Acknowledgments xxi

Introduction xxiii

1 Causes of Harmful Algal Blooms 1
Patricia M. Glibert and JoAnn M. Burkholder

1.1 Introduction 1

1.2 “Getting There”: The Classic Perspective on Introduced Species and Links to Cultural Eutrophication 2

1.2.1 Introduced Species 2

1.2.2 Anthropogenically Introduced Nutrients 3

1.3 “Being There”: Blooms and Why They Succeed 5

1.3.1 Nutrient-Related HAB 5

1.3.2 Resource Ratios, Nutrient Stoichiometry, and Optimal Nutrient Ratios 6

1.3.3 Diversity in Use of Forms of Nitrogen 9

1.3.4 Toxicity 10

1.3.5 Mixotrophy: Use of “Packaged” and Dissolved Particulate Nutrients 12

1.3.6 Other Adaptations 13

1.4 “Staying There”: Links to Physical Structure and Climate 14

1.4.1 Physical Structure: Large-Scale and Small-Scale Natural Hydrological Features 14

1.4.2 Physical Dynamics: Anthropogenic Hydrological Changes 15

1.4.3 Reinforcing Feedbacks 16

1.4.3.1 Trophic Disruptions 16

1.4.3.2 Biogeochemical Alterations 17

1.4.4 Climate Change 18

1.5 Conclusions 20

Acknowledgments 21

References 21

2 Detection and Surveillance of Harmful Algal Bloom Species and Toxins 39
Gregory J. Doucette, Linda K. Medlin, Pearse McCarron, and Philipp Hess

2.1 Introduction 39

2.2 Organism Detection 41

2.2.1 Visual/Optical 41

2.2.1.1 Light Microscopy (LM)/Utermöhl’s 41

2.2.1.2 Light Microscopy/Flow Cytometry 41

2.2.1.3 In Vivo Fluorometry 42

2.2.1.4 Spectral Absorbance/Spectroradiometry 43

2.2.2 Molecular 43

2.2.2.1 Whole Cell Format 44

2.2.2.2 Cell-Free Format 47

2.3 Toxin Detection 51

2.3.1 In Vivo Assays 53

2.3.1.1 Rat Bioassay 58

2.3.1.2 Mouse Bioassay 58

2.3.2 In Vitro Assays 59

2.3.2.1 Functional Assays 60

2.3.2.2 Structural Assays 66

2.3.2.3 Biosensors 71

2.3.3 Analytical Techniques 72

2.3.3.1 High-Performance Liquid Chromatography with Optical Detection (UV or FLD) 73

2.3.3.2 Liquid Chromatography–Mass Spectrometry (LC-MS) and Liquid Chromatography–Tandem Mass Spectrometry (LC-MS/MS) 75

2.3.3.3 Other Analytical Methods: Capillary Electrophoresis (CE), Matrix-Assisted Laser Desorption Ionization-Time of Flight (MALDI-TOF), and Laser Ablation Electrospray Ionization (LAESI) 78

2.3.3.4 Perspectives 79

2.4 Autonomous, In Situ Technologies 80

2.4.1 Environmental Sample Processor (McLane Research Laboratories) 81

2.4.2 Imaging Flow Cytobot (McLane Research Laboratories) 83

2.4.3 Optical Phytoplankton Discriminator (aka BreveBuster; Mote Marine Laboratory) 84

2.4.4 CytoBuoy (CytoBuoy b.v.) 85

2.4.5 SPATT Passive Samplers 86

2.5 Conclusions and Future Prospects 87

Disclaimer 89

References and Further Reading 89

3 Modeling Marine Harmful Algal Blooms: Current Status and Future Prospects 115
Kevin J. Flynn and Dennis J. McGillicuddy, Jr.

3.1 Introduction 115

3.2 Building Models to Describe Ecological Events 117

3.3 Limitations to What Models Can Do, and Why 119

3.3.1 Building Models 119

3.3.2 Model Complexity 119

3.3.3 The Need for Data 120

3.3.4 Validating Models 121

3.4 Modeling T-HAB and ED-HAB Events 121

3.5 How Good Are Current HAB Models? 122

3.6 Future Modeling of T-HAB and ED-HAB: Managing Expectations 128

3.7 Improving Our Capabilities 129

3.7.1 Changes in the Biological–Modeling Interface 129

Acknowledgments 130

References 130

4 Harmful Algal Blooms and Shellfish 135
Leila Basti, Hélène Hégaret, and Sandra E. Shumway

4.1 Introduction 135

4.2 Major Shellfish Poisonings 136

4.2.1 Paralytic Shellfish Poisoning (PSP) 136

4.2.2 Diarrheic Shellfish Poisoning (DSP) 137

4.2.3 Neurotoxic Shellfish Poisoning (NSP) 138

4.2.4 Amnesic Shellfish Poisoning (ASP) 139

4.2.5 Azaspiracid Shellfish Poisoning (AZP) 139

4.3 Other Toxins: Pectenotoxins (PTX) and Yessotoxins (YTX) 140

4.4 Emerging Shellfish Poisonings 141

4.5 Toxin Uptake, Accumulation, and Depuration 142

4.6 Shellfish Contamination in North America 143

4.6.1 Bivalves 143

4.6.1.1 Paralytic Shellfish Contamination 143

4.6.1.2 Diarrheic Shellfish Contamination 149

4.6.1.3 Neurotoxic Shellfish Contamination 150

4.6.1.4 Amnesic Shellfish Contamination 151

4.6.2 Gastropods 154

4.6.3 Crustaceans 162

4.7 Impacts on Shellfish 163

4.8 Conclusions and Perspectives 164

References and Further Reading 167

5 Vulnerabilities of Marine Mammals to Harmful Algal Blooms 191
Margaret H. Broadwater, Frances M. Van Dolah, and Spencer E. Fire

5.1 Introduction 191

5.2 Overview of Algal Toxins 192

5.2.1 Brevetoxins 193

5.2.2 Ciguatoxins 199

5.2.3 Diarrhetic Shellfish Poisoning Toxins 200

5.2.4 Domoic Acid 201

5.2.5 Paralytic Shellfish Toxins 206

5.2.6 Other Algal and Cyanobacterial Toxins 209

5.3 Impacts of Algal Toxins Specific to Marine Mammals 210

5.3.1 The Effects of Toxin Exposure Depend on Animal Physiology and Behavior 210

5.3.2 Emerging Issues: Non-acute and Multiple Toxin Exposure 211

5.3.3 Prospects for Managing Impacts of HAB 211

5.4 Considerations for the Evaluation of HAB Toxins in Marine Mammals 212

5.4.1 Sampling Marine Mammals for HAB Toxin Analysis 213

5.4.2 Priority Needs for Investigating HAB Toxin Involvement in Marine Mammal Morbidity and Mortality 214

Abbreviations 214

References and Further Reading 215

6 Interactions between Seabirds and Harmful Algal Blooms 223
Corinne M. Gibble and Brian A. Hoover

6.1 Introduction 223

6.2 Historical Interactions between HAB and Seabirds 224

6.2.1 Paralytic Shellfish Poisoning (PSP) 224

6.2.2 Neurotoxic Shellfish Poisoning (NSP) 227

6.2.3 Amnesic Shellfish Poisoning 228

6.2.4 Akashiwo sanguinea 228

6.2.5 Diarrheic Shellfish Poisoning (DSP) 229

6.2.6 CyanoHAB 230

6.3 Improved Monitoring and Establishment of Causality 231

6.3.1 Coordinating Monitoring and Pathology to Confirm Relationships between HAB and Seabird Mortality 231

6.3.2 Seabirds as Biological Indicators 233

6.4 Implications for Conservation 234

References 235

7 Food Web and Ecosystem Impacts of Harmful Algae 243
JoAnn M. Burkholder, Sandra E. Shumway, and Patricia M. Glibert

7.1 Introduction 243

7.2 Approaches, Pitfalls, Progress, and Goals 277

7.3 High-Biomass Algal Blooms 279

7.4 Emerging Recognition of the Roles of Allelochemicals 282

7.4.1 Microalgae 283

7.4.2 Thalloid Macroalgae 285

7.4.3 Filamentous Mat-Forming Macroalgae 287

7.5 Toxigenic Algae in Aquatic Food Webs 287

7.5.1 Toxic Microcystis aeruginosa Blooms across North America 289

7.5.2 Toxic Prymnesium parvum Blooms and Fish Communities in Two Texas Rivers 290

7.5.3 Toxic Pseudo-nitzschia Blooms in Coastal Upwelling Areas 292

7.5.4 Toxic Alexandrium Blooms in the Northeast 292

7.5.5 Toxic Karenia brevis Blooms along the Florida Coast 293

7.6 Ecosystem-Disruptive Algal Blooms 294

7.7 Future Directions 295

Appendix A: Scientific Names for Organisms Listed by Common Name in This Chapter, Also Indicating Species Affected by Karenia brevis (Kb) 297

References and Further Reading 301

8 Assessing the Economic Consequences of Harmful Algal Blooms: A Summary of Existing Literature, Research Methods, Data, and Information Gaps 337
Charles M. Adams, Sherry L. Larkin, Porter Hoagland, and Brian Sancewich

8.1 Introduction 337

8.2 Overview 338

8.3 Research Methodologies 338

8.4 Sources and Types of Data 347

8.5 Spatial and Temporal Scopes 348

8.6 Nature of the Hazard 349

8.7 Current Research Gaps 350

8.8 Conclusion 351

Acknowledgments 351

References and Further Reading 351

9 Public Health and Epidemiology 355
Lynn M. Grattan, Joe Schumacker, Andrew Reich, and Sailor Holobaugh

9.1 Introduction 355

9.2 What Is Public Health and Epidemiology? 355

9.3 HAB and Human Illness 356

9.3.1 Paralytic Shellfish Poisoning (PSP) 357

9.3.1.1 Exposure 357

9.3.1.2 Clinical Symptoms 361

9.3.1.3 Treatment 361

9.3.2 Amnesic Shellfish Poisoning (ASP) 361

9.3.2.1 Exposure 361

9.3.2.2 Clinical Syndrome 361

9.3.2.3 Treatment 362

9.3.3 Neurotoxic Shellfish Poisoning (NSP) 362

9.3.3.1 Exposure 362

9.3.3.2 Clinical Illness 363

9.3.3.3 Treatment 363

9.3.4 Brevetoxin Inhalation Syndrome (BIS) 363

9.3.4.1 Exposure 363

9.3.4.2 Clinical Illness 363

9.3.4.3 Treatment 363

9.3.5 Diarrhetic Shellfish Poisoning (DSP) 363

9.3.5.1 Exposure 363

9.3.5.2 Clinical Syndrome 364

9.3.5.3 Treatment 364

9.3.6 Ciguatera Fish Poisoning (CFP) 364

9.3.6.1 Exposure 364

9.3.6.2 Clinical Illness 364

9.3.6.3 Treatment 365

9.3.7 Azaspiracid Shellfish Poisoning (AZP) 365

9.3.7.1 Exposure 365

9.3.7.2 Clinical Syndrome 366

9.3.7.3 Treatment 366

9.3.8 Toxic Cyanobacteria 366

9.3.8.1 Exposure 366

9.3.8.2 Clinical Syndromes 366

9.3.8.3 Treatment 366

9.4 The HAB Manager’s Role in Preventing HAB-Related Illnesses 367

9.4.1 HAB Management Exemplars 367

9.4.2 The Native American Perspective from Washington State, USA: Domoic Acid and Paralytic Shellfish Toxins 367

9.4.2.1 Background 367

9.4.2.2 Tribal Capacity and Inclusion 369

9.4.2.3 Lessons Learned 369

9.4.3 The Florida Department of Health Perspective 369

9.4.3.1 Harmful Algal Blooms 370

9.5 HAB-Related Stressors and Human Resilience 370

9.6 Conclusion 371

References and Further Reading 371

10 Marine Biotoxin and Harmful Algae Monitoring and Management 377
Gregg W. Langlois and Steve L. Morton

10.1 Introduction 377

10.2 Identifying Sampling Program Needs 383

10.3 Developing a Sampling Program for Shellfish Monitoring 384

10.3.1 Shellfish Sampling Stations 384

10.3.2 Monitoring Shellfish Toxicity 386

10.4 Developing a Sampling Program for Phytoplankton Monitoring 388

10.4.1 Phytoplankton Sampling Stations 388

10.4.2 Monitoring Phytoplankton 389

10.5 Monitoring Other Fisheries 394

10.6 Novel Approaches and Advanced Tools to Enhance Monitoring Programs 396

10.6.1 Diversifying Program Participation: Volunteer Monitors 396

10.6.2 Field Testing for Toxins: PSP and ASP 399

10.6.3 Screening Tests for Toxins: DSP and PSP 401

10.6.4 SPATT 401

10.6.5 Oceanographic Data 402

10.7 Management Considerations 408

10.7.1 Commercial Shellfish 408

10.7.2 Recreational Shellfishing 411

10.8 Phytoplankton Sampling Protocol Examples 413

10.9 HAB Forecasting Links 413

Acknowledgments 413

References and Further Reading 413

11 Harmful Algal Bloom Education and Outreach 419
Mare Timmons, Mary Sweeney-Reeves, and Steve L. Morton

11.1 Introduction 419

11.2 K–12 Education 426

11.3 Web-Based and Distance Learning Education 427

11.4 Citizen Science 428

11.4.1 Contributions of Citizen Science 429

11.4.2 Connecting Citizen Science to Ocean Learning 431

11.4.2.1 Safety 431

11.4.2.2 Training Sessions 431

11.5 Conclusion 432

References and Further Reading 432

12 Prevention, Control, and Mitigation of Harmful Algal Bloom Impacts on Fish, Shellfish, and Human Consumers 435
Kevin G. Sellner and J.E. (Jack) Rensel

12.1 Introduction 435

12.2 HAB Prevention 435

12.2.1 Aquaculture Site Selection or Relocation 435

12.2.2 Nutrient Load Reductions 436

12.2.3 Phytoplankton Mixing, Increasing Turbulence, and Decreasing Residence Times (Mostly Freshwater Systems) 440

12.2.4 Reducing HA Introductions 441

12.3 Preventing and Reducing HAB Impacts on Shellfish and Fish 442

12.3.1 Preventing Human and Animal Exposures 442

12.3.1.1 Shellfish and Finfish Monitoring 442

12.3.1.2 Depuration and Detoxification 444

12.3.1.3 Food Processing 444

12.3.1.4 Cooking 445

12.3.1.5 Aerosols 445

12.3.1.6 Medical Treatments 445

12.4 HAB Controls 445

12.4.1 Protections 445

12.4.2 Biomass Removal 446

12.4.3 Capping 446

12.4.4 Nutrient Trapping in Sediments 446

12.4.5 Reductions of Algal Resting Stages (Cysts) 446

12.5 Mitigation of HAB 447

12.5.1 Detection 447

12.5.2 Chemical Additions 448

12.5.3 Flocculation 451

12.5.4 Barely Straw (Hordeum vulgare) 454

12.5.5 Other Treatments 455

12.5.5.1 UV Exposure 455

12.5.5.2 Cavitation 455

12.5.5.3 Ultrasound 455

12.5.5.4 Electrolysis 456

12.5.5.5 Hydraulics and Mixing 456

12.5.5.6 Biological Controls 456

12.6 Shellfish 458

12.7 Fish Mariculture 459

12.7.1 HAB Mitigation for Fish Mariculture 459

12.7.2 Best Management Practices for Fish Mariculture Siting, Including HAB and Eutrophication Issues 460

12.7.2.1 Local Land Use 460

12.7.2.2 Plankton Monitoring and Water Quality Assessments 460

12.7.2.3 Physical Hydrographic Considerations 461

12.7.2.4 Vertical Mixing Considerations 461

12.7.3 Mitigation of HAB at Fish Mariculture Facilities 461

12.7.4 HAB Mitigation Methods for Fish Mariculture 462

12.7.4.1 Feeding and Handling Practices 462

12.8 Conclusions 470

Acknowledgments 474

References 474

Further Reading 492

13 Harmful Algae Introductions: Vectors of Transfer, Mitigation, and Management 493
Shauna Murray and Gustaaf Hallegraeff

13.1 Summary 493

13.2 The Biogeographic Ranges of Harmful Algal Bloom Species 493

13.3 Vectors of Transfer 494

13.3.1 Natural Factors 494

13.3.2 Ballast Water 494

13.3.3 Translocation of Aquaculture Products 494

13.4 Molecular Evidence for Introductions of New Species to a Region 494

13.4.1 The Stalk-Forming Freshwater Fouling Diatom Didymosphenia geminata 495

13.4.2 Alexandrium pacificum and A. minutum in European and Japanese Waters 496

13.4.3 Gymnodinium catenatum in Australia and Europe 497

13.5 Prevention and Risk Reduction 498

13.5.1 Code of Practice on Translocation with Aquaculture Products 498

13.5.2 Warning for HAB in Ballast Water-Uptake Zones and When Translocating Aquaculture Products 498

13.5.3 Ballast Water Management 498

13.5.4 Other Precautionary Measures 500

13.6 Emergency Treatment Options 501

References 502

14 Culture and Culture Collections 507
Gary H. Wikfors and Steve L. Morton

14.1 Introduction 507

14.2 Step 1: Sampling the Environment 507

14.3 Step 2: Processing a Field Sample in the Laboratory to Confirm Presence of the Target Organism 509

14.4 Step 3: From Spark to Flame 511

14.5 Step 4: Long-Term Perpetuation of HAB Cultures 511

14.6 Epilogue 512

Further Reading 513

15 Harmful Macroalgal Blooms in a Changing World: Causes, Impacts, and Management 515
Brian E. Lapointe, JoAnn M. Burkholder, and Kathryn L. Van Alstyne

15.1 Introduction 515

15.2 Freshwater and Other Inland Macroalgae 516

15.3 Estuarine and Coastal Marine Macroalgae 519

15.4 Influences on Bloom Development 525

15.5 Nutrient Pollution 525

15.5.1 Sources 525

15.5.2 Indicators of Nutrient Pollution and Nutrient Sources 526

15.6 Uptake/Adsorption of Other Contaminants 526

15.7 Impacts on Human Health: Macroalgae as Substrata for Pathogens 527

15.8 Non-native Invasions 528

15.9 Ecological and Ecosystem-Level Impacts 529

15.9.1 Regime Shifts 530

15.9.2 Freshwater Macroalgal HAB 532

15.9.2.1 Filamentous Cyanobacteria 532

15.9.2.2 Filamentous Green Algae 533

15.9.3 Estuarine and Coastal Marine HAB 534

15.10 Effects of Blooms on the Chemistry of the Oceans and the Atmosphere 535

15.10.1 Changes to Carbonate Chemistry and pH 535

15.10.2 Release of Materials and Chemicals into Seawater 536

15.10.3 Release of Volatile Compounds 537

15.11 Management Strategies 537

15.12 Economic Impacts 539

15.13 Recycling Macroalgae Biomass 541

15.14 Forecast 542

References and Further Reading 542

16 Harmful Algal Species Fact Sheets 561

Alexandrium 563
Allan D. Cembella

Amphidomataceae 575
Urban Tillmann

Aureococcus anophagefferens Hargraves et Sieburth & Aureoumbra lagunensis DeYoe et Stockwell – Brown Tides 583
Christopher J. Gobler

Ceratium furca (Ehrenberg) Claparede & Lachmann 585
Steve L. Morton

Chattonella marina 587
Carmelo R. Tomas

Cochlodinium – Rust Tide 589
Christopher J. Gobler

Cyanobacteria 591
JoAnn M. Burkholder, Christopher J. Gobler, and Judith M. O’Neil

Dinophysis 597
Steve L. Morton

Fibrocapsa japonica 599
Carmelo R. Tomas

Gambierdiscus 601
Michael L. Parsons, Mindy L. Richlen, and Alison Robertson

Gymnodinium catenatum 605
Allan D. Cembella and Christine J. Band-Schmidt

Heterosigma akashiwo 613
Carmelo R. Tomas

Karenia brevis (Davis) Hansen et Moestrup – Florida Red Tide 615
Larry E. Brand

Ostreopsis 617
Michael L. Parsons, Mindy L. Richlen, and Alison Robertson

Pfiesteria piscicida Steidinger & Burkholder and Pfiesteria shumwayae Glasgow & Burkholder 621
JoAnn M. Burkholder and Harold G. Marshall

Prorocentrum 625
Patricia M. Glibert and JoAnn M. Burkholder

Prymnesium parvum (Carter) – “Golden Algae” 629
Daniel L. Roelke and Schonna R. Manning

Pseudo-nitzschia – seriata group; delicatissima group 633
Raphael Kudela

Takayama 637
Larry E. Brand

Appendix 1 Websites That Routinely Distribute Bulletins on the Presence of Harmful Algal Blooms (HAB) for Public Health 639

Appendix 2 State Agencies Providing Information and Updates on Toxic and Harmful Algal Blooms and Water Quality 641

Appendix 3 List of General Web Resources 645

Index 647