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Harmful Algal Blooms: A Compendium Desk Reference

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Sandra E Shumway at University of Connecticut
Sandra E Shumway
JoAnn Burkholder at North Carolina State University
JoAnn Burkholder
Steve L. Morton at National Oceanic and Atmospheric Administration
Steve L. Morton
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FFIRS 05/03/2018 10:43:28 Page iii
Harmful Algal Blooms
A Compendium Desk Reference
Edited by
Sandra E. Shumway
University of Connecticut
Groton, CT, USA
JoAnn M. Burkholder
North Carolina State University
Raleigh, NC, USA
Steve L. Morton
NOAA National Ocean Service
Charleston, SC, USA
FFIRS 05/03/2018 10:43:28 Page iv
This edition first published 2018
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Library of Congress Cataloging-in-Publication Data
Names: Shumway, Sandra E., editor. | Burkholder, JoAnn M. (JoAnn Marie),
editor. | Morton, Steve L., editor.
Title: Harmful algal blooms : a compendium desk reference / edited by Sandra E.
Shumway, JoAnn M. Burkholder, Steve L. Morton.
Description: Hoboken, NJ : John Wiley & Sons, 2018. | Includes index. |
Identifiers: LCCN 2017040583 (print) | LCCN 2017047559 (ebook) | ISBN
9781118994696 (pdf) | ISBN 9781118994689 (epub) | ISBN 9781118994658
(cloth)
Subjects: LCSH: Toxic algae. | Algal blooms–Toxicology.
Classification: LCC QK568.T67 (ebook) | LCC QK568.T67 H372 2018 (print) | DDC
579.8–dc23
LC record available at https://lccn.loc.gov/2017040583
Cover Design: Eric Heupel
Cover Image: Eric Heupel
Set in 9/11 pt WarnockPro-Regular by Thomson Digital, Noida, India
Printed and bound in Singapore by Markono Print Media Pte Ltd
10987654321
FFIRS 05/03/2018 10:43:28 Page v
We dedicate this book to
Robert R.L. Guillard and Theodore J. Smayda,
our esteemed colleagues, friends, and mentors.
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vii
Contents
List of Contributors xvii
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’s41
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
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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
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Contents
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
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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
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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
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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
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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
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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
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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 Stage 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
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List of Contributors
Charles M. Adams
University of Florida
Food and Resource Economics Department
Gainesville, FL
United States
Christine J. Band-Schmidt
CICIMAR-IPN
Depto. de Plancton y Ecología Marina
La Paz, B.C.S.
México
Leila Basti
Tokyo University of Marine Science and
Technology
Marine Environmental Physiology Laboratory
Department of Ocean Sciences
Tokyo
Japan
Larry E. Brand
University of Miami
Rosenstiel School of Marine and Atmospheric
Science
Department of Marine Biology and Ecology
Miami, FL
United States
Margaret H. Broadwater
NOAA National Ocean Service
National Centers for Coastal Ocean Science
Stressor Detection and Impacts Division
Charleston, SC
United States
JoAnn M. Burkholder
North Carolina State University
Department of Applied Ecology
Center for Applied Aquatic Ecology
Raleigh, NC
United States
Allan D. Cembella
Alfred Wegener Institute
Helmholtz Zentrum für Polar- und
Meeresforschung
Bremerhaven
Germany
Gregory J. Doucette
NOAA National Ocean Service
National Centers for Coastal Ocean Science
Marine Biotoxins Program
Charleston, SC
United States
Spencer E. Fire
Florida Institute of Technology
Biological Sciences
Melbourne, FL
United States
Kevin J. Flynn
Swansea University
College of Science
Swansea, Wales
United Kingdom
Corinne M. Gibble
University of California
Ocean Science Department
Santa Cruz, CA
United States
Patricia M. Glibert
University of Maryland
Center for Environmental Science
Horn Point Laboratory
Cambridge, MD
United States
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xviii List of Contributors
Christopher J. Gobler
Stony Brook University
School of Marine and Atmospheric Sciences
Southampton, NY
United States
Lynn M. Grattan
University of Maryland School of Medicine
Department of Neurology
Baltimore, MD
United States
Gustaaf Hallegraeff
University of Tasmania
Institute for Marine and Antarctic Studies (IMAS)
Hobart, Tasmania
Australia
Hélène Hégaret
Institut Universitaire Européen de la Mer
Laboratoire des Sciences de l’Environnement
Marin
UMR 6539 CNRS/UBO/IRD/IFREME
Plouzané
France
Philipp Hess
IFREMER
Laboratoire Phycotoxines
France
Porter Hoagland
Woods Hole Oceanographic Institution
Marine Policy Center
Woods Hole, MA
United States
Sailor Holobaugh
University of Maryland School of Medicine
Department of Neurology
Baltimore, MD
United States
Brian A. Hoover
University of California
Graduate Group in Ecology
Davis, CA
United States
Raphael Kudela
University of California, Santa Cruz
Ocean Sciences Department
Institute of Marine Sciences
Santa Cruz, CA
United States
Gregg W. Langlois
California Department of Public Health (retired)
Richmond, CA
United States
Brian E. Lapointe
Florida Atlantic University –Harbor Branch
Oceanographic Institute
Marine Ecosystem Health Program
Ft. Pierce, FL
United States
Sherry L. Larkin
University of Florida
Food and Resource Economics Department
Gainesville, FL
United States
Schonna R. Manning
University of Texas at Austin
Department of Molecular Biosciences
Austin, TX
United States
Harold G. Marshall
Old Dominion University
Department of Biological Sciences
Norfolk, VA
United States
Pearse McCarron
National Research Council of Canada
Halifax, Nova Scotia
Canada
Dennis J. McGillicuddy, Jr.
Woods Hole Oceanographic Institution
Department of Applied Ocean Physics and
Engineering
Woods Hole, MA
United States
Linda K. Medlin
Marine Biological Association of the United
Kingdom
The Citadel
Plymouth
United Kingdom
Steve L. Morton
NOAA National Ocean Service
Marine Biotoxins Program
Charleston, SC
United States
FLOC 03/31/2018 11:32:27 Page xix
xix
Shauna Murray
University of Technology Sydney
Climate Change Cluster (C3)
Ultimo, NSW
Australia
Judith M. O’Neil
University of Maryland Center for Environmental
Science
Horn Point Laboratory
Cambridge, MD
United States
Michael L. Parsons
Florida Gulf Coast University
Fort Meyers, FL
United States
Andrew Reich
Bureau of Environmental Health
Florida Department of Health
Tallahassee, FL
United States
J.E. (Jack) Rensel
Rensel Associates Aquatic Sciences
Arlington, WA
United States
Mindy L. Richlen
Woods Hole Oceanographic Institution
Biology Department
Woods Hole, MA
United States
Alison Robertson
University of South Alabama
and
Dauphin Island Sea Laboratory
Dauphin Island, AL
United States
Daniel L. Roelke
Texas A&M University
Department of Wildlife and Fisheries Sciences
College Station, TX
United States
Brian Sancewich
University of Florida
Food and Resource Economics Department
Gainesville, FL
United States
List of Contributors
Joe Schumacker
Quinault Department of Fisheries
Taholah, WA
United States
Kevin G. Sellner
Hood College
Center for Coastal and Watershed Studies
Frederick, MD
United States
Sandra E. Shumway
University of Connecticut
Department of Marine Sciences
Groton, CT
United States
Mary Sweeney-Reeves
University of Georgia
Marine Extension Service and Georgia Sea Grant
Athens, GA
United States
Urban Tillmann
Alfred Wegener Institute
Bremerhaven
Germany
Mare Timmons
University of Georgia
Marine Extension Service and Georgia Sea Grant
Savannah, GA
United States
Carmelo R. Tomas
University of North Carolina–Wilmington
Center for Marine Science
Wilmington, NC
United States
Kathryn L. Van Alstyne
Western Washington University
Shannon Point Marine Center
Anacortes, WA
United States
FLOC 03/31/2018 11:32:27 Page xx
xx List of Contributors
Frances M. Van Dolah
NOAA National Ocean Service
National Centers for Coastal Ocean Science
Stressor Detection and Impacts Division
Charleston, SC
United States
Gary H. Wikfors
NOAA Fisheries Service
Northeast Fisheries Science Center
Milford, CT
United States
FACKNOW 03/06/2018 10:34:7 Page xxi
xxi
Acknowledgments
The production of a multiauthored book is a long
and arduous task, and success depends first and
foremost upon the efforts and talents of the
contributors. The extraordinary talent and
patience of the authors are gratefully acknowl-
edged. The project could not have been com-
pleted without Noreen Blaschik and Elle Allen,
who assisted with numerousand varied tasks, and
created organization out of chaos. Eric Heupel
designed the food web diagram and provided the
cover artwork, and his talents made the mundane
aspects of graphics not only functional, but
understandable.
This book was made possible by grant
#NA14NMF4270023 from the DOC/NOAA/Salt-
onstall-Kennedy Program to Sandra E. Shumway
and Tessa L. Getchis. An executive summary of
this book is available:
Getchis, T.L., and S.E. Shumway. (Eds.) 2017.
Harmful Algae: An Executive Summary. Connect-
icut Sea Grant College Program. CTSG-17-08.
16 pp.
... Harmful algal blooms can occur, and have become more common, in nearly all waterbodies and present health risks because of the production of toxins, but even HABs that do not produce toxins can negatively affect the environment (Carmichael, 1994;Huisman et al., 2018;Paerl & Otten, 2013). Different genera of cyanobacteria can produce several types of cyanotoxins with varying modes of action and toxic effects (reviewed in Carmichael, 1994;Huisman et al., 2018;Shumway et al., 2018). One of the more common freshwater cyanotoxins is microcystin produced by the cyanobacteria Microcystis aeruginosa, but other cyanobacterial genera also produce microcystin (Harke et al., 2016). ...
... Along with direct effects of cyanotoxins on wildlife, other stressors could have additive or synergistic effects. One major factor influencing amphibian and reptile declines is habitat alteration and destruction, which can also influence the occurrence of HABs by increasing runoff and nutrient inputs, for example (Hallegraeff, 2003;Shumway et al., 2018). Algae can produce other toxic compounds such as depsipeptides and retinoids that can negatively affect humans and wildlife (Janssen, 2019;Sehnal et al., 2019;Yeung et al., 2020). ...
... Many studies reported nominal concentrations and did not verify toxin concentrations, but toxins could degrade over time in chronic studies (Schmidt et al., 2014), and it could be beneficial to verify concentrations to provide more reliable estimates and results. Most studies that did verify concentrations in exposure solutions or in animal tissues used ELISAs, which have lower accuracy and sensitivity compared with targeted analytical approaches (e.g., HPLC or LC-MS/MS) that can also identify other less studied cyanotoxins and their congeners (e.g., MC-RR and -YR, limnothrix toxins, or aetokthonostatin; Shumway et al., 2018). The development of new analytical methods may be necessary to increase the accuracy of quantification and allow for testing of multiple toxins while decreasing costs and allowing for increased availability to scientists conducting research with cyanotoxins (Text box 1, below). ...
Effects of Harmful Algal Blooms on Amphibians and Reptiles are Under-Reported and Under-Represented
Article
Full-text available
  • Jul 2024
  • ENVIRON TOXICOL CHEM
Harmful algal blooms (HABs) are a persistent and increasing problem globally, yet we still have limited knowledge about how they affect wildlife. Although semi‐aquatic and aquatic amphibians and reptiles have experienced large declines and occupy environments where HABs are increasingly problematic, their vulnerability to HABs remains unclear. To inform monitoring, management, and future research, we conducted a literature review, synthesized the studies, and report on the mortality events describing effects of cyanotoxins from HABs on freshwater herpetofauna. Our review identified 37 unique studies and 71 endpoints (no‐observed‐effect and lowest‐observed‐effect concentrations) involving 11 amphibian and 3 reptile species worldwide. Responses varied widely among studies, species, and exposure concentrations used in experiments. Concentrations causing lethal and sublethal effects in laboratory experiments were generally 1 to 100 µg/L, which contains the mean value of reported HAB events but is 70 times less than the maximum cyanotoxin concentrations reported in the environment. However, one species of amphibian was tolerant to concentrations of 10,000 µg/L, demonstrating potentially immense differences in sensitivities. Most studies focused on microcystin‐LR (MC‐LR), which can increase systemic inflammation and harm the digestive system, reproductive organs, liver, kidneys, and development. The few studies on other cyanotoxins illustrated that effects resembled those of MC‐LR at similar concentrations, but more research is needed to describe effects of other cyanotoxins and mixtures of cyanotoxins that commonly occur in the environment. All experimental studies were on larval and adult amphibians; there were no such studies on reptiles. Experimental work with reptiles and adult amphibians is needed to clarify thresholds of tolerance. Only nine mortality events were reported, mostly for reptiles. Given that amphibians likely decay faster than reptiles, which have tissues that resist decomposition, mass amphibian mortality events from HABs have likely been under‐reported. We propose that future efforts should be focused on seven major areas, to enhance our understanding of effects and monitoring of HABs on herpetofauna that fill important roles in freshwater and terrestrial environments. Environ Toxicol Chem 2024;00:1–14. Published 2024. This article is a U.S. Government work and is in the public domain in the USA. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.
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... Although no culture studies are available to define its specific ecological requirements, environmental conditions at the blooming station GA10 suggest that an averaged MLD of 25 m, surface temperature of 12.7°C, salinity of 33.7, and levels of nitrate and phosphate of 1.67 and 0.60 μM, respectively, may favor the growth of O. laticeps in natural assemblages. Additionally, the extraordinary bloom of the photosynthetic amphidomataceae dinoflagellates at station GA01 could be attributed to their small cell size, particular swimming modes, and their potential to produce intracellular toxins (Tillmann et al., 2019), which are effective strategies for avoiding predators and achieving high densities (Shumway et al., 2018). Over the last decades, multispecific blooms of Amphidomataceae have been documented in high abundance in the Argentine Sea (Ramírez et al., 2022), producers of Azaspiracids-2 (AZA-2) (Guinder et al., 2020;Tillmann et al., 2019). ...
Insights Into Protistan Plankton Blooms in the Highly Dynamic Patagonian Shelf and Adjacent Ocean Basin in the Southwestern Atlantic
Article
Full-text available
  • Mar 2025
Blooms of phototrophic protists play a crucial role in marine biogeochemical cycles, significantly impacting carbon fluxes and overall ecosystem productivity. Eukaryotes of the nano‐ and microplankton are responsible for the large spring and summer blooms visible from space in the highly dynamic southwestern Atlantic Ocean. Here, we investigated the composition and abundance of protistan plankton during late spring 2021 across three contrasting oceanographic regions of the southwestern Atlantic Ocean: the Patagonian continental shelf, the core of the Malvinas Current (MC), and the adjacent energetic open ocean in the Argentine basin. Using a combination of in situ sampling and satellite‐derived chlorophyll‐a, particulate inorganic carbon, sea surface temperature, and geostrophic currents, we identified marked differences in water masses and plankton communities. High chlorophyll‐a concentration over the outer continental shelf was related to blooms of phototrophic and mixotrophic dinoflagellates and large diatoms. This plankton accumulation over the shelf was associated with the permanent thermohaline front that develops along the shelf‐break, with upwelling as the main driver of high productivity. However, in waters of the MC and the open ocean protists exhibited lower biomass and diversity, with prevalence of nanoflagellates and coccolithophores. The results suggest that the water column stability and the N:Si and N:P nutrient ratios shape the distinct bloom‐forming functional types. This study contributes with data on taxonomic diversity identified by microscopy which, along with remote sensing approaches, provide insights into how protists respond to environmental changes at different spatial and temporal scales.
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... The appeal of biological techniques stems from their eco-compatibility and potential for sustained efficacy. Nevertheless, their use might be constrained by challenges such as grasping intricate ecological dynamics and the possibility of unforeseen repercussions [58]. The present review focuses on the different biotic organisms isolated and used to remove HABs and their mode of action. ...
Advancements in Biological Strategies for Controlling Harmful Algal Blooms (HABs)
Article
Full-text available
  • Jan 2024
Harmful algal blooms (HABs) are a primary environmental concern, threatening freshwater ecosystems and public health and causing economic damages in the billions of dollars annually. These blooms, predominantly driven by phytoplankton species like cyanobacteria, thrive in nutrient-rich, warm, and low-wind environments. Because of the adverse impacts of HABs, this review examines various control methods, focusing on biological strategies as sustainable solutions. While effective in disrupting algal populations, traditional chemical and physical interventions carry ecological risks and can be resource-intensive. Biological control methods, including biomanipulation and using algicidal microorganisms such as Streptococcus thermophiles, Myxobacteria, and Lopharia spadicea, emerge as eco-friendly alternatives offering long-term benefits. Additionally, barley and rice straw application has demonstrated efficacy in curbing HAB growth. These biological approaches work by inhibiting algal proliferation, disrupting cellular structures, and fostering algal cell aggregation. Despite their advantages over conventional methods, biological controls face challenges, including intricate ecological interactions. This article delves into the latest biological techniques aimed at eradicating HABs, intending to diminish their frequency and reduce toxin levels in aquatic environments. While most research to date has been confined to laboratory settings, scaling these methods to field applications presents hurdles due to the variability and complexity of natural ecosystems. The review underscores the need for further research and development in this critical area of environmental science.
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... Tang et al. (2021) and Yang et al. (2021aYang et al. ( , 2021b demonstrated the presence of paralytic shellfish toxins (PSTs) which can pose a threat to public health, with the highest levels reported in the hepatopancreas. Harmful algal blooms are a threat to shellfish aquaculture facilities globally (Shumway et al., 2018;Matsuyama and Shumway, 2009;Hégaret and Wikfors, 2009). While mussels are generally known to accumulate and depurate the toxins rapidly (Bricelj and Shumway, 1998), aquaculturists should be aware of the potential threats and effective monitoring programs should be available. ...
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... Over the past decades, as HAB have become a serious ecological issue in coastal ecosystems around the world, the mechanisms and consequences of HAB studies have been studied (Anderson et al., 2008;Zhou et al., 2008Zhou et al., , 2019Shumway et al., 2018). In the study area, the diatom and the dinoflagellate blooms occur successively every year. ...
Impacts of algal blooms on sinking carbon flux and hypoxia off the Changjiang River estuary
Article
  • Sep 2023
Based on 10 multidisciplinary investigations conducted from February 2015 to January 2016, the phytoplankton community and its association with ambient seawater physicochemical parameters in the Changjiang (Yangtze) River estuary (CE) and its adjacent waters were comprehensively examined. In total, 265 taxa were identified, belonging to 5 phyla and 94 genera. Diatoms (63.78%) and dinoflagellates (33.21%) were the dominant groups. The variation of diatom abundance showed a positive relationship with the nutrient concentrations while the dinoflagellate abundance showed a negative relationship. Two algal bloom events occurred during the investigation period. The Changjiang Diluted Water (CDW) induced environmental gradients in the upper layer, favoring the diatom bloom in July. The invasion of the nearshore Kuroshio branch current could affect the formation of a bloom of Prorocentrum donghaiense. With the blooming and senescence of phytoplankton, low dissolved oxygen (DO) and hypoxia occurred in the bottom waters. The bottom DO concentration displayed a significantly negative correlation with phytoplankton carbon flux. The present study provides straightforward evidence for the source of organic matter for oxygen consumption in the CE and its adjacent waters.
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... In general, the closure periods vary from weeks to months, according to the intensity and duration of the toxic bloom and the ability of each bivalve species to eliminate the toxins from their tissues (IPMA 2013(IPMA , 2021. The blue mussel Mytilus edulis is reported to reduce by 50% the concentration of PSP within 12 days in saltwater free of dinoflagellates at 15°C-20°C (Mons et al. 1998, Shumway et al. 2018). Closure periods due to HAB in 2018 showed significant economic impact on the mussel production area in SW Portugal, with the months of July to September continuously closed due to toxins, and nearly 2 wk in both May and October (IPMA 2014-2020), additionally, a toxicity event with PSP was reported in October 2018 that required the hospitalization of two patients with severe symptoms (Carvalho et al. 2019). ...
Potential Effects of Climate Change on Offshore Aquaculture of the Mediterranean Mussel (Mytilus galloprovincialis, Lamarck, 1819) in Portugal
Article
  • Sep 2023
There is increasing concern on how future climate change (CC) will affect fish and shellfish populations. The European Union funded the Climate change and European aquatic RESources (CERES) consortium to collaborate with industry and policy stakeholders to test CC scenarios through 24 “storylines” linked to specific regional fisheries or aquaculture activities. For this study, the focus is on “storyline 7” related to offshore longline aquaculture for Mediterranean (Med) mussel (Mytilus galloprovincialis, Lamarck, 1819) along the Atlantic coast at Sagres, Southern Portugal. CERES has compared two greenhouse gas emission scenarios in terms of Representative Concentration Pathways (RCP) 4.5 and 8.5 W m–2 for projected mean sea surface temperature (SST) and mean net primary production (PP) comparing the period 2000 to 2019 to the period 2080 to 2099. With regard to SST in the Algarve, the prediction is for an increase of up to 1°C and under RCP 4.5 and up to 2°C under RCP 8.5 by the end of the century, while the projected changes for net PP are much more variable, with a trend for a slight increase for both RCP 4.5 and 8.5. Some of the key research activities included an experimental study testing the combined effects of temperature (3°C, 8°C, 15°C, 20°C, 25°C) and chlorophyll (2.10 µg–1), the data from which was used for a WinShell mass balance model based on an individual Med mussel grown offshore at Sagres and then incorporated into the local-scale Farm Aquaculture Resource Management model to provide data for projecting climate-driven changes on production potential. Mussel weight at harvest and production yield at Sagres are similar under both emission scenarios, RCP 4.5 and 8.5 at periodic time periods between the years 2000 and 2099. The Med mussel was able to adapt to SST up to 25°C provided the PP was reasonable. A core activity of CERES is engagement with stakeholders, with the help of bow-tie analysis to reflect stakeholder concerns about the current and future factors affecting Med mussel production, as well as the development of a probabilistic Bayesian Belief Network model linking biological projections with economic consequences and policy measures to test whether current management systems can adapt to identified risks under CERES scenarios. Initial interactions with stakeholders showed that they were much more concerned with day-to-day issues, including failure of mussel spat recruitment, reduced mussel condition, and periodic closures due to harmful algal blooms, rather than any hypothetical future problems arising from CC. Nonetheless, there was much more interest when potential scenarios arising from CC were presented. The Med mussel does seem to be better adapted to higher SST compared with the blue mussel (Mytilus edulis).
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... Among these frontal phenomena, harmful algal blooms (HABs) are the motivating scenario of this paper. According to [3], "HABs cause human illness, largescale mortality of fish, shellfish, mammals, and birds, and deteriorating water quality". HABs occur when algae colonies experience abnormal growth, which results in the production of harmful toxins [4]. ...
Adaptive Sampling of Algal Blooms Using Autonomous Underwater Vehicle and Satellite Imagery: Experimental Validation in the Baltic Sea
Preprint
  • May 2023
This paper investigates using satellite data to improve adaptive sampling missions, particularly for front tracking scenarios such as with algal blooms. Our proposed solution to find and track algal bloom fronts uses an Autonomous Underwater Vehicle (AUV) equipped with a sensor that measures the concentration of chlorophyll a and satellite data. The proposed method learns the kernel parameters for a Gaussian process model using satellite images of chlorophyll a from the previous days. Then, using the data collected by the AUV, it models chlorophyll a concentration online. We take the gradient of this model to obtain the direction of the algal bloom front and feed it to our control algorithm. The performance of this method is evaluated through realistic simulations for an algal bloom front in the Baltic sea, using the models of the AUV and the chlorophyll a sensor. We compare the performance of different estimation methods, from GP to curve interpolation using least squares. Sensitivity analysis is performed to evaluate the impact of sensor noise on the methods performance. We implement our method on an AUV and run experiments in the Stockholm archipelago in the summer of 2022.
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... • general local disruption of ecosystem function; and • depletion of oxygen in the water column following the end of a bloom, leading to hypoxic conditions and mortalities (Lassus et al., 2016;Shumway et al., 2018). Furthermore, increases in both finfish and shellfish aquaculture in coastal regions have led to increased lethal and sub-lethal impacts on fish-and shellfish resources (Hallegraeff et al., 2021;Naylor et al., 2021). ...
Joint FAO/IOC/IAEA Technical guidance for the implementation of early warning systems for harmful algal blooms
Book
Full-text available
  • Apr 2023
Globally, there are 3 400 to 4 000 described species of marine microalgae but only 1 to 2 percent are considered to be harmful. Harmful algal blooms (HABs) have significant impacts on food safety and security through contamination or mass mortalities of aquatic organisms. The impacts and mass mortalities of marine species caused by harmful algae are not new and have been recorded for decades. However, there is growing concern that these events will increase due to accelerating global warming, climate change and anthropogenic activities. Indeed, if not properly controlled, aquatic products contaminated with HAB biotoxins are responsible for potentially deadly foodborne diseases and when rapidly growing, HAB consequences include reduced dissolved oxygen in the ocean, dead zones, and mass mortalities of aquatic organisms. Improving HAB forecasting is an opportunity to develop early warning systems for HAB events such as food contamination, mass mortalities, or foodborne diseases. Surveillance systems have been developed to monitor HABs in many countries; however, the lead-time or the type of data (i.e. identification at the species-level, determination of toxicity) may not be sufficient to take effective action for food safety management measures or other reasons, such as transfer of aquaculture products to other areas. Having early warning systems could help mitigate the impact of HABs and reduce the occurrence of HAB events. The Joint FAO-IOC-IAEA technical guidance for the implementation of early warning systems (EWS) for HABs will guide competent authorities and relevant institutions involved in consumer protection or environmental monitoring to implement early warning systems for HABs present in their areas (marine and brackish waters), specifically those affecting food safety or food security (benthic HABs, fish-killing HABs, pelagic toxic HABs, and cyanobacteria HABs). The guidance provides a roadmap for stakeholders on how to improve or implement an EWS for HABs and biotoxins, where appropriate. It is important to note that not all countries and institutions can implement the same level of EWS for HABs, and this guidance is intended mainly for those who seek to broaden existing early warning systems, or who are just beginning to consider putting a system in place
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Analysing the Socioeconomic Impacts of Fishing Closures Due to Toxic Algal Blooms: Application of the Vulnerability Framework to the Case of the Scallop Fishery in the Eastern English Channel
Article
Full-text available
  • Aug 2023
Harmful and toxic algal blooms (HABs) are an increasing concern for marine social-ecological systems. These unpredictable events threaten human health and may affect the viability of economic activities such as shellfish fisheries due to harvesting bans. Monitoring and early warning systems are developed to support management decisions to mitigate and reduce impacts. Nevertheless, HAB alert systems currently only focus on the environmental dimensions to identify the risk of bloom occurrences. Other socioeconomic dimensions associated with HABs are generally not taken into account to support decision making. Integrating information on the economic risk of HABs and on adaptive strategies of impacted communities would provide essential insights for decision makers. This study presents an analysis of how the potential impacts of HAB-related restrictions on economic activities can be effectively assessed to support decision making. A vulnerability-based approach is developed and applied to the case study of the French scallop fishery in the eastern English Channel. The results showed clear differences in vulnerability patterns between the studied fishing fleets despite their similar exposure. This is associated with the heterogeneity in individual characteristics in terms of sensitivity level and adaptive strategies. This research highlights the important effect of social factors such as adaptation in the magnitude of HAB impacts and supports the relevance of the vulnerability approach in the assessment of socioeconomic impacts of such events. Combining environmental and socioeconomic factors through a composite index can bridge the existing gaps in addressing and mitigating HAB impacts.
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Brand Ostreopsis Pfiesteria piscicida Steidinger & Burkholder and Pfiesteria shumwayae Glasgow & Burkholder 621
  • E Larry
Larry E. Brand Ostreopsis Pfiesteria piscicida Steidinger & Burkholder and Pfiesteria shumwayae Glasgow & Burkholder 621
Burkholder Prymnesium parvum (Carter) -"Golden Algae
  • 629
  • Patricia M Glibert
Patricia M. Glibert and JoAnn M. Burkholder Prymnesium parvum (Carter) -"Golden Algae" 629
Manning Pseudo-nitzschia -seriata group
  • L Daniel
  • Roelke
  • R Schonna
Daniel L. Roelke and Schonna R. Manning Pseudo-nitzschia -seriata group;