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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 rst published 2018
2018 John Wiley & Sons Ltd
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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. |
Identiers: LCCN 2017040583 (print) | LCCN 2017047559 (ebook) | ISBN
9781118994696 (pdf) | ISBN 9781118994689 (epub) | ISBN 9781118994658
(cloth)
Subjects: LCSH: Toxic algae. | Algal bloomsToxicology.
Classication: LCC QK568.T67 (ebook) | LCC QK568.T67 H372 2018 (print) | DDC
579.8dc23
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 Packagedand 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)/Utermöhls41
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 ChromatographyMass Spectrometry (LC-MS) and Liquid
ChromatographyTandem 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 BiologicalModeling Interface 129
Acknowledgments 130
References 130
4 Harmful Algal Blooms and Shellsh 135
Leila Basti, Hélène Hégaret, and Sandra E. Shumway
4.1 Introduction 135
4.2 Major Shellsh Poisonings 136
4.2.1 Paralytic Shellsh Poisoning (PSP) 136
4.2.2 Diarrheic Shellsh Poisoning (DSP) 137
4.2.3 Neurotoxic Shellsh Poisoning (NSP) 138
4.2.4 Amnesic Shellsh Poisoning (ASP) 139
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4.2.5 Azaspiracid Shellsh Poisoning (AZP) 139
4.3 Other Toxins: Pectenotoxins (PTX) and Yessotoxins (YTX) 140
4.4 Emerging Shellsh Poisonings 141
4.5 Toxin Uptake, Accumulation, and Depuration 142
4.6 Shellsh Contamination in North America 143
4.6.1 Bivalves 143
4.6.1.1 Paralytic Shellsh Contamination 143
4.6.1.2 Diarrheic Shellsh Contamination 149
4.6.1.3 Neurotoxic Shellsh Contamination 150
4.6.1.4 Amnesic Shellsh Contamination 151
4.6.2 Gastropods 154
4.6.3 Crustaceans 162
4.7 Impacts on Shellsh 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 Shellsh Poisoning Toxins 200
5.2.4 Domoic Acid 201
5.2.5 Paralytic Shellsh Toxins 206
5.2.6 Other Algal and Cyanobacterial Toxins 209
5.3 Impacts of Algal Toxins Specic 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 Shellsh Poisoning (PSP) 224
6.2.2 Neurotoxic Shellsh Poisoning (NSP) 227
6.2.3 Amnesic Shellsh Poisoning 228
6.2.4 Akashiwo sanguinea 228
6.2.5 Diarrheic Shellsh 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 Conrm 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: Scientic 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 Shellsh 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 Shellsh 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 Shellsh 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 Shellsh 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 Shellsh 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 Managers 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 Shellsh 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 Shellsh Monitoring 384
10.3.1 Shellsh Sampling Stations 384
10.3.2 Monitoring Shellsh 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 Shellsh 408
10.7.2 Recreational Shellshing 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 K12 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, Shellsh, 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 Shellsh and Fish 442
12.3.1 Preventing Human and Animal Exposures 442
12.3.1.1 Shellsh and Finsh Monitoring 442
12.3.1.2 Depuration and Detoxication 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 Shellsh 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 pacicum 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 Conrm 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 Inuences 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. ONeil
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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Pesteria piscicida Steidinger & Burkholder and Pesteria shumwayae
Glasgow & Burkholder 621
JoAnn M. Burkholder and Harold G. Marshall
Prorocentrum 625
Patricia M. Glibert and JoAnn M. Burkholder
Prymnesium parvum (Carter) –“Golden Algae629
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 lEnvironnement
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. ONeil
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 CarolinaWilmington
Center for Marine Science
Wilmington, NC
United States
Kathryn L. Van Alstyne
Western Washington University
Shannon Point Marine Center
Anacortes, WA
United States
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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
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Acknowledgments
The production of a multiauthored book is a long
and arduous task, and success depends rst 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.
... Dinoflagellate species are known to be a major component of harmful algal blooms (HABs) with a set of physical and chemical effects causing a significant hazard to ecosystems, fisheries, and animal and human health [2]. Physical effects can lead to depletion of oxygen in the water and an increase in viscosity due to the excretion of mucilage. ...
... Using these definitions, almost half the total assemblage from PPB was identified as HAB-related, being dominated by Gyrodinium spirale and G. dominans (Fig. 5). These two species were also dominant within the HAB subset at DR, although not to the same extent as at PPB. Due to the potential economic and health impacts of HABs, DinoREF was screened for sequences of potentially toxic dinoflagellates [2,27,32,56]. PPB is subject to high levels of direct and indirect anthropogenic influences, which could explain the up-to 1.6 fold higher representation of identified HAB-related taxa. ...
... The stronger environmental influence on HAB assemblages is also reflected by their correlation with four parameters (salinity, temperature, ODO, and depth), whereas bioluminescent assemblages correlated with only two ( Table 3). The first three parameters explaining HAB assemblages (salinity, temperature and ODO) are all influenced by anthropogenic activity, consistent with studies indicating that HABs are triggered by human impacts (reviewed by [2]). It is important to note that nutrients considered important stressors for dinoflagellate growth, such as nitrogen and phosphate, were not measured here. ...
Article
Full-text available
Background: Dinoflagellates are a ubiquitous and ecologically important component of marine phytoplankton communities, with particularly notable species including those associated with harmful algal blooms (HABs) and those that bioluminesce. High-throughput sequencing offers a novel approach compared to traditional microscopy for determining species assemblages and distributions of dinoflagellates, which are poorly known especially in Australian waters. Results: We assessed the composition of dinoflagellate assemblages in two Australian locations: coastal temperate Port Phillip Bay and offshore tropical waters of Davies Reef (Great Barrier Reef). These locations differ in certain environmental parameters reflecting latitude as well as possible anthropogenic influences. Molecular taxonomic assessment revealed more species than traditional microscopy, and it showed statistically significant differences in dinoflagellate assemblages between locations. Bioluminescent species and known associates of HABs were present at both sites. Dinoflagellates in both areas were mainly represented by the order Gymnodiniales (66%-82% of total sequence reads). In the warm waters of Davies Reef, Gymnodiniales were equally represented by the two superclades, Gymnodiniales sensu stricto (33%) and Gyrodinium (34%). In contrast, in cooler waters of Port Phillip Bay, Gymnodiniales was mainly represented by Gyrodinium (82%). In both locations, bioluminescent dinoflagellates represented up to 0.24% of the total sequence reads, with Protoperidinium the most abundant genus. HAB-related species, mainly represented by Gyrodinium, were more abundant in Port Phillip Bay (up to 47%) than at Davies Reef (28%), potentially reflecting anthropogenic influence from highly populated and industrial areas surrounding the bay. The entire assemblage of dinoflagellates, as well as the subsets of HAB and bioluminescent species, were strongly correlated with water quality parameters (R2 = 0.56-0.92). Significant predictors differed between the subsets: HAB assemblages were explained by salinity, temperature, dissolved oxygen, and total dissolved solids; whereas, bioluminescent assemblages were explained only by salinity and dissolved oxygen, and had greater variability. Conclusion: High-throughput sequencing and genotyping revealed greater diversity of dinoflagellate assemblages than previously known in both subtropical and temperate Australian waters. Significant correlations of assemblage structure with environmental variables suggest the potential for explaining the distribution and composition of both HAB species and bioluminescent species.
... Continental shelves encompass the coastal areas where primary productivity attains peaks resulting from the high photosynthetic activity of phytoplankton (Uitz et al. 2010;Gregg and Rousseaux 2019) where dinoflagellates and diatoms predominate. Many phytoplankton species are able to produce harmful algal blooms (HABs) in coastal zones, causing adverse effects on the environment, massive fish die-offs, and even seafood poisoning in humans Shumway et al. 2018). ...
... According to Taylor et al. (2008), the global distribution patterns of dinoflagellates show that benthic species are confined to the shallower waters of continental shelves, i.e., those closer to the coastline. This affinity of P. quadridentatum for the coastal zone may also be due to the river discharges and the dynamics of the currents that modify the turbulence of the water, due to the importance of hydrological features on the bloom-forming species (i.e., Glibert et al. 2018;Shumway et al. 2018). According Rodríguez-Gómez et al. (2019a, b), the rise of the cell density of P. quadridentatum occurs in the season of higher rainfall and the greatest river discharges (and nutrients concentration), in conjunction with low turbulence in the southwest Gulf of Mexico. ...
... It should be borne in mind, that other factors not addressed in this study as the biological interactions (i.e., allelopathy, competition, grazing, multispecific blooms) or the trophic mode (autotrophism o mixotrophy) might also favor or restrain the distribution of this species, and therefore it is a limitation of the models presented here. These factors have been related to distribution and growth of bloom-forming species (Flynn et al. 2018;Shumway et al. 2018;Prabhudessai et al. 2019 Flynn et al. (2018), an increasing number of dinoflagellates have been recognized as mixotrophs with important implications on removal competitors. In case of P. quadridentatum, the information about this kind of factors is scarce and, in most of the cases, is limited to regional records. ...
Article
Full-text available
This work was designed to analyze the current ecological niche of Peridinium quadridentatum var. quadridentatum and its harmful algal blooms (HABs) using species distribution models. A maximum entropy model was fitted to samples of occurrence records gathered from the scientific literature and using environmental data for the continental shelves of the world obtained from BIO-ORACLE. The geographic models plotted were sea surface temperature vs. salinity, nitrate vs. phosphate concentration, and radiation vs. chlorophyll-a concentration, to describe the environmental space occupied by P. quadridentatum. Our results show that P. quadridentatum is a dinoflagellate of wide thermohaline tolerance linked to sites near coastal areas, which might be related to some life-cycle stages. Both presence (pENM) and blooms (bENM) ecological niche models show that this species prospers near tropical and temperate latitudes. The pENM predicts a broader distribution range than the bENM, suggesting that some sites with favorable conditions for the occurrence of this species are not suitable for its proliferation and formation of HABs. The bENM predicts potential HABs limited in eutrophic areas, but not in hyper-eutrophic areas. As validation of the models, some occurrence records of this species (i.e., West Africa, Peru, and Fiji) were not included in the initial analyses. As a result, the pENM predicts its occurrence in those sites, so the models for current potential distribution and blooms incidences are credible.
... Harmful algal blooms (HABs) are naturally occurring phenomena that have been witnessed throughout history. They represent significant threats to human health, aquaculture resources and marine ecosystems (Shumway et al., 2018). The apparent rise in their global distribution, intensity and frequency has been the cause for increased concern for the sustainability of the aquaculture sector, which is an essential activity contributing significantly to meeting an ever-increasing global demand for food supplies. ...
... HABs have contaminated seafood with potent biotoxins and caused serious human intoxications globally (Shumway et al., 2018). AZAs, the causative toxins of the poisoning syndrome AZP, are the most recently discovered group of lipophilic marine phycotoxins. ...
Article
Apparent increases in harmful algal blooms worldwide have fostered attempts at mitigating their impacts on the aquaculture industry. The dinoflagellate species Azadinium spinosum has been described as the de novo azaspiracid (AZA) toxin producer of AZA-1 and -2 and been implicated in shellfish poisoning incidents (AZP) around Europe, regularly affecting shellfish mariculture operations. Several species of Azadinium have been confirmed in Irish coastal waters, and routine monitoring has shown disparities between Azadinum spp. cell count estimates in the water column and AZA concentrations in shellfish. A survey of bays on the southwest and west coasts of Ireland, carried out in August 2016, investigated the late summer distribution of Azadinium spp. and AZAs. Molecular analysis of water column samples showed very low levels of Az. spinosum. However, AZAs were found in 44% of samples, including in Az. spinosum negative samples. PCR-DGGE analysis was carried out using Amphidomataceae family specific primers on a selection of Az. spinosum negative, but AZA positive, samples. Subsequently sequenced DNA amplicons showed a high level of similarity with other Azadinium species suggesting that the species-specific molecular assays, in current use for monitoring Azadinium spp., are not capturing the likely greater diversity of the genus in Irish waters.
... These interactions are sufficiently sophisticated that they can lead to dose-response interactions between cells (Bittencourt-Oliveira et al., 2015;Song et al., 2017). Toxins and secondary metabolites in Microcystis are also powerful enough to affect the growth of higher trophic level organisms, including invertebrate predators (e.g., zooplankton) and fish, as well as higher aquatic plants (Jiang et al., 2011;Harke et al., 2016;Shumway et al., 2018). However, in order to survive, Microcystis must develop synergistic relationships (Cook et al., 2020). ...
... Microcystis and other cyanobacteria can adversely affect zooplankton survival through production of cyanotoxins as well as a suite of metabolites (Ibelings and Havens, 2008). Both cyanotoxins and protease inhibitors are known to affect factors such as food avoidance, food digestion, and molting in zooplankton (Martin-Creuzburg and Elert, 2004;Rohrlack et al., 2004Rohrlack et al., , 2005Hansson et al., 2007;Shumway et al., 2018). For USFE, the impact of Microcystis on lower food web trophic structure was demonstrated with bioassay FIGURE 9 | Median (bar), 25th and 75th confidence intervals (box), and maximum and minimum (whiskers) of DNA sequence counts in the clusters of orthologous groups (COG) of proteins database for cell functions of prokaryotes and eukaryotes. ...
Article
Full-text available
Microcystis blooms have occurred in upper San Francisco Estuary (USFE) since 1999, but their potential impacts on plankton communities have not been fully quantified. Five years of field data collected from stations across the freshwater reaches of the estuary were used to identify the plankton communities that covaried with Microcystis blooms, including non-photosynthetic bacteria, cyanobacteria, phytoplankton, zooplankton, and benthic genera using a suite of analyses, including microscopy, quantitative PCR (qPCR), and shotgun metagenomic analysis. Coherence between the abundance of Microcystis and members of the plankton community was determined by hierarchal cluster analysis (CLUSTER) and type 3 similarity profile analysis (SIMPROF), as well as correlation analysis. Microcystis abundance varied with many cyanobacteria and phytoplankton genera and was most closely correlated with the non-toxic cyanobacterium Merismopoedia , the green algae Monoraphidium and Chlamydomonas , and the potentially toxic cyanobacteria Pseudoanabaena , Dolichospermum , Planktothrix , Sphaerospermopsis , and Aphanizomenon . Among non-photosynthetic bacteria, the xenobiotic bacterium Phenylobacterium was the most closely correlated with Microcystis abundance. The coherence of DNA sequences for phyla across trophic levels in the plankton community also demonstrated the decrease in large zooplankton and increase in small zooplankton during blooms. The breadth of correlations between Microcystis and plankton across trophic levels suggests Microcystis influences ecosystem production through bottom-up control during blooms. Importantly, the abundance of Microcystis and other members of the plankton community varied with wet and dry conditions, indicating climate was a significant driver of trophic structure during blooms.
... Although dinoflagellates have considerable ecological importance for their contribution to marine primary production, they also have economic consequences from the harmful effects that can take place both during dense blooms (HAB), but also at very low densities through bioaccumulation of toxins, for example, in the tissues of filter feeding mollusks (Shumway et al., 2018). Dinoflagellates are an important issue for marine aquaculture and tourism, causing risk of food poisoning, skin irritations and fish kills. ...
Article
Full-text available
Changes in the composition of dinoflagellates from 1994 to 2001 at a station influenced by wind-induced seasonal upwelling off SW Portugal were analyzed in relation to oceanography. 194 taxa of dinoflagellates were detected, the most frequent belonged to the genera Tripos, Protoperidinium, Dinophysis, Diplopsalopsis, Prorocentrum and Lingulodinium. The composition of dinoflagellate communities followed a seasonal pattern, in association with oceanographic forcing and change of upwelling conditions. Harmful species such as Dinophysis acuminata, D. acuta, D. caudata, Gonyaulax spp. and Lingulodinium polyedra were found to develop during the upwelling season, typically comprising summer and early autumn in the West Iberian upwelling system, and also occasionally in the conditions following upwelling events in other seasons.
... The classification of observed phytoplankton taxa as potentially harmful was based on the IOC-UNESCO Taxonomic Reference List of Harmful Micro Algae (Moestrup et al., 2009), AlgaeBase (Guiry and Guirry, 2021), and other references (Kraberg et al., 2010;Shumway et al., 2018). Additionally, our dataset was complemented with information on the abundance of toxigenic phytoplankton species, measured at two RF lagoonal shellfish production areas, in the vicinity of FNW ("Faro 1") and OE ("Olhão 2"; see approximate location in Fig. 1) study areas, and the nearest coastal production area (L8), from the regular monitoring program undertaken by IPMA. ...
Article
This study aimed to assess the influence of treated wastewater disposal on Ria Formosa coastal lagoon (South Portugal), the largest national producer of bivalve mollusks. Water quality was evaluated at two areas under different wastewater loads and hydrodynamic conditions, using physico-chemical variables, bacterial indicators of contamination, chlorophyll-a concentration, phytoplankton abundance and composition. Samples were collected monthly, between October 2018 and September 2019. Minor influence of effluent discharge was detected at the eastern Olhão area, exposed to stronger hydrodynamics and higher wastewater load than the northwestern Faro area (ca. 2–4-fold total nitrogen and phosphorus). The lower load weakly flushed area showed a poorer water quality, up to 500 m from the discharge point, more marked during the spring-summer period. The intensity, persistence, and spatial extent of the wastewater footprint, lower for the highest-loading area, reflected the role of local hydrodynamic conditions, modulating the influence of wastewater discharge on lagoonal water quality.
... Harmful algal blooms (HABs) are environmental issues in all kinds of water systems worldwide, as these blooms cause an ecological or economic imbalance to the ecosystem (Watson et al., 2015). These algal blooms are caused by various environmental changes brought about by human activities, including climate change, change in oceanic conditions, translocation of native species, and most especially, eutrophication (Shumway, Burkholder & Morton, 2018 There have been many previous attempts to treat these harmful algal blooms, spanning several topics and methods for each. One such treatment is the use of chemical compounds such as copper sulfate, other copper-based algaecides and hydrogen peroxide to eliminate the algae population (Deng et al., 2017;Shen et al., 2019;Yan et al., 2019). ...
Preprint
Full-text available
Harmful algal blooms (HABs) are an environmental issue in all kinds of water systems worldwide, causing an ecological imbalance to various water bodies and posing health risks to humans. Currently, different countries employ different types of HAB countermeasures. This systematic review evaluated some biological, chemical, and physical HAB treatments studied from 2010 to 2020 to properly assess the negative and positive repercussions of the treatments, along with their applicability for implementation. Ecological impact of the treatments were also considered, if testing was done for this. This review also compared the research conducted in the Philippines with that of international studies to closely examine whether there are any gaps in Philippine HAB research and treatment implementation. The review found that chemical treatments, specifically clays, are currently the most practical and available HAB mitigation measure due to the numerous laboratory and field tests done on the method. Philippines' HAB treatment studies are also significantly less than international studies, and the country is also behind in the implementation of these treatments. Despite this, the Philippines was still able to produce quality studies that also considered ecological effects of the treatment, signifying that the HAB mitigation measures studied are intended to be publicly used in the future.
... This increase in nutrients causes eutrophication that, in most cases, promotes the proliferation of some phytoplanktonic populations (Camargo and Alonso, 2006;Schindler, 2006). Commonly referred to as harmful algal blooms (HABs), the intensity and size of these biological events have increased continuously over the past decades (Glibert et al., 2005;Shumway et al., 2018). ...
Article
The development of anthropic activities during the 20th century increased the nutrient fluxes in freshwater ecosystems, leading to the eutrophication phenomenon that most often promotes harmful algal blooms (HABs). Recent years have witnessed the regular and massive development of some filamentous algae or cyanobacteria in Lake Geneva. Consequently, important blooms could result in detrimental impacts on economic issues and human health. In this study, we tried to lay the foundation of an HAB forecast model to help scientists and local stakeholders with the present and future management of this peri-alpine lake. Our forecast strategy was based on pairing two machine learning models with a long-term database built over the past 34 years. We created HAB groups via a K-means model. Then, we introduced different lag times in the input of a random forest (RF) model, using a sliding window. Finally, we used a high-frequency dataset to compare the natural mechanisms with numerical interaction using individual conditional expectation plots. We demonstrate that some HAB events can be forecasted over a year scale. The information contained in the concentration data of the cyanobacteria was synthesized in the form of four intensity groups that directly depend on the P. rubescens concentration. The categorical transformation of these data allowed us to obtain a forecast with correlation coefficients that stayed above a threshold of 0.5 until one year for the counting cells and two years for the biovolume data. Moreover, we found that the RF model predicted the best P. rubescens abundance for water temperatures around 14°C. This result is consistent with the biological processes of the toxic cyanobacterium. In this study, we found that the coupling between K-means and RF models could help in forecasting the development of the bloom-forming P. rubescens in Lake Geneva. This methodology could create a numerical decision support tool, which should be a significant advantage for lake managers.
Chapter
Naturally occurring neurotoxins belonging to two structurally distinct groups of guanidinium alkaloids known collectively as saxitoxins (STXs) and tetrodotoxins (TTXs) share a high affinity and ion flux blockage capacity for voltage-gated sodium ion channels (Nav). Both toxin groups are produced by marine microorganisms and widely distributed among vector species in the oceans, but are also found in terrestrial species. The STXs are often referred to as paralytic shellfish toxins (PSTs) based on their accumulation in shellfish and the symptoms in humans after consumption of toxic seafood. Biosynthesis of STXs is confirmed in four genera of marine dinoflagellate and among about a dozen species of primarily freshwater and brackish water strains of filamentous cyanobacteria. The origin of the STX biosynthetic genes in dinoflagellates remains controversial and may represent multiple horizontal gene transfer (HGT) events from progenitor bacteria and/or cyanobacteria. The recent identification of the biosynthetic genes for STX analogs in both cyanobacteria and dinoflagellates has yielded insights into mechanisms of toxin heterogeneity among species and the evolutionary origins of the respective elements of the toxin gene cluster. The biogenic origins of TTXs and tetrodotoxicity remain even more enigmatic. The TTXs occur primarily in marine pufferfish species, and hence tetrodotoxicity is frequently described as pufferfish poisoning (PFP) after the toxin syndrome in human consumers of such toxic fish. In marine environments, TTXs also appear in invertebrate species, particularly of benthic feeders on suspended particulates and carnivorous vector species. Symbiotic colonizing bacteria or free-living bacteria sequestered via feeding from the water column or sediments are most often invoked as proximal sources of TTXs in marine macrofauna, but endogenous biosynthesis independent of bacteria cannot be excluded. The TTX biosynthetic pathway has not been completely elucidated, and the biosynthetic genes are unknown.
Article
Full-text available
Marine mammal cell cultures are a multifunctional instrument for acquiring knowledge about life in the world’s oceans in physiological, biochemical, genetic, and ecotoxicological aspects. We succeeded in isolation, cultivation, and characterization of skin fibroblast cultures from five marine mammal species. The cells of the spotted seal (Phoca largha), the sea lion (Eumetopias jubatus), and the walrus (Odobenus rosmarus) are unpretentious to the isolation procedure. The sea otter (Enhydra lutris) fibroblasts should be isolated by trypsin disaggregation, while only mechanical disaggregation was suitable for the beluga whale (Delphinapterus leucas) cells. The cell growth parameters have been determined allowing us to find the optimal seeding density for continuous and effective cultivation. The effects of nonpathogenic algal extracts on proliferation, viability, and functional activity of marine mammal cells in vitro have been presented and discussed for the first time.
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
  • 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;