global ecology and oceanography of harmful algal blooms ... · as a result of the havreholm meeting...

GEOHAB

Global Ecology and Oceanographyof Harmful Algal Blooms

Science Plan

An International Programme Sponsored by theScientific Committee on Oceanic Research (SCOR) and theIntergovernmental Oceanographic Commission (UNESCO)

Edited by: Patricia M. Glibert and Grant Pitcher

With the assistance of: Allan Cembella, John Cullen, and Yasuwo Fukuyo

Based on contributions by the GEOHAB Scientific Steering Committee:Patrick Gentien, Yasuwo Fukuyo, Donald M. Anderson, Susan Blackburn, Allan Cembella,John Cullen, Malte Elbrächter, Henrik Enevoldsen, Marta Estrada, Wolfgang Fennel,Patricia M. Glibert, Elizabeth Gross, Kaisa Kononen, Nestor Lagos, Thomas Osborn,Grant Pitcher, Arturo P. Sierra-Beltrán, Steve Thorpe, Edward R. Urban, Jr., Jing Zhang,and Adriana Zingone

April 2001

This report may be cited as: GEOHAB, 2001. Global Ecology and Oceanography of Harmful Algal Blooms,Science Plan. P. Glibert and G. Pitcher (eds). SCOR and IOC, Baltimore and Paris. 87 pp.

Science Plan

This document describes a Science Plan reviewed and approved by the Scientific Commission on OceanicResearch (SCOR) and the Intergovernmental Oceanographic Commission (IOC) of the U.N. Education,Scientific, and Cultural Organisation (UNESCO)

Copyright © 2001 SCOR and IOC.Published by SCOR and IOC, Baltimore and Paris, 2001.

Edward R. Urban, Jr.Executive Director, SCORDepartment of Earth and Planetary SciencesThe Johns Hopkins UniversityBaltimore, MD 21218 U.S.A.Tel: +1-410-516-4070Fax: +1-410-516-4019E-mail: [email protected]

This document is GEOHAB Report #1. Copies may be obtained from:

Henrik EnevoldsenProject CoordinatorIOC Science and Communication Centre onHarmful AlgaeBotanical Institute, University of CopenhagenØster Farimagsgade 2DDK-1353 Copenhagen K, DenmarkTel: +45 33 13 44 46Fax: +45 33 13 44 47E-mail: [email protected]

This report is also available on the web at:http://www.jhu.edu/~scorhttp://ioc.unesco.org/hab

Cover photos. Examples of causative organisms of harmful algal blooms, their impacts, and newapproaches that are required to understand their population dynamics. Upper left hand panel - vegetativecells of Ceratium furca, Prorocentrum micans, and Gymnodinium catenatum. Upper right hand photo -surface accumulation of Trichodesmium off the Great Barrier Reef, Australia. Lower left hand panel -fish kill caused by P. micans and C. furca on the west coast of South Africa. Lower right hand panel -remote observing system for continuous monitoring. Photos by Y. Fukuyo, P. Glibert, and W. Boicourt.

Back cover. Representative HAB species (upper photos), and mass mortality event by a red tide ofCochlodinium polykrikoides. Photos by Y. Fukuyo.

http://www.jhu.edu/~scor

http://ioc.unesco.org/hab

PREFACE ....................................................................................................................................... i

EXECUTIVE SUMMARY ......................................................................................................... iii

INTRODUCTION: The Global Problem of Harmful Algal Blooms ............................................. 1The Nature of HABs ................................................................................................................ 1Consequences of HABs ........................................................................................................... 2The Apparent Global Increase of HABs .................................................................................. 6

AN INTERNATIONAL PROGRAMME ON GEOHAB .............................................................. 8Emergence of the GEOHAB Programme ................................................................................ 8The GEOHAB Mission ............................................................................................................ 9The GEOHAB Goal ................................................................................................................. 9The GEOHAB Strategy: A Comparative Approach ................................................................ 9Organisation and Priorities of the GEOHAB Programme ..................................................... 13Links Between GEOHAB and Other International Activities ................................................ 14The Benefits of GEOHAB ..................................................................................................... 15

PROGRAMME ELEMENT 1: BIODIVERSITY AND BIOGEOGRAPHY ............................. 16Introduction............................................................................................................................ 16Overall Objective ................................................................................................................... 18The Strategy ........................................................................................................................... 18Specific Objective 1 ............................................................................................................... 18Specific Objective 2 ............................................................................................................... 22Specific Objective 3 ............................................................................................................... 24Outputs................................................................................................................................... 25

PROGRAMME ELEMENT 2: NUTRIENTS AND EUTROPHICATION ................................ 26Introduction............................................................................................................................ 26Overall Objective ................................................................................................................... 28The Strategy ........................................................................................................................... 28Specific Objective 1 ............................................................................................................... 29Specific Objective 2 ............................................................................................................... 31Specific Objective 3 ............................................................................................................... 33Specific Objective 4 ............................................................................................................... 34Outputs................................................................................................................................... 35

TABLE OF CONTENTS

GEOHAB

Global Ecology and Oceanography of Harmful Algal BloomsScience Plan

PROGRAMME ELEMENT 3: ADAPTIVE STRATEGIES....................................................... 36Introduction............................................................................................................................ 36Overall Objective ................................................................................................................... 37The Strategy ........................................................................................................................... 37Specific Objective 1 ............................................................................................................... 37Specific Objective 2 ............................................................................................................... 40Specific Objective 3 ............................................................................................................... 42Specific Objective 4 ............................................................................................................... 44Outputs................................................................................................................................... 45

PROGRAMME ELEMENT 4: COMPARATIVE ECOSYSTEMS ............................................ 46Introduction............................................................................................................................ 46Overall Objective ................................................................................................................... 46The Strategy ........................................................................................................................... 46Specific Objective 1 ............................................................................................................... 49Specific Objective 2 ............................................................................................................... 50Specific Objective 3 ............................................................................................................... 53Specific Objective 4 ............................................................................................................... 55Outputs................................................................................................................................... 56

PROGRAMME ELEMENT 5: OBSERVATION, MODELLING, AND PREDICTION ........... 58Introduction............................................................................................................................ 58Overall Objective ................................................................................................................... 58The Strategy ........................................................................................................................... 58Specific Objective 1 ............................................................................................................... 59Specific Objective 2 ............................................................................................................... 62Specific Objective 3 ............................................................................................................... 64Specific Objective 4 ............................................................................................................... 65Specific Objective 5 ............................................................................................................... 66Outputs................................................................................................................................... 67

LINKAGES AMONG PROGRAMME ELEMENTS ................................................................. 68

REFERENCES ............................................................................................................................ 70

GEOHAB SCIENTIFIC STEERING COMMITTEE ................................................................. 84

iPREFACE

The last two decades have been marked by a new appreciation of the serious impacts of the marinephenomena we now call harmful algal blooms (HABs). These occurrences of toxic or harmfulmicroalgae represent a significant and seemingly expanding threat to human health, fishery resources,and marine ecosystems throughout the world. Many causes, both natural and anthropogenic, may beresponsible for this dramatic expansion in HAB effects; it is likely that human activities are makingthe problems worse through increased nutrient inputs to coastal areas, transportation and dischargeof ballast water, and other factors.

Given that HAB problems may be expanding and that they have many causes, both natural andhuman assisted, what can be done about them in a practical sense? What information is needed forefficient management of affected marine ecosystems that simultaneously protects public and ecosystemhealth, encourages and supports aquaculture development, and contributes to policy decisions oncoastal zone issues such as wastewater disposal, aquaculture development, and dredging? Whatresearch and monitoring should be conducted to determine the extent to which human activities aremaking the HAB problem worse and what steps should be taken to minimize further impacts? Theanswers to these important practical questions, of course, require scientific investigation. Singleinvestigators and some national programmes are now conducting research and focused monitoringto answer such questions. To date, however, international co-ordination of individual and nationalresearch efforts has largely been absent.

The clear need for a co-ordinated international scientific programme on the ecology and oceanographyof HABs prompted the Scientific Committee on Oceanic Research (SCOR) and the IntergovernmentalOceanographic Commission (IOC) to form a partnership to develop such a programme. The firststep in this process was an international workshop sponsored by SCOR and IOC, which took placein Havreholm, Denmark on October 13-17, 1998. Thirty-seven scientists from twenty countriesparticipated in the workshop, chaired by Professor John Cullen. That workshop report is availableon the SCOR Website at www.jhu.edu/~scor.

As a result of the Havreholm meeting and report, and emerging activities on harmful algal blooms ina number of nations, SCOR and IOC formed a Scientific Steering Committee (SSC) for a newprogramme on the Global Ecology and Oceanography of Harmful Algal Blooms (GEOHAB). TheGEOHAB SSC worked diligently in 2000 to produce the GEOHAB Science Plan presented here.The plan was reviewed and approved by SCOR at SCOR’s General Meeting in October 2000.

With publication of this Science Plan, the GEOHAB SSC begins a new phase of its activity. Thisdocument will be used as the basis for a detailed plan for carrying out the proposed science over thenext decade. As the SSC develops the GEOHAB Implementation Plan, comments from the broaderinternational community of scientists who study HABs will be solicited. It will also be crucial toinvolve scientists who study other oceanographic factors that affect HABs, such as physical, chemical,and biological conditions in ocean areas where blooms occur. An important aspect of theImplementation Plan will be to describe how national programmes can co-ordinate to meet GEOHABobjectives and to plan for multinational research activities that will transcend national efforts andmake comparative studies possible.

PREFACE

ii PREFACE

We are grateful for the support for this project provided by the Maj and Tor Nessling Foundation(Finland), the U.S. National Aeronautics and Space Administration, the U.S. National Oceanic andAtmospheric Administration, and the U.S. National Science Foundation*. We wish to thank theGEOHAB SSC for their hard work and diligence in completing this Science Plan so quickly. Weparticularly appreciate guidance from Patrick Gentien (SSC Chair) and Yasuwo Fukuyo (SSC Vice-Chair) for guiding the process, and Patricia Glibert for co-ordinating the formatting and printing ofthe Science Plan. SSC members Patricia Glibert, Grant Pitcher, Allan Cembella, John Cullen, andYasuwo Fukuyo formed an editorial team that met several times to refine the report. Mark Trice andJane Hawkey at the Horn Point Laboratory, University of Maryland Center for Environmental Science,and A.P. van Dalsen at Marine and Coastal Management in Cape Town, South Africa, helped theSSC by assisting with graphics and layout of the Science Plan, and their efforts are greatly appreciated.Final thanks are due to Elizabeth Gross, former Executive Director of SCOR for her many efforts onbehalf of GEOHAB and the HAB community.

On behalf of the sponsors:

Henrik Enevoldsen, IOC Edward R. Urban, Jr., SCOR

* This document is based on work partially supported by the U.S. National Science Foundation under Grant No. 0003700.Any opinions, findings, and conclusions or recommendations expressed in this document are those of the authors anddo not necessarily reflect the views of the U.S. National Science Foundation.

iii

EXECUTIVE SUMMARY

Proliferations of algae in marine or brackishwaters can cause massive fish kills,contaminate seafood with toxins, and alterecosystems in ways that humans perceive asharmful. The scientific community refers tothese events with a generic term, “HarmfulAlgal Blooms” (HABs), while recognising thatsome species cause toxic effects even at lowcell densities, and that not all HAB species aretechnically “algae”. A broad classification ofHAB species distinguishes two groups: thetoxin producers, whichcan contaminateseafood or kill fish, andthe high-biomassproducers, which cancause anoxia andi n d i s c r i m i n a t emortalities of marinelife after reachingdense concentrations.Some HAB specieshave characteristics ofboth groups.

Although HABs were present long beforehuman activities began to impact coastalecosystems, a survey of affected regions andof economic losses and human poisoningsthroughout the world demonstrates clearly thatthere has been a dramatic increase in theimpacts of HABs over the last few decades.The HAB problem is now widespread andserious. Harmful effects attributed to HABsextend well beyond impacts on human healthand direct economic losses. When HABscontaminate or destroy coastal resources, thelivelihoods of local residents are threatened andthe sustenance of human populations iscompromised. Clearly, there is a pressing needto develop effective responses to the threat ofHABs through management and mitigation.This requires knowledge of the ecological andoceanographic factors that control the

distributions and population dynamics of HABspecies.

A great deal is known about harmful algae andHABs, but our ability to describe the factorscontrolling the dynamics of individual speciesis limited by critical gaps in understanding thephysiological, behavioural, and morphologicalcharacteristics of algae (including HABspecies), and how these interact withenvironmental conditions to promote the

selection for onespecies over another.

Successful research todate shows that the keyto explaining HABphenomena is toidentify and quantifyspecial adaptations ofHAB species that leadto their selection inp a r t i c u l a rhydrodynamic andecological conditions.

Thus, the central challenge before us is tounderstand the critical features andmechanisms underlying the populationdynamics of HAB species in a variety ofoceanographic regimes. This understandingcan be used as a basis for monitoring andpredicting the occurrence, movement, toxicity,and environmental effects of HABs. In turn,monitoring and prediction are essential formanagement and mitigation of HABs.

Because HAB species are found in marine andbrackish-water ecosystems worldwide, thecentral research problem can be addressedcomprehensively and effectively only throughinternational, interdisciplinary, andcomparative research on the dynamics ofHABs. Progress depends on advancement

EXECUTIVE SUMMARY

The impacts of HABs are numerous, and the effectsmay be felt by many components of the ecosystem.

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through targeted studies and technologicalinnovation in biology, ecology, chemical andphysical oceanography, modelling, and oceanobservation.

The SCOR-IOCProgramme on theGlobal Ecology andOceanography ofHarmful Algal Blooms(GEOHAB) was thusestablished to addressthe need for broad-basedadvancement in theunderstanding of HABs.The scientific goal ofGEOHAB will beapproached byaddressing researchquestions such as:

1. What are the factorsthat determine thechanging distribution ofHAB species, their genetic variability, and thebiodiversity of associated communities?

2. To what extent does increased eutrophicationinfluence the occurrences of HABs and theirharmful effects?

3. What are the unique adaptations of HABspecies and how do they help to explain theirproliferation or harmful effects?

4. To what extent do HAB species, theirpopulation dynamics, and communityinteractions respond similarly undercomparable ecosystem types?

The following Programme Elements have beenidentified as the key areas of research forGEOHAB studies.

Programme Element 1: Biodiversity andBiogeography

Knowledge of the present geographicdistribution of HAB species and of the long-term fluctuations in species composition isessential in explaining novel and recurrentHAB events and the extent to which HABs are

spreading globally.

The overall objective ofthis Programme Elementis to determine therelationships amongdistributions of HABspecies, biodiversity, andenvironmental change.

Programme Element 2:Nutrients andEutrophication

Concurrent withescalating humanactivities in coastalecosystems, theenvironmental andeconomic impacts ofHABs have increased in

recent decades. The relationships betweennutrient loading and increased frequency ofboth algal blooms and toxic algae are not wellknown.

The overall objective of this ProgrammeElement is to determine the significance ofeutrophication and nutrient transformationpathways to HAB population dynamics.

EXECUTIVE SUMMARY

The mission of GEOHAB is to:

Foster international co-operativeresearch on HABs in ecosystem typessharing common features, comparingthe key species involved and theoceanographic processes thatinfluence their population dynamics.

The scientific goal of GEOHAB isto:

Improve prediction of HABs bydetermining the ecological andoceanographic mechanisms underlyingtheir population dynamics, integratingbiological, chemical, and physicalstudies supported by enhancedobservation and modelling systems.

Effects of HABs include the development of highbiomass “red tides”, as shown by this Noctilucabloom in New South Wales, Australia.

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Programme Element 3: Adaptive Strategies

Each species has adaptive characteristics thatdefine its niche, that is, the suite of ecologicalfactors that determine its distribution andactivities. By characterising the adaptations ofdifferent HAB species, it should be possibleto describe patterns of species abundance asfunctions of hydrographic processes, nutrientdistributions, and community interactions.

The overall objective of this ProgrammeElement is to define the particularcharacteristics and adaptations of HABspecies that determine when and where theyoccur and produce harmful effects.

Programme Element 4: ComparativeEcosystems

Critical processes controlling HABs can beidentified by comparing the dynamics ofharmful algae and related species acrossecosystems, grouped according to theirhydrographic and chemical regimes and theirbiology.

The overall objective of this ProgrammeElement is to identify mechanisms underlyingHAB population and community dynamicsacross ecosystem types through comparativestudies.

Programme Element 5: Observation,Modelling, and Prediction

Fundamental research on HABs must beguided by, and validated with, observations ofphytoplankton dynamics in nature. Modellingsupports specific tasks and synthesisesfindings, leading to predictions of HABs.Effective detection and prediction of HABs areneeded to manage and mitigate their effects.

The overall objective of this ProgrammeElement is to improve the detection andprediction of HABs by developing capabilitiesin observation and modelling.

GEOHAB Approach

GEOHAB will foster scientific advancementin the understanding of HABs by encouragingand co-ordinating fundamental scientificresearch – multi-faceted, international, andinterdisciplinary, maintaining an ecological andoceanographic context. International, co-operative research on comparative ecosystemswill be encouraged, as will targeted studies onorganisms, processes, and methods, includingnew observational technologies, that are neededto understand and resolve influences ofenvironmental factors (both natural andanthropogenic) on distributions and trends inHABs. GEOHAB is not a funding programme,but rather a mechanism to facilitate thoseactivities that require co-operation amongnations, such as the development ofmethodologies, and the co-sponsorship ofcruise or research activities.

GEOHAB Benefits

Many benefits will accrue from GEOHAB.Better methodologies will be developed forpredicting HABs, their toxicity, and otherdeleterious effects. A better understanding ofthe physical and environmental mechanismsunderlying a diverse array of HABs will bedeveloped. GEOHAB projects will alsocontribute to improving global observationsystems that are required to resolve influencesof environmental factors (anthropogenic andclimate-related) on distributions and trends inHABs. Strong links between GEOHAB andother international efforts, such as the GlobalOcean Observing System (GOOS) willtherefore be forged. Through additional linksto national and international agenciesresponsible for protecting coastal resources andpublic health, the knowledge gained fromGEOHAB will be used to develop capabilitiesfor more effective management and mitigationof HAB problems.

EXECUTIVE SUMMARY

INTRODUCTION

INTRODUCTION: The Global Problem of Harmful Algal Blooms

The Nature of HABs

Marine planktonic algae form the basis of themarine food chain and, owing to their sheernumber and the huge size of the world ocean,they are responsible for the bulk of globalprimary production. When oceanographicconditions are suitable, they show significantpopulation increases known as blooms.Sometimes proliferations of these microalgaecause fish kills, contaminate seafood withtoxins, cause serious human health problems,or alter ecosystems in other ways that humansperceive as harmful.

The scientific community refers to these eventswith the generic term “Harmful Algal Blooms”(HABs); sometimes they are popularly called“red tides”, but this is a misnomer. The term“Harmful Algal Bloom” is not at all precise,and “algae” and “phytoplankton” are colloquialterms. A wide range of organisms is involved,including dinoflagellates, other flagellates,cyanobacteria, diatoms, and otherphytoplankton. Not all harmful algal eventsinvolve the development of significantaccumulations of biomass. Many HAB speciesare harmful at very low densities. HABs

include events caused by the proliferation ofbenthic microalgae that produce toxinstransferred through the food chain.

A broad classification of HABs distinguishestwo major groups of causative organisms: thosethat produce toxins, which can contaminateseafood or kill fish even when their cell densityis low, and those that do not produce toxins,but which cause other deleterious impacts, e.g.the consumption of oxygen as blooms decay,the production of scums, or the reduction ofhabitat for fish or shellfish.

As with all phytoplankton blooms, theproliferation of harmful algal species resultsfrom a combination of physical, chemical, andbiological mechanisms and interactions, manyof which remain poorly understood. AlthoughHABs are often linked to the increased inputof nutrients to coastal ecosystems as aconsequence of human activities, manyharmful events occur in areas where humanactivities or pollution are not considered to becontributing factors.

Public concern over HAB events is growing,as evidenced by headlines such as these thathave appeared in newspapers throughout theworld.

HABs have been linked to numerous fish killevents. In this 1994 fish kill in St. Helena Bayon the west coast of South Africa, the HABspecies Prorocentrum micans and Ceratiumfurca were the causative organisms. Lowoxygen and the subsequent generation ofhydrogen sulfide were responsible for themortality.

1

Consequences of HABs

Toxic and harmful blooms cause negativeimpacts and economic losses in many parts ofthe world. The consequences and mechanismsof impact of harmful blooms vary dependingon the species involved. Broadly speaking,there are four categories of deleterious effects,including risks to human health, loss of naturalor cultured seafood resources, impairment oftourism and recreational activities, anddamages to non-commercial marine resourcesand wildlife (Table 1). Each species or eventexerts predominantly one type of impact, butmany blooms have negative consequences inmore than one category.

While specific economic losses can beestimated from damage to fisheries oraquaculture, the total economic impact ofHABs is not easily assessed owing to the rangeof sectors of society impacted. Apart fromdirect economic losses associated with humanintoxications, fish kills, loss of market share,and declines in tourism, there are other serioushuman costs associated with the collapse offishing communities, as well as cascadingeconomic effects that are virtually incalculable.Furthermore, data on losses by the seafoodindustry are not always released to the publicand in many cases losses are never wellquantified. When HABs contaminate ordestroy coastal resources, the functioning ofecosystems may be impaired, and thelivelihood and food supply of localcommunities threatened.

Human Health Issues

Of major concern are the marine and brackish-water HAB species that cause public healthimpacts due to the production of toxins. Themost toxic species are recorded amongdinoflagellates, such as Pyrodiniumbahamense var. compressum and severalspecies of the genus Alexandrium, which canhave dramatic effects at barely detectableconcentrations (102-10 3 cells l-1). A number ofdiatoms and cyanobacteria also produceneurotoxins that can endanger human health.People can be poisoned when they consumefish and shellfish that have accumulatedphytoplankton toxins filtered from the water(Shumway et al. 1995). Toxicity to humans isalso caused by the consumption of gastropodsand crabs, as well as of certain fish speciesthat have accumulated algal toxins via the foodchain (Lewis et al. 1995). Examples of toxicsyndromes caused by HABs include ciguaterafish poisoning, and paralytic, diarrhetic,neurotoxic, azaspiracid and amnesic shellfishpoisoning (PSP, DSP, NSP, AZP, and ASP)associated mostly with shellfish consumption.Of additional concern are the respiratoryproblems linked to the onshore transport oftoxins in aerosols under particular wind andwave conditions (Baden 1983). Allergy-likereactions in humans, such as skin irritations,have also been reported in some coastal areasas a result of cyanobacterial blooms(Carmichael 1997).

INTRODUCTION 2

Red tides, causing visible water discolouration such as those produced by Noctilucablooms, may be noxious because of unpleasant odours and anoxic effects.

There are ongoing efforts to revise the nomenclature of many HAB species, including recent changes to the taxonomyof some unarmoured dinoflagellates (Daugbjerg et al. 2000). For consistency, we have retained the most commonlyused and widely accepted names at the time this document was prepared.

Table 1. Some deleterious effects caused by harmful algae in coastal and brackish waters(modified from Zingone and Enevoldsen 2000). Note that a single event may have severalnegative consequences.

EFFECT EXAMPLES OF CAUSATIVE ORGANISMSHuman healthParalytic shellfish poisoning (PSP) Dinoflagellates Alexandrium spp., Pyrodinium bahamense var.

compressum, Gymnodinium catenatumCyanobacteria Anabaena circinalis

Diarrhetic shellfish poisoning (DSP) Dinoflagellates Dinophysis spp., Prorocentrum spp.

Neurotoxic shellfish poisoning (NSP) Dinoflagellates Gymnodinium breve

Amnesic shellfish poisoning (ASP) Diatoms Pseudo-nitzschia spp., Nitzschia navis-varingica

Azaspiracid shellfish poisoning (AZP) unknown unknown

Ciguatera fish poisoning (CFP) Dinoflagellates Gambierdiscus toxicus

Respiratory problems and skin Dinoflagellates Gymnodinium breve, Pfiesteria piscicidairritation, neurological effects Cyanobacteria Nodularia spumigena

Hepatotoxicity Cyanobacteria Microcystis aeruginosa, Nodularia spumigena

Natural and cultured marine resourcesHaemolytic, hepatotoxic, Dinoflagellates Gymnodinium spp., Cochlodinium polykrikoides,osmoregulatory effects, and other Pfiesteria piscicida, Gonyaulax spp.unspecified toxicity Raphidophytes Heterosigma akashiwo, Chattonella spp.,

Fibrocapsa japonicaPrymnesiophytes Chrysochromulina spp. Phaeocystis pouchetii,

Prymnesium spp.Cyanobacteria Microcystis aeruginosa, Nodularia spp.

Negative effects on feeding behaviour Pelagophytes Aureococcus anophagefferens

Hypoxia, anoxia Dinoflagellates Prorocentrum micans, Ceratium furca

Mechanical damage Diatoms Chaetoceros spp.

Gill clogging and necrosis Prymnesiophytes Phaeocystis spp.

Tourism and recreational activitiesProduction of foam, mucilage, Dinoflagellates Noctiluca scintillans, Prorocentrum spp.discolouration, repellent odour Prymnesiophytes Phaeocystis spp.

Diatoms Cylindrotheca closteriumCyanobacteria Nodularia spumigena, Aphanizomenon

flos-aquae, Microcystis aeruginosa, Lyngbya spp.

Marine ecosystem impactsHypoxia, anoxia Dinoflagellates Noctiluca scintillans, Heterocapsa triquetra

Diatoms Skeletonema costatumPrymnesiophytes Phaeocystis spp.

Negative effects on feeding behaviour Pelagophytes Aureococcus anophagefferens, Aureoumbralagunensis

Reduction of water clarity Dinoflagellates Prorocentrum minimum

Toxicity to marine wild fauna Dinoflagellates Gymnodinium breve, Alexandrium spp.Diatoms Pseudo-nitzschia australis

INTRODUCTION3

The list of toxic algal species and relatedsyndromes has increased in recent years as havehuman activities within the coastal zone.Intensive monitoring operations have been setin place in many countries of the world toprotect human health; however, many areas arepresently not adequately controlled. About2000 cases of human poisoning have beenreported worldwide, and fatal events areestimated to exceed several hundred cases. Thenumber of actual cases is surely underestimatedowing to incorrect diagnoses, especially inisolated locations and when gastro-intestinalsymptoms are involved. In addition to theirdirect impact on human health, toxic algaeexert a negative effect on the exploitation ofmarine resources that are contaminated,causing incalculable economic damage to theseafood industry. As an example, in 1917, theharvest of wild shellfish in Alaska produced 5million pounds of product. Today, this industryis virtually non-existent as a consequence ofpersistent contamination by PSP (Neve andReichardt 1984).

Natural and Cultured MarineResources

While toxic algae indirectly impinge on use ofmarine resources, other HAB events candirectly affect wild and cultivated fish andinvertebrates that are valuable seafood. Thisgenerally occurs through the production ofspecific toxins, but damages due to mechanicalclogging, lesions of the gills, and anoxia arealso well documented.

Both natural fish stocks and farmed fish stockshave experienced massive mortalities (Rensel1995), which are caused by ichthyotoxicspecies such as the raphidophytes Heterosigmaakashiwo and Chattonella spp., a number ofdinoflagellates, and some prasinophytes. Abloom of Chrysochromulina polylepis in May-June 1988 in the Kattegat and Skagerrak area(North Sea) caused the death of 900 hundredtons of fish, including cod, salmon, and trout.Heterocapsa circularisquama has causedmassive kills of cultured shellfish since 1988in Japan. In summer 1997, anoxic conditionsthat accompanied bloom decay of non-toxicdinoflagellates caused the stranding of 2000tons of rock lobster at Elands Bay (SouthAfrica), with an estimated loss of 50 millionU.S. dollars. This was the worst of a long-termseries of anoxic episodes that are recurrent inthe area (Pitcher and Cockcroft 1998). Browntides produced by Aureococcusanophagefferens in bays of the midwesternAtlantic coast of the U.S.A. led to mortalities,recruitment failure, and growth inhibition ofcommercially important, suspension-feedingbivalves, including blue mussels and bayscallops (Bricelj and Lonsdale 1997).

In Japan and many other countries whereaquaculture operations are in place, noxiousblooms of dinoflagellates and raphidophyteskill finfish and shellfish, resulting in losses ofmillions of U.S. dollars per year. As thedemand for farmed species has increased, it islikely that the economic impact of HAB eventson the aquaculture industry will continue togrow.

INTRODUCTION 4

Throughout the world, large expanses ofcoastline are posted with signs such asthis, prohibiting the harvesting of shellfishdue to the potent algal toxins they haveaccumulated.

Tourism and Recreational Activities

Blooms of algae may have significant negativeeffects on tourism and on the recreational usesof coastal areas. Tourism and recreation dependon relatively high water quality, free fromvisible scums or mats, noxious smells, or skinirritants. Many coastal areas worldwide areaffected by such blooms, with a range of visualand human effects. For example, discolouredwater and mucilage, caused by a variety of non-toxic species, are recurrent on theMediterranean coast and often coincident withthe tourist season, while in the Baltic Sea,massive blooms of cyanobacteria are foundduring the warmest months and often preventthe recreational use of the sea.

Marine Ecosystem Impacts

Attempts to quantify the economic value ofnatural marine ecosystems are recent (Costanzaet al. 1997). It is nevertheless clear that lossesof non-commercial marine resources may alsohave severe consequences.

High biomass, non-toxic blooms of HABspecies can have significant deleterious effectson entire ecosystems. One such ecosystemeffect is the damage to seagrass or coral reefcommunities following a reduction in lightpenetration and anoxia. Severe light attenuationby brown tides results in significant reductionsin the photosynthetic capacity and leaf biomassof eelgrass beds, leading to the loss of nurseryhabitat for numerous fish and shellfish. Oxygendepletion following the degradation of non-toxic blooms can kill not only commerciallyimportant species, but also other animals andplants.

In addition to their effects on human healthand seafood, toxins can move through anecosystem in a manner similar to the flow ofcarbon or nutrients, and thus the impacts canbe far-reaching. Negative influences onviability, fecundity, recruitment, and growthare just beginning to be recognised. Marinemammals such as whales, dolphins, sea lionsand manatees, have all suffered morbidity andmortalities as a result of exposure to HABtoxins transferred through the food web(Scholin et al. 2000). Mass mortalities ofseabirds, including brown pelicans andcormorants, have also been linked to bloomsof diatoms whose toxins were transferred viaconsumption of contaminated planktivorousfish (Work et al. 1993).

INTRODUCTION5

Finfish and shellfish mortality in aquaculturedue to HABs results in large economic lossesas well as loss of product for consumption.

Mortalities of domestic fauna can occur whenblooms of toxic algae occur in fresh, brackish,or marine waters. Photo by W. Carmichael.

The Apparent Global Increaseof HABs

Harmful algal blooms are natural phenomenathat have occurred throughout recorded history.For example, references to what were most

likely outbreaksof HABs aredocumented inCaptain JamesCook’s journal,1770, uponarrival off theGreat BarrierReef, Australia,and also in

documents from Captain George Vancouver’svoyage to British Columbia in 1793 in an areanow known as Poison Cove. Indeed, Vancouvernoted that local native tribes considered it tabooto eat shellfish when the seawater becamephosphorescent. This phenomenon was latershown to be associated with some toxicdinoflagellate blooms. In the Baltic Sea,paleoecological records have revealed thepresence of cyanobacterial blooms more than8000 years ago (Bianchi et al. 2000).

It is now thought that HABs may be increasingworldwide (Anderson 1989, Smayda 1990,Hallegraeff 1993). Several reasons have beensuggested for the apparent increase infrequency, in distribution or severity, such as:

• Species dispersal through currents, storms,or other natural mechanisms

• Nutrient enrichment of coastal waters byhuman activities, leading to the selection for,and proliferation of, harmful algae

• Increased aquaculture operations, which canreveal the presence of previously unknownHAB species

• Transport and dispersal of HAB species viaballast water or shellfish seeding activities

• Long-term climatic changes

• Improved scientific methodology andmonitoring activities leading to the detectionof new species, toxins, or toxic events

The current lack of appropriate data preventsthe resolution of long-term trends in HABs inmany regions, but few would argue that theimpacts of these blooms are increasing andrepresent a serious constraint to the sustainabledevelopment of marine resources.

The global problem of HABs is serious andmuch larger than was previously recognised.Given the significant social and ecosystemimpacts from HABs, a global researchprogramme is clearly needed. If HABs areincreasing due to human activities, then theneed for such a research programme is evenmore urgent.

“The sea in manyplaces here is

cover’d with a kindof brown scum ..”

Captain James Cook,28 August, 1770

INTRODUCTION

Trichodesmium blooms are common on theGreat Barrier Reef, Australia. Similar bloomswere likely seen by Capt. James Cook. Suchblooms are unpleasant for tourists visiting theGreat Barrier Reef today. Photo by P. Glibert.

6

INTRODUCTION7

Paralytic shellfish poisoning (PSP) is a toxin syndrome caused by consumptionof seafood contaminated by certain HAB species. The above maps show thecumulative global increase in the recorded distribution of the causative organismsand the confirmed appearance of PSP toxins in shellfish at levels above theregulatory limit for human consumption.

Emergence of the GEOHABProgramme

Research on HABs emerged as a discipline inits own right at the First InternationalConference on Toxic Dinoflagellate Blooms,held in Boston, Massachusetts, U.S.A. in 1974.Since then, the field has expanded rapidly asconcerns about HABs have increased, and in2000 over 500 scientists from approximately50 countries attended the Ninth InternationalConference on Harmful Algal Blooms inTasmania, Australia.

The proceedings of the Fourth InternationalConference on Harmful Marine Phytoplanktonstated “that some human activities may beinvolved in increasing the intensity and globaldistribution of blooms,” and recommended“that international research efforts beundertaken to evaluate the possibility of globalexpansion of algal blooms and man’sinvolvement in this phenomenon”.Subsequently, a number of national andinternational initiatives were undertaken tostudy and manage HABs and their linkages toenvironmental change, consistent with theglobal nature of the phenomenon.

This increased awareness resulted in theMember States of the IntergovernmentalOceanographic Commission (IOC) requestingthe establishment of an internationalprogramme on HABs. The IOC Harmful AlgalBloom Programme was first formulated at aworkshop jointly sponsored by the ScientificCommittee on Oceanic Research (SCOR) inRhode Island in October 1991. TheIntergovernmental Panel on Harmful AlgalBlooms (IPHAB) was established in 1992 withthe overall programme goal “to foster theeffective management of, and scientificresearch on, harmful algal blooms in order tounderstand their causes, predict theiroccurrences and mitigate their effects.”

At the same time, the International Council forthe Exploration of the Sea (ICES) and the IOCestablished a joint Working Group on HarmfulAlgal Bloom Dynamics. A working group onthe Physiological Ecology of HABs was alsoestablished by SCOR and the IOC, whichrecommended that there should be aninternational programme emphasising theoceanography and ecology of HABs.

At its Fourth Session, IPHAB decided to worktowards the development of an internationalscience agenda on the ecology andoceanography of HABs and sought assistancefrom SCOR in this effort. The strengths of IOCand SCOR lent themselves to a naturalpartnership between these organisations in thedevelopment of a new international scienceprogramme on the ecology and oceanographyof HABs.

SCOR and IOC convened a workshop inOctober 1998 at which scientists from a broad

An International Programme on the Global Ecology andOceanography of Harmful Algal Blooms: GEOHAB

AN INTERNATIONAL PROGRAMME 8

range of biological, chemical, and physicaldisciplines discussed the state of understandingof HABs globally, and identified therequirements for a co-ordinated,interdisciplinary international researchprogramme. They recommended that SCORand IOC undertake a joint effort on the GlobalEcology and Oceanography of Harmful AlgalBlooms (GEOHAB) and the recommendationwas accepted and approved.

The GEOHAB Mission

Acknowledging that the HAB problem isglobal, but recognising that insufficient effortshave been directed toward studying thebiological, chemical, and physical factors thatregulate HAB dynamics and impacts, theSCOR/IOC GEOHAB Programme has as itsmission to:

The GEOHAB Goal

To achieve the mission of GEOHAB, theoverall scientific goal is to:

The GEOHAB Strategy:A Comparative Approach

The approach of the GEOHAB Programme iscomparative, from the cellular to the ecosystemlevel. This approach is based on the view thatthe ecology and oceanography of HABs canbest be understood through the study ofcausative organisms and affected systems inrelation to comparable species and systems.The GEOHAB strategy is also to identify theparticular adaptations of HAB species and tostudy processes at multiple temporal and spatialscales. Important physical processes occur onscales ranging from those controllingturbulence to internal waves, eddies, andcurrents, while important biological processesoccur at subcellular and cellular levels as wellas at the population, community, and ecosystemlevels.

The approach of GEOHAB is to apply multipletechniques to fully understand the biological,chemical, and physical factors regulating HABdynamics and impacts. Field studies areessential, as are laboratory and mesocosmstudies. Modelling the population dynamics(Table 2) will be critical in every aspect of thesestudies. Improved global observation systemswill be required to resolve influences ofenvironmental factors (anthropogenic andclimate-related) on the distributions and trendsin HABs.

Therefore, the GEOHAB Programme fostersresearch that is interdisciplinary, focusing onthe important interactions among biological,chemical, and physical processes. GEOHABresearch must also be multifaceted as theproblems are complex and interactions andprocesses occur on a broad range of scales.Finally, GEOHAB research should beinternational in scope to encompass the globalissues of HAB events and benefit from skilland experience gained by HAB investigatorsworldwide.

AN INTERNATIONAL PROGRAMME

Foster international co-operativeresearch on HABs in ecosystem typessharing common features, comparingthe key species involved and theoceanographic processes thatinfluence their population dynamics.

Improve prediction of HABs bydetermining the ecological andoceanographic mechanisms underlyingtheir population dynamics, integratingbiological, chemical, and physicalstudies supported by enhancedobservation and modelling systems.

9


Studies on population dynamics of HABs will lead to a better understanding of events such ascyanobacterial blooms in the Baltic Sea.

Table 2. Modelling of population dynamics.

A robust mathematical equation for the local number of organisms per unit volume can be written in the followingform:

is the time rate of change of the state variable n, the number of cells of a particular HAB species per unitvolume. Population dynamics is defined as the change of n in space and time.

n represents growth by cell division. The growth rate is determined by intrinsic genetic factors, as well as byenvironmental factors, such as nutritional and light history, turbulence, temperature, and salinity.

mn is the direct loss of organisms through mortality. This term includes processes such as grazing, mechanicaldamage, and death from infections by viruses or other pathogens.

includes the three-dimensional, time-variable transport of cells by the water flow, for example, meancirculation, tidal currents, wind drift, and turbulence (often identified as turbulent diffusion). “Disappearance” ofblooms due to offshore flow would appear in this term.

is the motion of organisms relative to the water, described as velocity, v. This term includes swimming,sinking, or rising due to buoyancy, and slippage, relative to the local flow that arises for a variety of reasons suchas size and shape.

In general, there is a set of state variables, ni , corresponding to different species, and a corresponding set ofequations governing many direct and coupled biological, chemical, and physical processes. Environmentalprocesses affect the population dynamics in several of the terms of this equation, while the coupled processescover a broad range of temporal and spatial scales, with many non-linearities. A major challenge is to understandthe processes to a level of detail that allows a simplified mathematical formulation (parameterisation) and thatstill reproduces the salient features of HAB population dynamics.

n = n - mn - (nv) - (nu)t

nt

(nu)

(nv)

For some HABs, the physical-biological interactions are dominated by physical processes such as large-scale advection and transport phenomena in coastal ecosystems. In other cases, biological factors suchas swimming and aggregation behaviour are the dominant processes affecting the distribution of a HAB

AN INTERNATIONAL PROGRAMME11

AN INTERNATIONAL PROGRAMME

species. For these reasons, physical and biological processes must be considered from a multi-disciplinaryperspective and not in isolation.

12

Organisation and Priorities ofthe GEOHAB Programme

GEOHAB is an international programme to co-ordinate and build upon related national,regional, and international efforts in HABresearch. The GEOHAB Programme will assistin bringing together investigators fromdifferent disciplines and countries to exchangetechnologies, concepts, and findings. This maytake the form of formal or informal workshops,working groups, and collaborating teams ofinvestigators. GEOHAB is not a research-funding programme per se, but instead willfacilitate those activities that require co-operation among nations. This might includethe development and sharing of methodologies;efficient use of major resources, such asresearch vessels; and co-ordination andstandardisation of data management, makingfeasible the integration of results and a globalsynthesis. GEOHAB projects will be fundedby a variety of national and internationalsources; the programme will therefore be a

coalescence of projects at many levels, fromlarge, multi-investigator, multi-national fieldinvestigations, to co-ordinated laboratorystudies on specific processes or methods.

GEOHAB has defined five ProgrammeElements that serve as a framework to guidepriorities and research. These include:Biodiversity and Biogeography; Nutrients andEutrophication; Adaptive Strategies;Comparative Ecosystems; and Observation,Modelling, and Prediction.

Research and technical advances will beencouraged in several ways. For example,major field programmes such as thoseenvisioned under Comparative Ecosystemswill be expected to include observation andmodelling components, incorporatingcharacterisation of the sites with measurementsand models prior to and during process studies.In addition, targeted research, such as thatconducted within the Adaptive Strategies orNutrients and Eutrophication components, will


While the Programme Elements of GEOHAB are individually described and justified, thegoals of GEOHAB will only be advanced through the linkages between the ProgrammeElements.

be directed toward addressing gaps in ourabilities to observe or model properties andprocesses. The resulting technicalachievements will be incorporated rapidly intoresearch programmes, and observation andmodelling systems. Through the developmentof in situ and remote sensing techniques andthe creation of networks of laboratories tomonitor, collate, and disseminate data, thepriorities of GEOHAB will be advanced in theform of more effective monitoring systems,risk assessment, and improved forecasts of thetiming, magnitude, and effects of HABs.

Links Between GEOHAB andOther International Activities

Three international programmes with scientificinterests that overlap with those of GEOHABare the Land-Ocean Interactions in the CoastalZone (LOICZ), Global Ocean EcosystemDynamics (GLOBEC), and the Global OceanObserving System (GOOS) programmes. Thefirst two are part of the InternationalGeosphere-Biosphere Programme (IGBP).

The major goals of LOICZ are thequantification of fluxes of nutrients and waterfrom coastal drainage basins to estuaries andthe coastal ocean, and of nutrient budgets forcoastal ecosystems. The complementary goalsof GEOHAB include quantifying the effects

of anthropogenic nutrient enrichment on thepopulation dynamics of HABs.

GLOBEC emphasises the roles of physicalprocesses and zooplankton in the trophicdynamics of food webs that support marinefisheries. The focus of GEOHAB is on thedynamics of HABs that have significant effectson the trophic dynamics linking nutrients andphytoplankton productivity to zooplankton andfisheries.

Clearly, co-ordination with LOICZ andGLOBEC must be a high priority forGEOHAB. Co-ordination will include thedesign and implementation of research projectsand the exchange of data and information toachieve the related objectives of bothprogrammes. National programmes will, ofcourse, be integral to the activities ofGEOHAB.

The Global Ocean Observing System (GOOS)is designed to monitor the oceans and developsufficient understanding of environmentalchange to achieve the goals of sustainabledevelopment and integrated management of themarine environment and its natural resources.GOOS has been charged with promoting thedevelopment of observation systems that willimprove documentation and prediction of theeffects of human activities and climate change


GEOHAB will co-operate and co-ordinate with relevant national, regional, and internationalprogrammes.


Massive cyanobacterial blooms in the Baltic Sea are common in the summermonths. Understanding the factors leading to these and other HAB events, andultimately improving prediction of such HABs, is the aim of GEOHAB.

on marine ecosystems and the living resourcesthey support.

The knowledge and tools generated byGEOHAB will benefit the coastal componentof GOOS in the form of more effectiveoperational monitoring systems, data-basedrisk assessment, and improved forecasts of thetiming, magnitude, and effects of HABs. Inturn, it is expected that GOOS will encouragethe implementation and development ofsustained observing systems required todocument HAB trends, evaluate the efficacyof management actions (HAB mitigation), anddefine those areas that require additionalresearch.

The Benefits of GEOHAB

A better understanding and quantification ofthe factors that regulate the dynamics of HABsin the context of physical and chemical forcing,ecosystem dynamics, and human influenceswill be used to improve strategies formonitoring, prediction, and mitigation ofHABs. Through links to national agencies andinternational organisations responsible forprotecting coastal resources and public health,the knowledge gained from GEOHAB will beused to develop international capabilities formore effective management and mitigation ofHAB problems. Linking basic scientificresearch directly to societal needs should resultin an effective contribution of science to theprotection of the intrinsic and economic valueof coastal marine ecosystems.

PROGRAMME ELEMENT 1

INTRODUCTION

On a global basis, there is evidence of changesin the distribution of harmful species, with newrecords in areas previously unaffected by thesephenomena (Anderson1989, Smayda 1990,Hallegraeff 1993).Increased interactionwith the coastal zone andgreater awareness of theproblems caused bymicroalgae havecontributed to moreeffective detection ofharmful species. On theother hand, several alternative scenarios couldaccount for the appearance of previouslyunrecorded species in a newarea. These include theintroduction of non-indigenous harmful species,followed by possibleacclimation and geneticadaptation to attain andmaintain HAB status. Also,differential stimulation ofpopulation growth of apreviously unrecorded orrare species followingenvironmental change mayresult in the emergence ofthe harmful species as adominant organism. Finally,the appearance of new HABevents in previouslyunaffected areas may be aconsequence of themanifestation of noxioustraits in strains formerlythought to be benign.

Knowledge of the presentgeographic distribution of

PROGRAMME ELEMENT 1: Biodiversity and Biogeography

HAB species and of the long-term fluctuationsin species composition are essential fordistinguishing novel and recurrent HABevents, and for evaluating the global spreadinghypothesis (Anderson 1989, Smayda 1990,

Hallegraeff 1993).Within the context ofHAB research andmanagement, severalbiodiversity issues needto be addressed. Theseinclude determination ofthe number of distincttaxa to be classified(taxonomic diversity),and determination of the

variation in primary gene sequences andexpressed gene products (genetic diversity).Patterns of variation and changes in

biodiversity should beassessed at scales spanningthe genetic structure ofpopulations or blooms of asingle species, torelationships amongpopulations, to the generaldiversity of phytoplanktonpopulations in areas proneto HAB events. A highdegree of genetic variabilityis typically associated withphenotypic characteristicssuch as growth rates,environmental tolerance,and, in the case of harmfulspecies, cell toxicity. Theuse of molecular techniques– including nucleic acidsequencing and genotyping– offers much promise inidentifying geneticvariations over theirgeographic range.Molecular data can also beemployed to evaluate

Biodiversity is defined as thecollection of genomes, species, andecosystems occurring in ageographically-defined region.

Committee on BiologicalDiversity in Marine Systems

Many harmful species can form restingstages or enter quiescent phases thatallow their survival in the dark. Ballastwater discharge is one mechanism bywhich these species may be introducedto new regions.

16

PROGRAMME ELEMENT 1

hypotheses regarding the introduction of HABtaxa into new environments. Detailedknowledge of the genetic characteristics of aspecies across a wide spatial scale may providevaluable information regarding mechanisms ofadaptation and dispersal, allowing tracking andpossible prediction of expansion or patterns ofrecession.

In the framework of the international co-operation fostered by GEOHAB, the overallresult expected from this investigation is adetailed analysis of biodiversity at varioustaxonomic and genetic levels, as they relate toboth static geographic and dynamicclimatological, oceanographic, andanthropogenic features. In this context, patternsand trends in the distribution of speciesendangering human welfare and ecosystem

health will become clearer and the response ofharmful species to natural and human-inducedchanges thus become more predictable. Studiesof HAB species distributions and biodiversitywill also provide an indication of chronicproblems related to shifts in species dominanceand environmental vulnerability to theintroduction of foreign harmful species.

In summary, this Programme Element aims toaddress the following research question:

What are the factors that determinethe changing distribution of HABspecies, their genetic variability, andthe biodiversity of the associatedcommunities?

17

A conceptual model of the linkages and relationships of the components in ProgrammeElement 1. These various components of biogeography and biodiversity must bestudied over a wide range of temporal and spatial scales and compared for differentecosystems.

OVERALL OBJECTIVE

THE STRATEGY

GEOHAB will foster co-ordinated andcomparative studies on changing distributionsand biodiversity of HAB taxa. Thedevelopment and application of appropriatetechnologies for species discrimination andassessment of genetic variation should beaccomplished through the exchange of culturedmaterial and natural samples collected from allregions of the world. Through thestandardisation of methods, speciesdistribution and biodiversity canbe compared among differentecosystems. GEOHAB willfacilitate the interpretation ofgenetic variability of harmfulspecies at the level of discrete localpopulations and ultimately on aglobal scale.

A summary of the objectives andtypes of tasks that might beaddressed under this ProgrammeElement, as well as the anticipatedoutcomes, is provided in Figure1.1.

Specific Objective #1

Assess the genetic variability ofHAB species in relation to theirtoxicity, population dynamics,and biogeography

Rationale

A suite of methods has been developed forassessing the phylogenetic relatedness amongspecies, for recognising intraspecific genetic

diversity, and for complementing themorphological characterisation of harmful andother species. For example, moleculartechniques coupled with morphologicalobservations have allowed for discriminationof toxic and non-toxic specimens of the diatomPseudo-nitzschia at the species level (Hasle1995, Manhart et al. 1995), and have revealedthe existence of new species in the haptophytegenus Phaeocystis, which had been consideredmonospecific (Medlin et al. 1994, Zingone etal. 1999). On the other hand, research on somespecies of the dinoflagellate generaAlexandrium and Gymnodinium hasdemonstrated high genetic variability withinspecies, often with a high sequence similarityamong selected strains of differentmorphospecies from the same geographicalarea (Scholin and Anderson 1996, Bolch et al.1999).

There are many examples of how variation inecophysiological characteristics reflects anunderlying genetic variability (Brand 1989).The existence of both toxic and non-toxic

To determine the relationships amongdistributions of HAB species,biodiversity, and environmental change

PROGRAMME ELEMENT 1 18

Many HAB species have a high degree of genetic variability thatis not always morphologically expressed. Nevertheless, withincertain species there may be morphologically stable andgeographically disjunct varieties. For example, Pyrodiniumbahamense var. compressum produces long chains of apicallycompressed cells, whereas var. bahamense occurs as short chainsor individual cells that are roughly isodiametrical. Note that thespiny cyst form of this species does not resemble the vegetativecell of either variety, and that spine length and overall morphologyare subject to environmental influences.

Figure 1.1 Summary of Programme Element 1: Biodiversity andBiogeography.

OVERALL OBJECTIVE Programme Element 1: To determine therelationships among distributions of HAB species, biodiversity, andenvironmental change

1Assess the genetic variability of HABspecies in relation to their toxicity,

population dynamics, andbiogeography

• Characterise HAB species using morphology, moleculargenetics, biochemical composition, and other cellularproperties

• Develop diagnostic tools for the discrimination of HABtaxa at various taxonomic levels

• Evaluate the population genetics of HAB species overthe annual cycle

• Assess the relatedness of different strains of HABspecies at different locations

• Conduct global biogeographic analyses of key HABtaxa

• Examine the distributional pattern of HAB species inthe water column, benthic habitats, and thesedimentary record

• Evaluate the potential for survival and growth of aHAB species from a given area in other geographicalregions

• Evaluate whether HAB species have been introducedinto new regions by natural or anthropogenicprocesses

2Determine the changes in thebiogeographical range of HAB

species caused by naturalmechanisms or human activities

• Characterise the biodiversity of the microalgalcommunity, including HAB organisms, in differentecosystems

• Identify shifts in species succession and microalgaldiversity over seasonal time-scales in environmentssubject to HAB events

• Define possible links between changes in biodiversityand environmental factors on a multi-annual time-scale, including hindcasting from historical data

OUTPUTS• New tools for detecting harmful and potentially harmful organisms• Comprehensive inventories of harmful species at local, regional, and global scales• Foundation for assessing the importance of human-assisted dispersal of HAB organisms• Quantitative assessment of historical relationships between climate variability, human activities,

and HABs

3Determine changes in microalgal

species composition and diversity inresponse to environmental change

PROGRAMME ELEMENT 119

strains within a single species, and even amongisolates originating from the same locality orbloom event, is an extreme demonstration ofgenetic variability within a species (Scholinand Anderson 1993, Anderson et al. 1994,Cembella and Destombe 1996). In addition,mating compatibility (Destombe and Cembella1990) may also vary within a single species.

Isolates of the same species obtained at diverselocalities have shown a great deal of variabilityin their ecophysiological characteristics;examples include Gymnodinium catenatumfrom Spain, Japan, and Australia (Hallegraeffand Fraga 1998) and Pseudo-nitzschiaobtained from diverse localities worldwide(Bates et al. 1998). Intraspecific variabilityinfluences many types of physiologicalresponses that are relevant to ecological successand the harm caused by a species in differentenvironments and under different conditions.Much of this variation may have adaptivesignificance in terms of population dynamics.It is particularly important to know the extentto which intraspecific variability is related togenetic differences as regulated byenvironmental variables.

The assessment of genetic variability within asingle species along a biogeographic gradient,and among different populations in the samearea, represents the baseline for thecharacterisation of harmful organisms and forthe definition of the functional role of

biodiversity. At a local scale, the degree ofgenetic variability for a given species is a proxyfor its capability to adapt and thrive underdifferent environmental conditions. As anexample, the annual alternation of blooms ofdifferent strains of a species could explain whysome species persist for longer periods thanothers. Cyst maturation in Alexandriumtamarense populations from shallow coastallagoons and offshore cyst beds of the Gulf ofMaine has been shown to be regulated byenvironmental conditions or by an endogenousclock, respectively (Anderson and Keafer1987). On the regional to global scale, geneticanalyses could account for different bloomdynamics and reveal the presence of crypticspecies or species complexes within a singlemorpho-species. This kind of information isnecessary for the development of models ofbloom dynamics of single species in differentecosystems. Finally, knowledge of the geneticstructure of a species over its distributionalrange provides the basis for the reconstructionof pathways of spreading and colonisation intonew areas.

Example Tasks

• Characterise HAB species usingmorphology, molecular genetics,biochemical composition, and other cellularproperties


Among chain-forming HAB species, such asGymnodinium catenatum, chain length is afunction of both genetic and environmentalfactors. Chain-forming isolates from naturalpopulations often lose the ability to form longchains and atypical cells of distortedmorphology may be produced after manygenerations in culture.

Taxonomic identification of certain HAB speciesusing morphological characteristics iscomplicated by the high degree of variationexpressed among and within populations. Forexample, the cells of Dinophysis shown herevary with respect to pigmentation, thecalornamentation, length of the list (“wing”), andgeneral cell shape, yet they belong to the samespecies.

For ease of understanding biogeographical, taxonomic and phylogenetic relationships among HAB taxa,the data are often presented as a cluster diagram or multi-dimensional ordination. In cluster diagramsor “trees” the relatedness may be shown quantitatively according to principles of numerical techniques(similarity in diagnostic traits) or phylogenetic analysis, by inferring shared derived characteristics(cladistics). Often the branch lengths are used to indicate “genetic distance” between taxa. The upperleft panel shows the relatedness among prymnesiophytes based on small sub-unit ribosomal RNAsequences using the distantly related dinoflagellate Prorocentrum as an “outgroup” to root the tree(from Zingone et al. 1999). In the upper right panel, the tree represents the genetic distance (X-axisscale) among cultured isolates and natural populations of Alexandrium from eastern Canada (GSL=Gulf of St. Lawrence; SLE = St. Lawrence estuary; BF=Bay of Fundy; NS = Nova Scotia) based onsimilarity in PSP toxin composition (from Cembella and Destombe 1996). An alternative representationof the same toxin data set shows the application of principal components analysis, an ordination methodin multi-dimensional space, with axes indicating the principal toxin components. The encircled pointsrepresent populations from the St. Lawrence ecosystem.


• Develop diagnostic tools for thediscrimination of HAB taxa at varioustaxonomic levels

• Evaluate the population genetics of HABspecies over the annual cycle

• Assess the relatedness of different strains ofHAB species at different locations


Determine the changes in thebiogeographical range of HAB speciescaused by natural mechanisms or humanactivities

Rationale

HAB organisms may be categorised into twobroad groups based on their biogeographicaldistribution. Certain speciesmay have a rathercircumscribed distributionwithin very narrowenvironmental constraints.For example, species such asPyrodinium bahamense arerestricted to tropical andsubtropical regions in thePacific Ocean and CaribbeanSea (Hallegraeff and Maclean1989), while species such asAlexandrium catenella arefound only in temperatewaters at mid- to highlatitudes. Other species,including the benthicdinoflagellate Prorocentrumlima and the raphidophyteHeterosigma akashiwo, havea rather cosmopolitandistribution, from temperateto tropical waters.

Climatic shifts have resultedin long-term sustainedchanges to oceanographic

features and other environmental conditions.For example, after the last ice age, the openingof the Bering Strait connected the North Pacificand North Atlantic Oceans. This conditionwould have permitted the invasion of manyplanktonic species from one ocean to the other,perhaps accounting for the cosmopolitandistribution of most of the extant taxa.Comparative studies of the geographicaldistribution of HAB species in relation to theenvironment should provide a probabilisticmodel of the likelihood of spreading orinvading another ecosystem. For example,current knowledge on the restricted distributionof Pyrodinium bahamense within tropical andsubtropical waters suggests that this species isunlikely to establish viable populations inwaters with low temperatures and salinities.The same rationale suggests that Alexandriumcatenella would probably not be viable intropical waters owing to its low tolerance forsustained high temperatures. In the few cases


The El Niño - Southern Oscillation (ENSO) is the result of a cyclicwarming and cooling of the surface ocean of the central and easternPacific. This region of the ocean is normally colder than its equatoriallocation would suggest, mainly due to the influence of north-easterlytrade winds; however, during periods when this cold water influencediminishes, solar heating of the tropical Pacific results in an El Niñoevent. Several attempts have been made to link the appearance andbiogeographical extent of specific HAB events, particularly in thetropics, to El Niño, but the data are inconclusive and reasons for thiscorrelation (even if apparent) are inconclusive. In this figure, thecoincidence of ENSO events and major toxic red tides of Pyrodiniumbahamense (1978-1997) are shown for the western Pacific (fromUsup and Azanza 1998). Arrows indicate specific occurrences in thePhilippines and Malaysia. The Southern Oscillation Index (SOI) is ameasure of the difference between sea level pressure between Darwinand Tahiti caused by this cyclic warming and cooling of the easternand central Pacific - negative SOI values indicate “ocean warming”associated with ENSO.

in which HAB speciesare able to produce aresting stage, whichmay be fossilised (suchas Gymnodiniumcatenatum, Pyrodiniumbahamense), cystrecords may providevaluable insight intopaleo-climatologicalevents and relatedfluctuations in speciesdominance, as well asevidence of the globalspreading or recessionof a given species.

Human activities, suchas the discharge ofballast from ships andthe transport of liveaquaculture stock, havealmost certainlyresulted in theintroduction of alienspecies, including those responsible for HABs,into other regions. For example, thedinoflagellate Heterocapsa circularisquama isthought to have been introduced from tropicalor sub-tropical waters through transfer ofstocks of juvenile oysters, and to have spreadwithin Japan in subsequent years by movementof oyster spat to other locations. The only well-documented case of human-assisted transferof a harmful species is the introduction ofGymnodinium catenatum to Tasmania,probably via ballast water discharge (McMinnet al. 1997).

Knowledge of the distribution of differentgenotypes over the geographic range ofharmful species is a powerful tool toreconstruct its pathways of dispersal to newareas. In addition, mechanisms wherebyinvading species are introduced and canbecome established in new areas should be wellunderstood in order to mitigate the potentialspreading of harmful species.


Changes in the biogeographical distribution of previously described and novelHAB species have resulted in ecological devastation and massive losses offisheries and aquaculture resources in many areas of the world. For example,the recently described dinoflagellate Heterocapsa circularisquama firstappeared in Japan in 1988. Since then, blooms of this species have spreadrapidly to other areas of the Japanese coast, with massive blooms (>106

cells L-1) causing heavy damage to shellfish aquaculture, particularly in westernJapan (from Matsuyama 1999). It is still unclear if H. circularisquama isendemic to Japan or whether it was introduced from tropical regions throughtransfer of shellfish stock or via advection in the prevailing northward currents.

Several HAB species produce resting stages andcysts that sink in the water column. The analysis ofthese stages in the sediments can provide insightsinto the distribution of the species integrated overtime and space. For species producing fossilisablestages, such as some dinoflagellates andcyanobacteria, the analysis of fossil sediments mayallow the reconstruction of their past geographicrange. As an example, Pyrodinium bahamense ispresently restricted to coastal waters of the tropicsand subtropics, but fossil records dating back tothe Pleistocene, show that the species range reachedhigher latitudes in both hemispheres in the past(Matsuoka 1989), possibly under different climaticconditions. Recently, a live cyst has been found offPortugal (Amorim and Dale 1998). Is this the firstindication of a new range expansion for this species?

Example Tasks

• Conduct global biogeographic analyses ofkey HAB taxa

• Examine the distributional pattern of HABspecies in the water column, benthichabitats, and the sedimentary record

• Evaluate the potential for survival andgrowth of a HAB species from a given areain other geographical regions

• Evaluate whether HAB species have beenintroduced into new regions by natural oranthropogenic processes


Determine changes in microalgal speciescomposition and diversity in response toenvironmental change

Rationale

Phytoplankton distributions in coastal and shelfwaters are characterised by a high degree ofvariability over a wide range of scales.Compositional shifts, changes in dominantspecies, and the emergence of previouslyunrecorded or rare species are well knownphenomena. These shifts in biodiversity areparticularly important when they involveharmful algae, thereby affecting humanactivities. In some cases, the emergence ofharmful events in new areas may be associatedwith an increase in the abundance of thecausative species. For example,Chrysochromulina polylepis andChrysochromulina leadbeateri were sporadicand rare components of the local microflora inScandinavian waters prior to their respectivemassive blooms in 1988 and 1991 (Moestrup1994). The biodiversity of endemicphytoplankton populations is insufficientlyknown, therefore it is difficult to ascertainwhether a previously unrecorded HAB

organism has been introduced or whether it hasmerely escaped detection in the past owing toinadequate sampling. This could be the casewith the diatom Pseudo-nitzschia australis,which has been known to occur in the Gulf ofCalifornia since 1985 (Hernández-Becerril1998), but has only recently been associatedwith the production of domoic acid. In mostcases, it is not possible to trace the historicalabundance of the species prior to harmfulevents owing to the absence of appropriatetime-series data. Consequently, it is difficultto determine if recent toxicity is a result of anincrease in the abundance of establishedpopulations, environmental influences ontoxicity, or the introduction of a toxic strain.

Seasonal changes in species composition aredriven by such factors as annually recurrentpatterns of light, water column structure, andnutrient availability. However, high interannualvariability is often recorded in the initiation,duration, and species composition of seasonalblooms that may include harmful species inan unpredictable fashion. As an example,blooms of Gymnodinium catenatum inTasmanian waters (Hallegraeff et al. 1995) andof Aureococcus anophagefferens along theeastern coast of U.S.A. (Bricelj and Lonsdale1997), show high interannual and seasonalvariability. In contrast, annual toxic blooms ofAlexandrium ostenfeldii and Alexandiumtamarense along the eastern coast of NovaScotia, Canada are remarkably predictable(Cembella et al. 1998). In Laguna Madre,Texas, a bloom of Aureoumbra lagunensispersisted for seven years, demonstrating thelong-term persistence of a harmful speciesfollowing a shift in environmental and weatherconditions (DeYoe and Suttle 1994).

Changes in populations, including HABspecies, have often been associated with localinterannual meteorological variations, as wellas with large-scale climatic fluctuations.Examples include the periodicity of blooms ofPyrodinium bahamense var. compressum insoutheast Asia (Maclean 1989) and the recent


blooms of fish-killing species in Hong Kong(Yin et al. 1999), both of which showed arelationship with the El Niño - SouthernOscillation. Blooms of the cyanobacteriumTrichodesmium, in several areas of the NorthPacific subtropical gyre, also followed anENSO event, in 1992 (Karl et al. 1997). In theGullmar Fjord in Sweden, the presence of toxicphytoplankton blooms has been related tophase changes in the North Atlantic Oscillation(NAO) (Belgrano et al. 1999).

The different driving forces determining long-term plankton variability may interact in apoorly discernible fashion, either by enhancingor dampening the respective effects. One ofthe most ambitious research goals of GEOHABis to ascertain to what extent populationchanges resulting in increased HAB activityare caused by natural variability and/or humanactivities.

Example Tasks

• Characterise the biodiversity of themicroalgal community, including HABorganisms, in different ecosystems

• Identify shifts in species succession andmicroalgal diversity over seasonal time-scales in environments subject to HABevents

• Define possible links between changes inbiodiversity and environmental factors on amulti-annual time-scale, includinghindcasting from historical data

OUTPUTS

The results of this Programme Element shouldlead to:

• New tools for detecting harmful andpotentially harmful organisms

• Comprehensive inventories of harmfulspecies at local, regional, and global scales

• Foundation for assessing the importance ofhuman-assisted dispersal of HAB organisms

• Quantitative assessment of historicalrelationships between climate variability,human activities, and HABs

Episodic meteorological events, such as HurricaneFloyd which hit the east coast of the United Statesin 1999, can result in major changes in theecosystem through the delivery of freshwater,sediments, or nutrients, all of which can lead tochanges in species composition. Photo by UnitedStates Geological Survey.


PROGRAMME ELEMENT 2: Nutrients and Eutrophication

INTRODUCTION

Concurrent with escalating influences ofhuman activities on coastal ecosystems, theenvironmental and economic impacts of HABshave increased in recent years. Of particularconcern is the potentialrelationship between HABsand the growingeutrophication of coastalwaters. This linkage hasoften been suggested(Smayda 1990, Riegman1995, Richardson andJørgensen 1996) as coastalwaters receive large quantities of nutrients fromagricultural, industrial, and sewage effluents.Although it may seem reasonable to assume acausal relationship between human activities

and an expansion of HAB events, theunderlying mechanisms are not known. It isimperative to know how present trends inpollution and nutrient loading relate to algalblooms in general, as well as how they promotethe development of particular species. The key

to this knowledge is anunderstanding of theecology andoceanography of HABsat both regional andglobal scales.

The sources of nutrientsthat may stimulate

blooms are many, from sewage to atmosphericand groundwater inputs, to agricultural andaquaculture runoff and effluent. It has beenestimated that the flux of phosphorus to the

PROGRAMME ELEMENT 2

Eutrophication is the process ofincreased organic enrichment of anecosystem, generally throughincreased nutrient inputs.

Nixon 1995

26

Schematic representation of potential links between nutrient inputs, algal responses, and theexpression of HAB effects.

oceans has increased 3-fold compared to pre-industrial, pre-agricultural levels, while the fluxof nitrogen has increased even moredramatically (Smil 2001). For example, the fluxof nitrogen to the rivers of the North Sea hasincreased 10-fold during this period, andhuman activity is thought to have increased thenitrogen inputs to the northeastern UnitedStates by 6-8 fold (Boynton et al. 1995,Howarth 1998).

The responses of ecosystems to nutrientloading are variable. For example, the effectsof nutrient loading on phytoplankton dependon the extent to which growth rates or netbiomass yield are limited by the supply ofambient nutrients (Malone et al. 1996). Thus,in some cases the response may be an increasein growth rate or turnover of one or morespecies, while in other cases the response maybe an overall increase in algal biomass. Effectsare also dependent on the time scale of thenutrient addition; responses of phytoplanktonto variable nutrient supply may range fromhours to days when the growth rate is nutrientlimited, to weeks when standing crops ofphytoplankton are limited by nutrients(Caperon et al. 1971).

The result of eutrophication is often an increasein total algal biomass, due to the development

of one or more species or groups. Increases inhigh biomass blooms in parallel with increasednutrient enrichment have been reported for theSouth China Sea (Qi et al, 1993), the BlackSea (Bodeanu and Ruta 1998), Hong Kong(Lam and Ho 1989), among many otherlocations. Such blooms may have deleteriouseffects including overgrowth and shading ofseaweeds, oxygen depletion of the water fromthe decay of algal biomass, suffocation of fishfrom stimulation of gill mucus production, andmechanical interference with filter feeding.Deleterious effects on the benthos may also beconsiderable. Of additional concern with thedevelopment of high biomass algal blooms isthe poor transfer of energy to higher trophiclevels, as many blooms are not efficientlygrazed, resulting in decreased transfer ofcarbon and other nutrients to fish stocks. SomeHAB species secrete allelopathic substancesthat inhibit co-occurring species (Pratt 1966,Gentien and Arzul 1990), and suppression ofgrazing occurs above a threshold concentrationof the HAB species (Tracey 1988).

The extent and the mechanisms wherebynutrient enrichment may lead to thedevelopment of toxin producing HAB speciesis poorly understood. Although eutrophicationmay be associated with an increasing numberof high-biomass blooms and other HAB events,

PROGRAMME ELEMENT 2

From Hong Kong (left) to the tributaries of the Chesapeake Bay, U.S.A. (right), high biomass bloomsresult in discoloured water, hypoxia, and toxicity of fish and shellfish. Through the efforts of GEOHAB,a greater understanding of the roles of environmental factors, such as nutrient loading, and anthropogenicinfluences in bloom development will be obtained, and better prediction and mitigation strategies canbe developed. Photos by M. Dickman and P. Glibert.

27

the specific relationshipsleading to the increasedfrequency of toxin-producers,or the increased production oftoxin within these organisms areoften poorly characterised.Therefore, the means to mitigateimpacts of eutrophication ontoxic HABs are not known andhave been the subject of muchcontroversy and debate.

Efforts to understand therelationships between nutrientloading and algal blooms havelargely focused on total nutrientloads and altered nutrient ratios that result fromselected nutrient addition or removal.Alterations in the composition of nutrient loadshave been correlated with shifts from diatom-dominated to flagellate-dominated assemblages(Smayda 1997). A 23-year time series off theGerman coast documents the generalenrichment of coastal waters with nitrogen andphosphorus, and a resulting shift in the relativenutrient composition. This shift wasaccompanied by a 10-fold increase inflagellates and a concomitant decrease indiatoms (Radach et al. 1990). In Tolo Harbour,Hong Kong, the human population within thewatershed grew 6-fold between 1976 and 1986,during which time the number of red tideevents increased 8-fold (Lam and Ho 1989).The underlying mechanism is presumed to beincreased nutrient loading from populationgrowth. Similarly, the number of red tide eventsin Chinese coastal waters increased sharplyfrom 1975 to 1993, due largely to alterednitrogen to phosphorus ratios from increasingatmospheric emissions and deposition ofpollutants (Zhang 1994).

In addition to nutrient uptake requirements, thegeographic range and biomass of algalpopulations are affected by several otherfactors. These include physical forcings,nutrient supply, the physiology and behaviourof algal species, and the trophodynamics, all

of which interact to determine the timing,location, and biomass of a bloom, which in turndetermines the harmful consequences. Yet,these relationships are far from understood.


OVERALL OBJECTIVE

THE STRATEGY

GEOHAB will foster robust quantitativeapproaches to distinguish direct effects ofeutrophication from climate-related influenceson HABs. To fully resolve direct impacts ofanthropogenic nutrient inputs on HABs, it willbe necessary to understand the effects ofnutrients in a regional and a global context.By addressing the effects of nutrients on HABdevelopment on scales ranging from cellular

PROGRAMME ELEMENT 2

To determine the significance ofeutrophication and nutrienttransformation pathways to HABpopulation dynamics

28

Outbreaks of harmful algal blooms in Chinese coastal watersincreased 10-fold from 1975 to 1993 (redrawn from Zhang 1994).

To what extent does increasedeutrophication influence theoccurrences of HABs and theirharmful effects?

regulation to regional comparative systems,GEOHAB will strengthen the theoretical basisof issues related to nutrient regulation ofspecies diversity in planktonic ecosystems.

A summary of the objectives and types of tasksthat might be addressed under this ProgrammeElement, as well as the anticipated outcomes,is provided in Figure 2.1.


Determine the composition and relativeimportance to HABs of different nutrientinputs associated with human activities andnatural processes

Rationale

A broad range of anthropogenic activities mayresult in significant alteration of nutrientcycling in coastal environments. However, theimpacts of differing anthropogenic activitiesare not necessarily the same. For example,wastewater contributes roughly 70% of thenitrogen inputs to Long Island Sound, largelyfrom the sewage of New York City. Similarly,sewage is responsible for up to 80% of thenitrogen delivered to Kaneohe Bay, Hawaii,and Narragansett Bay, Rhode Island (Nixonand Pilson 1983, National Research Council1993). Yet, non-point sources of nutrients,such as agricultural operations, fossil-fuelcombustion, and animal feeding operationsmay be of greater concern for coastaleutrophication and for HABs. Nutrient inputfrom agricultural runoff can vary in quantity,influenced by rain and other environmentaleffects, and it can also differ in composition,based on the form of fertiliser in use. Adramatic trend in world fertiliser productionis the increased proportion of urea, nowrepresenting up to 40% of all fertiliserproduced (Constant and Sheldrick 1992).

Groundwater may be an important nutrientsource to some coastal zones, and has beenlinked to HABs. However, such linkages are

often complex and difficult to proveconclusively. In the Long Island bays of NewYork, it has been suggested that reducedrainfall decreases the input of dissolvedinorganic nitrogen, which in turn leads to anincrease in dissolved organic nitrogen andstimulates the growth of Aureococcusanophagefferens (LaRoche et al. 1997). Thisstudy further suggests that there can be asignificant time lag between the humanactivities that enrich the groundwater and theHAB impact; in this case, the brown tides oftoday may reflect increases in development andfertiliser applications of 10 to 20 years ago.

Atmospheric nutrient input is one of the mostrapidly increasing sources of nutrients to thecoastal zone. Current estimates suggest thatfrom 20-40% of nitrogen inputs are ultimatelyderived from atmospheric sources, fromindustrial, urban, or agricultural sources (Duce1986, Fisher and Oppenheimer 1991, Paerl1995, 1997). Experimental manipulations havedemonstrated that nutrients carried in rainwatermay disproportionately stimulatephytoplankton more than the addition of asingle nitrogen source (Paerl 1997). Bloomsin the Yellow Sea of China, which haveescalated in frequency over the past severaldecades have been related to atmosphericdeposition in addition to direct nutrient runoff(Zhang 1994). It has been suggested that atypical rain event over the Yellow Sea maysupply sufficient nitrogen, phosphorus, andsilicon to account for 50-100% of the primaryproduction of a HAB event (Zhang 1994).

Aquaculture and cage culture systems representanother source of nutrients, due to the highadditions of fertilizer or feed, or to the intensivebiological transformations that occur in thesesystems. Nutrients released from aquaculturesites may impact a region 3-9 times the size ofthe aquaculture zone (Sakamoto 1986).Depending on whether such a site is wellflushed or quiescent, the effect on planktonproductivity and species development will vary(Wu et al. 1994, Romdhane et al. 1998).


Figure 2.1 Summary of Programme Element 2: Nutrients andEutrophication.

OVERALL OBJECTIVE Programme Element 2: To determine thesignificance of eutrophication and nutrient transformation pathways toHAB population dynamics

OUTPUTS• Guidance for development of policies related to eutrophication and HABs• Improved basis for establishing site selection criteria for aquaculture operations• Quantitative baseline information for integrated coastal management

4Determine the role of nutrient cycling

processes in HAB development

• Determine nutrient transformation and regenerationprocesses in relation to HABs

• Assess the functional relationships between HABspecies and the co-occurring non-HAB organisms, interms of nutrient pathways and fluxes

• Measure toxin production in HAB species in culture atdifferent stages of growth and under differentnutritional conditions

• Determine the nutrient-dependent factors thatregulate toxin synthesis

• Determine the role of nutrient supply in the productionof noxious foams and scums

3Determine the effects of varyingnutrient inputs on the harmful

properties of HABs

• Assess the importance of different nutritionalstrategies among HAB species and in comparison tonon-HAB species

• Quantify the nutrient uptake and growth kinetics forHAB species in relation to competing organisms

• Determine the conditions under which a HAB speciesmay adopt alternative nutritional strategies

2Determine the physiological

responses of HAB and non-HABspecies to specific nutrient inputs

• Conduct retrospective analyses of the temporal andspatial extent of HAB occurrences associated withnutrient loading

• Determine the relative importance of nutrient loadingfrom human activities and natural processes to HABevents

• Compare HAB events in diverse regimes under varyingconditions of eutrophication

1Determine the composition andrelative importance to HABs of

different nutrient inputs associatedwith human activities and natural

processes


The impacts of nutrients from all sources, andtheir potential to lead disproportionately to aHAB event will depend on whether the HABspecies is present in the assemblage and thecomposition of the nutrient pool, as well as thephysics of the water body receiving thenutrients. Equivalent nutrient inputs todifferent systems may have differential effectson HAB development due to difference inecosystem structure and function.

Example Tasks

• Conduct retrospective analyses of thetemporal and spatial extent of HABoccurrences associated with nutrient loading

• Determine the relative importance ofnutrient loading from human activities andnatural processes to HAB events

• Compare HAB events in diverse regimesunder varying conditions of eutrophication


Determine the physiological responses ofHAB and non-HAB species to specificnutrient inputs

Rationale

Nutrient limitation of phytoplankton growthis a fundamental factor that restricts theaccumulation of biomass and may determinethe outcome of competition among species inmixed assemblages. Nutrients can stimulate orenhance the impact of toxic or harmful speciesin several ways. At the simplest level, harmfulphytoplankton may increase in abundance dueto nutrient enrichment, but remain in the samerelative fraction of the total phytoplanktonbiomass (that is, all species are affected equallyby the enrichment). Alternatively, there maybe a selective enrichment of the HAB speciesby nutrient enrichment. It is increasinglyrecognised that certain species or groups of

species have nutritional requirements orpreferences, and therefore may be favouredwhen the environment is altered in such a wayas to increase the relative availability of thepreferred nutrient source.

This concept is often expressed as the nutrientratio hypothesis (Tilman 1977, Smayda 1990,1997), which argues that human activities havealtered nutrient ratios in such a way as to favourharmful or toxic forms. For example, diatoms,the vast majority of which are harmless, requiresilicon in their cell walls, whereas otherphytoplankton do not. Since silicon is notabundant in sewage effluent or agriculturalwastewater runoff, but nitrogen andphosphorus are, the N:Si or P:Si ratios incoastal waters have increased in regionsreceiving sewage effluent. In theory, diatomgrowth will cease when Si supplies aredepleted, but other phytoplankton can continueto proliferate. Red tides of Tolo Harbour inHong Kong exemplify this effect. From 1976to 1989, there was an 8-fold increase indinoflagellate-dominated red tides coincidentwith a 6-fold increase in human population, a2.5-fold increase in nitrogen and phosphorusloading (Lam and Ho 1989).

It was further demonstrated for Tolo Harbourthat when N:P ratios fell below ~10:1,dinoflagellates such as Prorocentrum micans,P. sigmoides, and P. triestrium, increased inabundance (Hodgkiss 2001). In a similarmanner, blooms of Gymnodinium mikimotoiin Tunisian aquaculture lagoons have beenshown to increase when the N:P ratio declinesseasonally (Romdhane et al. 1998).

There are other types of human developmentthat can also affect nutrient ratios. The buildingof dams may decrease the availability of silicateto coastal waters (Zhang et al. 1999). In thedevelopment of the massive Three Gorges Damin the upstream region of the Changjiang(Yangtze River), the potential foreutrophication and ecosystem changes due toalterations in the N:Si or N:P ratios have beengreatly debated (Zhang et al. 1999).


Some phytoplankton species, including HABspecies, may preferentially use organic sourcesover inorganic sources of nutrients when bothare supplied, suggesting that their growth maybe promoted when organic sources areabundant (Cembella et al. 1984, Taylor andPollinger 1987, Berg et al. 1997). For example,Aureococcus anophagefferens has been shownto preferentially use organic nitrogen overnitrate (Lomas et al. 1996, Berg et al. 1997).Such a nutritional preference may be animportant factor regulating the dynamics of thisspecies and co-occurring organisms.Furthermore, some phytoplankton species,including HAB species, may rely onmixotrophy to supplement their carbon ornitrogen requirements, providing an additionaladaptive mechanism to survive and proliferateunder conditions unfavourable for the growthof other algae (Sanders and Porter 1988,

Stoecker 1999). Indeed, the ichthyotoxicdinoflagellate Pfiesteria piscicida is not anautotroph, and consumes fragments ofepidermal tissue and blood cells from affectedfish as well as bacteria and other small algalcells (Burkholder and Glasgow 1997, Lewituset al. 1999).

Several cyanobacterial species (e.g.,Trichodesmium, Anabaena, Nodularia,Aphanizomenon) are capable of fixingmolecular nitrogen and may therefore formmassive blooms in circumstances where thegrowth of other phytoplankton is limited bynitrogen.

While there have been many advances in ourunderstanding of nutrient uptake pathways formany species, these pathways and preferencesare complex. Many HAB species share similarnutrient preferences or uptake mechanisms


Measurements of the rate of uptake of nutrients have proven to be insightful in determiningnutritional preferences of HAB species. In this example, the rates of nitrogen uptake weredetermined using 15N tracer techniques for two different bloom populations. The Aureococcusanophagefferens bloom occurred off Long Island, New York, while the Prorocentrum minimumbloom occurred in Chesapeake Bay, Maryland, U.S.A. Both species exhibited rapid rates ofuptake in short-term incubations, and exhibited preferences for ammonium, urea, and aminoacids over nitrate (adapted from Berg et al. 1997, and Glibert and Fan, unpublished data).

with non-HAB species. The challenge is tounderstand under what conditions specificnutrient preferences may impart an advantageto HAB species.

Example Tasks

• Assess the importance of differentnutritional strategies among HAB speciesand in comparison to non-HAB species

• Quantify the nutrient uptake and growthkinetics for HAB species in relation tocompeting organisms

• Determine the conditions under which aHAB species may adopt alternativenutritional strategies


Determine the effects of varying nutrientinputs on the harmful properties of HABs

Rationale

While relatively few organisms have beenexamined, the available data suggest that theamounts and forms of toxins produced withincertain HAB species may vary withphysiological status, including nutritional state.Cellular toxin content of species from a varietyof taxonomic groups varies dramatically duringnutrient starvation in culture. For example, theabundance of saxitoxins in Alexandriumspecies can vary by more than an order ofmagnitude depending on whether phosphorusor nitrogen is limiting (e.g., Hall 1982, Boyeret al. 1987, Anderson et al. 1990). Likewise,domoic acid production in Pseudo-nitzschiaspecies varies with silicate availability (Bateset al. 1991, Bates and Douglas 1993), andChysochromulina polylepis, theprymnesiophyte responsible for massive fishand invertebrate mortalities in Sweden andNorway in 1987, has been shown to be moretoxic when phosphorus is limiting (Edvardsen

et al. 1990, Granéli et al. 1993). Nutrientenrichment may also stimulate toxinproduction. It has been shown in the laboratory,for example, that urea may stimulate toxinproduction in Gymnodinium breve (Shimizuet al. 1995). Combined nitrogen has also beenshown to enhance Microcystis and Anabaenatoxicity. Clearly, the effects of nutrientavailability on toxicity have major implicationswith respect to our efforts to understand themanner in which HABs are influenced by, and,in turn, impact the environment.

As toxins are secondary metabolites, theirproduction will depend on the physiologicalcondition of the cells (Flynn and Flynn 1995).Differences in toxin production may thereforebe related to changes in the growth rate or thestage of growth of an organism. Production ofalgal toxins can also be modulated by co-occurring bacteria (Bates et al. 1995) and insome cases, bacteria themselves may representautonomous sources of phycotoxins (Kodamaet al. 1988, Doucette and Trick 1995).

The relationship between nutrient availabilityand the development of other potentiallyharmful effects of algae, such as the productionof mucilage, foams, and scums, is not wellelucidated. Blooms of Phaeocystis spp., whichrecur in the Barents Sea, Norwegian fjords, andalong the coast of the North Sea, are wellknown for depositing thick layers of odorousfoam on the beaches (Lancelot et al. 1987). Thefoams are caused by the exudation of protein-rich compounds by the algae, which are thenwhipped into foams by wave action(Richardson 1997). Phaecystis bloomstypically follow spring diatom blooms andappear to develop mucilagenous colonies whennitrate is the dominant source (Lancelot 1995).The negative impacts of the blooms and foams,including the clogging of fish gills and visiblenuisance to beach visitors and fishermen,warrants considerable more effort onunderstanding the relationship betweennutrient availability and these events.


Example Tasks

• Measure toxin production in HAB speciesin culture at different stages of growth andunder different nutritional conditions

• Determine the nutrient-dependent factorsthat regulate toxin synthesis

• Determine the role of nutrient supply in theproduction of noxious foams and scums


Determine the role of nutrient cyclingprocesses in HAB development

Rationale

The effects of nutrient inputs on HABs are notalways direct; there are indirect pathways bywhich nutrients can influence the developmentof HABs. For example, nutrients may beconsumed and/or transformed from one formto another, thereby increasing their

bioavailability for HAB species. On a seasonalscale, in estuarine systems, such as theChesapeake Bay, U.S.A., nutrient input in thespring is largely in the form of nitrate and israpidly assimilated by diatoms, which, in turn,sink and decompose. Subsequently during thewarmer summer months, nitrogen is releasedvia sediment processes in the form ofammonium, which then serves to support anassemblage dominated by flagellates, includingdinoflagellates (Malone 1992, Glibert et al.1995). The shallow, brackish Baltic Sea ischaracterised by efficient cycling ofphosphorus coupled with effective removal ofnitrogen, leading to a prevalence of a low N:Pratio. These conditions are especiallyfavourable for nitrogen-fixing cyanobacteria.Furthermore, cyanobacteria are favoured inconditions where anoxia in the bottom layerleads to a release of chemically boundphosphorus from the sediments. The releaseof phosphorus from this reservoir may prolongthe harmful consequences of anthropogenicloading for years or decades after reductionsin phosphorus input into the system (Carmenand Wulff 1989).


A high biomass bloom of the prymnesiophyte Phaeocystis pouchetii on theBelgian coast. Photo by V. Rousseau, courtesy of Eurohab Science Initiative,1998.

On shorter time scales, nutrients may be takenup by a particular species in one form andreleased in another by the same organism, orby its grazer. The cyanobacteriumTrichodesmium, which forms massive bloomsin tropical and subtropical waters, derives itsnitrogen via the fixation of N

2. However, much

of this nitrogen is rapidly released asammonium and dissolved organic nitrogen(Karl et al. 1992, Glibert and Bronk 1994,Glibert and O’Neil 1999). This releasednitrogen is therefore available to support thegrowth of other microbial populations thatcannot otherwise derive their required nitrogenin nutrient impoverished waters. Numerousconsortial associations involving other nitrogenfixing cyanobacterial bloom taxa (Anabaena,Aphanizomenon, Nodularia) and bacterialepiphytes have been shown to lead to enhancedgrowth of cyanobacterial “hosts” (Paerl 1988,Paerl and Pinckney 1996). Relationshipsbetween nutrient inputs, and the variousprocesses by which nutrients are recycled andtransformed are critical for understandingHAB growth strategies.


Example Tasks

• Determine nutrient transformation andregeneration processes in relation to HABs

• Assess the functional relationships betweenHAB species and the co-occurring non-HABorganisms, in terms of nutrient pathways andfluxes

OUTPUTS


• Guidance for development of policies relatedto eutrophication and HABs

• Improved basis for establishing site selectioncriteria for aquaculture operations

• Quantitative baseline information forintegrated coastal management

Among the toxic dinoflagellates, Pfiesteria piscicida and related species have been implicated ascausative agents of some major fish kills along the east coast of the United States. Although nutritionalstimuli influencing P. piscicida are complex, there are strong indications that this organism maythrive in systems that are impacted by eutrophication, particularly estuaries and tributaries receivingrunoff and/or aerial deposition from agricultural and intensive animal operations.Photos by C. Hobbs and J. Burkholder.

PROGRAMME ELEMENT 3: Adaptive Strategies

INTRODUCTION

HAB species are diverse with respect to theirmorphology, phylogeny, life history transitions,growth requirements, capacity for productionof toxins and other bio-active compounds, andtheir intraspecific and interspecificinteractions. Each species has a differentcombination of characteristics that defines itsecological niche, that is, the suite of factorsthat determines its distribution and activities.Although variations in species-specificcharacteristics are well described for manyHAB organisms, the basis for intraspecificvariability is poorly understood. Furtherresearch is needed to determine the relativecontribution of genetic components versusexpressed characteristics (phenotype) to thisobserved variability.

Adaptations are heritable traits that confer aselective advantage upon those individuals inthe population capable of expressing them. Asfor all species, it can be assumed that manycharacteristics of harmful algae evolved andare maintained by natural selection and are thusadaptive. Adaptations are expressed at differentscales, influencing processes at the level of thecell, colony, whole population, and community.Nevertheless, it must be recognised that not allvariation is adaptive, in the sense that itnecessarily provides a selective advantage. Forexample, morphological variations, such aschanges in cell shape, size, and the productionof spines, microfilaments, and horns in manyphytoplankton species are often considered tobe adaptations. But true adaptations arenotoriously difficult to discriminate from shortterm phenotypic consequences ofenvironmental perturbation. The challenge isto define unique adaptations of HAB speciesthat account for their survival and persistence,and in some instances, their dominance duringbloom events. By understanding the

adaptations of different HAB species, it shouldbe possible to describe and predict patterns ofspecies abundance and harmful effects asfunctions of hydrographic processes, nutrientdistributions, and community interactions.Improved generalisations about the causes andconsequences of HABs would be particularlyuseful in management and mitigation of theireffects.

It might be argued that once the physiologicalcharacteristics of a single species are welldescribed, it should be possible to predict itspresence and abundance, based on someknowledge of the environmental conditions. Acorresponding view is that a given species willhave maximum growth potential in conditionswhere environmental parameters – such aslight, temperature, nutrient concentrations, orturbulence – are optimal for vegetative growth.However, the response of organisms in naturalecosystems is much more complicated; multi-form life strategies, migratory behaviour,complex trophic interactions, and small-scalephysical-biological interactions allow a speciesto exploit a spectrum of environmentalconditions. By multi-faceted exploitation ofecological niches, the species may be able tosurvive and thrive in situations apparently farfrom its optimal requirements. In addition,while many classical physiological studiesfocus on the response of an organism to a singleparameter, physical, chemical, and biologicalparameters interact and often varyindependently in nature, thereby producingnon-linear effects. Clear examples are the roleof small-scale turbulence on nutrientassimilation (Karp-Boss et al. 1996) andgrazing (Marrasé et al. 1990) and therelationships between water mixing andphotoacclimation (Lewis et al. 1984). In thecontext of particular ecosystems, interactionsbetween organisms and water circulation areessential to understand transport, population


confinement, and persistence of certain blooms(Anderson 1997, Hallegraeff and Fraga 1998,Garcés et al. 1999).

Information on adaptive strategies shouldprovide the physiological bases for explainingwhy HAB species occur and proliferate. Thiscan be used to address relationships betweenHABs and eutrophication, to complementstudies of biodiversity and biogeography, tosupport research on population dynamics incomparable ecosystems, and to guide theconstruction and parameterisation of modelsto predict HABs. The integration of thisknowledge along a broad range of temporal andspatial scales will allow the development ofintegrative models coupling the biology of aspecies with physical and chemical processes.


OVERALL OBJECTIVE

THE STRATEGY

GEOHAB will foster the application ofcommon techniques and the development ofinnovative technologies to enable detection ofparticular cell properties. Investigations ofdifferent HAB species and different strains ofa single species from ecosystems worldwideis essential to ascertain their growthcharacteristics, physiological properties, andpersistence in specific ecosystems. GEOHABwill also encourage the establishment ofreference collections of HAB species.

What are the unique adaptations ofHAB species and how do they help toexplain their proliferation or harmfuleffects?



Define the characteristics of HAB speciesthat determine their intrinsic potential forgrowth and persistence

Rationale

There is considerable diversity among HABspecies with respect to patterns of growth andbloom formation in natural ecosystems. Thereare numerous explanations for the differentpatterns of bloom initiation and development,many of which are the result of uniqueadaptations of HAB organisms. Studies of cellcharacteristics related to vegetative growth andlife-history transitions and their response toenvironmental factors are therefore essentialto understanding the population dynamics ofHABs.

The influences of important environmentalfactors, such as light, temperature, andturbulence, on the physiological, behavioural,and life history processes related to the growthof harmful algae have been quantified for onlya few clones of some HAB species.Nevertheless, comprehensive data on thedegree of intraspecific variability are rare andthe interactions of physiological, behavioural,and life history processes with keyenvironmental factors are not well known.

There is evidence of substantial differencesamong populations of the same speciessampled from different locations and atdifferent times (Bolch et al. 1999, Doblin etal. 1999). It is therefore important to studygrowth and behavioural characteristics ofstrains of a particular species from a numberof globally distributed locations.Understanding the effects of all these factor

PROGRAMME ELEMENT 3

Define the particular characteristicsand adaptations of HAB species thatdetermine when and where they occurand produce harmful effects

37

Figure 3.1 Summary of Programme Element 3: Adaptive Strategies.

3Describe and quantify chemical andbiological processes affecting species

interactions

• Identify key bio-active compounds that mediatespecies interactions

• Assess the importance of toxin production in selectivegrazing

• Characterise modes of action of bio-active compoundson other organisms

• Identify morphological, physiological, life-history, andbehavioural characteristics that form the basis forcommon patterns of species in nature

• Assess the role of toxins and other bio-activecompounds in determining functional groups

4Identify the functional role of cell

properties

• Quantify the effects of small-scale turbulence onnutrient acquisition, growth, and motility

• Assess the factors controlling vertical migrationbehaviour

• Define the effect of fluctuating environmental regimeson growth processes and life history events includingexcystment and encystment.

• Determine the functional role of size, shape, mucusproduction, and the formation of colonies oraggregates

2Define and quantify biological-

physical interactions at the scale ofindividual cells

1Define the characteristics of HAB

species that determine their intrinsicpotential for growth and persistence

• Determine tolerance ranges and optima for growthand toxin production in response to a suite ofenvironmental variables

• Culture and compare growth of multiple strains ofindividual species under different environmentalconditions

• Characterise environmental influences on life historyevents, including resting stages

OVERALL OBJECTIVE Programme Element 3: Define the particularcharacteristics and adaptations of HAB species that determine when andwhere they occur and produce harmful effects

OUTPUTS• Establishment of HAB strains and species within an international network of reference culture

collections• Identification of key adaptive strategies of particular HAB species• Ecologically-based classification of different species according to their adaptations and

characteristics• Quantification, parameterisation, and prioritisation of ecophysiological processes at the cellular level

for incorporation into models


interactions requires the use of diverse strainsof HAB species in culture under carefullycontrolled multi-dimensional experimentalregimes.

Many HAB species have complex life historiesthat include different morphotypes as well asthe formation of various types of resting stages.For example, in certain dinoflagellates andraphidophytes, the formation of resting stages(or cysts) with resistant walls expands thetolerance range of the species and thereforeallows extension of its geographicaldistribution. The induction of sexuality canhave important short-term consequences for thepopulation growth. During the initiation ofsexual reproduction, the generation timeincreases dramatically as the asexual(vegetative) cell division rate declines,effectively to zero for those cells that becomegametes. Although not all cells in a populationparticipate in sexual reproduction, the netpopulation growth rate may even be negativebecause of reduction in cell numbers throughfusion of gametes and subsequent hypnozygoteformation.

Although the critical importance of restingcysts in the bloom strategies of HAB speciesis recognised (Anderson 1998, Imai and Itakura1999), for most HAB species there aresignificant unknown elements, for example, thesexual basis for resting cyst formation(heterothallism, homothallism, matingsystems), dormancy period, encystment and

Cell growth can be defined in many ways,including changes in cell number, size, volume,or mass. With respect to HAB dynamics, thefollowing conventional definitions arecommonly used:

Growth rate is the change in cell numberwith time. The growth rate is limited byintrinsic factors, such as the rate of DNAreplication in the cell cycle, as well as byexternal conditions.

Generation time is the time required forcells to double in number (also called the“doubling time”). The time for one completecell division cycle is called the division time.For many bloom-forming species, this typicallyranges from several hours to a few days.

Population growth rate is the net rate ofchange in cell numbers in a population, usuallyexpressed within a defined water volumeunder natural conditions. This parameter isestimated from the increase in cell numbersthrough time, and thus includes cell lossesdue to physical transport and biological factorssuch as grazing.


In the life history of a typical cyst-formingdinoflagellate, such as that depicted herefor Gymnodinium catenatum, there is analternation of asexual stages (vegetativecells) with sexual forms (zygotes). Thefusion of gametes formed from vegetativecells results in the formation of a swimmingplanozygote, which subsequently loses itsflagella to form a zygotic resting stage (orcyst). Both external environmental triggers(light, temperature, nutrients) andendogenous rhythms have been implicatedin inducing life cycle transitions in variousspecies. Transitions between vegetative andresting stages can influence populationdynamics by determining the size of the“seed” stock or inoculum for subsequentbloom initiation.

excystment cues, and the numerical and geneticcontribution of cysts to bloom dynamics.Complete descriptions of life cycles, includingthe definition of mating-type systems,dormancy requirements of resting stages, andthe effect of environmental factors on inducingcyst production and germination are needed.

The motile asexual stage of Chattonellaantiqua, a marine raphidophyte implicated innumerous incidents of mass mortalities of fish,may undergo sexual reproduction underunfavourable environmental conditions afterbloom events. A roughly spherical haploidresting cyst is formed and persists in thesediment until excystment is triggered,typically by a change in the environmentalregime, such as a shift in temperature.

One of the most common harmfulconsequences of blooms of Phaeocystis speciesis the nuisance caused by the dense foamsproduced by the colonial life-cycle stage.Although several researchers have addressedthe transition between colonial and flagellatedstages, many aspects of the life cycle of thisspecies, as well as the environmental factorsdriving transitions among the different stages,are still hypothetical (Rousseau et al. 1994).Such stage transitions are clearly subject tostrong selective pressure and environmentalregulation. The challenge is to describe the lifehistory strategies and to establish how theyrespond to environmental forcing in theecosystems in which they are expressed.

Example Tasks

• Determine tolerance ranges and optima forgrowth and toxin production in response toa suite of environmental variables

• Culture and compare growth of multiplestrains of individual species under differentenvironmental conditions

• Characterise environmental influences onlife history events, including resting stages


Define and quantify biological-physicalinteractions at the scale of individual cells

Rationale

The mechanisms through which HAB speciesinteract with their environment must becharacterised to understand and predict theirdistributions and effects in natural waters.

Small-scale turbulence needs to be consideredbecause it may have significant consequencesfor the growth and decline of HABs throughits influence on the transport of nutrients, andby direct impairment of growth (Estrada andBerdalet 1998). Some phytoplankton,including Alexandrium species, are verysensitive to turbulent motion even at low levels(White 1976, Thomas et al. 1995), whereasothers seem to benefit from higher levels ofturbulence that enhance nutrient availabilityand uptake, thereby increasing the rate of cellgrowth and division (Kiørboe 1993). Diatomshave recently been shown to react within a few

PROGRAMME ELEMENT 3

Reference culture collections are essential instudies of adaptive strategies of HAB species.Such collections provide genetically consistentstrains that can be shared among laboratoriesfor experiments under defined environmentalconditions. Photo by T. Kana.

40

seconds to external shear and chemical stimuli(Falciatore et al. 2000), faster than thevariations in mechanical stress within smalleddies under ocean conditions. The generalityand ecological significance of such responsesshould be assessed for HAB species.

Physical processes, such as wind-mixing,convection and upwelling, can profoundlyinfluence the irradiance field experienced byphytoplankton, and thus the conditions forphotosynthesis and growth. Consequently,phytoplankton species have developed a rangeof physiological and behavioural adaptationsfor different mixing regimes, which mayinclude vertical migration (Cullen andMacIntyre 1998). Some species are adapted toexploit fluctuating irradiance associated withrapid vertical mixing (Ibelings et al. 1994).

Adaptations for life in strongly stratified watersinclude physiologically regulated changes inbuoyancy (Walsby and Reynolds 1980) andmotility (Kamykowski 1995), resulting invertical migration or the maintenance of stable

subsurface layers of phytoplankton. Theseadaptations must be understood to explain theselection for HAB species in particularhydrographic regimes.

Physical processes strongly influence thebiological responses of phytoplankton cells, butbiological processes can also influence physicalcharacteristics of the water. For those HABspecies that produce dense blooms, theprocesses of flocculation and deflocculationmay change their physical and chemicalenvironment, as well as the spatio-temporaldistribution of cells. The production anddisintegration of cellular flocculations andcolonies is partly a non-linear interaction ofcell stickiness and turbulence (Kiørboe andHansen 1993, Hansen et al. 1995).Flocculation, cell adhesion, and aggregationneed to be better understood, as do the effectsof water movement and organism motility oncommunication among cells and colonies, andbetween these organisms and their physico-chemical environment (Jenkinson and Wyatt1992).

Research on the importance of the size andshape of organisms, including phytoplankton,has gradually progressed for several decades(such as Margalef 1978, Vernadskiy 1978,Kamenir and Khaylov 1987, Reynolds 1997).However, this work has been hampered bydifficulties in assessing the contributions bysoft structures, such as mucus sheaths andprocesses projecting from pores, as well as hardstructures (such as siliceous setae) to thefunctional dimensions of organisms. Thesefeatures, which may represent adaptations forparticular hydrodynamic regimes, can also beresponsible for harmful effects, such as theclogging or laceration of gills of fish. Studiesof functional size and shape of HAB speciesand how morphological features vary inresponse to turbulence (as well as to otherenvironmental influences) is thus essential toa fundamental understanding of both HABpopulation dynamics and the expression ofharmful effects.


Many morphological and physiologicalcharacteristics of HAB species may be adaptivestrategies. Examples shown in this panelinclude: buoyancy/sinking regulation throughadjustment of ion balance, gas vacuoles, colonyformation, and spine production, and the useof external wings/rudders and chain formationto optimize swimming capacity.

Example Tasks

• Quantify the effects ofsmall-scale turbulenceon nutrient acquisition,growth, and motility

• Assess the factorscontrolling verticalmigration behaviour

• Define the effect off l u c t u a t i n genvironmental regimeson growth processesand life history eventsincluding excystmentand encystment

• Determine thefunctional role of size,shape, mucus production, and the formationof colonies or aggregates


Describe and quantify chemical andbiological processes affecting speciesinteractions

Rationale

Harmful algae do not exist in isolation innatural ecosystems and thus they are influencedby interactions between individual cells of thesame and other species. Food-web interactionshave a profound effect on the populationdynamics of HAB species. Processes such ascompetition and grazing can strongly affect thenet growth rates of phytoplankton in nature.

Bio-physical constraints may have a profoundeffect on the microenvironment surroundingcells of HAB species and their competitors andpredators. For example, even a low level ofmucus as produced by some harmful algae maymake respiration (Jenkinson and Arzul 1998)

and filter-feeding more energetically costlyand slower. Mucus tends to show its mostpronounced properties, such as increasedpolymeric viscosity and elasticity, inassociation with algae, with increasing effectvarying with increasing phytoplanktonabundance (Jenkinson and Biddanda, 1995).This is consistent with abundant organismshaving a relatively greater potential to interactwith each other and to change theirenvironment to their selective advantage.

Chemical interactions (including the effects oftoxins and other bio-active compounds) arelittle understood but they may be critical forcommunication within populations of HABspecies, as has been hypothesised forAlexandrium (Wyatt and Jenkinson 1997). Inaddition, these substances could influencegrowth and the outcomes of interspecificinteractions in the presence of competitors(allelochemical effects) and predators, asshown in the case of Heterosigma akashiwo(Pratt 1966, Tomas and Deason 1981). Theproduction and utilisation of trace organicsubstances such as vitamins and chelators alsorepresent biological processes that can strongly


A flowchart describing the relationships between environmental forcing,physiological rate processes, biochemical pool concentrations, cell division,and behaviour for a hypothetical dinoflagellate (modified from Kamykowskiet al. 1999). The circled letters refer to functions that must be defined ina detailed model.

influence interactions amongspecies.

The production of phycotoxins aspotential anti-predator defencemechanisms is a good example ofa chemically mediated interaction.Toxin production may haveimportant implications for themaintenance and dynamics ofharmful algal blooms by inhibitinggrazing. To date, however,evidence that some HAB speciesare in fact toxic to their potentialgrazers such as copepods, is ratherequivocal (Turner and Tester 1997). Forexample, whereas some authors have reportedpre-ingestive rejection of toxic Alexandriumstrains by copepods (Huntley et al. 1986),others have found that some copepods wereunaffected and fed at high rates on both toxicand non-toxic Alexandrium cells (Teegardenand Cembella 1996). Most of these studies,however, both in the laboratory and in situ,have been carried out during the course ofshort-term (one day) grazing experiments. Afurther caveat is that the grazing responses ofcopepods are highly species-specific and mayvary according to the state of pre-conditioning(starved versus replete individuals), the preyconcentration, and the diversity of the foodregime offered. Furthermore, few studies havebeen made to evaluate long-term effects ofexposure to algal toxins, as would be the caseduring a HAB bloom lasting several days toweeks, when zooplankton grazers would haveless choice in available prey species. Finally,the sub-lethal effects on zooplankton grazersof acute exposure to phycotoxins andconsequent effects on fertility, quality andquantity of egg production, and hatchingsuccess must be investigated as a long termfactor in the “top-down” control of bloomdynamics.

HAB species can employ different trophicstrategies, including the utilisation of organiccompounds (Carlsson and Granéli 1998),

nitrogen fixation, andconsumption of prey organisms(e.g., mixotrophy; Granéli andCarlsson 1998, Hansen 1998).These processes and the extent towhich they contribute to bloomsare not well known for most HABspecies. However, specific trophicstrategies may be crucial toproliferation of HAB species andmust be investigated in the contextof adaptations, effects ofeutrophication, and the modellingof ecosystem processes.

Example Tasks

• Identify key bio-active compounds thatmediate species interactions

• Assess the importance of toxin productionin selective grazing

• Characterise modes of action of bio-activecompounds on other organisms

Laboratory studies are essential tounderstanding adaptive strategies. Controlledexperiments with cultured cells can be usedto discriminate genetic factors that are trulyadaptive, in that they offer a selectiveadvantage, from short-term responses toenvironmental conditions. Photo by M Trice.


Many bloom-formingflagellates havephagotrophic capabilities –the ability to engulf andingest particulate materialfor nutritional purposes,even, in some cases, largeprey species as is shownhere.


Identify the functional role of cell properties

Rationale

Harmful species belong to several distinctphylogenetic groups, and therefore havedifferent morphologies, ecophysiologicalrequirements, and growth dynamics.Ecological diversity is evident even at theintraspecific level. For example, Heterosigmaakashiwo is able to thrive in many differentenvironmental conditions (see Smayda 1998for a review), and different bloom mechanismshave been suggested for Gymnodiniumcatenatum in Tasmanian and Atlantic Spanishwaters, respectively (Hallegraeff and Fraga1998).

Nevertheless, convergentm o r p h o l o g i c a l ,physiological andecological traits are alsocommon among harmfulspecies, despitec o n s i d e r a b l ephylogenetic distances.To reduce the naturalcomplexity and facilitatethe development ofconceptual andnumerical models ofHAB dynamics, it isdesirable to recognise,among HAB species,common patterns ofresponse toenvironmental factors.These common patternsmay be based onsimilarities inm o r p h o l o g i c a l ,ecophysiological (suchas life strategies, trophiccharacteristics), orbehavioural (such asswimming, migration)

adaptations. In this context, functional groupscan be recognised as sets of organisms sharinga particular suite of adaptations.

The aim of the specific objective consideredhere is complementary to the aspect of thelarge-scale ecosystem studies that focuses onthe identification of groups of speciescommonly co-occurring in nature. The speciesconstituting these recurrent groups can beconsidered as examples of ecologicalconvergence; their study can help to identifythe cellular properties forming the basis fortheir common distributional patterns.

Efforts to interpret the ecological implicationsof morphological or other phenotypicphytoplankton characteristics have been

reviewed by Sournia(1982), Elbrächter(1984), Fogg (1991), andKiørboe (1993), amongothers. However, whilesome cellular properties(such as size) have welldescribed ecologicalimplications (e.g., fastersinking for largerorganisms), thesignificance of manyother features isunknown.

The range ofmorphological variabilityexhibited among HABspecies is impressive.Some species occur assingle cells whereasothers may formcolonies, including largeaggregates formed bymucilage production.Chain formation inflagellated HAB specieshas been shown toenhance swimming speed(Fraga et al. 1989). Cells

PROGRAMME ELEMENT 3

What are “life-forms” or “functionalgroups”?

“… ‘life-forms’… can be conceived asthe expression of adaptationsyndromes of organisms to certainrecurrent patterns of selective factors.I have chosen as principal factors thoserelated to the supply of external energy,i.e., supply of nutrients and decayingturbulence.” (Margalef 1978).

“Functional groups are groupings ofspecies based on physiology,morphology, life history, or other traitsrelevant to controls on an ecosystemprocess…” (Hooper and Vitousek 1997).

“… a functional group is a non-phylogenetic classification leading to agrouping of organisms that respond ina similar way to a syndrome ofenvironmental factors… a functionalgroup is the basis for a context-specificsimplification of the real world to dealwith predictions of the dynamics of thesystems or any of their components…”(Gitay and Noble 1997).

44

may be non-motile and only passively subjectto dispersion, flagellated and thus capable ofswimming, or non-motile, but able to regulatetheir cell buoyancy. Certain species may exhibitaspects of all of these properties at variousstages of their life history.

Differences in size, shape, and surface/ volumeratio influence properties such as nutrientuptake capacities and reaction to small-scaleturbulence (Karp-Boss et al. 1996). In addition,size and shape affect grazing vulnerability andthe spectrum of potential grazers.

Different functional groups can be representednot only by different species, but also bydifferent stages of the cell division or life cycle.Alternative life histories of HAB organismscreate both functional diversity within a speciesand commonalities among species. Forexample, some organisms undergoasynchronous cell division, apparentlyindependent of the photoperiod, whereas othersmay divide only during a narrow window ofthe light/dark cycle. The life history of a speciesmay include resting stages – often but notinvariably with an obligatory dormancy periodbefore resuming vegetative reproduction(Pfiester and Anderson 1987).

Another aspect of functional groups refers totoxic properties. Species with differentmorphologies and phylogenetic affinities, andfound in diverse habitats, may neverthelessproduce a similar suite of toxins. For example,PSP toxins are found in species of thedinoflagellates Alexandrium, Gymnodinium,Pyrodinium, and certain strains of thecyanobacteria Aphanizomenon and Anabaena(Cembella 1998). Conversely, toxin productionmay vary among strains of the same speciesand depend upon environmental factors (suchas nutrient concentration).

Example Tasks

• Identify morphological, physiological, life-history, and behavioural characteristics thatform the basis for common patterns ofspecies in nature

• Assess the role of toxins and other bio-activecompounds in determining functionalgroups

OUTPUTS


• Establishment of HAB strains and specieswithin an international network of referenceculture collections

• Identification of key adaptive strategies ofparticular HAB species

• Ecologically-based classification ofdifferent species according to theiradaptations and characteristics

• Quantification, parameterisation, andprioritisation of ecophysiological processesat the cellular level for incorporation intomodels


Time-depth fluorescence showing diel verticalmigration of the toxic dinoflagellate Gymnodiniumcatenatum at Killala Bay in the Huon Estuary,Tasmania. In vivo fluorescence of chlorophyll pigmentis used to track the rhythmic movement of cells inthe water column. From CSIRO Marine Research.

PROGRAMME ELEMENT 4: Comparative Ecosystems

INTRODUCTION

HABs occur in pelagic and benthic ecosystems,and these can often be classified operationally,according to their physical and chemicalcharacteristics and their particular biology.Comparative approaches have a long traditionin ecology but have been relatively underusedin aquatic sciences (Cole et al. 1991). There isa need therefore to develop marine ecosystemtypologies and to then classify marineecosystems into these similar types for thepurposes of comparison.

Comparisons of ecosystems allow the synthesisof knowledge and data needed to group HABsfrom similar habitat types and to distinguishthe mechanisms controlling their populationdynamics. The adaptive strategies of key HABspecies will also be better understood in thecontext of particular ecosystem types orparticular processes.

Having identified characteristic marineecosystem types and having classifiedecosystems, understanding the response ofHABs to perturbation or change within thesesystems (both natural, such as climatevariability, and anthropogenic, such aseutrophication) is important. Similarecosystems should respond in broadly similarways, therefore the identification of earlywarning indicators of system changes withinand across ecosystem types will greatly helpprediction and possible mitigation of the effectsof change on the incidence of HABs. It willalso permit extension of predicted responsesto similar but less well studied ecosystems.Identification of divergences from predictedresponses will also be informative.


OVERALL OBJECTIVE

THE STRATEGY

GEOHAB will foster similar fieldinvestigations in comparable ecosystems fromdifferent regions, accompanied by theexchange of technology and data.Classification of systems based on physical,chemical, and biological regimes will bepossible through GEOHAB. Through such acomparative approach, the identification of thecritical processes controlling HABs in differenthydrographic, chemical, and biological regimeswill be possible.


To what extent do HAB species, theirpopulation dynamics, and communityinteractions respond similarly undercomparable ecosystem types?

PROGRAMME ELEMENT 4

To identify mechanisms underlyingHAB population and communitydynamics across ecosystem typesthrough comparative studies

46

Figure 4.1 Summary of Programme Element 4: Comparative Ecosystems.

OVERALL OBJECTIVE Programme Element 4: To identify mechanismsunderlying HAB population and community dynamics across ecosystemtypes through comparative studies

1Quantify the response of HAB species

to environmental factors in naturalecosystems

• Develop methods for in situ estimation of physiologicalrates of HAB species

• Incorporate studies of resting stage dynamics intofield investigations

• Parameterise the vertical migration and buoyancyregulation of HAB species in natural ecosystems

2Identify and quantify the effects ofphysical processes on accumulation

and transport of harmful algae

• Characterise the hydrodynamic processes of particularecosystems and prioritise their effects on HABdynamics

• Identify and quantify the specific suite of biologicalfeatures associated with HABs in particularhydrographic regimes

• Measure key biological variables at spatial andtemporal scales consistent with those of the physicalvariables

3Identify and quantify the community

interactions influencing HABdynamics

• Determine the effects of bioactive compounds withinnatural communities on HAB dynamics

• Determine the importance of density-dependentprocesses in HABs

• Quantify the effects of microbial pathogens on HABs• Determine the role of grazing control in HAB dynamics

4Define functional groups in

communities containing HABspecies

• Determine groups of co-occurring taxa or assemblageswithin given ecosystem types

• Establish the distribution of functional groups andtheir relationship to environmental factors

• Identify common morphological, physiological, andlife-history features within HAB species and define theenvironmental characteristics that support thesespecific features

OUTPUTS• Identification of common physiological and behavioural characteristics of HAB species in given

ecosystem types• Quantitative descriptions of the effects of physical forcing on bloom dynamics• Bases for developing management and mitigation strategies tailored to the characteristics of

particular organisms


Example ecosystem types, as defined by their bathymetry, hydrography, nutrient status,productivity, and trophic structure:• Upwelling systems, such as those off the coast of Portugal and Spain, Peru, Mazatlan

in Mexico, the west coast of the United States, Australia, Japan, West Africa, andSouthern Africa.

• Estuaries, fjords, and coastal embayment systems, as in the United States, Canada,Australia, southeast Asia, Philippines, Mexico, Scandinavia, and Chile.

• Thin-layer producing systems along most coasts, including the Atlantic coast ofFrance, Sweden, California, and in East Sound, Washington.

• Coastal lagoon systems such as in the United States, Mexico, Brazil, and France.

• Shelf systems affected by basin-wide oceanic gyres and coastal alongshore currentssuch as off the northwestern European coast, the Gulf of Mexico and Gulf of Mainein the United States, and off the coast of southeastern India.

• Systems strongly influenced by eutrophication, such as in Hong Kong, Black Sea,Baltic Sea, Adriatic Sea, Seto Inland Sea of Japan, and the mid-Atlantic regions ofthe United States.

• Brackish or hypersaline water systems such as the Baltic Sea, St. Lawrence, DeadSea, and Salton Sea.

• Benthic systems associated with ciguatera in the tropics or DSP in temperate waters.The above list is not intended to be comprehensive or exclusive, and these systemsare offered only as examples of the types of ecosystems that could be studied andcompared within GEOHAB. Upper right photo by F. Kristo.



Quantify the response of HAB species toenvironmental factors in natural ecosystems

Rationale

Studies of species responses at the ecosystemlevel are essential to understanding thepopulation dynamics of HABs. The specificgrowth rate of a species is determined by manymetabolic processes, including photosynthesis,and nutrient uptake and assimilation, all ofwhich are under genetic control. The netpopulation growth of a species is controlledby external environmental factors, includingphysical transport, grazing, and othercommunity interactions. An important step inthe investigation of HABs should therefore bea series of studies that characterize the responseof populations to thephysical, chemical, andbiological characteristicsof the naturalenvironment.

For example, turbulencehas significantconsequences for thegrowth and decline ofHABs by influencing thetransport of nutrients,the mixing ofphytoplankton throughgradients of light, and bydirect impairment ofgrowth. Many HABspecies are motile, andunder certaine n v i r o n m e n t a lconditions theirswimming behavior orbuoyancy may result inthe formation of high-density patches (e.g.,Franks 1992, Cullen andMacIntyre 1998,Kamykowski et al.

1998). Diel vertical movement by motile cellsin a stratified environment undoubtedly hasfunctional significance, maximizing encounterfrequencies for sexual reproduction,minimizing grazing losses, and allowing cellsto optimize nutrient acquisition at depth andlight-dependent photosynthetic reactions nearthe surface. Some cyanobacterial species areable to regulate their vertical positioning in thewater column by synthesis and collapse of gasvesicles and by accumulation of photosynthetic“ballast.” The challenge is to identify whichconditions will cause a particular species tobloom or conversely to cause its strategy to fail.

Another survival and growth strategy thatshould be explored involves the benthic restingstages of many HAB species. These cysts orspores provide a recurrent seed source orinoculum for planktonic populations. The


The distribution of Alexandrium tamarense cysts in the nearshore watersof the Gulf of Maine. Two distinct seedbeds are evident in the offshorewaters. These are thought to play an important role in the timing andlocation of bloom development for this toxic dinoflagellate, but new methodsand approaches are needed to quantify this input. (Source: D.M. Anderson,unpublished data)

capacity to form resting stages may be a criticalfactor in determining not only the geographicdistribution of species, but also their cellularabundance over time (Anderson and Wall 1978,Anderson 1998, Imai et al. 1998). Therefore,it is important to establish the role of variousenvironmental factors in regulating restingstage formation and germination, and toquantify these processes.

These are a few examples of the manyphysiological, behavioural, and life historyprocesses of HAB species that interact withenvironmental factors. Population studiesshould allow the identification of the commonmechanisms and processes that underlie thedynamics of HAB species occurring withinparticular ecosystem types.

Example Tasks

• Develop methods for in situ estimation ofphysiological rates of HAB species

• Incorporate studies of resting stagedynamics into field investigations

• Parameterise the vertical migration andbuoyancy regulation of HAB species innatural ecosystems


Identify and quantify the effects of physicalprocesses on accumulation and transport ofharmful algae

Rationale

The geographic range, persistence, andintensity of HABs are determined by bothphysical and biological factors. For example,the initiation of a bloom requires successfulrecruitment of a population into a water mass.This may result from excystment of restingcells during a restricted set of suitableconditions (such as Alexandrium in the Gulf

of Maine; Anderson and Keafer 1987);transport of cells from a source region whereblooms are already established (such asGymnodinium catenatum in northwest Spain;Fraga et al. 1988), and exploitation of unusualclimatic or hydrographic conditions (such asPyrodinium bahamense in the Indo-WestPacific; Maclean 1989). Once a population isestablished, its range and biomass are affectedby physical controls such as the transport andaccumulation of biomass in response to waterflows (such as Franks and Anderson 1992),by the swimming behaviour of organisms(Kamykowski 1974, Cullen and Horrigan1981) and by the maintenance of suitableenvironmental conditions (includingtemperature and salinity, stratification,irradiance, and nutrient supply; Whitledge,1993). Thus, physical forcings, nutrient supply,and the behaviour of organisms all interact todetermine the timing, location, and ultimatebiomass achieved by the bloom, as well as itsimpacts.

Physical processes that are likely to influencethe population dynamics of HAB species areoperative over a broad range of spatial andtemporal scales. Large-scale, mean circulationaffects the distribution of water masses andbiogeographical boundaries. Theunderstanding of the main features of meancirculation is sufficient to devise models of thecirculation of many estuaries, coastal currents,and upwelling areas. Time-dependent,atmospherically and tidally-forced models areavailable for many geographic regions (suchas the North Sea, Baltic, Bay of Biscay, Gulfof Maine and Gulf of Mexico) and may be usedto predict the movement and development ofHABs, although considerable uncertaintyremain, however, in forecasting theirdispersion. Many examples of the influence ofmesoscale circulation on HAB populationdynamics may be found. Eddies from the deepocean can, for example, impinge on slope andshelf regions, affecting the transfer of algaeand nutrients across the shelf break. This typeof transport may be involved in the delivery of


the Florida red tide organism Gymnodiniumbreve to nearshore waters from an offshorezone of initiation (Steidinger et al. 1998).Although eddies are difficult to resolve throughsampling at sea, they can usually be detectedthrough satellite remote sensing of temperature,sea-surface height, or ocean colour.

Processes at intermediate scales result in theformation of convergence zones, fronts, andupwelling. There are many examples of theimportance of fronts in phytoplankton bloomdynamics, and several prominent studiesinvolve HAB species (Franks 1992). Forexample, a linkage has been demonstratedbetween tidally generated fronts and the sitesof massive blooms of the toxic dinoflagellateGymnodinium mikimotoi (= Gyrodiniumaureolum) in the North Sea (Holligan 1979).The pattern generally seen is a high surfaceconcentration of cells at the frontalconvergence, contiguous with a subsurfacechlorophyll maximum that follows the slopinginterface between the two water massesbeneath the stratified side of the front. The

surface signature of the chlorophyll maximum,sometimes visible as a red tide, may be 1-30km wide. Chlorophyll concentrations aregenerally lower and much more uniform on thewell-mixed side of the front. The significanceof this differential biomass accumulation isbest understood when movement of the front

and its associated cells brings toxic G.mikimotoi populations into contact with fishand other susceptible resources, resulting inmassive mortalities. This is an example wheresmall-scale physical-biological coupling resultsin biomass accumulation, and larger-scaleadvective mechanisms cause the biomass tobecome harmful.

The rias of northwest Spain are a group ofoceanic bays noted for their prolific productionof blue mussels. Here, PSP toxicity is notprimarily due to the in situ growth of toxic cells,but rather to the transport and introduction ofblooms that originate elsewhere. Similarmeteorology, hydrography, and patterns ofPSP are found in the California and Benguela


The processes regulating cyanobacterial blooms in the Baltic have been identified at the scales depictedabove (Kononen and Leppänen 1997).

current systems. A comparative approach maytherefore aid in developing a fundamentalunderstanding of the linkage between large-scale forcings and the pattern of PSP toxicity.

The importance of small-scale physicalprocesses in HAB development is observed inthe layering of the physical, chemical, andbiological influences in stratified coastalsystems. Off the French coast, for example, athin layer of dinoflagellates, including the HABspecies Dinophysis cf. acuminata, has beenobserved in the proximity of the thermocline(Gentien et al. 1995). Several HAB species areknown to form thin, subsurface layers ofuncertain cause and unknown persistence, atscales as small as 10 cm in the vertical and aslarge as 10 km in the horizontal dimension.One simple kinematic explanation is that theselayers result from the stretching of horizontalinhomogeneities by the vertical shear ofhorizontal currents. This produces anenvironment potentially favouring motile

organisms that can maintain their position inthis layer. Resolution of the biological,physical, and chemical mechanisms underlyingthese aggregations should be an important areaof GEOHAB investigation.

Tidal- and wave-induced currents generateturbulence in the bottom boundary layer. Onekey element of this interaction involves thebenthic resting stages of many HAB species,which serve to re-colonise the water column.The magnitude and timing of the contributionof motile cells through cyst germination, andthe physical, chemical, or biologicalmechanisms that influence that process aremajor unknowns in HAB dynamics (Anderson1998). Although cyst germination is of greatimportance to the bloom dynamics of manyHAB species, it is still not known whether thegermination that occurs is gradual andpredominantly from the surface sediments, oris episodic and dominated by the resuspensionof sediments following erosion of deepersediment layers.


A schematic representation of the complex arrayof physical processes affecting the shelf zone ofthe Benguela upwelling system (Shannon et al.1990), a region prone to HABs. Wind is adominant factor at all spatial scales, having adirect influence on large-scale currents, localupwelling and frontal dynamics, and thedynamics of the surface mixed layer.Consequently, the formation of red tides hasbeen closely linked to the prevailing winds ofthe Benguela (Pitcher et al. 1998). The seasonaldevelopment of subsurface dinoflagellate bloomsis associated with increased stratification duringthe upwelling season, which depends in a fairlypredictable way on the wind and insolation. Thedinoflagellate populations appear as a surfacebloom in the region of the upwelling front, whichis displaced from the coast during the activephase of upwelling. Red tides form and impacton the coast following relaxation of upwellingand the onshore movement of the upwellingfront, as cross-shelf currents become weaker anddirected onshore. During these periods ofdecreased wind stress, net poleward surface flowis responsible for the southward propagation ofred tides.

The above represent some well establishedexamples of the effects of physical processeson the distribution of harmful algae. There are,however, many examples where the physicalprocesses common to particular ecosystems arepoorly characterised and understood andtherefore their influence on HAB speciesremains uncertain. Comparative studiesprovide an opportunity to ascertain anddescribe the physical processes common toparticular ecosystem types and to evaluate theimportance of these processes to thedistribution of HABs within those ecosystems.

Example Tasks

• Characterize the hydrodynamic processes ofparticular ecosystems and prioritise theireffects on HAB dynamics

• Identify and quantify the specific suite ofbiological features associated with HABs inparticular hydrographic regimes

• Measure key biological variables at spatialand temporal scales consistent with those ofthe physical variables


Identify and quantify the communityinteractions influencing HAB dynamics

Rationale

The growth and accumulation of the cells thatcause HABs, is, in many cases, a consequenceof the interaction of those cells with othermembers of the planktonic community. Forexample, viruses are now known to havesignificant impacts on the dynamics of marinecommunities and some viruses have beenfound to infect algae and have been implicatedin the demise of red or brown tide blooms(Fuhrman and Suttle 1993).

Similarly, recent research suggests that bacteriacould play an important role in controllingHABs and regulating their impacts, includingtheir toxicity. An intriguing example is thebacterium responsible for the decline ofGymnodinium mikimotoi blooms (Ishida et al.1997). A bacterial strain isolated at the end ofa G. mikimotoi bloom was found to exhibitstrong and very specific algicidal activityagainst this dinoflagellate species. Bacteriamay also interact with HABs in a positivemanner by stimulating their growth.Cyanobacteria, in particular, establish mutuallybeneficial consortia by chemotacticallyattracting and supporting micro-organismsinvolved in nutrient cycling and the productionof growth factors (Paerl and Millie 1996). Adifferent type of bacterial interaction withHAB species was described by Bates et al.(1995), who showed that the toxicity of thediatom Pseudo-nitzschia was dramaticallyenhanced by the presence of bacteria inlaboratory cultures. The extent to which anyof the above interactions occur in naturalwaters, and affect HAB dynamics is notknown, and represents an important line ofinquiry.

Interactions also occur between HAB speciesand other algae. For example, it has long beenargued that production of allelopathic exudates


Viruses may dramatically influence planktoniccommunities. In the above figure, cells ofAureococcus anophagefferens fromNarragansett Bay are shown infected withpolyhedral virus particles (from Sieburth et al.1988). Similarly, Nagasaki et al. (1994a,b)linked the collapse of a red tide bloom ofHeterosigma to the appearance of virusparticles within algal cells.

allows some harmful species to outcompete co-occurring phytoplankton (Pratt 1966, Smayda1998). Some HAB species that form thinsubsurface or surface layers of cells atextraordinary densities (Gentien et al. 1995,Smayda 1998) may do so because this allowsthem to change the ambient water chemistryand light penetration in a manner that detersgrazing or that inhibits co-occurring algalspecies. These ecological strategies areappealing, but there are few directinvestigations of these mechanisms or theireffects on the plankton community.Quantification of these effects in the contextof HAB population dynamics is virtually non-existent.

A vast number of toxins and other biologicallyactive compounds are produced by HABspecies. These compounds are generallyclassified as secondary metabolites becausethey are not directly involved in the pathwaysof primary metabolism. Their functionalsignificance and eco-evolutionary roles areusually unknown. Field observations suggestthat some compounds produced by HABspecies serve to reduce grazing losses. Fish andzooplankton avoid dense concentrations ofcertain HAB species (Fiedler 1982), andlaboratory studies indicate that toxic speciesare rejected by at least some predators orgrazers either by pre-ingestive selection or afteringestion of a threshold dosage of toxic cells(Ives 1987, Teegarden and Cembella 1996).Reductions in grazer abundance can also playa key role in bloom development. This mightresult from physical factors or behaviouralstrategies, which lead to spatial separation ofharmful algal species and grazers. Localreductions in grazer abundances may also bein direct response to the HAB (that is,avoidance or mortality induced by the HAB),or in response to the effects of past HAB eventson grazer populations. In those cases wheregrazers are abundant, grazing control may stillnot be exerted because toxins or small prey sizereduce the ability of the grazers to ingest theHAB species. The response of zooplankton and

other grazers to toxic algae is often species-specific in terms of behavioural responses andtoxin susceptibility (Huntley et al. 1986, Uyeand Takamatsu 1990). It is therefore necessaryto conduct studies of community interactionson a location- or HAB-specific basis.

Grazing control of HABs can also depend onthe population density of the harmful alga, asdemonstrated for the brown tides inNarragansett Bay, U.S.A., where suppressionof grazing occurs above a thresholdconcentration of the alga (Tracey 1988). Athreshold effect may also occur if the dailyproduction of new harmful cells becomes largeenough to saturate the ingestion response ofthe grazers and the ability of grazers to increasetheir populations. In that case, populationgrowth can accelerate dramatically (Donaghay1988). A breakdown of grazing control hasbeen implicated in the brown tides inNarragansett Bay (Tracey 1988) and in Texas(Buskey and Stockwell 1993) and removal orloss of the grazer population has been reportedto precede or accompany bloom development(Montagna et al. 1993). There is, however, littlequantitative information on how the nature ofthe grazer response influences the timing,magnitude, and duration of HABs. Modelparameterisation of these effects is thus not yetpossible.

Moving to higher trophic levels, zooplanktonimpaired by ingesting harmful algae may bemore susceptible to predation, and thus maybecome an important vector for transferringtoxins in the pelagic food-web. Alternatively,zooplankton fecal pellets may also be importantsources of toxin to benthic communities.Herbivorous fish can accumulate and transfertoxins, and even cause mass mortalities of themarine birds that consume them (Work et al.1993). Mortality of marine mammals linkedto trophic transfer of HAB toxins has also beenreported (Geraci et al. 1989). During theirfood-web transfers, toxins may be bio-accumulated, excreted, degraded, orstructurally modified, as in the case of


enzymatic bio-transformation of PSP toxins insome bivalve molluscs (Cembella et al. 1993).In order to understand the effects of HABspecies on the marine food web, the pathwaysby which toxins are transferred andtransformed and the differential susceptibilityof marine organisms to these toxins must bedetermined.

Example Tasks

• Determine the effects of bioactivecompounds within natural communities onHAB dynamics

• Determine the importance of density-dependent processes in HABs

• Quantify the effects of microbial pathogenson HABs

• Determine the role of grazing control inHAB dynamics


Define functional groups in communitiescontaining HAB species

Rationale

The composition of microalgal communitiesincluding HAB species varies strongly in spaceand time and reflects two fundamentalselection features, notably life-form andspecies-specific selection. As has beenrecognized for terrestrial ecosystems (Gitayand Noble 1997), it is not feasible to developmodels for every species and ecosystem.Reynolds (1997) pointed out that thedominance of the better adapted species in astrongly selective environment is a probability,not a mechanistic certainty. Therefore, precisecommunity composition may, in practice, beimpossible to predict. Recent modelling hasshown that competitive interactions maygenerate oscillations and chaotic behaviour of


The extent to which grazing can control HABsdepends upon the abundance of grazers, their abilityto ingest the harmful algal species, and the effectsof the HAB species on the grazers. Some copepodsand other macrozooplankton reduce their grazingwhen they encounter dense blooms of some toxicdinoflagellates, perhaps as a result of impairedmotor control and elevated heart rates (Sykes andHuntley 1987). These mechanisms provide anexplanation of the vertical distribution of a denselayer of Gymnodinium splendens (chlorophyll a) andvarious zooplankton species in southern Californiancoastal waters (Fiedler 1982). The distributionssuggest active avoidance of the subsurface bloomby macrozooplankton. The observed lower rate offeeding by herbivores within the layer indicated afurther reduction in grazing pressure on thisdinoflagellate population. These behaviouralresponses may help explain the formation andpersistence of dinoflagellate blooms.

species abundances and allow the persistenceof a great diversity of competitors, even in awell-mixed environment with only a fewlimiting resources (Huissman and Weissing1999). The formulation of functional groupsprovides a basis for simplification in order toimprove predictive ability relative to thedynamics of the system.

Some functional classifications ofphytoplankton are based on empiricallyobvious morphological or physiological traits.Margalef (1978) devised a conceptual modelin which functional groups of phytoplanktonwere interpreted as adaptations to a turbulentenvironment and were plotted against axesrepresenting nutrient availability and theintensity of turbulence. In this context, thetypical phytoplankton succession, from fast-growing diatoms to motile dinoflagellates, isdriven by seasonal changes leading from a wellmixed, nutrient-rich water column to anutrient-poor, stratified environment. Thismodel was later redesigned (Margalef et al.1979) to include a “red tide sequence” as aparallel trajectory to the typical succession, inan environment in which a relatively highnutrient concentration was associated withrelatively low turbulence. Along similar lines,Reynolds and Smayda (1998) proposed atriangular habitat template, in whichsuccessional changes and external forcing,such as storms or seasonal mixing, wererepresented in different axes. Cullen andMacIntyre (1998) reconsidered Margalef’s(1978) model emphasizing physiological andbiochemical adaptations that could beexperimentally quantified. These models havebeen useful in providing a general conceptualframework. However, little is known of thefunctional significance of manymorphological, physiological, or behaviouralfeatures of phytoplankton (Sournia 1982,Elbrächter 1984, Fogg 1991, Kiørboe 1993,Kamykowski et al. 1998) and even less isknown for benthic microalgae. Progress in theinterpretation of the ecological implications ofthese phytoplankton characteristics and their

role as adaptive strategies will have to be basedboth on field studies and studies at the cellularlevel.

Example Tasks

• Determine groups of co-occurring taxa orassemblages within given ecosystem types

• Establish the distribution of functionalgroups and their relationship toenvironmental factors

• Identify common morphological,physiological, and life-history featureswithin HAB species and define theenvironmental characteristics that supportthese specific features

OUTPUTS


• Identification of common physiological andbehavioural characteristics of HAB speciesin given ecosystem types

• Quantitative descriptions of the effects ofphysical forcing on bloom dynamics

• Bases for developing management andmitigation strategies tailored to thecharacteristics of particular organisms


PROGRAMME ELEMENT 4

The conceptual model of Margalef (above - modified from Margalef, 1978; see also Margalef et al.1979) places phytoplankton life-forms in an ecological space defined by nutrient concentration, asrelated to specific growth rate (r, with dimension t- -1) and an expression of turbulence (coefficient ofvertical eddy diffusivity). Red tides appear along a path parallel to that of the typical phytoplanktonsuccession, but in situations of increased nutrient availability relative to turbulence intensity. Theletters r and K are commonly used in the logistic growth equation to indicate, respectively, specificgrowth rate and environmental carrying capacity. In the figure, they refer to a classification ofphytoplankton into r-strategists, species with high specific growth rates (r), which tend to dominateinitial succession stages, and K-strategists, species with higher potential for survival, which tend todominate in late phases of the succession.

The position of phytoplankton communities as trajectories in the ecological matrix of Reynolds (bottomleft) is defined by nutrient availability (which decreases along with phytoplankton succession) andexternal forcing (mixing intensity). C, S and R indicate the position of appropriately adapted taxa (C= competitor, S = stress tolerant and R = disturbance-tolerant, ruderal or “rubbish-loving”). Amplificationof the top left hand corner of the previous figure (bottom right), shows the typical successionalsequence and the HAB sequence which, with more nutrients available, selects for algae with strongercompetitor-strategist characteristics (modified from Reynolds and Smayda 1998).

57

PROGRAMME ELEMENT 5: Observation, Modelling, andPrediction

INTRODUCTION

To describe, understand, and predict thepopulation dynamics and environmental effectsof harmful algae, it is necessary to characterisedistributions of HAB species and othercomponents of their communities in relationto the environmental factors that ultimatelycontrol bloom dynamics. This requiresspecialised and highly resolving measurementsto observe and describe the biological,chemical, and physical interactions thatdetermine the population dynamics ofindividual species in natural communities.Equally important are synoptic and long-termmeasurements of biological, chemical, andphysical variability as related to HABs in thecontext of regional processes. Such co-ordinated observation programmes (that is,monitoring systems) are central to thedevelopment and evaluation of early warningand prediction systems. Ultimately, effectivemonitoring is needed to support decision-making for the protection and management ofcoastal resources.

Models are effective tools for describing thecomplex relationships among physical,chemical, and biological variability inecosystems. They can range from quantitativedescriptions of physiological processes asfunctions of temperature, light, and nutrientconcentration, to empirical predictions ofHABs (such as, blooms will occur after majorrunoff events), to detailed numerical forecastsbased on simulations of algal growth andbehaviour as influenced by localhydrodynamics. Models help to develop anunderstanding of the processes that determinethe population dynamics of HABs, and theyare extremely useful in the construction andtesting of hypotheses. Prediction of HABs is agoal, but success will be limited at first. Eveninaccurate predictions are useful in revealing

incompletely described factors that areimportant in the dynamics of HABs.Ultimately, the development, evaluation, andutility of predictive models depend on theavailability of appropriate observations, thatis, those that can be related directly to themodels.

Progress in observing, modelling, andpredicting HABs depends on innovation, co-ordination and focus. New instruments andsensing systems for characterising variabilityin coastal ecosystems are being developed at arapid pace. However, their application in thedetection, study, and prediction of HABs isonly beginning, and some crucial capabilities,such as the means to detect single species insitu, are still in the development stage. In turn,models of marine ecosystem dynamics arebecoming increasingly effective at describingecological interactions and the influence ofphysics on the dynamics of plankton. A focuson HABs, with close interaction amongbiologists, oceanographers, and modellers, isneeded to further the objectives of GEOHAB.Consequently, improvements in observationand modelling in support of detection,understanding, and prediction of HABs arecentral aims of GEOHAB.

OVERALL OBJECTIVE

THE STRATEGY

GEOHAB will foster the development of newobservation technologies and models to supportfundamental research on HABs, improve

PROGRAMME ELEMENT 5

To improve the detection andprediction of HABs by developingcapabilities in observation andmodelling

58

monitoring, and develop predictivecapabilities. Because capabilities in coastalobservation and modelling are advancingrapidly on many fronts, co-ordination and co-operation among the different elements of theGEOHAB programme is essential. Theintention is to ensure rapid and effectiveintegration of new knowledge, technicalcapabilities, and data across disciplines andregions.

A summary of the objectives and types of tasksthat might be addressed under this ProgrammeElement, as well as the anticipated outcomesis provided in Figure 5.1.


Develop capabilities to observe HABorganisms in situ, their properties, and theprocesses that influence them

Rationale

Fundamental research on HABs must beguided by and validated with observations ofphytoplankton dynamics in nature. Todetermine why HABs occur, it is necessary todescribe the temporal and spatial developmentsof the target species in specific ecosystems.This requires observation and modelling of thephysical-biological interactions that supportthe specific life strategies of HAB species inrelation to other members of the planktoncommunity. Consequently, measurements ofphysical and chemical properties andprocesses, along with quantitative detectionand characterisation of the plankton, must bemade within a spatial and temporal frameworkthat is appropriate for characterising bloomdynamics. One important objective, seldom ifever attained in HAB research, is to match thescales and specificity of observations withthose of the models that describe environmentalinfluences on phytoplankton dynamics. Thus,GEOHAB will encourage the development ofnovel observation systems that characterise

physical, chemical, and biological variabilityon appropriate scales. The scales need to bedefined through observation and modelling.

To describe population dynamics, distributionsof the target organisms must be determined atthe species level; other members of thecommunity should be identified and quantifiedas taxonomic or functional groups. Thisanalysis is traditionally done through visualmicroscopic examination, a slow and tediousprocess that is poorly suited for research onthe dynamics of HABs. Simply, resources areinadequate to obtain and analyse enoughsamples to describe adequately thedistributions of species in space and time. Also,some species are extremely difficult (such as,within the genus Alexandrium) or impossible(such as, Pseudo-nitzschia) to distinguish withlight microscopy alone. These constraints alsohamper efforts for routine monitoring.Automated methods are needed, and severalapproaches are being pursued, includingantibody probes (Shapiro et al. 1989) andnucleotide probes (Scholin et al. 1999), whichcan be adapted for use in semi-automated bulk-sample analysis and single-cell analysis usingmicroscopy or flow cytometry. Meanwhile,bio-optical oceanographers continue efforts toextract information on species composition ofphytoplankton from measurements of oceancolour and other optical properties of surfacewaters (Stuart et al. 1998, Ciotti et al. 1999,Schofield et al. 1999, Kirkpatrick et al. 2000).

Identification of individual species in situ isnot enough. To describe and understandecological controls on the activities and effectsof harmful algae in nature, physiological statusand toxicity of harmful algae must bedetermined along with identification andquantification. Fortunately, labelling anddetection methods similar to those foridentifying species can be used to assessbiochemical or physiological properties suchas the presence of a toxin (Lawrence andCembella 1999), enzyme activity (González-Gil et al. 1998), and photosynthetic capability


Figure 5.1 Summary of Programme Element 5: Observation, Modelling,and Prediction.

OVERALL OBJECTIVE Programme Element 5: To improve the detectionand prediction of HABs by developing capabilities in observation andmodelling

• Develop techniques and sensors for simultaneousmeasurements of the distributions of phytoplankton,predators, and physical and chemical parameters

• Develop methods for rapid identification of HABspecies

• Develop assays of physiological status and toxicity atthe cellular level in natural samples

1Develop capabilities to observe HABorganisms in situ, their properties,and the processes that influence

them

• Develop models of physiological processes of HABspecies

• Develop theoretical descriptions of HABs as communityphenomena, including responses to perturbations

• Conduct coupled physical-chemical-biologicalsimulations, guided and tested by comparisons withobservations

• Support the design of field and monitoringprogrammes by results of simulations

• Develop new automated systems for monitoring HABs• Establish test sites for development and evaluation of

systems for monitoring phytoplankton (including HABspecies) in situ and with remote sensing

• Help to develop procedures for internationalintegration and management of data from monitoringprogrammes

3Develop and evaluate systems for

long-term monitoring of HAB species

• Conduct retrospective analysis leading to empiricalpredictive models

• Test and refine the predictive models throughmonitoring and analysis

4Develop capabilities for describingand predicting HABs with empirical

models

OUTPUTS• New instrument systems and analytical techniques to support fundamental research on HABs• Models to describe the coupling of physical, chemical, and biological processes important to HABs• Advanced systems for monitoring HABs and environmental processes in coastal waters• Prototype early warning and prediction systems for HABs

• Develop comprehensive observation and predictionsystems at selected sites

• Use real-time data assimilation in predictive models

5Develop capabilities in real-time

observation and prediction of HABs

PROGRAMME ELEMENT 5

2Develop models to describe and

quantify the biological, chemical, andphysical processes related to HABs

60

(Olson et al. 1996). GEOHABwill encourage development ofthese analytical methods toaddress key questionsconcerning environmentalinfluences on physiologicalprocesses.

For HAB research, the long-term goal is automatedidentification of species in situ,and assessment of theirphysiological and biochemicalproperties. Considering thatflow cytometers are beingadapted for deployment in theocean (Dubelaar et al. 1998),and new optical instruments arebeing introduced regularly(Sieracki et al. 1998,Weidemann et al. 1998,Kirkpatrick et al. 2000), thisgoal is worth pursuing, if onlyfor target species of particularinterest.

Many of the new observationalcapabilities required forGEOHAB are being developedas part of research programmesthroughout the world, withoutstrong ties to HAB research. Co-ordination of efforts andadditional emphasis on HABswill provide great benefits.GEOHAB will thereforeencourage direct linkagesbetween the HAB studiesoutlined in previous sections andresearch on new observationsystems and approaches, withinGEOHAB and with otherprogrammes.

Observation and modelling will be improved by pursuing specificobjectives in three complementary contexts: fundamental research(i.e., experimental research, modelling and process studies),monitoring, and prediction. There are many links between theseobjectives: When new analytical approaches, such as nucleotideprobes or active fluorescence techniques, are introduced throughexperimental research, observation technologies useful for HABresearch can be developed (A→B). In turn, observation technologies,such as flow cytometry, can be used in many new ways forexperiments (B→A). Process studies, often complemented byexperimental research in the laboratory (and vice-versa), guidedescriptive modelling (A,E→C), which in turn provides a frameworkfor constructing and testing hypotheses through observation andexperimentation (C→A,E). Monitoring systems require appropriateobservation technologies (B→D) and interpretations (e.g., of oceancolour algorithms), which are developed and validated throughexperimentation and modelling (A,E→C→D). Simulation models areuseful in the design of monitoring systems (C→D). Results frommonitoring programmes are important for the design andimplementation of process studies and in the testing and refinementof models (D→E,C). Also, deployment in a monitoring system is arigorous test of an observation technology, important in productimprovement (D→B). Through data assimilation techniques or thedevelopment of empirical models, monitoring systems can be usedfor early warning and prediction (C,D→F). Data assimilation modelsprovide now-casts, that is, statistical interpolations andextrapolations of available data, which are excellent products formonitoring programmes (F→D) and for directing detailed processstudies (F→E). Continuous comparison of predictions withobservations provides the means for improving descriptive andforecast models (F→C).


Example Tasks

• Develop techniques and sensors forsimultaneous measurements of thedistributions of phytoplankton, predators,and physical and chemical parameters

• Develop methods for rapid identification ofHAB species

• Develop assays of physiological status andtoxicity at the cellular level in naturalsamples


Develop models to describe and quantify thebiological, chemical, and physical processesrelated to HABs

Rationale

Modelling is a cross-cutting activity thatsupports specific tasks and synthesises thefindings of all Programme Elements.GEOHAB will foster the development of a newgeneration of models adaptable to HABs. Theprocess will be characterised by closeinterdisciplinary interaction of experimentalistsand modellers, to develop a qualitative andquantitative understanding of HABs in avariable physical environment.

Generally, a range of processes acting ondifferent scales must be integrated to simulateecosystem processes, including thedevelopment of HABs and the effects ofharmful algae, such as toxicity or the formationof noxious scums or foams. For thedevelopment of models it is always necessaryto reduce complexity by isolating the mostimportant processes. This involves, forexample, reducing the number of biologicalstate variables to a minimum and theparameterisation of sub-grid processes, that is,those that are not explicitly resolved.Consequently, the simulation of ecosystemsdepends on a hierarchy of models describing

physiological processes, vegetative growth, andlife history transitions of phytoplankton,complemented by models of communityinteractions; all of which are influenced byenvironmental factors such as light,temperature, salinity, and nutrient supply asdescribed by models of the physical andchemical environment.

Advanced three-dimensional circulationmodels coupled with models of chemical andbiological processes allow simulations of theresponses of systems to physical (such asirradiation, wind, freshwater runoff) andchemical (nutrient input from rivers,atmosphere) forcing. These simulationscapture the thermodynamics (T,S), theadvection (circulation, fronts and eddies) andthe turbulent diffusion due to small-scaleprocesses in response to meteorologicalforcing, and they include interactions withinthe food web. Ecologically important physicalprocesses can therefore be described in arealistic manner. The principal challenge nowis to incorporate more realistic descriptions ofbiological and chemical processes into thesephysical models through the translation ofexperimental results and observations intomodel equations. This requires effective, two-way flows of information between biologistsand modellers. The resulting coupled modelspromote understanding of problems thatdepend on the interaction of physics andbiology, that is, effects that cannot be explainedby biology or physics alone. Model simulationscan be very helpful in the development andtesting of hypotheses and in the design oflaboratory experiments and samplingprogrammes for process studies. Experimentalsimulations of different scenarios can also helpto identify the specific adaptations that favourblooms of the harmful species.

Coupled models can be used to predict HABs.Prediction is evaluated by comparison withobservations, so a temporal and spatialcorrespondence between observations andmodels, which minimises the differencesbetween them, is an important goal. With


increasing refinement of the models, theirpredictive potential will be enhanced. Accurateprediction is essential for effective earlywarning and mitigation. Although this may bea distant goal, much can be learned aboutecological dynamics from comparisons ofpredictions with observations. Even if theaccuracy of predictions compared withobservations is initially poor, the lessons willbe used to improve subsequent models.

Example Tasks

• Develop models of physiological processesof HAB species

• Develop theoretical descriptions of HABsas community phenomena, includingresponses to perturbations

• Conduct coupled physical-chemical-biological simulations, guided and tested bycomparisons with observations

• Support the design of field and monitoringprogrammes by results of simulations


Advances in observation technologies make it possible tocharacterise distributions of HAB organisms, membersof their communities, and physical/chemical propertieson a broad range of scales. Members of the microplankton>20 µm are automatically detected using a flowCAM (top)which has the potential to provide continuous informationon abundance of HAB organisms and community structure(from the Bigelow Laboratory flowCAM web page; seeSieracki et al. 1998). Thin layers of phytoplankton can beformed by physical processes that are modelled in thecentre-left panel and compared with high resolutionmeasurements (fluorescence trace “Drop 8”) from T.J.Cowles (Franks 1995). The seasonal progression ofphytoplankton abundance is resolved vertically using abuoy that measures attenuation of solar irradiance at490 nm (lower left; Kd(490), m-1; Cullen et al. 1997).Aircraft can assess distributions of phytoplankton on scalesfrom meters to tens of kilometres, using photography orimaging radiometry (photo from Franks 1997). Forsynoptic views of conditions on the regional- to basin-scale, there is no substitute for satellite sensors, such asSeaWiFS, which obtained the image of chlorophyll fromocean colour during a red tide in the Bohai (from CCAR/HKUST, Hong Kong).

PROGRAMME ELEMENT 5


Develop and evaluate systems for long-termmonitoring of HAB species

Rationale

Harmful algal blooms are episodic and patchy,so observations of algal distributions in relationto physical and chemical properties should beboth continuous and synoptic. Although thisideal is unachievable, a new generation ofoceanographic instruments can providecontinuous measurements of many physical,chemical, and biological properties fromautonomous moorings, in vertical profile andalong ship tracks. Also, remote sensing fromaircraft and satellites can provide synopticviews of coastal processes when conditionsallow.

Monitoring systems can play a key role indescribing multi-scale variability thatinfluences coastal ecosystems and hence thepopulation dynamics of HABs. For example,long-term monitoring documents ecologicalvariability over a large range of temporal scales;several long time-series have demonstrateddramatic changes in ecosystems forced byclimatic shifts that are now appreciated to havefar-reaching effects (McGowan et al. 1998,Karl 1999). In the context of HABs, long-termrecords on regional scales are essential todistinguish local anthropogenic effects (e.g.,from eutrophication) from changes related toclimate variability, such as the El Niño -Southern Oscillation phenomenon. Monitoringalso serves the important role of detecting rareor transient events. So, if analysed carefully,data from well designed monitoring andmodelling systems could contribute effectivelyto early warning and prediction of algalblooms. Monitoring data are also of great valuefor verification and refinement of models.

Discrete sampling for microscopicenumeration of plankton, determination ofchemical constituents (e.g., toxicity, nutrients)or molecular characterisation, and perhaps

detailed vertical sampling at selected sites, willalways be part of monitoring programmes.Temporal and spatial variability in thesediscrete measurements is often difficult tointerpret. Continuous and synoptic recordsfrom a monitoring programme, reconciledthrough now-cast models with results ofdiscrete sampling as discussed below, can

64

Advanced monitoring systems. Automatedmoorings can be equipped with sensorsto monitor continuously the temperatureand salinity of the water column, depth-resolved currents, and meteorologicalconditions. Passive optical sensors canmeasure ocean colour and the attenuationof sunlight with depth. The correspondingoptical properties, spectral reflectance andattenuation, can be related to theconstituents of the water, includingphytoplankton and dense HABs, both atthe surface and in layers. Other opticalinstruments with their own light sources,such as fluorometers and absorption-attenuation meters, show great promisefor autonomous characterisation ofphytoplankton and environmentalconditions in coastal waters. Oceanobservation moorings, pictured here, havebeen deployed in several locations, suchas the Chesapeake Bay, Maryland, of theUnited States. Photo courtesy of CBOS.

provide the environmental context forinterpretation of detailed, but intermittentsampling. For example, now-casts coulddescribe the temporal relationship between aset of discrete samples and an episodic eventsuch as an upwelling pulse or an algal bloom.

Development of autonomous monitoringsystems has begun (Johnsen et al. 1997, Glennet al. 2000). However, costs for instrumentsare relatively high, some of the measurements(such as ocean colour) are difficult to interpretor to correct for interference, and instrumentsdeployed in the water are subject to foulingand disturbance. Nevertheless, thedevelopment of coastal observation systems isstrongly justified, as demonstrated by theestablishment of the Coastal OceanObservations Panel (COOP; Malone and Cole2000). HABs are an ecologically prominentcomponent of coastal variability, and regionalprocesses must be understood to describe theirseasonal and interannual variability. Close co-ordination between HAB research andinternational efforts to develop coastalmonitoring systems is important to GEOHABand to the broader community that will rely oncoastal monitoring for protection andmanagement of coastal resources. In order tounderstand the dynamics of HABs in a globalcontext, it is also essential to integrate andmanage data from a broad range of monitoringsources, including conventional samplingprogrammes, in situ systems, and remotesensing.

Example Tasks

• Develop new automated systems formonitoring HABs

• Establish test sites for development andevaluation of systems for monitoringphytoplankton (including HAB species) insitu and with remote sensing

• Help to develop procedures for internationalintegration and management of data frommonitoring programmes


Develop capabilities for describing andpredicting HABs with empirical models

Rationale

Monitoring programmes alone are very usefulfor describing and understanding the dynamicsof HABs, but they provide limited means foradvance warning of blooms or harmful effects.Predictions of HABs are needed, whatever thesource of information. For example, importantdecisions relevant to mitigating the effects ofharmful blooms must rely on empirical orconceptual models relating algal populationdynamics to environmental forcing, such asclimate variability (e.g., El Niño) versus humaninfluences, such as nutrient loading. A greatdeal of work has been done addressing theinfluences of nutrient loading on algal blooms,but many uncertainties persist. Given that largeamounts of data have been collected but not


In situ nutrient analysers will increasingly beused for monitoring nutrient loading. Uponlaboratory calibration, they can be deployedfor periods of weeks to months. Photo by M.Trice.

analysed in the context of HABs, opportunitiesexist for retrospective studies relating HABsto environmental forcing, including humanactivities. Studies of the sediment record canalso provide much information on theoccurrence of phytoplankton, including HABspecies, relative to environmental factors.Evaluation of the conclusions and implicitpredictions of these studies can only beimproved if observation systems are upgradedso that more data can be acquired withimproved temporal and spatial resolution.

Although GEOHAB will encourage thedevelopment of new autonomous observationsystems and modelling approaches, it is wellrecognised that throughout the world greatquantities of relevant data will be collectedthrough established procedures and analysedusing a variety of approaches leading toempirical or conceptual models. Capabilitiesfor empirical predictions will be enhanced byco-ordination in the collection and analysis ofdata and through international co-operation inthe sharing of data and development of models.Comparison of predictions with newobservations is crucial. In co-operation withCOOP, GEOHAB will encourage theseactivities.

Example Tasks

• Conduct retrospective analysis leading toempirical predictive models

• Test and refine the predictive modelsthrough monitoring and analysis


Develop capabilities in real-time observationand prediction of HABs

Rationale

Empirical models that explain HABs areneeded. However, automated forecast systemsfor HABs are an ultimate goal. Real-time

observation and prediction systems could guidetraditional monitoring programmes andprovide a proactive means for responding toHABs. Also, predictive models can guidefundamental research because they are basedon knowledge about HABs that is testeddirectly by comparison of forecast withobservations.

Forecasting systems will require near real-timeobservation capabilities linked directly tohydrodynamic/biological models. Theseobservation-prediction networks must detectand forecast over ecologically relevant scales,so they should utilise remote sensing and insitu observation systems. To improve thequality of forecasts, adaptive sampling by shipsand autonomous vehicles can be initiated tocollect detailed data (such as speciescomposition, detailed vertical structure) inspecific regions within the forecast grid.Conversely, the now-casts and forecastsprovide an unprecedented opportunity forbiologists to devise sampling strategies tocharacterise episodic events, which can play adisproportionately large role in structuringphytoplankton communities and are poorlysampled using traditional protocols. Therefore,real-time observation and prediction systemswill be critical in studying the populationdynamics of HABs.

The scientific field of ocean forecasting hasadvanced rapidly through the use of dataassimilation methods adopted from themeteorology community. Assimilation of datainto oceanographic models is accomplishedthrough a variety of methods (Walstad andMcGillicuddy 2000). Coastal ocean forecastingnetworks generally work in a recursive mode:the data-assimilative model provides a now-cast that is moved forward in time 2-4 days bya circulation model driven by surface-boundaryforcing from a weather prediction system.During the forecast cycle, additional field dataare assimilated to constrain the modeldynamics to provide improved now-casts forthe next set of forecasts. Several coupledphysical-biological models have been


constructed with data assimilative methods(Ishizaka 1990, Fasham and Evans 1995,Lawson et al. 1995, Matear 1995) providing ablueprint for future data assimilative modelsof HAB events.

Although recent advances in instrumentationand data assimilative modelling provide thecomponents necessary for building algalforecasting systems (Schofield et al. 1999),numerous hurdles must be overcome before wecan expect to predict HAB events effectively.Many of the needs for development of HABforecasting systems have already beenidentified in this Science Plan: they representthe knowledge and capabilities we require todescribe the population dynamics of harmfulalgae. Real-time observation and prediction ofHABs can therefore be pursued by co-ordinating the acquisition of new knowledge,the development and establishment ofobservation systems, and the integration ofmodels with data in forecasting efforts.

Example Tasks

• Develop comprehensive observation andprediction systems at selected sites

• Use real-time data assimilation in predictivemodels

OUTPUTS


• New instrument systems and analyticaltechniques to support fundamental researchon HABs

• Models to describe the coupling of physical,chemical, and biological processes importantto HABs

• Advanced systems for monitoring HABsand environmental processes in coastalwaters

• Prototype early warning and predictionsystems for HABs


Schematic for a now-cast/forecast system that includes adaptive sampling of events poorly resolved bymonitoring activities. From Schofield et al. 1999, modified from Glenn et al. 1999.

LINKAGES AMONG PROGRAMME ELEMENTS

The scientific goal of GEOHAB is toimprove prediction of HABs bydetermining the ecological andoceanographic mechanismsunderlying their populationdynamics. Understanding, and ultimatelypredicting, HABs will require the broad rangeof observations described in the individualProgramme Elements as well as co-ordinationamong those elements. Although manyactivities and objectives have been presentedindependently for each element, these mustultimately be linked and integrated to achievethe understanding required.

Programme Element 5, Observation,Modelling, and Prediction, establishes theframework for prediction based on observation

and modelling. Modelling will be based onHAB biomass and population dynamics.Parameterisation of processes such as growth,mortality, and turbulent dispersion will requireinformation from each of the ProgrammeElements, as will model validation. Forexample, Programme Element 1, Biodiversityand Biogeography, will contribute toprediction by documenting the present andhistorical distribution of key HAB species andtheir life cycle stages. Biodiversity studies willaddress the genetic variability within local,regional, and global populations of thosespecies. This is necessary because growth ormortality rates determined for a single strainof a species may not apply to all strains of thatspecies even within a region. Similarly,physiological, behavioural, or rate dataobtained for a species in one area may not be

LINKAGES AMONG PROGRAMME ELEMENTS 68

The integration of findings from the individual Programme Elements described in this Science Plan isrequired to achieve not only an understanding of HAB organisms and associated events, but also todevelop predictive capabilities.

LINKAGES AMONG PROGRAMME ELEMENTS

applicable to the same species from anotherregion. Programme Element 2, Nutrients andEutrophication, will contribute the rate dataand cycling parameters specific for nutrients,again recognizing the differential response ofthe range of HAB species. The potentialimportance of anthropogenic nutrient loadingin the development of both high biomass andtoxic blooms will also be addressed.Programme Element 3, Adaptive Strategies,seeks to reduce the genetic and physiologicalcomplexities studied in the first twoProgramme Elements by identifying functionalgroups of species that interact with theenvironment in similar ways. For example,species that undergo diel vertical migration willexploit stratified waters characterized byconsistent light and temperature regimes,whereas non-motile species are better suitedto turbulent regimes. Nitrogen-fixing speciesmay thrive in waters where other speciescannot because of a shortage of dissolvedinorganic nitrogen. Behavioural andphysiological adaptations can thus account forthe survival and persistence of certain HABspecies or functional groups in particular

ecosystem types. Programme Element 4,Comparable Ecosystems, integrates thefindings of biodiversity, nutritional, andeutrophication effects, and adaptive strategiesby examining, through field studies in differenthydrographic and ecological systems, thephysical, chemical, and biologicalcharacteristics of the environment. Improvedunderstanding of HAB population dynamics,and ultimately, improved predictions of HABevents within particular ecosystem types,clearly requires the integration of knowledgederived from the five Programme Elements.

In summary, GEOHAB is acombined experimental,observational, and modellingprogramme, using current andinnovative technologies in amultidisciplinary approachconsistent with the multiple scalesand oceanographic complexity ofHAB phenomena.

69

Red tide caused by Gymnodinium mikimotoi in the commercial andfishing port of Tanabe Bay, on the Pacific coast of Honshu, Japan. Redtides such as this can cause devasting impacts on ecosystems and onaquaculture industries. In this photo, the small white areas off theisland are fish-culture cages which experienced stress from this redtide. Photo by Y. Fukuyo.

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Work, T.M., A.M. Beale, L. Fritz, M.A.Quilliam, M.W. Silver, K.R. Buck, andJ.L.C. Wright. 1993. Domoic acidintoxication of brown pelicans andcormorants in Santa Cruz, California. In T.J.Smayda and Y. Shimizu (eds.), ToxicPhytoplankton Blooms in the Sea. ElsevierScience Publishers, B.V. Amsterdam, pp.643-650.

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Wu, R.S.S., P.K.S. Lam, D.W. Mackay, T.C.Lau, and V. Yam. 1994. Impact of marinefish farming on water quality and bottomsediment: A case study in the sub-tropicalenvironment. Mar. Environ. Res. 38:115-145.

Wyatt, T. and I.R. Jenkinson. 1997. Notes onAlexandrium population dynamics. J.Plankton Res. 19:551-575.

Yin, K., P.J. Harrison, J. Chen, W. Huang, andP.-Y. Qian. 1999. Red tides during spring1998 in Hong Kong: Is El Niño responsible?Mar. Ecol. Prog. Ser. 187:289-294.

Zhang, J. 1994. Atmospheric wet depositionsof nutrient elements: Correlations withharmful biological blooms in the NorthwestPacific coastal zones. Ambio 23:464-468.

Zhang, J., Z.F. Zhang, S.M. Liu, Y. Wu, H.Xiong, and H.T. Chen. 1999. Humanimpacts on the large world rivers: Would theChangjiang (Yangtze River) be anillustration? Global Biogeochem. Cycles13:1099-1105.

Zingone, A., M.-J. Chrétiennot-Dinet, M.Lange, and L. Medlin. 1999. Morphologicaland genetic characterisation of Phaeocystiscordata and P. jahnii (Prymnesiophyceae),two new species from the MediterraneanSea. J. Phycol. 35:1322-1337.

Zingone, A. and H.O. Enevoldsen. 2000. Thediversity of harmful algal blooms: Achallenge for science and management.Ocean and Coastal Management 43:725-748.

GEOHAB SCIENTIFIC STEERING COMMITTEE

GEOHAB SCIENTIFIC STEERING COMMITTEE

Patrick Gentien, ChairInstitut Français de Recherche pourl’Exploitation de la MerCREMA-CNRS/IFREMERBP5 - 17137 L’Houmeau, FranceTel: +33-(0)5-46500630Fax: +33-(0)5-46500660E-mail: [email protected]

Yasuwo Fukuyo, Vice-ChairAsian Natural Environmental Science CenterThe University of TokyoYayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657JapanTel: +81-3-5841-2782Fax: +81-3-5841-8040E-mail: [email protected]

Donald M. AndersonBiology DepartmentMail Stop 32, Redfield 332Woods Hole Oceanographic InstitutionWoods Hole MA 02543-1049 U.S.A.Tel: +1-508-289-2351Fax: +1-508-457-2027E-Mail: [email protected]

Marcel BabinLaboratoire d’Océanographie de VillefrancheUniversité Pierre et Marie Curie / CNRSQuai de la Darse, B.P. 806238 Villefranche-sur-Mer CedexFranceTel: +33-4-93-76-37-12Fax: +33-4-93-76-37-39E-mail: [email protected]

Susan BlackburnCSIRO Microalgae Research CentreCSIRO Marine ResearchGPO Box 1538 Hobart, Tasmania 7001AustraliaTel: +61-3-62325307Fax: +61-3-62325090E-mail: [email protected]

Allan CembellaInstitute for Marine BiosciencesNational Research Council1411 Oxford StreetHalifax, Nova Scotia B3H 3Z1, CanadaTel: +1-902-426-4735Fax: +1-902-426-9413E-mail: [email protected]

John Cullen(1999-2000)Department of OceanographyDalhousie UniversityHalifax, Nova Scotia, Canada B3H 4J1Tel: 902-494-6667Fax: 902-494-3877E-mail: [email protected]

Malte Elbrächter(1999-2000)Deutsches Zentrum für Marine BiodiversitätForschungs-Institut SenckenbergWattenmeerstation SyltHafenstrasse 43D-25992 List/Sylt, GermanyE-mail: [email protected]

Henrik Enevoldsen *Project CoordinatorIOC Science and Communication Centre onHarmful AlgaeBotanical Institute, University of CopenhagenØster Farimagsgade 2DDK-1353 Copenhagen K, DenmarkTel: +45 33 13 44 46Fax: +45 33 13 44 47E-mail: [email protected]

Marta EstradaInstitut de Ciències del Mar CSICPaseo Joan de Borbó s/nBarcelona 08039, SpainTel: +34-93-2216416Fax: +34-93-2217340E-mail: [email protected]

84

GEOHAB SCIENTIFIC STEERING COMMITTEE85

Wolfgang FennelInstitut für Ostseeforschung Warnemuende an der Universitaet Rostock18119 Rostock, GermanyTel: +49 381 5197 110Fax: +49 381 5197 480E-mail: [email protected]

Patricia M. GlibertHorn Point LaboratoryUniversity of Maryland Center forEnvironmental ScienceP. O. Box 775, Cambridge MD 21613, U.S.A.Tel: +1-410-221-8422Fax: +1-410-221-8490E-mail: [email protected]

Elizabeth Gross *(1999-2000)Department of Earth and Planetary SciencesThe Johns Hopkins UniversityBaltimore, MD 21218 U.S.A.Tel: +1-410-516-4070Fax: +1-410-516-4019E-mail: [email protected]

Kaisa KononenMaj and Tor Nessling FoundationFredrikinkatu 20 B 16Fin-00120 Helsinki, FinlandTel: +358-9-43426611Fax: +358-9-43425555E-mail: [email protected]

Nestor LagosDepartamento de Fisiologia y BiofisicaFaculdad de MedicinaUniversidad de ChileIndependencia 1027, Casilla 70005Santiago, ChileTel: +56-2-678 6309Fax: +56-2-777 6916E-mail: [email protected]

Thomas OsbornDepartment of Earth and Planetary SciencesThe Johns Hopkins UniversityBaltimore, MD 21218 U.S.A.Tel: +1-410-516-7519Fax: +1-410-516-7933E-mail: [email protected]

Grant PitcherMarine and Coastal ManagementPrivate Bag X2, Rogge Bay 8012Cape Town, South AfricaTel: +27 21 402-3345Fax: +27 21 439-9345E-mail: [email protected]

Arturo P. Sierra-BeltránMarine Pathology Unit. CIBNORA.P. 128 La Paz, 23000MexicoTel: +52 112 53 633 ext 3809Fax: +52 112 53 625E-mail: [email protected]

Steve ThorpeSchool of Ocean and Earth ScienceSouthampton Oceanography CentreEuropean Way, Southampton SO14 3ZHUnited KingdomTel: +44-1248-490-210Fax: +44-1248-716-367E-mail: [email protected]

Edward R Urban, Jr. *Executive Director, SCORDepartment of Earth and Planetary SciencesThe Johns Hopkins UniversityBaltimore, MD 21218 U.S.A.Tel: +1-410-516-4070Fax: +1-410-516-4019E-mail: [email protected]

* Ex-Officio Members

Jing ZhangState Key Laboratory of Estuarine and CoastalResearchEast China Normal University3663 Zhongshan Road NorthShanghai 200062, ChinaTel: +86-21-62233009Fax: +86-21-62546441E-mail: [email protected]

Adriana Zingone *Stazione Zoologica ‘A. Dohrn’Villa Comunale80121 Napoli, ItalyTel: +39 081 5833295Fax: +39 081 7641355E-mail: [email protected]

GEOHAB SCIENTIFIC STEERING COMMITTEE 86

Harmful Algal Blooms (HABs) are the cause of

massive fish kills, shellfish contamination, human

health problems, and detrimental effects on

marine and coastal ecosystems. HABs are caused

by a variety of species, some of which are toxic

and some of which cause indirect harm to the

environment. The key to better prediction of these

events, and ultimately their mitigation, is an

understanding of the ecology and oceanography

of their population dynamics. The GEOHAB

(Global Ecology and Oceanography of Harmful

Algal Blooms) Programme is aimed toward fostering international co-operative research

on HABs in a range of ecosystems, and toward developing and applying innovative

technologies in support of their detection and prediction.

GEOHAB

Mass mortality of flat-fish by a red tide ofCochlodinium polykrikoides.

global ecology and oceanography of harmful algal blooms ... · as a result of the havreholm meeting...

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