E. Graneli J.T.Turner (Eds.)

Ecology of Harmful Algae

With 45 Figures, 13 in Color, and 15 Tables

4u Springer

Contents

Part A Harmful Algae and Their Global Distribution

1 An Introduction to Harmful Algae 3E. GRANELI and J.T. TURNER

References 7

2 Molecular Taxonomy of Harmful Algae 9S. JANSON and P.K. HAYES

2.1 Introduction 92.2 Dinophyta (Dinoflagellates) 102.2.1 General Morphology 102.2.2 Dinophysis 112.2.3 Alexandrium 112.2.4 Protoperidinium, Prorocentrum 122.2.5 Karenia, Karlodinium, Takayama 132.2.6 Amphidinium, Cochlodinium, Gyrodinium 142.3 Cyanobacteria (Blue-Green Algae) 142.3.1 Anabaena, Aphanizomenon, Nodularia 142.3.2 Microcystis 152.3.3 Trichodesmium 162.4 Bacillariophyta (Diatoms) 172.4.1 Amphora, Pseudo-nitzschia,Nitzschia 172.5 Concluding Remarks 17References 18

X Contents

3 The Biogeography of Harmful Algae 23N. LUNDHOLM and 0. MOESTRUP

3.1 Biogeography and Species Concepts 233.1.1 Genetic Variation 243.2 Biogeographical Distribution 253.3 Distribution of Harmful Species 263.3.1 Dinoflagellates 263.3.2 Diatoms 273.3.3 Haptophytes 293.3.4 Raphidophyceans 293.3.5 Cyanobacteria 31References 32

4 Importance of Life Cycles in the Ecologyof Harmful Microalgae 37K.A. STEIDINGER and E. GARCES

4.1 Introduction 374.2 Phases of Phytoplankton Bloom Development

and Life Cycles 394.2.1 Initiation 394.2.2 Growth and Maintenance 414.2.3 Dispersal/Dissipation/Termination 444.3 Environmental Factors versus Biological Factors

Affecting Transition 444.4 Status of Knowledge and Direction Needed 45References 47

Part B The Ecology of Major Harmful Algae Groups

5 The Ecology of Harmful Dinoflagellates 53J.M. BURKHOLDER, R.V. AZANZA, and Y. SAKO

5.1 Introduction 535.2 General Ecology 545.2.1 Motility 545.2.2 Temperature, Light, Salinity and Turbulence 555.2.3 Nutrition: the Continuum from Auxotrophy to Parasitism . 56

Contents

5.3 Blooms, Including To:5.4 Human Influences . ,5.5 Conceptual FramewoiReferences

6

6.16.26.2.16.2.26.2.36.2.46.2.56.36.3.16.3.26.3.36.3.46.3.5

The Ecology of Harm]Within Prymnesioph]B. EDVARDSEN and 1.1

IntroductionClass PrymnesiophyaTaxonomy, MorpholojDistribution and AbuiAutecology and EcoplToxicity and Toxins .Ecological StrategiesClass RaphidophyceaeTaxonomy, MorpholojDistribution and AbuiAutecology and EcophToxicityEcological Strategies

References

The Ecology of HarmfS.S. BATES and V.L. TR

7.17.27.37.47.57.6

IntroductionToxin-Producing Diat(Domoic Acid in the MiPhysiological EcologyMolecular Tools for StiConclusions and Direc

References

8

8.18.2

Ecology of Harmful QH.W.PAERLandR.S.F

IntroductionEnvironmental Factors

Contents XI

5.3 Blooms, Including Toxic Outbreaks 595.4 Human Influences 605.5 Conceptual Frameworks to Advance Understanding 61References 64

6 The Ecology of Harmful FlagellatesWithin Prymnesiophyceae and Raphidophyceae 67B. EDVARDSEN and I. IMAI

6.1 Introduction 676.2 Class Prymnesiophyceae (Division Haptophyta) 676.2.1 Taxonomy, Morphology and Life History 676.2.2 Distribution and Abundance 686.2.3 Autecology and Ecophysiology 696.2.4 Toxicity and Toxins 706.2.5 Ecological Strategies 716.3 Class Raphidophyceae (Division Heterokontophyta) . . . . 726.3.1 . Taxonomy, Morphology and Life History 726.3.2 Distribution and Abundance 736.3.3 Autecology and Ecophysiology 746.3.4 Toxicity 756.3.5 Ecological Strategies 75References 77

7 The Ecology of Harmful Diatoms 81S.S. BATES and V.L. TRAINER

7.1 Introduction 817.2 Toxin-Producing Diatoms, Genus Pseudo-nitzschia 827.3 Domoic Acid in the Marine Food Web 837.4 Physiological Ecology of Pseudo-nitzschia spp 847.5 Molecular Tools for Studying Pseudo-nitzschia 867.6 Conclusions and Directions for Future Research 87References 88

8 Ecology of Harmful Cyanobacteria 95H.W. PAERL and R.S. FULTON HI

8.1 Introduction 958.2 Environmental Factors Controlling CyanoHABs 97

XII Contents

8.2.1 Nutr ients 978.2.2 Physical-Chemical Factors: Salinity and Turbulence 102

8.2.3 Salinity and Turbulence 1028.3 CyanoHAB Interactions with Micro/Macroorganisms . . . . 104

8.4 CyanoHAB Management 106

References 107

9 Brown Tides I l lC. J. GOBLER and W. G. SUNDA

9.1 Background I l l9.2 Nutrients and Physical Factors 1139.3 Sources of Cell Mortality 117References 120

Contents

11.3 In Situ Growth Rates11.4 Are Harmful Algal S]11.5 Conclusions . . . .References

12

12.112.212.312.412.5

Harmful Algae and C

M.J.W.Veldhuisand(

Introduction . . . .

Mortality of HABs .Death Due to HABs

Mechanisms to Avoid

Ecological ImplicatioReferences

Part C The Ecology and Physiology of Harmful Algae

10 Harmful Algal Bloom Dynamics in Relationto Physical Processes 127EG. FIGUEIRAS, G.C. PITCHER, and M. ESTRADA

10.1 Introduction 12710.2 Physical Constraints: From Diffusion to Advection 12810.3 Life-Forms 12910.4 Algal Communities 13010.5 Retention and Transport 13110.5.1 Retention-Reduced Exchange 13110.5.2 Transport 133References 136

11 Ecological Aspects of Harmful Algal In Situ PopulationGrowth Rates 139W. STOLTE and E. GARCES

11.1 Introduction 13911.2 Ecological Interpretation of In Situ Growth Rate

Measurements 140

13

13.113.213.313.413.513.6

The Diverse NutrientFocus on OsmotrophP. M. GLIBERT and C.

Introduction and TenOsmotrophy PathwayCellular Costs and BeEcological SignificancA Comment on EvoluConclusions . . . .

References

14 Phagotrophy in HarmD. STOECKER, U. TILLJ

14.1 Introduction14.2 Phagotrophy and its A14.3 Relationship of Phago14.4 Significance of PhagolReferences

Contents XIII

11.3 In Situ Growth Rates; Variation Among Taxonomic Groups . 14311.4 Are Harmful Algal Species r-or K-Strategists? 14711.5 Conclusions 149References 149

12 Harmful Algae and Cell Death 153M.J.W. Veldhuis and C.P.D. Brussaard

12.1 Introduction 15312.2 Mortality of HABs 15612.3 Death Due to HABs 15712.4 Mechanisms to Avoid Cell Mortality 15812.5 Ecological Implications 159References 160

13 The Diverse Nutrient Strategies of Harmful Algae:Focus on Osmotrophy 163P. M. GLIBERT and C. LEGRAND

13.1 Introduction and Terminology 16313.2 Osmotrophy Pathways and Methods to Explore Them . . . . 16413.3 Cellular Costs and Benefits of Osmotrophy 16713.4 Ecological Significance of Osmotrophy 16813.5 A Comment on Evolutionary Aspects of Osmotrophy . . . . 17013.6 Conclusions 171References 171

14 Phagotrophy in Harmful Algae 177D. STOECKER, U. TILLMANN, and E. GRANELI

14.1 Introduction 17714.2 Phagotrophy and its Advantages 18014.3 Relationship of Phagotrophy to Toxicity 18214.4 Significance of Phagotrophy 184References 185

XIV Contents

15 Allelopathy in Harmful Algae:A Mechanism to Compete for Resources? 189E. GRANELI and RJ. HANSEN

15.1 Harmful Algal Species Known of Allelopathy 18915.2 Approaches to Demonstrate/Study Allelopathy -

Pitfalls and Strength/Weaknessesof Experimental Approaches 189

15.3 Which Toxins are Involved in the Allelopathic Effects? . . . 19215.4 Influence of Abiotic and Biotic Factors on Allelopathy . . . 19415.4.1 Abiotic Factors 19415.4.2 Biotic Factors 19615.5 Ecological Significance of Allelopathy in Marine Ecosystems 198References 199

16 Trace Metals and Harmful Algal Blooms 203W.G. SUNDA

16.1 Introduction 20316.2 Chemistry and Availability of Metals 20416.3 Trace Metals as Limiting Nutrients 20516.4 Trace Metal Toxicity 20716.5 Trace Metal Effects on HABs: Domoic Acid Production

in Pseudo-nitzschia 20816.6 Trace Metal Effects on Other HAB Species 210References 211

17 Molecular Physiology of Toxin Productionand Growth Regulation in Harmful Algae 215A. CEMBELLA and U. JOHN

17.1 Introduction 21517.2 Phycotoxin Biosynthesis 21617.3 Growth and Regulation of Toxin Production 21717.4 Toxin Production Through the Cell Cycle 21917.5 Molecular Approaches to Growth and Toxin Expression . . 22017.6 Current and Future Perspectives 223References 226

Contents

18

18.118.218.318.418.518.6

Chemical and PhysicE. Graneli and K. Fly

Introduction . . . .Growth Stage and ToPhysical Factors InfliInorganic Nutrients;Organic Matter and 1Conclusions . . . .

References

19 Relationships Betwe<M. KODAMA, G.J. Dot

19.1 Introduction . . . .19.2 Diversity of Algal-As:19.2.1 Bacteria Associated v19.2.2 Spatio-Temporal Reh19.3 Bacterial Influences c

and Toxins19.3.1 Bacterial Effects on A19.3.2 The Role of Bacteria i19.3.3 Bacterially-Mediated

of Algal Toxins . . .19.4 Potential Implication19.5 Future Directions/Re:References

Part D Harmful Algae and tl

20

20.120.220.220.220.2

.1

.2

.3

Harmful Algae InteraPlanktonic GrazersJ.T. TURNER

Introduction . . . .Planktonic GrazersHeterotrophic Dinofl;Tintinnids and AloricRotifers

Contents

18 Chemical and Physical Factors Influencing Toxin ContentE. Graneli and K. Flynn

xv

229

18.1 Introduction 22918.2 Growth Stage and Toxin Production 22918.3 Physical Factors Influencing Toxin Content 23018.4 Inorganic Nutrients and Toxin Content 23118.5 Organic Matter and Toxin Content 23718.6 Conclusions 238References 239

19 Relationships Between Bacteria and Harmful AlgaeM. KODAMA, G.J. DOUCETTE, and D.H. GREEN

243

19.1 Introduction 24319.2 Diversity of Algal-Associated Bacteria 24419.2.1 Bacteria Associated with Harmful Algal Species 24419.2.2 Spatio-Temporal Relationships Between Bacteria and Algae 24619.3 Bacterial Influences on Algal Growth, Metabolism,

and Toxins 24719.3.1 Bacterial Effects on Algal Growth 24719.3.2 The Role of Bacteria in Toxin Production 24819.3.3 Bacterially-Mediated Release and Metabolism

of Algal Toxins 24919.4 Potential Implications of Interactions Among Bacteria . . . 25019.5 Future Directions/Research Needs/Critical Questions . . . . 251References 252

Part D Harmful Algae and the Food Web

20 Harmful Algae Interactions with MarinePlanktonic Grazers 259J.T. TURNER

20.1 Introduction 25920.2 Planktonic Grazers 26020.2.1 Heterotrophic Dinoflagellates and other Flagellates 26020.2.2 Tintinnids and Aloricate Ciliates 26120.2.3 Rotifers 261

XVI Contents

20.2.4 Copepods and other Mesozooplankton 26220.3 HAB Toxin Accumulation in Zooplankton 26320.4 Selective Grazing and Feeding Deterrence by Harmful Algae 26320.5 Impact of Zooplankton Grazing on Formation

and Termination of HA Blooms 26420.6 Conclusions 265References 266

21 Pathogens of Harmful Microalgae 271P.S. SALOMON and I. IMAI

21.1 Introduction 27121.2 Viruses 27121.2.1 Host Specificity 27321.3 Algicidal Bacteria 27321.3.1 Modes of Algicidal Activity and Specificity 27321.3.2 Ecology of Algicidal Bacteria and Harmful Microalgae . . . 27421.3.3 Seaweed Beds as Prevention of HABs 27521.4 Parasitic Fungi 27521.4.1 Host Specificity 27621.5 Parasitic Protists 27621.5.1 Host Specificity 27821.5.2 Host Avoidance of Parasitic Infection 27821.6 Conclusions and Future Perspectives 279References 280

22 Phycotoxin Pathways in Aquatic Food Webs:Transfer, Accumulation, and Degradation 283G. J. DOUCETTE, I. MANEIRO, I. RIVEIRO, and C. SVENSEN

22.1 Introduction 28322.2 Bacteria 28322.3 Zooplankton 28522.4 Bivalves 28622.5 Benthic Invertebrates (Non-Bivalves) 28722.6 Fishes 28822.7 Seabirds and Marine Mammals 28922.8 Summary and Conclusions 290References 293

Contents

Part E Studying and Mitigj

23 Molecular ApproachLife Cycles: ImplicatR. W. LITAKER and P.

Introduction . . . .Identifying Life CyclHybridization (FISHNuclear Staining to IGenomic Approache:and Meiotic Life CydMeasuring Genetic RDuring Sexual ReproFuture Application oland DNA MicroarrayConclusions . . . .

23.123.2

23.3

23.4

23.5

23.6

23.7References

24

24.124.2

24.3

24.3.124.3.224.4

24.4.124.4.2

24.4.3

24.5

Laboratory and Fieldto Aid the Detection iK. METFIES, K. TOBE,

Introduction . . . .Ribosomal RNA Sequfor Phylogenetic StudFluorescent in Situ H]for Identifying IntactTSA-FISH for Flow QTSA-FISH for Solid PIDetecting Many SpeciUsing DNA Probe ArrMicroarrays on GlassHandheld Array DeviiDetectionDNA Probe Arrays foiof Species Using the EConclusions

References

Contents

Part E Studying and Mitigating Harmful Algae: New Approaches

XVII

23 Molecular Approaches to the Study of PhytoplanktonLife Cycles: Implications for Harmful Algal Bloom EcologyR. W. LITAKER and P. A. TESTER

299

23.1 Introduction 29923.2 Identifying Life Cycle Stages Using Fluorescence In Situ

Hybridization (FISH) 29923.3 Nuclear Staining to Determine Ploidy and Growth Rates . . 30123.4 Genomic Approaches to Identifying Mitotic

and Meiotic Life Cycle Stages 30223.5 Measuring Genetic Recombination

During Sexual Reproduction 30523.6 Future Application of Reverse Transcriptase Assays

and DNA Microarrays in Life Cycle Studies 30523.7 Conclusions 307References 307

24 Laboratory and Field Applications of Ribosomal RNA Probesto Aid the Detection and Monitoring of Harmful Algae . . . 311K. METFIES, K. TOBE, C. SCHOLIN, and L.K. MEDLIN

24.1 Introduction 31124.2 Ribosomal RNA Sequences as Markers

for Phylogenetic Studies and Species Identification 31224.3 Fluorescent in Situ Hybridization (FISH)

for Identifying Intact Cells 31224.3.1 TSA-FISH for Flow Cytometry 31424.3.2 TSA-FISH for Solid Phase Cytometry 31524.4 Detecting Many Species Simultaneously

Using DNA Probe Arrays 31624.4.1 Microarrays on Glass Slides and Fluorescence Detection . . 31624.4.2 Handheld Array Device That Uses Electro-Chemical

Detection 31824.4.3 DNA Probe Arrays for Autonomous Detection

of Species Using the Environmental Sample Processor (ESP) 31924.5 Conclusions 320References 321

XVIII Contents

25 Mitigation and Controls of HABs 327H.G. Kim

25.1 Introduction 32725.2 Mitigation Strategies and Control of HABs 32825.2.1 Precautionary Impact Preventions 32825.2.2 Direct and Indirect Bloom Controls 32925.2.3 Contingency Plans for Fish Culture 33425.3 Conclusions 335References 335

Part F Human Impact on Harmful Algaeand Harmful Algae Impact on Human Activity

26 The Complex Relationships Between Increasesin Fertilization of the Earth, Coastal Eutrophicationand Proliferation of Harmful Algal Blooms 341P.M. Glibert and J.M. Burkholder

26.1 Introduction 34126.2 Global Trends in Population, Agricultural Fertilizer

Usage and Implications for Export to Coastal Waters . . . . 34126.3 Nutrient Limitation versus Eutrophication:

Basic Conceptual Framework 34326.4 Nutrient Loading, Nutrient Composition, and HABs . . . . 34426.5 Factors Complicating the Relationship

Between Eutrophication and HABs 34726.6 Conclusions 350References 351

27

27.127.227.2.127.2.227.2.327.3

"Top-Down" Predation Control on Marine Harmful AlgaeJ.T. Turner and E. Grane"li

355

Introduction 355"Top-down" Predators 357Medusae 357Ctenophores 358Fishes 358Case Studies 359

Contents

27.3.1 Black Sea27.3.2 Mesocosm Studies27.4 Conclusions . . .References

28 Climate Change and IB. Dale, M. Edwards, a

28.128.228.328.428.5

IntroductionEvidence from the PasResults from PlanktonResults from the SedirConclusions

References

29

29.129.229.3

29.3.129.3.229.3.329.429.4.129.4.229.4.329.5

Anthropogenic IntrodG. HALLEGRAEFF and

Potential Transport VeVector Surveys for MicEvidence for Successfuof Non-Indigenous Mi-Absence in Historic SaSediment Cyst CoresIncreasing Molecular IManagement Options 1Warning System for HiBallast Water ExchangtTreatment Options .Conclusions

References

30

30.130.230.330.430.5

The Economic Effects <P. Hoagland and S. Scat

IntroductionScientific Concerns .Economic Concerns .Why Measure EconomiEconomic Losses

Contents XIX

27.3.1 Black Sea 35927.3.2 Mesocosm Studies 36027.4 Conclusions 362References 363

28 Climate Change and Harmful Algal Blooms 367B. Dale, M. Edwards, and P. C. Reid

28.1 Introduction 36728.2 Evidence from the Past 36928.3 Results from Plankton Records 37028.4 Results from the Sedimentary Record of Dinoflagellate Cysts 37228.5 Conclusions 375References 376

29 Anthropogenic Introductions of Microalgae 379G. HALLEGRAEFF and S. GOLLASCH

29.1 Potential Transport Vectors for Microalgae 37929.2 Vector Surveys for Microalgae 38029.3 Evidence for Successful Establishment

of Non-Indigenous Microalgae 38129.3.1 Absence in Historic Samples 38129.3.2 Sediment Cyst Cores 38129.3.3 Increasing Molecular Evidence 38229.4 Management Options to Reduce Risk of Introductions . . . 38329.4.1 Warning System for HABs in Ballast-Water-Uptake Zones . 38329.4.2 Ballast Water Exchange Studies on Phytoplankton 38429.4.3 Treatment Options 38629.5 Conclusions 388References 388

30 The Economic Effects of Harmful Algal Blooms 391P. Hoagland and S. Scatasta

30.1 Introduction 39130.2 Scientific Concerns 39230.3 Economic Concerns 39230.4 Why Measure Economic Losses? 39330.5 Economic Losses 394

XX Contents

30.6 Economic Impacts 39730.7 Estimates of National Economic Effects 39830.8 Conclusions 401References 402

Subject Index 403

Contributors

AZANZA, R.V.

Marine Science Institute, UniverQuezon City, Philippines, e-mail

BATES, S.S.

Fisheries and Oceans Canada, GiNew Brunswick, E1C 9B6, Canad

BRUSSAARD, C.P.D.

Royal Netherlands Institute for SThe Netherlands, e-mail: corina.l

BURKHOLDER, J.M.

Center for Applied Aquatic EcoloNorth Carolina State University, 1e-mail: joann_burkholder@ncsu.

CEMBELLA,A.

Alfred Wegener Institute for Pola12, Bremerhaven, Germany, e-ma

DALE, B.

Geoscience Department, UniversiNorway, e-mail: barri.dale@geo.u

DOUCETTE, G.J.

NOAA/National Ocean Service, 21South Carolina 29412, USA, e-mai