison, in the Virgin Islands neither the num-
most frequently reported non-bacterial ill- ber of CFP incidents nor G. toxicus abundance
ness associated with eating fish in the exhibit notable fluctuations. Overall, the spatio-
United States and its territories. temporal variability of CFP in a local area cor-
The actual number of responds largely to the patchiness of G. toxicus
Cases is, however, esti- populations; however, it is difficult to explain
mated to be 2-5-fold higher, since there is no the often rapid, localized changes in the con-
confirmatory laboratory test, and diagnosis de- centration of this species based on a response
pends on a patient's clinical presentation. to any one environmental factor (e.g., tempera-
Southern Florida, together with Puerto Rico ture, salinity, nutrients, etc.). The variable, lo-
and the Hawaiian islands, account for the ma- calized occurrence of ciguatoxic dinoflagellates
jority of documented CFP incidents in the U.S. within a region may also be related to their
In the Virgin Islands, it is estimated that nearly rafting on drift algae, which is considered to
50% of the adults have been poisoned at least be a primary means of dispersal.
once. Many CFP intoxications have been re- Phenotypic variation in toxicity observed
ported from temperate "inland" locations in between clones from distinct geographical ar-
the U.S., resulting from the commercial distri- eas are stable in acclimated cultures and thus
bution of sub-tropical and tropical fish species. are indicative of genetic differences. For CFP
Gambierdiscus toxicus, an epibenthic di- cases occurring in the Caribbean and eastern
noflagellate, is the organism primarily respon- Atlantic, gastrointestinal symptoms occur first,
sible for ciguatera fish poisoning (Yasumoto et while the characteristic neurological manifes-
al., 1977). G. toxicas produces ciguatoxin pre- tations of cigyatera develop later and may per-
cursors and analogues that are biotransformed sist for weeks to months or even years, pro-
during food-web transfers into ciguatoxin, the ducing chronic disabilities. Conversely, in the
causative neurotoxin (Lewis and Holmes, Pacific, neurological symptoms are exhibited
1993). The ciguatera toxins are transported first, while gastrointestinal symptoms are mi-
through herbivorous fish to carnivorous spe- nor or absent. These patterns in symptomology
cies, where they accumulate and persist over may reflect different geographic distributions
extended periods. Fish exposed to ciguatoxin of individual CFP toxin(s).
exhibit impaired swimming behavior, and as a Presently, no coordinated, systematic moni-
result may be subject to increased predation. toring progams exist for CFP in the U.S. and
Other toxic dinoflagellates, including species its territories. This poisoning syndrome has a
of Prorocentrum, Ostreopsis and Coolia, share significant impact on commercial and recre-
the same epiphytic habitat and entry routes ational fishing activities in the U.S. and
into the food chain as G. toxicus, but remain throughout the world.
only circumstantially linked to CFP since their Questions for future research include:
toxins are not known to occur in fish at levels Are there environmental factors that pro-
that can affect humans. mote G. toxicus blooms or cause increases
G. toxicus does not form pelagic blooms of in the toxicity of this dinoflagellate? and, if
motile cells, but is most prolific in shallow wa- so, can they be incorporated into predictive
ters (3-15 m) primarily as an epiphyte on red indices of CFP events?
and brown macroalgae associated with coral Can human activities such as reef destruc-
reefs and protected embayments. Field and tion or pollution increase the scale of the
laboratory studies have established the tem- problem?
perature and salinity ranges of G. toxicus as What roles do toxic species of Prorocentrum,
20-3411C and 25-40 psu, respectively. Ciguatera 0streopsis and Coolia play in CFP?
endemic areas in both the Caribbean and Pa- Where and how are ciguatoxin precursors
cific are characterized by oceanic salinities and and analogues biotransformed in herbivo-
are primarily associated with island land rous and/or carnivorous fish? How do
masses; CFP is essentially absent along conti- ciguatera toxins affect food-web function?
nental perimeters. In Florida, most cases of Are there genetic markers that define the
ciguatera are contracted in the summer, which toxin content and profile of individual di-
is consistent with the elevated G. toxicus abun- noflagellate clones?
dance observed during this period. By com-

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
51

------- ----

Macroalgae cause problems phosphorus-rich domestic wastewater gener-
throughout the coastal waters of ated in the Florida Keys that enters coastal
the U.S. This summary for waters via groundwater discharge (septic tanks,
S
thern Florida provides one cesspits, and injection wells) and surface wa-
OL.
example of the nature and ter outfalls. This cumulative nutrient enrich-
scale of the problem. ment can cause high biomass algal blooms,
Over the past several de- which include the red algae Laurencia intricata
cades blooms of and Spyridia ftlamentosa, the brown algae
macroalgae (seaweeds) Dictyota sp. and Sargassurn ftlipendula, and
have been increasing the green algae Enterornorpha sp., Codium
along many of the world's isthmocladum, and Halimeda sp.
developing coastlines in re- Macroalgal blooms in South Florida, as well
sponse to nutrient enrich- as other factors, have contributed to the marked
ment @Ssociated with coastal eutrophication. decline in extent and vigor of seagrass ecosys-
In southern Florida, a diverse group of oppor- tems that provide a vital nursery habitat for
tunistic macroalgal species outcompete, over- pink shrimp, spiny lobster, and finfish. These
grow, and replace seagrass and coral reef eco- commercially-valuable marine species support
systems that are adapted to stable, oligotrophic multi-million dollar recreational and commer-
conditions. Moreover, once they are estab- cial fisheries that have undergone drastic de-
lished, the macroalgal blooms may remain in clines over the past decade. The Florida Reef
an environment for years to decades until the Tract, the third largest coral reef in the world
nutrient supply decreases. This is in contrast and the only coral reef system in North
to phytoplankton blooms that are usually rela- America, supports the largest recreational dive
tively short-lived (days to weeks). industry in the world. This valuable reef sys-
The negative effects of eutrophication in- tem is being overgrown by macroalgal species.
clude nuisance blooms of macroalgae and at- The trend could lead to ecological collapse of
tached filamentous epiphytes that reduce light the Florida Reef Tract, with subsequent eco-
availability to seagrasses (Sand-Jensen, 1977; nomic losses in the tourist-related industries
Twilley et al., 1985; Silberstein et al., 1986). that support the most visited coral reef and
This results in lower seagrass productivity, habi- largest marine sanctuary in the world.
tat loss from hypoxia/anoxia, and eventual die- Questions for future research include:
off of sensitive species (LaPointe et al., 1994). What are the physiological and ecological
Nutrient enrichment of Florida Bay and the mechanisms that regulate the ability of
Florida Reef Tract results from multiple nutri- macroalgae to alter the patterns of nutrient
ent sources and supply mechanisms, includ- storage and primary production by reduc-
ing: 1) advection of phosphorus-rich water ing the role of benthic macrophytes
from the eastern Gulf of Mexico into Florida (seagrasses) and increasing the importance
Bay; 2) nitrogen-rich inputs from land-based of pelagic phytoplankton communities?
agricultural activities that enter coastal waters How does increased macroalgal biomass ac-
through the Everglades via groundwater dis- celerate nutrient release from sediment pore
charge and surface runoff; and 3) nitrogen and waters underlying seagrass communities,
and how does this lead ultimately to
seagrass die-off?
What are the mechanisms for benthic-pe-
lagic coupling of nutrients and primary pro-
duction? How does increased nutrient avail-
ability mediate a shift in primary production
from reef corals to macroalgal HABs?
What are the existing nutrient inputs and
their relationship to the initiation, growth,
and maintenance of macroalgal blooms on
the Florida Reef Tract? How does nutrient
enrichment affect the early life histories of
Seaweed washed onto a Florida beach. Photo by B. LaPointe. bloom-forming macroalgae?

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
521

XICO@@*'KEGIDN'@i@t@l'"M@sy.,@@@@Bi@w@N DE

For over 5 years, regions of the South creased ammonium, its persistence was facili-
Texas coast Centered around the Laguna tated by severe declines in grazer populations
Madre have experienced a continuous, and continued low rates of advection and
dense algal bloom re- physical dispersion (Buskey and Stockwell,
ferred to as the 1993). However, generalizations about nutri-
"brown tide." The ent effects, flushing, and trophic antagonism
nearly monospecific are not sufficient to predict the occurrence,
bloom has been persistence, or long term effects of the brown
caused by high tide.
-5 x 109
densities (1 The environmental and economic impact of
cells/L) of a small the Texas brown tide stems from effects on sev-
(4-5 @tm diameter) eral components of the food-web. Zooplank-
chrysophyte similar to ton and larval fish do not eat the brown tide
Aureococcus anophagefferens alga, but more importantly, after a threshold
that causes brown tides on the cell density is reached, their mortality in-
U.S. northeast coast. Brown tide creases. Eggs of important estuarine fish spe-
blooms occur in shallow (1-2 m cies (e.g., red and black drum, spotted seatrout)
depth) embayments and lagoons that have have reduced hatching and the young larvae
minimal advective transport and/or dispersion. rapidly die from lack of food. Large declines
The onset of the bloom was preceded by a in the abundance of benthic filter feeders have
drought (that increased the salinity) and se- also been observed. Exudate (s) from the brown
vere freezes during periods of extremely low tide organisms are thought to be responsible
tides (Whitledge, 1993). Declines in inverte- for these effects, but specific inhibitory com-
brate populations and widespread fish kills pounds have not yet been identified. Another
were associated with these conditions. High harmful effect of dense brown tides is a de
ambient concentrations of nutrients ' especially Cline in the abundance of seagrasses due to
nitrogen in the form of ammonium, resulted light absorption by the microalgae. Severe long-
from the decaying fish. Ammonium is impor- term ecological changes thus result from the
tant because the Texas brown tide species can- combination of loss of seagrass habitat and the
not utilize nitrate (DeYbe and Suttle, 1994). reduced abundance of secondary consumers
Although bloom initiation depended on the in- in the water and sediments. The economic
losses to tourism and recreational fishing
Chlorophyll Data From S1 caused by the Texas brown tide are estimated
to be several million dollars annually.
Important questions for future research in-
clude:
50-. * To what extent do external nutrient sources
40 -- and their elemental composition moderate
brown tide blooms?
9 What external or internal factors besides
30 nutrient availability lead to the decline or
20- dissipation of a brown tide bloom?
* To what extent do brown tide organisms
10. modify environmental conditions so as to
enhance their survival?
* What is the nature of the growth and feed-
Jan-89 Jun-89 Nov-89 Apr-90 Sep-90 Feb-91 Jul-91 Dec-91 May-92Sep-92 Feb-93 Jul-93 ing inhibition associated with brown tide
blooms? Are toxins involved?

Chlorophyll-a data from Station C (the mouth of Baffin Bay)
from March 1989 through February 1993, documenting the per-
sistent brown tide that is still blooming in the Laguna Madre.
Unpublished data from Dr. Dean Stockwell, University of Texas
Marine Science Institute.

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
153

Paralytic Shellfish Poisoning (PSP). Para- offshore waters and cells to coastal sites,
lytic shellfish poisoning has a long can those events be detected and predicted
history on the U.S. west coast, hav- using moored instruments and weather fore-
ing been reported by early European casts?
explorers and coastal Indian tribes. What effect do recurrent blooms of toxic di-
The dinoflagellate, Alexandrium noflagellates have on west coast ecosystems,
catenella is apparently the primary at all levels from zooplankton to fish and
PSP producer in open coastal envi- marine mammals?
ronments of the California and Oregon Domoic acid-producing diatom blooms.
v coasts, but relatively little is known about Domoic acid poisoning (DAP) , associated with
1
t bl om dynamics due to a lack of field ASP in humans, first became a concern along
S 0
surveys focused on this species. What little the west coast of North America in Septem-
is known has been gleaned from shellfish-toxin her, 1991 when more than 100 brown pelicans
C7 monitoring programs (Price et al., 1991). In and cormorants were found dead or suffering
California, blooms of A. catenella cause toxic- from unusual neurological symptoms in
ity nearly every year. PSP toxins are usually Monterey Bay, CA (Fritz et al., 1992; Work et
highest during July and August with most toxic al., 1993). This event was attributed to a bloom
events occurring from May to October. PSP is of the permate diatom, Pseudo-nitzschia aus-
known to accumulate in numerous benthic tralis (Buck et al., 1992; Garrison et al.. 1992).
filter feeders, and there is considerable vari- At the peak of the 1991 bloom, domoic acid
ability among species with respect to levels were > 10 gg/L and R australis reached
toxin retention (Price et al., 1991). over 101 cells/L. Since the 1991 autumn bloom,
Hydrographic mechanisms underly- domoic acid has been detected in both autumn
ing the PSP problems along the west and spring plankton assemblages in Monterey
coast are poorly understood. A good Bay, but with domoic acid concentrations usu-
case can be made that PSP outbreaks ally < 1-5 gg/L, and P. australis densities of
in some areas of California occur follow- 104-101 cells/L. Blooms during the 1991-1994
ing the relaxation of seasonal upwelling. This period often have been comprised of two or
moves offshore waters and their established three potentially toxic species (i.e., P. austra-
dinoflagellate populations rapidly to the coast, lis, P. pungens f. multiseries, and P.
causing increases in toxicity far faster than can pseudodelicatissima); however, P. australis is
be attributed to in situ growth alone. A similar believed to be the main source of the toxin.
mechanism linking shellfish toxicity to changes Domoic acid production from locally-isolated
in upwelling conditions has been reported for clones has only been confirmed for R austra-
the northwest coast of Spain (Fraga et al., lis (Garrison et al., 1992) and R pungens f.
1988), where hydrographic conditions re- multiseries (Villac et al., 1993).
semble those along the northern California Monitoring studies in Monterey Bay suggest
coast. blooms of P. australis are most common and
A number of questions underlying Califor- persist longer during the summer to autumn
nia and west coast PSP outbreaks remain to months (Buck et al., 1992; Walz et al., 1994).
be resolved: Hydrographic conditions during this period are
� Where are the source populations for the characterized by warmer sea-surface tempera-
coastal blooms? If cysts are involved, where tures, thermal stratification, and lower concen-
are the seedbeds located? Do blooms spread trations of organic nutrients. In contrast, P.
from one or a few points of origin or do australis blooms in southern California appear
isolated blooms develop simultaneously in to be most common in the late spring to early
several locations in response to similar hy- summer months, and may be associated with
drographic conditions? Do blooms originate upwelling pulses (Lange et al., 1994).
in offshore waters, 'to be advected onshore The 1991 domoic acid producing bloom in
with changes in meteorological conditions? Monterey Bay was somewhat unusual because
� What are the important meteorological or toxin was transmitted through the pelagic food-
hydrographic forcings underlying toxicity in web via Northern anchovies to seabirds. An-
the different regions along the coast? chovies are also consumed by marine mam-
� If outbreaks are tied closely to transport of mals, several finfish (Morejohn et al., 1978),

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
541

and are occasionally eaten by human consum- 9 Is domoic acid production in natural popu-
ers. Domoic acid has also been found in other lations triggered by nutrient stress?
grazing zooplankton (Buck et al., 1992; a How is domoic acid transported in marine
Haywood and Silver, 1994). With the excep- food-webs? Are there effects on consumers
tion of seabirds, nothing is known of the ef- at all trophic levels?
fects or impact of domoic acid on the pelagic Other Potential HAB Problems. Dinoflagel-
food-web. late species (e.g., Dinophysis spp.) associated
It is difficult to assess the costs associated with diarrhetic shellfish poisoning (DSP), nox-
with the domoic acid blooms. In California, ious bloom- forming species such as
much of the cost of the domoic acid blooms is Phaeocystis pouchetii, and setose diatom spe-
associated with the monitoring program con- cies (e.g., Chaetoceros convolutus and C.
ducted by the California Department of Health concavicomis), that damage gills of pen-raised
Services (Langlois et al., 1993) and U.S. Food finfish (see below) are found throughout the
and Drug Administration (FDA). The Califor- California Current region. Red-tides, apparently
nia Department of Health Services presently all caused by non-toxic species, are common
monitors domoic acid in conjunction with its during the summer months.
established PSP monitoring program, using in- Questions related to potential HAB problems
tertidal mussels as "sentinel" organisms. This include:
strategy may prove to be inadequate because * What are the effects of high-density, mono-
mussel monitoring is apparently not able to specific blooms of non-toxic, "red tide" form-
detect domoic acid when it is present in plank- ing species on food-web structure?
tonic assemblages in low concentration (Walz e What are the occurrences and distributions
et al., 1994). Mussel, rock crab, and razor clam of the potentially harmful species in Cali-
harvesting is a small sport fishing activity in fornia coastal waters?
California and their monetary losses from 9 How are HAB species dynamics related to
blooms are difficult to assess. hydrographic events on short-term, sea-
Domoic acid-producing blooms are a rela- sonal, and interannual time scales?
tively new phenomena in U.S. waters. Unan- 9 What is the importance of meso-scale fea-
swered questions about these blooms include: tures and short-term events on bloom dy-
� What are the sources of domoic acid in West namics?
Coast waters? How many species of Pseudo- e How do the life cycles of the HAB species
niLzschia are toxic? Are there other sources?. influence their distribution and population
� How is domoic acid production related to cycles?
bacteria?

ell- -

A pelican killed by dornoic acid. Photo by I Work.

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
155

F'1111
GIONj. A #_YA,
A

In the Pacific Northwest, public health and as predatory snails, has become a problem
economic problems from HABs are (Matter, 1994).
related to paralytic shellfish poison- Important questions concerning PSP out-
Ing (PSP), domoic acid poisoning breaks in western Washington include:
(DAP), and mortalities of pen-reared Where are the source populations for the
salmonids; diarrhetic shellfish poison- blooms? Are cysts involved? If so, where are
ing (DSP) is a potential but as yet un- the seed beds?
verified problem for the area. What meteorological or hydrographical
Paralytic Shellfish Poisoning. Fol- forcings affect toxicity? Are outbreaks related
IV lowing the deaths of three people and to upwelling events or other transport of off-
mass mortalities of seabirds in 1942, the shore waters and cells to coastal areas? Can
Washington coast from Dungeness Spit on those events be detected/predicted? What
the Strait of Juan de Fuca -to the mouth of hydrographic conditions are necessary for
the Columbia River is closed each year from 1 blooms in inland waters?
Ilk April through 31 October for the harvest of bi- Do nutrients regulate/limit blooms in some
valve molluscs. PSP was not a problem in Puget areas?
Sound until 1978, but since then, it has appar- Amnesic Shellfish Poisoning. Domoic acid
ently spread southward with some closures was first found in razor clams on the Oregon/
now happening every year in central Puget Washington coasts in late October 1991, and
Sound. The first closure in southern Puget both commercial and recreational harvests of
Sound occurred in 1988 and in northern razor clams were halted. Other bivalves, in-
Hood Canal in 1991. cluding cornercially grown oysters and mus-
The causative organisms are mem- sels were tested and did not contain the toxin.
bers of the dinoflagellate genus However, domoic acid was also present in the
Alexandrium. Species known from the viscera of Dungeness crabs and their commer-
% area are A. catenella, A. acatenella, and cial harvest was closed for a short time. Since
A. tamarense. Two other potentially toxic 1991, the fall and spring recreational seasons
species, A. ostenfeldii and A. hiranoi have been for razor clams have been delayed, shortened,
identified recently in British Columbia (Taylor or not opened due to domoic acid. Further-
and Horner, 1994). more, depuration of domoic acid from razor
Hydrographic mechanisms underlying the clams is apparently slow (Drum et al., 1993;
PSP problem in western Washington are poorly Horner et al., 1993). In November 1994,
understood. There have been no sustained field domoic acid was found for the first time in
programs, so bloom dynamics and physical mussels from southern Hood Canal.
forcings remain significant and important un- The causative organisms have not been
knowns. PSP along the ocean coast and in identified with certainty, but it has been as-
coastal bays appears to be caused by blooms sumed that species of the diatom genus Pseudo-
originating offshore. In Puget Sound, blooms nitzschia are to blame. Known toxin-produc-
originate in situ and toxicity may be wide- ing species present in Washington waters
spread or very localized (Nishitani and Chew, include R australis, P. pungens f. multiseries,
1988). A combination of physical factors and and R pseadodelicatissirna. Both P pungens f.
nutrient supply may explain why PSP has not pungens and R pungens f. multiseries were
been a problem in central and southern Hood present i .n the bloom in Hood Canal when
Canal (Rensel, 1993). Some PSP outbreaks have domoic acid was found in mussels.
been correlated with El Nifio events (Erickson As with PSP, hydrographic conditions related
and Nishitani, 1985). to domoic acid occurrence are not known.
Economic impacts include the costs of shell- Pseudo-nitzschia spp. are rarely seen in samples
fish and phytoplankton monitoring by state collected in nearshore waters when razor clams
health officials, the closure of many beaches are most toxic, but perhaps the cells originate
to the recreational harvest of shellfish during offshore and are advected to the coast. There
the summer months, and lost tourist trade. has been no offshore sampling since the 1991
Commercial sales may be affected if the pub- incident. It is possible that a series of Pseudo-
lic thinks shellfish are contaminated. Recently, nitzschia blooms occurred, extending from
the harvest of non-traditional shellfish, such California to Alaska, linked to unusually warm

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
.56

weather conditions during the night. Vertical stability of the water
associated with an column is probably an important factor in
ENSO event in 1991. maintaining blooms.
The 1991 domoic The harmful diatom species Chaetoceros
acid incident caused concavicornis, C. convolutus, and perhaps C.
an estimated $15 - danicus have long setae armed with short sec-
$20 million in dam- ondary spines and may kill at fairly low con-
ages to the Oregon/ centrations (< 101 cells/Q. Chains of cells ap-
Washington coastal parently become lodged between secondary
economy. Losses in- larnellae in the fish gills and cause blood hy-
cluded health effects, poxia as a result of mucus production. These
lost and/or delayed diatoms may be restricted to near-surface wa-
sales, lower prices, ters or mixed throughout the water column
lost jobs, bankrupt- depending on local hydrographic conditions.
Mortality of cies, and lost recreational opportunities and Most fish growers have their own phytoplank-
farmed fish. tourist trade. No estimate is available for losses ton monitors who sample at the pen sites on a
since 1991. daily basis from April through September. They
Unanswered questions with regard to also rely on reports from other phytoplankton
domoic acid and ASP include: monitoring programs. Economic losses are
� What are the causative organisms? Are about $0.5 million per event.
Pseudo-nitzschia spp. the only ones involved Unanswered questions here include:
or are other diatoms and/or macroalgae also * What environmental conditions cause
culprits? blooms of Heterosigma?
� What is the source of the organisms? Is there e Does Heterosigma produce a toxin? If so,
an offshore bloom that is advected to in- what is it? How does it kill the fish? What
shore localities? In Puget Sound, are there environmental conditions are needed for
local seed populations in sonie areas? toxin production?
� What is the life cycle of the Pseudo-nitzschia 9 Are fish killed by Heterosigma safe to eat?
Spp.? * Are Chaetoceros concavicornis and C.
� What environmental conditions are needed convolutus the only Chaetoceros species that
for domoic acid production by the cells? kill fish or can any species with secondary
� How do the razor clams and Dungeness spines (e.g., C. danicas) or capilli (long, hair-
crabs obtain domoic acid? How long does it like siliceous spines, e.g., C. radicans) on
take them to depurate domoic acid? Under the setae kill fish?
what conditions? * Can harmful Chaetoceros species and/or
* Has the Washington incident been one event other harmful phytoplankton species influ-
with slow depuration or is there continual ence the distribution and abundance of fin-
reintoxication? fish in inland waters of Washington State?
Finfish Mortalities. Catastrophic losses of 9 What environmental factors affect the tim-
cultured and wild fish sometimes occur due to ing and magnitude of harmful Chaetoceros
species of phytoplankton that do not cause ill- blooms in inland waters?
nesses in humans. Blooms of the raphidophyte 9 Are phytoplankton associated with summer
flagellate Heterosigma carterae (sometimes mortality of finfish? If so, which species?
called H. akashituo or, erroneously, Other HAB problems. Ceratiurn fusus and
01isthodiscus luteus) have occurred in British Gyrnnodinium sanguineum have been linked
Columbia every year since the early 1960s and to mortality of oyster larvae and adults
fish kills have been reported most years since (Cardwell et al., 1977, 1979) and spot prawns
1986; in Washington, fish kills occurred in pen- (Rensel and Prentice, 1980) in southern Puget
reared fish in 1989 and 1990, and wild fish in Sound. There is no indication of a chemical
1994. Losses to the fish growers are about $4- toxin and mortality may be due to mechanical
5 million per year when blooms occur. The means or oxygen stress when blooms decay.
way Heterosigma kills is not known, but su- The major questions for these species are:
peroxide radicals may be involved because fish 9 How do they cause mortality?
can be protected with the addition of superox- 9 How often do they cause shellfish mortal-
ide dismutase (Yang et al., 1993). This organ- ity? Could these dinoflagellates, or other
ism is a vertical migrator, usually occurring in phytoplankton species, be implicated in
surface waters during the day and at depth summer mortality of oysters?

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
57

PACIFIC COAST REGION (ALASKA): PSP, ASP, BITTER CRAB DISEASE

Alaska, with 54% of the U.S. suggesting that blooms originate or grow better
coastline, has a significant prob- near the headwaters. It is certainly possible that
lem managing the impacts of the rising tide or certain wind patterns may push
HABs. Although some baseline toxic algae into shallow areas, but there is a
information is available, vir- growing perception that blooms originate off-
tually all studies have shore and move inland. Despite the prevalence
been either of short of PSP, large areas of the coast remain relatively
duration and/or re- free of toxins.
stricted to small geo- In 1917, 5 million pounds of shellfish prod-
graphic areas. No studies have critically ucts were harvested from Alaskan waters, but
and specifically evaluated HABs on a broad today the state's commercial bivalve industry
geographic scale. is virtually nonexistent. The destruction of the
Paralytic Shellfish Poisoning. PSP is the clam industry, estimated at 25-50 million
most significant HAB problem in Alaska. Nu- pounds of bivalves per year, is in large part a
merous beaches, bays, and coves in the south- result of product contamination by PSP (Neve
east and east are periodically or perpetually and Reichardt, 1984). Other commercially valu-
plagued with high levels of saxitoxins in blue able species, such as Dungeness crabs, are also
mussels, butter, little necks, and horse clams, affected by PSP, presumably from consump-
geoduck, oysters, and cockles. Commercially tion of tainted bivalves. Other economically
valuable crabs are also affected. The causative valuable crustaceans have riot tested positive
species is apparently Alexandrium catenella, but for PSP.
other toxin-producing species may also be Only commercially harvested shellfish are
present. Toxic blooms have been reported in presently tested for PSP on a routine basis. Re-
almost every month of the year, making it diffi- cently, the Alaska Department of Conservation
cult to ascribe bloom conditions to any particu- (DEC) instigated a multicomponent program
lar environmental or hydrographical condition. to detect PSP and identify blooms. The pro-
One frequently reported trend is that shellfish gram relies on local fish farmers trained to iden-
from headwaters of estuaries have more toxin tify toxic dinoflagellates from their swimming
than those collected near the mouths, perhaps patterns, satellite imagery to identify and track

Please do not eat Pakiusap, huwag Es imposible
any clams or mussels kakain ng kahit anong diferenciar los
It is impossible to tell uri ng klam. ostinoes
contaminated shell- Imposibling malaman conaminados con los
fish from safe ones. kung alin ang may buenos.
Cooking does not lason a wala. Kabit Cocinandolos no
destroy the poison, iluto ay hindi maaalis destrulle el veneno y
and Paralytic ang lason sa klam at parasitos ostiones
Shellfish Poisoning maaari kang mamatay contaminandos te
can kill you. sa Paralytic Shellfish pueden matar.
Poisoning.

4. REGIONAL HAB PHENOMENA IN THE UNITED STATES
581

blooms, and a citizen monitoring program with 9 Do blooms of Pseudo-nitzschia occur in Alas-
an 800 number for reporting PSP illnesses, dis- kan waters? Are any of the populations
colored water, fish kills, unusual behavior of toxic?
seabirds or mammals, etc. This program needs e What are the seasonal and geographic dis-
to be coupled with physical, chemical, and bio- tributions of Pseudo-niLzschia spp., and what
logical oceanographic studies being conducted controls their abundance and toxicity?
on the coast to provide insights into bloom for- Other potential HAB Problems. Phaeocystis
mation, spread, and collapse. blooms occur occasionally in Alaska, and un-
Questions that need to be answered with der conditions that are not well understood.
regard to PSP in Alaska include: This alga can be a major component of the
� What algal species are involved? spring bloom or form a second, smaller bloom
� What are their seasonal and geographic dis- later. It produces both acrylic acid and DMSP,
tributions? but the ecological and environmental impacts
� What hydrographic and environmental fac- of these compounds are not known. Southeast-
tors contribute to blooms? ern Alaska shares with Washington State the
� What information is needed to guide the de- presence of several potentially harmful dia-
velopment of a shellfish industry in a re- toms, e.g., Chaetoceros convolutus and C.
gion with extensive PSP problems? concavicornis, however no problems have been
Domoic Acid. Alaska does not have a se- associated with these species, since fish farm-
vere problem with domoic acid, but low levels ing is not yet a major industry..
have been found in razor clams and Pseudo- A parasitic dinoflagellate, Hematodinium
nitzschia pungens and P. australis have been sp., has been of increasing concern since 1985
found in Alaskan waters. Whether they pro- because it causes "bitter crab" disease. The
duce domoic acid is not known. parasite infects crabs during their molt (Love
While domoic acid is not yet a problem in et al., 1993; Meyers et al., 1987). Once estab-
Alaska, some questions are still pertinent: lished, it is 100 % lethal and the crab meat be-
comes unmarketable before the crabs die.
Questions with regard to Phaeocystis and
Hematodinium include:
e 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?

"L10-
These dormant cysts allow toxic Alexandrium species to survive winter tem-
peratures and repopulate the water column in the spring. Photo by D. Wall.

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APPENDIX. LIST OF WORKSHOP PARTICIPANTS
165

Dr. Mary Altalo Dr. Quay Dortch
Deputy Director Louisiana University Marine Consortium
Scripps Institution of Oceanography 8124 Highway 56
UCSD Chauvin, LA 70344
La Jolla, CA 92093-0218 Tel: 504 851-2800
Tel: 619 534-2836 Fax: 504 851-2874
Fax: 619 4S3-0167 E-mail: [email protected]
E-Mail: [email protected] Dr. Gregory J. Doucette
Dr. Donald M. Anderson National Marine Fisheries Service
Department of Biology SEFSC - Box 12607
Woods Hole Oceanographic Institution Charleston, SC 29422
Woods Hole, MA 02543-1049 Tel: 803 762-8528
Tel: S08 289-2351 Fax: 803 762-8700
Fax: 508 457-2134 E-mail: [email protected]
E-mail: [email protected] Dr. Peter J.S. Franks
Dr. Susan Banahan Scripps Institution of Oceanography
NOAA/Coastal Ocean Office UCSD
1315 East West Highway La Jolla, CA 92093-0218
Silver Spring, MD 20910 Tel: 619 534-7523
Tel: 301-713-3338 Fax: 619 534-6500
Fax: 301-713-4044 E-mail: [email protected]
E-mail: [email protected] Dr. Greta A. Fryxell
Dr. V. Monica Bricelj Texas A & M
Marine Sciences Research Center Department of Oceanography
SUNY College Station, TX 77843
Stony Brook, NY 11794-5000 Tel: 409 845-4543
Tel: 516 632-8663 Fax: 409 845-6331
Fax: 516 632-8820 E-mail: [email protected]
E-mail: mbriceljOccmail.sunysb.edu Dr. Sylvia B. Galloway
Dr. Peter Barile National Marine Fisheries Service
Division of Ocean Sciences Southeast Fisheries Science Center
National Science Foundation P. 0. Box 12607
4201 Wilson Blvd. - Rm. 725 Charleston, SC 29422
Arlington, VA 22230 Tel: 803 762-8525
Tel: 703 306-1587 Fax: 803 762-8700
Fax: 703 306-0390 E-mail: [email protected]
E-mail: pbarileC&nsf.gov
Dr. David L. Garrison
Dr. JoAnn M. Burkholder Institute of Marine Science
North Carolina State University Applied Sciences Building
Department of Botany, Box 7612 University of California, Santa Cruz
Raleigh, NC 27695-7612 Santa Cruz, CA 95064
Tel: 919 515-2726 Tel: (408) 459-4789
Fax: 919 SIS-3436 Fax: (408) 459-4882
E-mail: [email protected] E-mail: d1garris @cats. ucsc. edu
Dr. Edward J. Buskey Dr. W. Rockwell Geyer
University of Texas at Austin Dept. Applied Ocean Physics and Engineering
Marine Science Institute - Woods Hole Oceanographic Institution
P. 0. Box 1267 Woods Hole, MA 02543
Port Aransas, TX 78373-1267 Tel: 508 289-2868
Tel: 512 749-6794 Fax: 508 457-2194
Fax: 512 749-6777 E-mail: [email protected]
E-mail: [email protected] Dr. Sherwood Hall
Dr. Leon Cammen FDA - HFS 426
National Sea Grant College Program 200 C. Street, SW
NOAA/ R/ORI Washington, DC 20204
1315 East-West Highway Tel: 202 205-4818
Sliver Spring, MD 20910 Fax: 202 205-4881
Tel: 301 713-2434 E-mail:
Fax: 301 713-0799 Dr. R. Patrick Hassett
E-mail: Icammenardc.noaa.gov Arizona State University
Dr. John J. Cullen Zoology Department
Department of Oceanography Tempe, Arizona 85287
Dalhousie University Tel: 602 965-0044
Halifax, NS B3H 4JI Canada Fax: 602 965-2519
Tel: 902 494-6667 E-mail: [email protected]
Fax: 902 494-3877 Dr. Rita A. Horner
E-mail: [email protected],ca University of Washington
Dr. Percy L. Donaghay School of Oceanography, Box 357940
University of Rhode Island Seattle, WA 98195-7940
Graduate School of Oceanography Tel: 206 543-8599
Narragansett, Rhode Island 02881 Fax: 206 S43-0275
Tel: 401 792-6944, Fax: 401 792-6240 E-mail: [email protected]
E-mail: [email protected]

APPENDix. LIST OF WORKSHOP PARTICIPANTS
661

Dr. Daniel Kamykowski Dr. Howard H. Seliger
NC State University McCollum-Pratt Institute
Marine Earth Atmosphere Sciences The Johns Hopkins University
Box 8208 - 1125 Jordan Hall Charles and 34th Sts
Raleigh, NC 27695 Baltimore, MD 21218
Tel: 919 515-7894 Tel: 410 516-7330
Fax: 919 515-7802 Fax: 410 516-5213
E-mail: [email protected] E-mail: seligerOjhuvms.hcf.jhu.edu
Dr. Maureen Keller Dr. Theodore J. Smayda
Bigelow Laboratory for Ocean Sciences Narragansett Marine Lab
P. 0. Box 475 - McKown Point Graduate School Oceanography
W Boothbay Harbor, ME 04575-0475 University of Rhode Island
Tel: (207) 633-9600 Kingston, RI 02881
Fax: (207) 633-9641 Tel: 401 792-6171
E-mail: [email protected] Fax: 401 792-6682
Dr. Brian E. LaPointe E-mail: tsmayda(&gsosunl.gso.uri.edu
Harbor Branch Oceanographic Institution Dr. Karen A. Steidinger
Rt. 3, Box 297A Dept. of Environmental Protection
Big Pine Key, FL 33043 Florida Institute of Marine Research
Tel: 305 872-2247 100 Eighth Ave. S.E.
Fax: 305 872-2247 St. Petersburg, FL 33701-5095
E-mail: [email protected] Tel: 813 896-8626
Fax: 813 823-0166
Dr. Darcy J. Lonsdale E-mail: Steidinger - K@ sellers. dep.state. fl. us
Marine Sciences Research Center Dr. Phillip R. Taylor
State University of New York Division of Ocean Science
Stony Brook, NY 11794-5000 National Science Foundation
Tel: 516 632-8712 @_-Vilson Blvd. - Room 725
Fax: 516 63. ton, VA 22230
E-mail: dloj DATE DUE 306-1587
Dr. Thomas C )3 306-0390
Horn Point : [email protected]
P. 0. Box 7;____ :a A. Tester
Cambridge, Ial Marine Fisheries Service
Tel: 410 228 @ast Fisheries Center
Fax: 410 47( _)rt Lab - 101 Rivers Island Rd.
E-mail: mal )rt, NC 28516
Dr. David Mill 9728-8792
Southern R(_ 19 728-8784
USDA-ARS - : ptester(&hatteras.bea.nmfs.gov
New Orlean- _Ao R. Tomas
Tel: 504 286- - Environmental Protection
Fax: 504 28( 1 Marine Research Institute
E-mail: dmi.- hth Avenue S.E.
Dr. Thomas 0 _rsburg, FL 33701-5095
The Johns F - 3 896-8626 X 420
Olin Hall 3 823-0166
Baltimore, I\--- Tomas_Casellers. dep. state. fl. us
Tel: 410 516- _____---2aliela
Fax: 410 516-- ! Biological Laboratory
E-mail: osbc tems Center
Dr. Hans W Pa- Hole, MA 02543
PAINTEO IN U.S.A. 3 548-3705
Institute of I GAYLOR.DlNo. 2333 rdA; j08 540-6902
University of North Carolina, E-mail: [email protected]
Chapel Hill, 3431 Arendell Street
Morehead City, North Carolina 28S57 Dr. Terry E. Whitledge
Tel: 919 726-6841 Marine Science Institute
Fax: 919 726-2426 The University of Texas at Austin
E-mail: [email protected] P. 0. Box 1267
Port Aransas, TX 78373-1267
Dr. F. Gerry Plumley Tel: 512 749-6769
Instituteof Marine Science Fax: 512 749-6777
University of Alaska, Fairbanks E-mail: terry@ utmsi, zo. utexas. edu
Fairbanks, AK 99775-1084
Tel: 907 474-6786
Fax: 907 474-7204 Top Photo: Foam covered beaches and fisherman's
E-mail: fffgp @aurora. alaska. edu nets clogged with mucilage are common manifes-
Dr. Christopher A. Scholin tations of Pheocystis blooms in many parts of the
Monterey Bay Aquarium Research Institute world. The organism is present in U.S. waters, but
RO. Box 628 has not yet caused problems.
Moss Landing, CA 95039
Tel: 408 775-1779 Bottom Photo: Sponges and corals overgrown by
Fax: 408 775-1638 the seaweed Codium isthmocladum in Southeast
E-mail: [email protected] Florida. Photo by B. LaPoint.

1@ew'

jt'

v1%
lop

THE ECOLOGY AND OCEANOGRAPHY OF HARMFUL ALGAL BLOOMS

Over the last several decades, the United States has ex-
perienced an escalating and worrisome trend in the in-
cidence of problems associated with harmful and toxic
algae (commonly called "red tides"). Formerly only a
few regions were affected, but now virtually every
coastal state is threatened, in many cases over large
geographic areas and by more than one harmful or toxic
species. Impacts 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.

These economic, public health, and ecosystem impacts are strong, practical
motivations for a coordinated, multidisciplinary research program. This report
presents a research agenda for such a program: ECOHAB-The ECology and
Oceanography of Harmful Algal Blooms.