[From the U.S. Government Printing Office, www.gpo.gov]




                                                                                                                                                                                                4i

                                                                                                                                   i  z

                                                                                        @@ al

                                                                            I




                                                                                                                                               AIL


                                                                777,
                                                                                                                      ("Y
                                                                                                                                                                'ALGAL BLOOMS
             7',                                                                                      c       X kIr
                                                                                                                                     JE @f

                                                                                                                                      Agenda
























               QK
                568
                  T67
                E26
                1995





                                                                                                                                                                                                                                                                                                                                                  - - --------


















                                                                                                                                                              x
                                                                                                                                                                  NO


                         4 'be,







                                                                                                 Alt.,



                                             10


















                                                      the"










                          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










             2


                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









                                                                                                                                                3


              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:
                                      ï¿½ 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
                                      ï¿½ 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.
                                      ï¿½ Characterize the physiological responses
                                        and tolerances of HAB species to differing           Specific objectives:
                                        environmental conditions.                               Determine the extent to which HAB events
                                      ï¿½ 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.
                                      ï¿½ 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-
                                      ï¿½ Determine the functional role of toxins and/            tween nutrient inputs and population dy-
                                        or exudates produced by HAB species.                    namics of HAB species.
                                      ï¿½ 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
                                      ï¿½ 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-
                                      ï¿½  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.
                                      ï¿½  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
                                      ï¿½  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
                                      ï¿½  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
                                      ï¿½  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.






                                                                                                                                           17

             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






                                        V







                                                                          W4



                  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

                             0


                           -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, ï¿½ 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


                                                                                                                      18


                                                                          NJ

                                                              PA



                                              ------------
                                                 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




                                                                                                                             IL


                                                                                                                     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

                                                                                                                      T_



                                               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
                                    ï¿½  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
                                    ï¿½ 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-
                                    ï¿½  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-
                                       ï¿½ 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
                                       ï¿½  How is domoic     acid production   related to         cycles?
                                          bacteria?
















                                                                                           ell- -











                                                                        7_

                                       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
                                           ï¿½  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?
                                           ï¿½  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?
                                           ï¿½  What is the life cycle of the Pseudo-nitzschia             9  Are fish killed by Heterosigma safe to eat?
                                              Spp.?                                                      *  Are Chaetoceros concavicornis and C.
                                           ï¿½  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
                                           ï¿½  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
                                     ï¿½ What algal species are involved?                     spring bloom or form a second, smaller bloom
                                     ï¿½ What are their seasonal and geographic dis-          later. It produces both acrylic acid and DMSP,
                                       tributions?                                          but the ecological and environmental impacts
                                     ï¿½ What hydrographic and environmental fac-             of these compounds are not known. Southeast-
                                       tors contribute to blooms?                           ern Alaska shares with Washington State the
                                     ï¿½ 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?









                                                   t




                    "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.









                                                                                                                                                                    59


                 S. LITERATURE CITED


                                         Ahmed, F.E. (Ed). 1991, Seafood Safety. National                Bates, S.S., Leger, C., Keafer, B.A., Anderson, D.M.
                                             Academy Press, Wash. D.C. 432 pp.                               (1993). Discrimination between domoic-acid-pro-
                                         Anderson, D.M. 1995. Toxic red tides and harmful                    ducing and non-toxic forms of the diatom
                                             algal blooms: a practical challenge in coastal                  Pseudonitzschia pungens using immunofluores-
                                             oceanography. Rev. Geophysics, Suppl. U.S. Na-                  cence. Mar. Ecol. Prog. Ser. 100:185-195.
                                             tional Report to the Int. Union of Geodesy and              Bates, S.S., C.J. Bird, A.S.W. deFreitas, R. Foxall, M.
                                             Geophysics 1991-1994. pp. 1189-1200.                            Gilgan, L.A. Hanic, G.R. Johnson, A.W.
                                         Anderson, D.M. 1989. Toxic algal blooms and red                     McCulloch, P. Odense, R. Pocklington, M.A.
                                             tides: a global perspective. In: T. Okaichi, D.M.               Quilliam, P.G. Sim, J.C. Smith, D.V. Subba Rao,
                                             Anderson, and T. Nemoto (eds.), Red Tides: Biol-                E.C.D. Todd, J.A. Walter, and J.L.C. Wright. 1989.
                                             ogy, Environmental Science and Toxicology.                      Permate diatom Nitzschia pungens as the primary
                                             Elsevier, New York. pp. 11-16.                                  source of domoic acid, a toxin in shellfish from
                                         Anderson, D.M. and A.W.White. 1992. Marine                          eastern Prince Edward Island, Canada. Can. J.
                                             biotoxins at the top of the food chain. Oceanus                 Fish. Aquat. Sci. 46:1203-1215.
                                             35:55-61.                                                   Bates, S.S., A.S.W. deFreitas, J.E. Milley, R.
                                         Anderson, D.M. and B.A. Keafer. 1987. An endog-                     Pocklington, M.A. Quilliam, J.C. Smith, and J.
                                             enous annual clock in the toxic marine dinoflagel-              Worms. 1991. Controls on domoic acid produc-
                                             late Gonyaulax tamarensis. Nature 325:616-617.                  tion by the diatom Nitzschia. pungens f. multiseries
                                                                                                             in culture: nutrients and irradiance. Can. J. Fish.
                                         Anderson, D.M. and B.A. Keafer. 1992. Paralytic Shell-              Aquat. Sci. 48:1136-1144.
                                             fish Poisoning on Georges Bank: in situ growth or           Bates, S.S. and D.J. Douglas. 1993. Laboratory stud-
                                             advection of established dinoflagellate popula-                 ies of domoic acid production by Pseudonitzschia
                                             tions. In: J. Wiggen and C.N.K. Mooers                          pungens. Harmful Algae News 6:6-7.
                                             (eds.). Proceedings of the Gulf of Maine Scientific
                                             Workshop, Urban Harbors Institute, Univ. Mass.              Bates, S.S., D.J. Douglas, G.J. Doucette, and C. L6ger.
                                             Boston. pp. 217-224.                                            1995. Effects of reintroducing bacteria on domoic
                                         Anderson, D.M., Keafer, B.A., Kulis, D.M., Waters,                  acid production by axenic cultures of the diatom
                                             R.M., Nuzzi, R. 1993. An immunofluorescent sur-                 Pseudonitzschia pungens f. multiseries. In: P.
                                             vey of the brown tide chrysophyte Aureococcus                   Lassus, G. Arzul, E. Erard-Le Derm, P. Gentien,
                                             anophagefferens along the northeast coast of the                and C. Marcaillou-Le Baut (eds.), Harmful Ma-
                                             United States. J. Plankton. Res. 15: 563-580.                   rine Algal Blooms. Lavoisier Publishing, Paris. pp.
                                         Anderson, D.M. and P.S. Lobel. 1987. The continu-                   401-406.
                                             ing enigma of ciguatera. Biol. Bull. 172:89-107.            Berdalet, E. 1992. Effects of turbulence on the ma-
                                                                                                             rine dinoflagellate Gymnodinium, nefsonii. J.
                                         Anderson, D.M. and K.D. Stolzenbach, 1985. Selec-                   Phycol. 28:267-272.
                                             tive retention of two dinoflagellates in a well-            Berdalet, E. and M. Estrada. 1994. Effects of nitro-
                                             mixed estuarine embayment: the importance of                    gen and phosphorous starvation on nucleic acid
                                             diel vertical migration and surface avoidance. Mar.             and protein content of Heterocapsa sp. J. Plank-
                                             Ecol. Prog. Ser. 25:39-50.                                      ton Res. 16:303-316.
                                         Anderson, D.M. and D.Wall. 1978. Potential impor-               Blumberg, A.F. and G.L. Mellor. 1987. A description
                                             tance of benthic cysts of Gonyaulax tamarensis                  of a three-dimensional coastal ocean circulation
                                             and G. excavata in initiating toxic dinoflagellate              mode. In: Three-Dimensional Coastal Ocean Mod-
                                             blooms. J. Phycol. 14:224-234.                                  els, N.S. Heaps, ed. Coastal and
                                         Anderson, D.M., D.M. Kulis,, J.J. Sullivan, S. Hall,            Bomber, J.W., D.R. Tindall, and D.M. Miller. 1989.
                                             and C. Lee. 1990a Dynamics and physiology of                    Genetic variability in toxin production among sev-
                                             saxitoxin production by the din o flagellates                   enteen clones of Gambierdiscus toxicus
                                             Alexandrium spp. Mar. Biol. 104:511-524.                        (Dinophyceae). J. Phycol. 25:617-625.
                                         Anderson, D.M,, D.M. Kulis, J.J.Sullivan, and S. Hall.
                                             1990b. Toxin composition variations in one iso-             Boyer, G.L., J.J. Sullivan, R.J. Andersen, P.J. Harrison,
                                             late of the dinoflagellate Alexandrium. fundyense.              and F.J.R.Taylor. 1987. Effects of nutrient limita-
                                             Toxicon 28:885-893.                                             tion on toxin production and composition in the
                                                                                                             marine dinoflagellate Protogonyaulax tamarensis.
                                         Anderson, D.M., D.M. Kulis, G.J. Doucette, J.C.                     Mar. Biol. 96:123-128.
                                             Gallagher, and E. Balech. 1994. Biogeography of             Bricelj, V.M. and S.H. Kuenstner. 1989. Effects of the
                                             toxic dinoflagellates in the genus Alexandrium
                                             from the northeastern United States and Canada.                 -brown tide" on the feeding physiology and
                                             Mar. Biol. 120:467-478.                                         growth of bay scallops and mussels. In: E.M.
                                                                                                             Cosper, V.M. Bricelj and E.J. Carpenter (eds.),
                                         Anderson, D.M., S.B. Galloway, and J.D. Joseph.                     Novel Phytoplankton Blooms: Causes and Impacts
                                             1993. Marine Biotoxins and Harmful Algae: A                     of Recurrent Brown Tides and Other Unusual
                                             National Plan. Woods Hole Oceanographic Insti-                  Blooms. Coastal and Estuarine Studies, Vol. 35.
                                             tution Tech. Rep. WHOI-93-02. 59 pp.                            Springer-Verlag, Berlin. pp. 491-509.
                                         Anderson, D.M., S.W. Chisholm, and C.J. Watras.                 Bricelj, V.M., J. Epp, and R.E. Malouf, 1987. Intraspe-
                                             1983. Importance of life cycle event in the popu-               cific variation in reproductive and somatic growth
                                             lation dynamics of Gonyaulax tamarensis. Mar.                   cycles of bay scallops Argopecten irradians. Mar.
                                             Biol. 76:179-189.                                               Ecol. Prog. Ser. 36: 123-137.
                                         Bass, A.E., R.E. Malouf, and S.E. Shurnway, 1990.
                                                                                                                                           ,10 ?1



















































                                             Growth of northern quahogs (Mercenaria
                                             mercenaria [Linnaeus, 1758]) fed on picoplankton.
                                             J. Shellfish Res. 9:299-307.








                                            S. LITERATURE CITED
           601

                                            Buck, K.R., L. Uttal-Cooke, C.H. Pilskaln, D.L. Roelke,           Chao, S.-Y. 1987. Wind-driven motion near inner shelf
                                                M.C. Villac, G.A. Fryxell, L. Cifuentes, and F.P.                 fronts. J. Geophys. Res. 92:3849-3860.
                                                Chavez. 1992. Autecology of Pseadonitzschia. aus-             Cosper, E.M., V.M. Bricelj, and E.J. Carpenter (eds.).
                                                tralis Frenguelli, a suspected domoic acid pro-                   1989a. Novel Phytoplankton Blooms: Causes and
                                                ducer, from Monterey Bay, California. Mar. Ecol.                  Effects of Recurrent Brown Tides and Other Un-
                                                Prog. Ser. 84:293-302.                                            usual Blooms. Coastal and Estuarine Studies, Vol.
                                            Burkholder, J.M. and H.B. Glasgow, Jr. 1995. Re-                      35. Springer-Verlag, Berlin. 799 pp.
                                                sponse of the toxic estuarine dinoflagellate,                 Cosper, E.M. W. Dennison, A. Milligan, E.J. Carpen-
                                                Pfiesteria piscicida to N and P from organic and                  ter, C. Lee, J. Holzapfel, and L. Milanese. 1989b.
                                                inorganic sources. In: Abstracts, Annual Meeting,                 An examination of the environmental factors im-
                                                American Society of Limnology and Oceanogra-                      portant to initiating and sustaining "brown tide"
                                                phy, June 11-15, Reno, Nevada.                                    blooms. In: E.M. Cosper, V.M. Bricelj, and E.J.
                                            Burkholder, J.M., H.B. Glasgow, Jr., and C.W Hobbs.                   Carpenter (eds.), Novel Phytoplankton Blooms:
                                                In press. Distribution and environmental condi-                   Causes and Effects of Recurrent Brown Tides and
                                                tions for fish kills linked to a toxic ambush-preda-              Other Unusual Blooms. Coastal and Estuarine
                                                tor dinoflagellate. Mar. Ecol. Prog. Ser.                         Studies, Vol. 35. Springer-Verlag, Berlin. pp. 317-
                                            Burkholder, J.M., H.B. Glasgow, Jr., and K.A.                         340.
                                                Steidinger. 1995. Stage transformations in the com-           Cullen, J.J. and S.G. Horrigan. 1981. Effects of ni-
                                                plex life cycle of an ichthyotoxic "ambush-preda-                 trate on the diurnal vertical migration, carbon to
                                                tor" dinoflagellate. In: P. Lassus, G. Arzul, E. Erard-           nitrogen ratio, and the photosynethetic capacity
                                                Le Denn, P. Gentien, C. Marcaillou-Le Baut (eds.),                of the dinoflagellate, Gymnodinium splendens.
                                                Harmful Marine Algal Blooms. Lavoisier Publish-                   Mai. Biol. 62:81-89.
                                                ing, Paris. pp. 567-S72.                                      Currin, C.A., H.W Paerl, G.K. Suba, and R.S. Alberte.
                                            Burkholder, J.M., E.J. Noga, C.H. Hobbs, and H.B.                     1990. Immunofluorescence detection and charac-
                                                Glasgow, Jr. 1992. New 'phantom' dinoflagellate                   terization of N   2 -fixing microorganisms from
                                                is the causative agent of major estuarine fish kills.             aquatic environments. Limnol. OceanOgL 35:59-
                                                Nature 358:407-410.                                               71.
                                            Buskey, E.J. and D.A. Stockwell. 1993. Effects of a               DeLong, E. F., G. S. Wickham, N. R. Pace. 1989. Phy-
                                                persistent "brown tide" on zooplankton popula-                    logenetic stains: ribosomal RNA-based probes for
                                                tions in the Laguna Madre of South Texas. In: T.J.                the identification of single cells. Science 243: 1360-
                                                Smayda. and Y. Shimizu (eds.), Toxic Phytoplank-                  1364.
                                                ton Blooms in the Sea. Elsevier Science Publ. BY.,            Dennison, W.C., G.J. Marshall, and C. Wigand. 1989.
                                                Amsterdam. pp. 659-666.                                           Effect of 'brown tide' shading on eelgrass (Zostera
                                            Caperon, J. and J. Meyer. 1972. Nitrogen- I imited                    marina L.) distributions. In: E.M. Cosper, V.M.
                                                growth of marine phytoplankton. II. Uptake ki-                    Bricelj, and E.J. Carpenter (eds.), Novel Phy-
                                                netics and their role in nutrient-limited growth of               toplankton Blooms: Causes and Impacts of Re-
                                                phytoplankton. Deep-Sea Res. 19:619-632.                          current Brown Tides and Other Unusual Blooms.
                                            Cardwell, R.D., S. Olsen, M.I. Carr, and E.W.                         Coastal and Estuarine Studies, Vol. 35. Springer-
                                                Sanborn. 1979. Causes of oyster larvae mortality                  Verlag, Berlin. pp. 67S-692.
                                                in southern Puget Sound. NOAA Tech. Mem. ERL                  DeYbe, H.R. and C.A. Suttle. 1994. The inability of
                                                MESA-39. 73 pp,                                                   the Texas "brown tide" alga to use nitrate and the
                                            Cardwell, R.D., C.E. Woelke, M.I. Carr, and E.W,                      role of nitrogen in the initiation of a persistent
                                                Sanborn. 1977. Evaluation of water quality of                     bloom of this organism. J. Phycol. 30:800-806.
                                                Puget Sound and Hood Canal in 1976. NOAA Tech.                Donaghay, P.L, 1985, An experimental test of the rela-
                                                Mem. ERL MESA-21. 36 pp.                                          tive significance of food quality and past feeding
                                            Cartsson, P., E. Gran6li, and P. Olsson. Grazer elimi-                history to the limitation of egg production of the
                                                nation through poisoning: One of the mechanisms                   estuarine copepod Acartia tonsa. Arch. Hydrobiol.
                                                behind Chrysochromulina polylepis blooms. In:                     Beih. Ergebn. Limnol. 21:235-245.
                                                Graneli, E., B. Sundstrom, L. Edler, and D.M.                 Donaghay, P.L. 1988. The role of temporal scales of
                                                Anderson (Eds.),Toxic Marine Phytoplankton,                       acclimation, food quality and trophic dominance
                                                Elsevier, New York. pp. 116-122.                                  in controlling the evolution of copepod feeding
                                            Cembella, A.D., N.J. Antia, and P.J. Harrison. 1984.                  behavior. Bull. Mar. Sci. 43:469-485.
                                                The utilization of inorganic and organic phospho-             Donaghay, P.L., H.M. Rines and J.M. Sieburth. 1992.
                                                rus compounds as nutrients by eukaryotic                          Simultaneous sampling of fine scale biological,
                                                microalgae: a multidisciplinary perspective. Part.                chemical and physical structure in stratified wa-
                                                1. CRC Crit. Rev. Microbiol. 10:317-391.                          ters. Arch. Hydrobiol. Beih. Ergeb. Limnol. 36:97-
                                            Cembella, D., S.E. Shurnway, and N.I. Lewis, 1993.                    108.
                                                Anatomical distribution and spatio-temporal varia-            Dortch, Q., T.L. Roberts, J.R. Clayton, Jr., and S.I.
                                                tion in paralytic shellfish toxin composition in two              Ahmed. 1983. RNA/DNA ratios and DNA concen-
                                                bivalve species from the Gulf of Maine. J. Shell-                 trations as indicators of growth rate and biomass
                                                fish Res. 12:389-403.                                             in planktonic marine organisms. Mar. Ecol. Prog.
                                            Cembella, A.D., J.J. Sullivan, G.I. Boyer, F.J.R. Tay-                Series. 13:61-71.
                                                lor, and R.J. Andersen. 1987. Variation in para-              Doucette, G.J. 1995. Interactions between bacteria
                                                lytic shellfish toxin compositibn within the                      and harmful algae: a review. Natural Toxins 3:65-
                                                Protogonyaulax tarnarensisIcatenella species com-                 74.
                                                plex: red tide dinoflagellates. Biochem. System.              Doucette, G.J. and C.G. Trick. 199S. Characteriza-
                                                Ecol. 15:171-186.                                                 tion of bacteria associated with different isolates
                                            Chang, J. and E.J. Carpenter. 1991. Species specific                  of Alexandrium tamarense. In: P. Lassus, G. Arzul,
                                                phytoplankton growth rates via diel DNA synthe-                   E. Erard-Le Denn, P. Gentien, C. Marcaillou-Le
                                                sis cycles. V. Application to natural populations                 Baut (eds.), Harmful Marine Algal Blooms.
                                                in Long Island Sound. Mar. Ecol. Prog. Ser. 78: 115-              Lavoisier Publishing, Paris. pp. 33-38.
                                                122.







                                          5. LITERATURE CITED
                                                                                                                                                                   61


                                          Douglas, D.J., U.P. Ramsey, J.A. Walter, and J.L.C.            Gentien, P. and G. ArzuL 1990. Exotoxin production
                                             Wright. 1992. Biosynthesis of the neurotoxin                    by Gyrodiniurn cf. aureolum (Dinophyceae). J.
                                             domoic acid by the marine diatom Nitzschia                      Mar. Biol. Ass. U.K. 70:571-581.
                                             pungens forma multiseries, determined with["Cl-             Geraci, J.R., D.M. Anderson, R.J. Timperi, D.J. St.
                                             labelled precursors and nuclear magnetic reso-                  Aubin, G.A. Early, J.H. Prescott, and C.A. Mayo.
                                             nance. J. Chem. Soc. Chem. Commun. 1992:714-                    1989.     Humpback whales               (Megaptera
                                             716.                                                            novaeangliae) fatally poisoned by dinoflagellate
                                          Drum, A.S., T.L. Siebens, E.A. Crecelium., and R.A.                toxin. Can. J. Fish. Aquat. Sci. 46:1895-1898.
                                             Elston. 1993. Domoic acid in the Pacific razor clam         Geyer, W.R. and R.P. Signell. 1992. A reassessment
                                             Sliqua patula (Dixon, 1789). J. Shellfish Res.                  of the role of tidal dispersion in estuaries and
                                             12:443-450.                                                     bays.Estuaries: 15:97-108.
                                          Edvardsen, B., F. Moy, and E. Paasche. 1990.                   Glasgow, H.B., Jr., J.M. Burkholder, D.E. Schmechel,
                                             Hemolytic activity in extracts of Chrysochrornulina             P.A. Tester, and P.A. Rublee. In press. Insidious'
                                             polylepis grown at different levels of selenite and             effects of a toxic dinoflagellate on fish survival
                                             phosphate. In: E. Gran6li, B. Sundstr6m, L. Edler               and human health. J. Toxicol. Environ. Health.
                                             and D.M. Anderson (eds.), Toxic Marine Phy-                 Gran6li, E., E. Paasche, and S.Y. Maestrim. 1993.
                                             toplankton. Elsevier Science Publ., New York. pp.               Three years after the Chrysochromalina polylepis
                                             284-289.                                                        bloom in Scandinavian waters in 1988: some con-
                                          Eppley, R.W., 0. Holm-Hansen, and J.D.H. Strickland.               clusions of recent research and monitoring. In:
                                             1968. Some observations on the vertical migra-                  T.J. Smayda and Y. Shimizu (eds.), Toxic Phy-
                                             tion of dinoflagellates. J, Phycol. 4:333-340.                  toplankton Blooms in the Sea. Elsevier Science
                                          Eppley, R.W., J.N. Rogers, and J.J. McCarthy. 1969.                Publ. B.V., Amsterdam. pp. 23-32.
                                             Half-saturation constants for uptake of nitrate and         Habas, E.J. and C.K. Gilbert. 1974. The economic
                                             ammonium by marine phytoplankton. Limnol.                       effects of the 1971 Florida red tide and the dam-
                                             Oceanogr. 14:912-920.                                           age it presages for future occurrences. Environ.
                                          Erickson, G.M. and L. Nishitani. 1985. The possible                Letters 6:139-147.
                                             relationship of El Nifio/Southern Oscillation events        Hall, S. 1982. Toxins and toxicity of Protogonyaulax
                                             to interannual variation in Gonyaulax populations               from the northeast Pacific. Ph.D. Thesis, Univ. of
                                             as shown by records of shellfish toxicity,. In: W. S.           Alaska, Fairbanks. 196 pp.
                                             Wooster and D.L. Fluharty (eds.), El Nifto North.           Hall, S., G. Strichartz, E. Moczydlowski, A.
                                             Niho Effects in the Eastern Subarctic Pacific Ocean.            Ravindran, and P.B. Reichardt. 1990. The saxitox-
                                             Washington Sea Grant Program, University of                     ins: sources, chemistry, and pharmacology. In: S.
                                             Washington, Seattle. pp. 283-290.                               Hall and G. Strichartz (eds.), Marine Toxins: Ori-
                                          Falconer, I.R. (ed.) 1993. Algal Toxins iri Seafood and            gin, Structure, and Molecular Pharmacology.
                                             Drinking Water. Academic Press, London. 224 pp.                 American Chemical Society Symposium Series No.
                                          Falkowski, P.G., T.S. Hopkins, and J.J. Walsh, 1980.               418. Washington, D.C. pp. 29-65.
                                             An analysis of factors affecting oxygen depletion           Hallegraeff, G.M. 1993. A review of harmful algal
                                             in the New York Bight. J. Mar. Res. 38:479-506.                 blooms and their apparent global increase.
                                          Fiedler, P.C. 1982. Zooplankton avoidance and re-                  Phycologia 32:79-99.
                                             duced grazing responses to Gymnodinium                      Hayhome, B.A., D.M. Anderson, D.M. Kulis, and D.J.
                                             splendens (Dinophyceae). Limnol. Oceanogr.                      Whitten. 1989. Variation among congeneric di-
                                             27:961-965.                                                     noflagellates from the northeastern United States
                                          Fraga, S., D.M. Anderson, 1. Bravo, B. Reguera, K.A.               and Canada. 1. Enzyme electrophoresis. Mar. Biol.
                                             Steidinger, and C.M. Yentsch. 1988. Influence of                101:427-435.
                                             upwelling relaxation on dinoflagellates and shell-          Haywood, G.J., and M.W. Silver. 1994. The concen-
                                             fish toxicity in Ria de Vigo, Spain. Estuar. Coast.             tration of domoic acid by zooplankton. Abstract.
                                             Shelf Sci. 27:349-361.                                          EOS 75:89.
                                          Franks, P.J.S. 1992. Sink or swim: accumulation of             Holmes, R.W., P.M, Williams, and R.W. Eppley. 1967.
                                             biomass at fronts. Mar. Ecol. Prog. Ser. 82:1-12.               Red water in La Jolla bay, 1964-1966. Limnol.
                                          Franks, P.J.S. and D.M. Anderson. 1992a. Alongshore                Oceanogr. 12:503-512.
                                             transport of a toxic phytoplankton bloom in a               Horner R.A., J.R. Postel, and J.E. Rensel. 1991. Nox-
                                             buoyancy current: Alexandrium tarnarense in the                 ious phytoplankton blooms and marine salmon
                                             Gulf of Maine. Mar. Biol. 112:153-164.                          culture in Puget Sound, Washington. In: J.R.
                                          Franks, P.J.S. and D.M. Anderson. 1992b. Toxic phy-                Forbes (ed.), Pacific Coast Research on Toxic
                                             toplankton blooms in the southwestern Gulf of                   Marine Algae. Can. Tech. Rep. H@ydrogr. Ocean Sci.
                                             Maine: testing hypotheses of physical control us-               135:59-61.
                                             ing historical data. Mar. Biol. 112:165-174.                Horner, R.A., M.B. Kusske, B.P. Moynihan, R.N. Skin-
                                          Fritz L., M.A. Quilliam, J.A. Walter, J.C.L. Wright,               ner, and J.C. Wekell. 1993. Retention of domoic
                                             A.M. Beale, and T.M. Work. 1992. An outbreak of                 acid by Pacific razor clams, Sliqua patula (Dixon,
                                             domoic acid poisoning attributed to the pennate                 1789): preliminary study. J. Shellfish Res. 12:451-
                                             diatom Pseudonitzschia australis. J. Phycol.28:439-             456.
                                             442.                                                        Huntley, M. 1982. Yellow water in La Jolla Bay, Cali-
                                          Fulton, R.S. and H.W. Paerl. 1987. Toxic and inhibi-               fornia, July 1980. 11. Suppression of zooplankton
                                             tory effects of the blue-green alga Microcystis                 grazing. J. Exp. Mar. Biol. Ecol. 63:81-91.
                                             aeruginosa on herbivorous zooplankton. J. Plank-            Huntley, M., P. Sykes, S. Rohan, and V. Marin. 1986.
                                             ton Res. 9: 837-855.                                            Chemically-mediated rejection of prey by the cope-
                                          Garrison D.L., S.M. Conrad, P.P. Eilers, and E.M.                  pods Calanus paciftcus and Paracalanus parvus:
                                             Waldron. 1992. Confirmation of domoic acid pro-                 mechanism, occurrence and significance. Mar.
                                             duction     by     Pseudonitzschia         australis            Ecol. Prog. Ser. 28:105-120.
                                             (Bacillariophyceae) cultures. J. Phycol. 28:604-            Kahn, J. and M. Rochel. 1988. Measuring the eco-
                                             607.                                                            nomic effects of brown tides. J. Shellfish Res.
                                                                                                             7:677-682.








                                            5. LITERATURE CITED
           621

                                            Kamykowski, D. 1974. Possible interactions between                 Matter, A.L. 1994. Paralytic shellfish poisoning: toxin
                                                phytoplankton and semidiurnal internal tides. J.                  accumulation in the marine food-web, with em-
                                                Mar. Res. 32:67-89.                                               phasis on predatory snails. Puget Sound Estuary
                                            Kamykowski, D. 1979. The growth response of a                         Program, U.S. EPA 190/R-94-005. 44 pp.
                                                model Gymnodinium splendens in stationary and                  Meyers, T.R., T.M. Koeneman, C. Botelho, and S.
                                                wavy water columns. Mar. Biol. 50:289-303.                        Short. 1987. Bitter crab disease: a fatal dinoflagel-
                                            Kamykowski, D. 1981. The simulation of a southern                     late infection and marketing problem for Alaskan
                                                California red tide using characteristics of a si-                Tanner crabs, Chionoecetes baiTdi. Dis. Aquat. Org.
                                                multaneously-measured internal wave field. Ecol.                  3:195-216.
                                                Model. 12:253-265.                                             Millie, D.F., Baker, M.C., Tlicker, C.S., Vinyard, B.T.
                                            Karnykowski, D. 1995. Trajectories of autotrophic ma-                 and Dionigi, C.P. 1992. High resolution, airborne
                                                rine dinoflagellates. Journal of Phycology 31:200-                remote-sensing of bloom forming phytoplankton.
                                                208.                                                              J. Phycol. 28:281-290.
                                            Keafer, B.A., and D.M. Anderson. 1993. Use of re-                  Milligan, K.L.D.and Cosper, E.M. 1994. Isolation of
                                                motely-sensed sea surface temperatures in stud-                   virus capable of lysing the brown tide microalga,
                                                ies of Alexandriura tamarense bloom dynamics.                     Aureococcus anophagefferens. Science 266:805-
                                                In: T.J. Smayda and Y. Shimizu (eds.), Toxic Phy-                 807.
                                                toplankton Blooms in the Sea. Elsevier Science                 Montagna, P.A., D.A. Stockwell, and R.D. Kalke.
                                                Publ. B.V., Amsterdam. pp. 763-768.                               1993. Dwarf surfclam Malinia lateralis (Say, 1822)
                                            Kodama, M., T. Ogata, and S. Sato. 1988. Bacterial                    populations and feeding during the Texas brown
                                                production of saxitoxin. Agric. Biol. Chem.                       tide event. J. Shellfish Research 12:433-442.
                                                52:1075-1077.                                                  Morejohn G.V., J.T Harvey, and L.T. Krasnow. 1978.
                                            Lam, C.WY and K.C. Ho. 1989. Red tides in Tolo                        The importance of Loligo opalescens in the food-
                                                Harbour, Hong Kong. in: T. Okaichi, D.M. Ander-                   web of marine invertebrates in Monterey Bay, Cali-
                                                son, and T. Nemoto (eds.), Red Tides: Biology,                    fornia. Calif. Dept. Fish Game, Fish. Bulletin.
                                                Environmental Science and Toxicology. Elsevier,                   169:67-98.
                                                New York. pp, 49-52.                                           Murakawa, M. 1987. Marine Pollution and counter-
                                            Landsberg, J.H., K.A. Steidinger, and B.A. Blakesley.                 measures in Japan. Oceanus 30:SS-60.
                                                1995. Fish-killing dinoflagellates in a tropical ma-           Neve, R.A. and P.B. Reichardt. 1984. Alaska's shell-
                                                rine aquarium. In: P. Lassus, G. Arzul, E. Erard-                 fish industry,. In: E.P. Ragelis (ed.) Seafood Tox-
                                                Le Derm, P. Gentien, C. Marcaillou-Le Baut (eds.),                ins. American Chemical Society Symposium Se-
                                                Harmful Marine Algal Blooms. Lavoisier Publish-                   ries 262. Washington, D.C. pp. 53-58.
                                                ing, Paris. pp. 65-70.                                         Nishitani, L. and K. Chew. 1988. PSP toxins in the
                                            Lange, C.B., F.M.H. Reid, and M. Vernet. 1994. Tem-                   Pacific coastal states: monitoring programs and
                                                poral distributions of the potentially toxic diatom               effects on bivalve industries. J. Shellfish Res.
                                                Pseudonitzschia australis at a coastal site in south-             7:653-669.
                                                ern California. Mar. Ecol. Prog. Ser. 104:309-312.             Noga, E.J., L.  Khoo, J.B. Stevens, Z. Fan, and J.M.
                                            Langlois, G.W., K.W Kizer, P. Smith, K. Hansgen,                      Burkholder. In press. Novel toxic dinoflagellate
                                                and R. Howell. 1993. Preliminary results of the                   causes epidemic disease in estuarine fish. Mar.
                                                California phytoplankton monitoring program. In:                  Poll. Bull.
                                                Abstracts, Sixth International Conference on Toxic             Okaichi, T. 1989. Red tide problems in the Seto in-
                                                Marine Phytoplankton, Nantes, France, October                     land Sea, Japan. In: T. Okaichi, D.M. Anderson,
                                                18-22, 1993. p. 119.                                              and T. Nemoto (eds.), Red tides: Biology, Envi-
                                            LaPointe, B.E. and J.D. O'Connell. 1989. Nutrient-                    ronmental Science, and Toxicology. Elsevier, New
                                                enhanced growth of Cladophora prolifera in                        York. pp. 137-142.
                                                Harrington Sound, Bermuda: eutrophication of a                 Okubo, A. 1971. Oceanic diffusion diagrams. Deep-
                                                confined, phosphorus-limited marine ecosystem.                    Sea Res. 18:789-802.
                                                Estuar. Coast. Shelf Sci. 28:347-360.                          Orellana, M.V, and M.J. Perry. 1992. An immunoprobe
                                            LaPointe, B.E., D.A. Tomasko, and WR, Matzie. 1994.                   to measure Rubisco concentrations and maximal
                                                Eutrophication and trophic state classification of                photosynthetic rates of individual phytoplankton
                                                seagrass communities in the Florida Keys. Bull.                   cells. Limnol.Oceanogr. 37:478-490.
                                                Mar. Sci. 54:696-717.                                          Oshima, Y., Sugino, K., Yasumoto, T. 1989. Latest
                                            Lewis, R.J. and M.J. Holmes. 1993. Origin and trans-                  advances in HPLC analysis of paralytic shellfish
                                                fer of toxins involved in ciguatera. Comp.                        toxins. In: S. Natori, K. Hashimoto,and Y. Ueno
                                                Biochem. Physiol. 106C:615-628.                                   (eds.) Mycotoxins and Phycotoxins. Elsevier,
                                            Lin, S., Chang, J. and E. J. Carpenter. 1994. Detec-                  Amsterdam. pp. 319-326
                                                tion of proliferating cell nuclear antigen analog in           Paerl, H.W 1988a. Nuisance phytoplankton blooms
                                                four species of marine phytoplankton                              in coastal, estuarine and inland waters. Limnol.
                                                J.Phycol.30: 449-456.                                             Oceanogr. 33:823-847.
                                            Love, D.C., S.D. Rice, D.A. Moles, and WD. Eaton.                  Paerl, H.W. 1988b. Growth and reproductive strate-
                                                1993. Seasonal prevalence and intensity of bitter                 gies of freshwater blue- green algae
                                                crab dinoflageltate infection and host mortality                  (Cyanobacteria),. In: C.D. Sandgren (ed.), Growth
                                                in Alaskan Tanner crabs Chionoecetes bairdi from                  and Reproductive Strategies of Freshwater Phy-
                                                Auke Bay, Alaska, USA. Dis. Aquat. Org. 15:1-7.                   toplankton. Cambridge University Press, Cam-
                                            Maclean, J.L. 1989. Indo-Pacific red tides, 1985-1988.                bridge. pp. 261-315.
                                                Marine Pollution Bulletin 20:304-310.                          Paerl, H.W. 1990. Physiological ecology and regula-
                                            Maranda, L., D.M. Anderson, and Y. Shimizu. 1985.                     tion of N fixation in natural waters. Adv. Micro-
                                                Comparison of toxicity between populations of                     bial Ecol'11:305-344.
                                                Gonyaulax tarnarensis of eastern North American
                                                waters. Estuar. Coast. Shelf Sci. 21:401-410.
                                            Martin, P. 1985. Simulation of the mixed layer at OWS
                                                November and Papa with several models. J.
                                                Geophys. Res. 90:903-916.







                                         5. LITERATURE CITED
                                                                                                                                                                63


                                         Peterson, C.H. and H.C. Surnmerson. 1992. Basin-              Shurnway, S.E. (ed.). 1988. Toxic algal blooms: haz-
                                            scale coherence of population dynamics of an                   ards to shellfish industry. J. Shellfish Res. 7:587-
                                            exploited marine invertebrate, the bay scallop:                705@
                                            implications of recruitment limitation. Mar. Ecol.         Shurnway, S.E. 1990. A review of the effects of algal
                                            Prog.'Ser. 90:257-272.                                         blooms on shellfish and aquaculture. J. World
                                         Pollingher, U. and E. Zemet. 1981. In situ and experi-            Aquacult. Soc. 21:65-104.
                                            mental evidence of the influence of turbulence             Shurnway, S., S. Sherman-Caswell, and J. Hurst. 1988.
                                            on cell division processes of Peridinium cinctum               Paralytic shellfish poisoning in Maine: monitor-
                                            forma ivestii (Lemm.) Lefevre. Br. Phycol. J.                  ing a monster. J. Shellfish Res. 7:643-652.
                                            16:281-287.                                                Sieburth, J. M., P.W. Johnson and P.E. Hargraves.
                                         Porter, K.G. and J.D. Orcutt Jr. 1980. Nutritional ad-            1988. Ultrastructure and ecology of Aureococcus
                                            equacy, manageability, and toxicity as factors that            anophagefferens gen. et sp. nov. (Chrysophyceae):
                                            determine food quality of green and blue-green                 the dominant picoplankter during a bloom in
                                            algae for Daphnia. In WE. Kerfoot (ed.), Evolu-                Narragansett Bay, Rhode Island, summer 1985. J.
                                            tion of Zooplankton Communities. University                    Phycol. 24:416-425.
                                            Press of New England, Hanover. pp. 268-281.                Silberstein, K., A.W. Chiffings, and A.J. McComb.
                                         Prandle, D. 1991. A new view of near-shore dynam-                 1986. The loss of seagrass in Cockburn Sound,
                                            ics based on observations from HF radar. Prog.                 Western Australia. III. The effect'of epiphytes on
                                            Oceanogr. 27:403-438.                                          productivity of Posidonia australis Hook. F. Aquat.
                                         Pratt, D.M. 1966. Competition between Skeletonema                 Bot. 24:355-371.
                                            costaturn and Olisthodiscus luteus in Narragansett         Smayda, T.J. 1990. Novel and nuisance phytoplank-
                                            Bay and in culture. Limnol. Oceanogr. 11:447-45 S.             ton blooms in the sea: evidence for a global epi-
                                         Price, D.W, K.W, Kizer, and K.H Hansgen. 1991.                    demic. In: E. Gran6li, B. Sundstr6m, L. Edler, and
                                            California's paralytic shellfish poisoning preven-             D.M. Anderson. (eds.), Toxic Marine Phytoplank-
                                            tion program, 1927-89. J. Shellfish Res. 10:119-               ton. Elsevier, New York. pp. 29-40.
                                            145.                                                       Smayda, T.J. 1992. Global epidemic of noxious phy-
                                         Radach, G., J. Berg, and F. Hagmeier. 1990. Long-                 tOpIdnkton blooms and food chain consequences
                                            term changes of the annual cycles of meteoro-                  in large ecosystems. In: K. Sherman, L.M.
                                            logical, hydrographic, nutrient and phytoplank-                Alexander, and B.D. Gold (eds.), Food Chains,
                                            ton time series at Helgoland and at IV ELBE I in               Models and Management of Large Marine Ecosys-
                                            the German Bight. Cont. Shelf Res. 10:305-328.                 tems. Westview Press, San Francisco. pp. 275-307.
                                         Rensel, J.E. 1993. Factors controlling paralytic shell-       Smith, J.C., P. Odense, R Angus, S. Bates, C.J. Bird,
                                            fish poisoning (PSP) in Puget Sound, Washing-                  P. Cormier, A.S.W. deFreitas, C. L6ger, D. O'Neil,
                                            ton. J. Shellfish Res. 12:371-376.                             K. Pauley, and J. Worms. 1990. Variation in domoic
                                         Rensel, J.E. and E.F. Prentice. 1980. Factors control-            acid levels in Nitzschia species: implications for
                                            ling growth and survival of cultured spot prawn,               monitoring programs. Bull Aquacult. Ass. Can.
                                            Pandalus platyceros, in Puget Sound, Washing-                  90:27-31.
                                            ton. Fish. Bull. 78:781-788.                               Smith, S.A., E.J. Noga, and R.A. Bullis. 1989. Mor-
                                         Rensel, J.E., R.A. Horner, and J.R. Postel. 1989. Ef-             tality in Tilapia aurea due to a toxic dinoflagel-
                                            fects of phytoplankton blooms on salmon aquac-                 late bloom. Proc. 3rd Int. Colloquium Path. Mar.
                                            ulture in Puget Sound, Washington: initial re-                 Aquaculture 167-168.
                                            search. Northw. Environ. J. 5:53-69.                       Steidinger, K.A. and G.A. Vargo. 1988. Marine di-
                                         Reynolds, C.S. and A.E. Walsby. 1975. Water blooms.               noflagellate blooms: dynamics and impacts. In
                                            Biol. Rev. 50:437- 481.                                        C.A. Lembi and J. R. Waaland (eds.), Algae and
                                         Robineau B., G.L. Fortier and A.D. Cembella. 1991.                Human Affairs. Cambridge University Press, New
                                            Poteniial impact of a toxic dinoflagellate                     York. pp. 373-401. .
                                            (Alexandrium excavaturn) bloom on survival of              Steidinger, K.A., E.W. Truby, J.K. Garrett, and J.M.
                                            fish and crustacean larvae. Mar. Biol. 198:293-301.            Burkholder. 1995. The morphology and cytology
                                         Sako, Y., N. Naya, T. Yoshida, C.H. Kim, A. Uchida,               of a newly discovered toxic dinoflagellate. In: P.
                                            and Y. Ishida. 1995. Studies on stability and he-              Lassus, G. Arzul, E. Erard-De Denn, P. Gentien, C.
                                            redity of PSP toxin composition in the toxic di-               Marcaillou-Le Baut (eds.), Harmful Marine Algal
                                            noflagellate Alexandriurn. In: P. Lassus, G. Arzul,            Blooms. Lavoisier Publishing, Paris. pp. 83-88.
                                            E. Erard-Le Derm, P. Gentien, and C. Marcaillou-           Steidinger, K.A., J.M. Burkholder, H.B. Glasgow, Jr.,
                                            Le Baut (eds.), Harmful Marine Algal Blooms.                   C.W. Hobbs, JX Garrett, E.W Truby, E.J. Noga,
                                            Lavoisier Publishing, Paris. pp. 401-406.                      and S.A. Smith. Submitted. Pflesteria piscicida,
                                         Sand-Jensen, K. 1977. Effect of epiphytes on eelgrass             gen. et sp. nov, (Pfiesteriaceae, fam. nov.), a new
                                            photosynthesis. Aquat. Bot. 3:55-63.                           toxic dinoflagellate with a complex life cycle and
                                         Sanders, R.W, and K. G. Porter. 1988. Phagotrophic                behavior. J. Phycol.
                                            phytoflagellates. In: K. Marshall (ed.), Advances          Surnmerson, H.C. and C.H. Peterson. 1990. Recruit-
                                            in Microbial Ecology 10. Plenum Press, New York.               ment failure of the bay scallop, Argopecten
                                            pp. 167-192.                                                   irradians concentricus, during the first red tide,
                                                                                                           Ptychodiscus brevis, outbreak recorded in North
                                         Seliger, H. H., J. H. Carpenter, M. Loftus, and W. D.             Carolina. Estuaries 13:322-331.
                                            McElroy. 1970. Mechanism for the accumulations
                                            of high concentrations of dinoflagellates in a bi-         Swanson, R.I. and C.J. Sindermann (eds.). 1979. Oxy-
                                            oluminescent bay. Limnol. Oceanogr. 15: 234-245.               gen depletion and associated benthic mortalities
                                                                                                           in New York Bight, 1976. NOAA Professional Pa-
                                         Shimizu, Y. 1993. Microalgal metabolites. Chemical                per 11. Rockville, MD. 345 pp.
                                            Reviews. 93: 1685-1698.                                    Sykes, P. A. and M. E. Huntley. 1987. Acute physi-
                                         Shimizu, Y., Norte, M., Hori, A., Genenah, A., and                ological reactions of Calanus pacificas to selected
                                            Kobayashi, M. 1984. Biosynthesis of saxitoxin ana-             dinoflagellates: direct observations. Mar. Biol.
                                            logues: the unexpected pathway. J. Am. Chem.                   94:19-24.
                                            Soc. 106: 6433-6434.








                                           S. LITERATURF CITED
           641

                                           Taylor, F.J.R. 1993. Current problems with harmful             Wall, D. 1971, Biological problems concerning
                                              phytoplankton blooms in British Columbia wa-                    fossilizable dinoflagellates. Geoscience and Man.
                                              ters. In: T.J. Smayda and Y. Shimizu (eds.), Toxic              3:1-15.
                                              Phytoplankton Blooms in the Sea. Elsevier Sci-              Walz, P.M., D.L. Garrison, W.M. Graham, M.A.
                                              ence Publ. BX, Amsterdam. pp. 699-703.                          Cattey, R.S. Theerdema, and M.W. Silver. 1994.
                                           Taylor, F.J.R. and R.A. Horner. 1994. Red tides and                Domoic acid producing diatom blooms in
                                              other problems with harmful algal blooms in Pa-                 Monterey Bay, California: 1991-1993. Natural Tox-
                                              cific Northwest coastal waters. In: R.C.H. Wilson,              ins 2:271-279.
                                              R.J. Beamish, F. Aitkens, and J. Bell (eds.), Re-           Watras, C.J., S.W. Chisholm, and D.M. Anderson.
                                              view of the marine environment and biota of Strait              1982. Regulation of growth in an estuarine clone
                                              of Georgia, Puget Sound, and Juan de Fuca Strait:               of Gonyaulax tamarensis Lebour: salinity-depen-
                                              Proceedings of the BC/Washington Symposium                      dent temperature responses. J. Exp.. Mar. Biol.
                                              on the Marine Environment, Jan 13 & 14, 1994.                   Ecol. 62:25-37.
                                              Can. Tech. Rep. Fish. Aquat. Sci. 1948:175-185.             White, A.W. 1981. Marine zooplankton can accumu-
                                           Taylor, F.J.R. and U. Pollingher. 1987, Ecology of Di-             late and retain dinoflagellate toxins and cause fish
                                              noflagellates. In: F.J.R. Taylor (ed.), The Biology             kills. Limnol. Oceanogr. 26:103-109.
                                              of Dinoflagellates. Blackwell Scientific Publ., Ox-         Whitledge, T.E. 1993. The nutrient and hydrographic
                                              ford. pp. 398-529.                                              conditions prevailing in Laguna Madre, Texas be-
                                           Tester, P.A., M.E. Geesey, and F.M. Vukovich. 1993.                fore and during a brown tide bloom. In: T.J.
                                              Gymnodinium breve and global warming: What                      Smayda and Y. Shimizu (eds.), Toxic Phytoplank-
                                              are the possibilities? In T.J. Smayda and Y.                    ton Blooms in the Sea, Elsevier Science Publ. B.
                                              Shimizu (eds.), Toxic Phytoplankton Blooms in                   V., Amsterdam. pp. 711-716.
                                              the Sea. Elsevier Science Publ. B. V., Amsterdam.           Work, T.M., A.M. Beale, L. Fritz, M.A. Quilliam, M.W
                                              pp. 67-72.                                                      Silver, K.R. Buck, and J.L.C. Wright. 1993. Domoic
                                           Tester, P.A., R.P. Stumpf, F.M. Vukovich, P.K. Fowler,             acid intoxication of brown pelicans and cormo-
                                              and J.T. Tbrner. 1991. An expatriate red tide bloom:            rants in Santa Cruz, California. In: T.J. Smayda
                                              transport, distribution, and persistence. Limnol.               and Y. Shimizu (eds), Toxic Phytoplankton Blooms
                                              Oceanogr. 36:1053-1061.                                         in the Sea. Elsevier Science Publ. BX, Amsterdam.
                                           Therriault, J.C., J. Painchaud, and M. Levasseur.                  pp. 643-649.
                                              1985. ontrolling the occurrence of Protogonyaulax           Yang, C.Z., A.M. Yousif, T. Perkins, and L.J. Albright.
                                              tarnarensis and shellfish toxicity in the St.                   1993. The mode of action of the toxic phytoplank-
                                              Lawrence estuary: Freshwater runoff and the sta-                ter, Heterosigma akashiwo on juvenile sockeye
                                              bility of the water column. pp. 141-146 In: D. M.               salmon (Oncorhynchus nerka). In: Abstracts, Sixth
                                              Anderson, A.W. White and D. G. Baden (eds.)                     International Conference on Toxic Marine Phy-
                                              Toxic Dinoflagellates, Elsevier, New York.                      toplankton, Nantes, France, October 18-22, 1993.
                                           Thomas, W.H. and C.H. Gibson. 1990. Quantified                     p. 277.
                                              small-scale turbulence inhibits a red tide di-              Yasumoto, T., 1. Nakajima, E. Chunque, and R.
                                              noflagellate Gonyaulax polyedra Stein. Deep-Sea                 Adachi. 1977. Finding of a dinoflagellate as a likely
                                              Res. 37:1583-1593.                                              culprit of ciguatera. Bull. Jpn. Soc. Sci. Fish.
                                           Tomas, C. R. 1980. Olisthodiscus luteas                            43:1021-1026.
                                              (Chrysophyceae). V. Its occurrence, abundance               Yentsch, C.M., B. Dale, and J.W, Hurst. 1978. Coex-
                                              and dynamics in Narragansett Bay, Rhode Island.                 istence of toxic and non-toxic dinoflagellates re-
                                              J. Phycol. 16:157-166.                                          sembling Gonyaulax tamarensis in New England
                                           Tracey, G.A. 1988. Feeding reduction, reproductive                 coastal waters (N.W. Atlantic). J. Phycol. 14:330-
                                              failure, and mortality in Mytilus edulis during the             332.
                                              1985 "brown tide" in Narragansett Bay, Rhode                Young, W.R., P.B. Rhines, and C.J.R. Garrett. 1982.
                                              Island. Mar. Ecol. Prog. Ser.-50:73-81.                         Shear-flow dispersion, internal waves and hori-
                                           Trainer, V. L. and Baden, D. G. 1991. An enzyme                    zontal mixing in the ocean. J. Phys. Oceanogr.
                                              immunnassay for the detection of Florida red tide               12:515-527.
                                              brevetoxins. Toxicon 29:1387-1394.                          Zimmerman, J.T.F., 1986. The tidal whirlpool: A re-
                                           Twarog, B.M., T. Hidaka, and H. Yamaguchi. 1972.                   view of horizontal dispersion by tidal and residual
                                              Resistance of tetrodotoxin and saxitoxin in nerves              currents. Netherlands J. Sea Res. 20:133-lS4.
                                              of bivalve molluscs. Toxicon 10:273-278.
                                           Twilley, R.R., W.M. Kemp, K.W. Staver, J.C.
                                              Stevenson, and W.R. Boynton. 1985. Nutrient
                                              enrichment of estuarine submerged vascular plant
                                              communities: 1. Algal growth and effects on pro-
                                              duction of plants and associated communities.
                                              Mar. Ecol. Prog. Ser. 23:179-191.
                                           Tyler, M. A. and H. H. Seliger. 1978. Annual subsur-
                                              face transport of a red tide dinoflagellate to its
                                              bloom area: water circulation patterns and organ-
                                              ism distributions in the Chesapeake Bay. Limnol.
                                              Oceanogr. 23: 227-246.
                                           Tyler, M.A. and H.H. Seliger. 1981. Selection for a
                                              red tide organism: physiological responses to the
                                              physical environment. Limnol. Oceanogr. 26:310-
                                              324,
                                           Villac, M.C., D.L. Roelke, F.P. Chavez, L.A. Cifuentes,
                                              and G.A. Fryxell. 1993. Pseudonitzschia australis
                                              Frenguelli and related species from the west coast
                                              of the U.S.A.: occurrence and domoic acid pro-
                                              duction. J. Shellfish Res. 12:4S7-46S.








                                       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.














                                                                     t















                                                                     Al




                                                                                                                                                          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.