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Ecology of Invertebrate Diseases

ISBN: 978-1-119-25607-6
680 pages
January 2018
Ecology of Invertebrate Diseases (1119256070) cover image

Description

A rapidly growing interdisciplinary field, disease ecology merges key ideas from ecology, medicine, genetics, immunology, and epidemiology to study how hosts and pathogens interact in populations, communities, and entire ecosystems. Bringing together contributions from leading international experts on the ecology of diseases among invertebrate species, this book provides a comprehensive assessment of the current state of the field. Beginning with an introductory overview of general principles and methodologies, the book continues with in-depth discussions of a range of critical issues concerning invertebrate disease epidemiology, molecular biology, vectors, and pathogens. Topics covered in detail include:

  • Methods for studying the ecology of invertebrate diseases and pathogens
  • Invertebrate pathogen ecology and the ecology of pathogen groups
  • Applied ecology of invertebrate pathogens
  • Leveraging the ecology of invertebrate pathogens in microbial control
  • Prevention and management of infectious diseases of aquatic invertebrates                                             

Ecology of Invertebrate Diseases is a necessary and long overdue addition to the world literature on this vitally important subject. This volume belongs on the reference shelves of all those involved in the environmental sciences, genetics, microbiology, marine biology, immunology, epidemiology, fisheries and wildlife science, and related disciplines. 

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Table of Contents

List of Contributors xvii

Preface xxi

Section I Introduction 1

1 General Concepts in the Ecology of Invertebrate Diseases 3
Ann E. Hajek and David I. Shapiro-Ilan

1.1 Introduction 3

1.1.1 What Is Disease? 4

1.1.2 Terminology and Measurements 5

1.1.2.1 Prevalence/Incidence 5

1.1.2.2 Pathogenicity/Virulence 5

1.1.2.3 Infection/Infectivity 6

1.1.2.4 Immunity 6

1.1.2.5 Transmission 7

1.1.2.6 Epizootic and Enzootic Diseases 7

1.1.2.7 Cycles of Infection 8

1.1.2.8 R0 and the Host Density Threshold 10

1.1.3 Factors Influencing the Ecology of Invertebrate Diseases 11

1.1.3.1 Host Range 12

1.2 Types of Studies 13

1.3 Why Study the Ecology of Invertebrate Diseases? 13

1.4 What this Book Covers 14

Acknowledgments 16

References 16

2 Methods for Studying the Ecology of Invertebrate Diseases and Pathogens 19
Raquel Campos-Herrera and Lawrence A. Lacey

2.1 Introduction 19

2.2 Traditional Methods for Studying Diseases 19

2.2.1 Sampling Goals 19

2.2.2 Sampling Regimes 20

2.2.3 Methodologies 20

2.2.3.1 Searching for Infected Insects Using General Entomological Sampling Methods 23

2.2.3.2 Selective Media 23

2.2.3.3 Extraction Methods 24

2.2.3.4 Airborne Spore Sampling 24

2.2.3.5 Insect Baiting 24

2.2.3.6 Dispersal of Entomopathogens: Mark–Release–Recapture Method 25

2.3 Molecular Tools to Assist in the Detection and Quantification of Pathogens and their Impact on the Host 25

2.3.1 Employment of Proteins: The Beginning of the Molecular Era in Invertebrate Pathology 26

2.3.2 Techniques Based on the Nucleic Acids: the “Pre ]Omics” Era 27

2.3.3 Advanced Techniques: qPCR, NGS, and the Arrival of the ]Omics Era 31

2.4 Traditional Versus Molecular Methods: Advantages and Limitations 33

2.5 Advancing the Frontiers of Ecology using Pathogens and Diseases 36

2.6 Conclusion38

Acknowledgments 38

References 38

Section II The Basics of Invertebrate Pathogen Ecology 49

3 The Pathogen Population 51
Leellen F. Solter and James J. Becnel

3.1 Introduction 51

3.2 Characteristics of Pathogens 51

3.2.1 Invasiveness and Infectivity 52

3.2.1.1 Routes of Entry 53

3.2.1.2 Establishment of Infection and Tissue Tropism 54

3.2.2 Pathogenicity, Virulence, and Pathogen Replication 55

3.2.2.1 Virulence Factors 57

3.2.2.2 Attenuation or Enhancement of Virulence 58

3.2.3 Latency 59

3.2.4 Obligate, Opportunistic, and Facultative Pathogens 60

3.2.5 Transmission 61

3.2.5.1 Horizontal Transmission 61

3.2.5.2 Vertical Transmission 62

3.2.5.3 Indirect Transmission 63

3.2.6 Genetic Variability and Potential for Coevolution with Hosts 64

3.2.6.1 Species and Strains 64

3.2.6.2 Host Specificity 65

3.3 Pathogen Effects on Host Development and Behavior 66

3.4 Pathogen Populations 67

3.4.1 Density ]Dependent Pathogens 67

3.4.2 Density ]Independent Pathogens 68

3.4.3 Pathogen Persistence in the Host Population 68

3.4.3.1 Chronic Infections and Vertical Transmission 69

3.4.3.2 Alternative and Alternate/Intermediate Hosts 69

3.4.3.3 Pathogen Survival in Cadavers and in Plant Tissues 70

3.4.3.4 Latency in Host Populations 70

3.4.4 Persistence of Pathogen Stages in the Environment 71

3.5 Dispersal and Spatial Distribution of Pathogens 72

3.5.1 Physical Factors: Wind and Water Dispersal 73

3.5.2 Biological Factors 73

3.5.3 Spatial Distribution 74

3.6 Pathogen Interactions 75

3.6.1 Interactions with other Biological Agents 75

3.6.2 Interactions with Pesticides and other Chemicals 77

3.6.3 Enhancing Factors 77

3.7 Conclusion 78

References 79

4 The Host Population 101
Louela A. Castrillo

4.1 Introduction 101

4.2 General Host Factors 103

4.2.1 Routes of Pathogen Acquisition 103

4.2.2 Insect Species, Life Stage, Age, and Gender 103

4.2.3 Population Density 104

4.3 Barriers to Microbial Infection 105

4.3.1 Insect Integument 105

4.3.2 Tracheae 107

4.3.3 Insect Gut 108

4.3.3.1 Peritrophic Membrane and Basal Lamina 108

4.3.3.2 Conditions in the Gut Lumen 108

4.3.3.3 Sloughing of Infected Epidermal Cells 109

4.4 Defenses against Microbial Infection 110

4.4.1 Innate Immune System 110

4.4.1.1 Constitutive Innate Immunity: Cellular Immunity 110

4.4.1.2 Constitutive Innate Immunity: Phenoloxidase 113

4.4.1.3 Induced Innate Immunity: Reactive Oxygen Species 113

4.4.1.4 Induced Innate Immunity: Antimicrobial Peptides 114

4.4.2 Microbiome ]Based Defenses 117

4.4.2.1 Gut Microbiota 117

4.4.2.2 Intracellular Symbionts 118

4.4.3 Behavioral Defenses 119

4.4.3.1 Avoidance/Evasion 120

4.4.3.2 Grooming and Hygienic Behaviors 121

4.4.3.3 Diet ]Based Prophylactic and Therapeutic Defenses 122

4.4.3.4 Thermoregulation 123

4.4.3.5 Deposition of Antimicrobial Compounds 123

4.5 Resistance via Priming 124

4.6 Conclusion 125

Acknowledgments 126

References 126

5 Abiotic Factors 143
Dana Ment, Ikkei Shikano and Itamar Glazer

5.1 Introduction 143

5.2 The Surviving Unit 143

5.2.1 Nematodes 143

5.2.2 Fungi 144

5.2.3 Viruses 145

5.2.4 Bacteria 146

5.3 Abiotic Factors Affecting Invertebrate Pathogens 146

5.3.1 Temperature 146

5.3.1.1 Nematodes 147

5.3.1.2 Fungi 148

5.3.1.3 Viruses 150

5.3.1.4 Bacteria 152

5.3.2 Moisture and Humidity 152

5.3.2.1 Nematodes 153

5.3.2.2 Fungi 154

5.3.2.3 Viruses 155

5.3.2.4 Bacteria 156

5.3.3 Ultraviolet Radiation 156

5.3.3.1 Nematodes 157

5.3.3.2 Fungi 157

5.3.3.3 Viruses 158

5.3.3.4 Bacteria 158

5.3.4 Chemical Inputs 159

5.3.4.1 Nematodes 159

5.3.4.2 Fungi 160

5.3.4.3 Viruses 160

5.3.4.4 Bacteria 161

5.3.5 Other Habitat Characteristics 162

5.3.5.1 Nematodes 162

5.3.5.2 Fungi 163

5.3.5.3 Viruses 164

5.3.5.4 Bacteria 165

5.4 Mechanisms of Survival 165

5.4.1 Nematodes 165

5.4.2 Fungi 166

5.4.3 Viruses 166

5.4.4 Bacteria 167

5.5 Conclusion 167

References 169

6 The Biotic Environment 187
Jenny S. Cory and Pauline S. Deschodt

6.1 Introduction 187

6.2 Tritrophic Interactions 188

6.2.1 Further Complexity 190

6.3 Pathogen– Natural Enemy Interactions 191

6.3.1 Entomopathogen–Entomopathogen Interactions 191

6.3.2 Entomopathogen–Parasitoid Interactions 195

6.3.2.1 Effects of Pathogens on Parasitoids 195

6.3.2.2 Effects of Parasitoids on Pathogens 197

6.3.2.3 Population Level Effects 198

6.3.3 Pathogen–Predator Interactions 199

6.3.4 Conclusion 200

6.4 Microbe- Mediated Defense 200

6.4.1 Heritable Symbionts 201

6.4.2 Do Gut Microflora Influence Pathogen Susceptibility? 202

6.4.3 Future Directions 204

6.5 Conclusion 204

Acknowledgments 204

References 205

Section III Ecology of Pathogen Groups 213

7 Viruses 215
Trevor Williams

7.1 Introduction 215

7.2 Diversity of Invertebrate Pathogenic Viruses 216

7.3 Distribution of Invertebrate Pathogenic Viruses 219

7.4 Key Aspects of Pathogen Ecology 220

7.5 Transmission 221

7.5.1 Horizontal Transmission 221

7.5.1.1 Estimating Horizontal Transmission 223

7.5.2 Vertical Transmission 223

7.6 Persistence 225

7.6.1 Persistence within the Host 225

7.6.2 Persistence Outside of the Host 226

7.6.2.1 Persistence on Plants 227

7.6.2.2 Persistence in Soil 229

7.6.2.3 Persistence in Water 230

7.7 Dispersal 231

7.7.1 Host ]Mediated Dispersal 231

7.7.2 Environmental Factors Involved in Dispersal 232

7.7.3 Biotic Factors that Assist the Dispersal of Viruses 233

7.7.3.1 Predators 233

7.7.3.2 Parasitoids 234

7.7.3.3 Other Organisms 234

7.7.4 Agricultural Practices that Affect Dispersal 234

7.7.5 Spatial Patterns of Dispersal 235

7.8 Genetic Diversity in Viruses 235

7.8.1 Genetic Diversity is Pervasive in Virus Populations 235

7.8.2 Genetic Diversity Favors Virus Survival 237

7.8.3 What Generates So Much Genetic Diversity? 238

7.8.4 How Is Genetic Diversity Transmitted? 239

7.9 Role of Host Behavior in Virus Ecology 240

7.9.1 Foraging Decisions: What and Where to Eat 240

7.9.2 The Risks of Cannibalism 241

7.9.3 Sexually Transmitted Viral Diseases 241

7.9.4 Ecological Consequences of Host Manipulation by Viruses 242

7.9.4.1 Molecular Basis for Host Manipulation 243

7.10 Dynamics of Viruses in Host Populations 244

7.10.1 Pathogenic Viruses Can Regulate Populations 244

7.10.2 Ecosystem Characteristics that Favor Virus Transmission 246

7.10.3 Climate Change and Insect–Virus Population Dynamics 247

7.11 Influence of Abiotic Factors on Viruses 248

7.11.1 Effect of Ultraviolet Light on Viruses 248

7.11.2 Seasonal Effects on Viruses 250

7.11.3 Effect of Temperature on Viruses 250

7.11.4 Humidity, Moisture and Precipitation 251

7.11.5 Effect of pH on Viruses 251

7.12 Biotic Factors that Interact with Virus Populations 253

7.12.1 Plant Phenology, Structure, and Nutritional Value 253

7.12.2 Phytochemical–Virus Interactions 253

7.12.3 Virus Interactions with Alternative Hosts 254

7.12.4 Competition and Facilitation in Virus Interactions with Other Organisms 255

7.12.4.1 Virus Interactions with Parasitoids 255

7.12.4.2 Virus Interactions with Other Pathogens 257

7.12.4.3 Virus Interactions with Microbiota 258

7.13 Conclusion 258

Acknowledgments 259

References 259

8 Bacteria 287
Trevor A. Jackson, Colin Berry and Maureen O’Callaghan

8.1 Introduction 287

8.2 Bacterial Pathogens and Associations with Insects 288

8.3 Pathogenicity and Virulence 294

8.3.1 Pathogenicity 295

8.3.2 Virulence 299

8.4 Disease Transmission 300

8.5 Survival in the Environment 301

8.5.1 Soil 302

8.5.2 Aqueous Environments 304

8.5.3 On the Phylloplane and In Planta 304

8.6 Population Dynamics: Epizootics and Enzootics 305

8.7 Evolution 308

8.8 Ecology Guiding Use of Bacterial Entomopathogens in Microbial Control 309

8.9 Conclusion 311

References 312

9 Fungi 327
Ann E. Hajek and Nicolai V. Meyling

9.1 Introduction 327

9.1.1 Fungal Systematics and Taxonomy 328

9.1.2 Relevance of Fungal Systematics and Taxonomy in Ecology 330

9.2 Fungal Biology and Pathology 331

9.2.1 Biology and Pathology of Major Groups of Fungal Pathogens 331

9.2.1.1 Entomophthoromycotina, Entomophthorales 331

9.2.1.2 Ascomycota, Hypocreales 333

9.2.2 Distribution Patterns and Habitat Associations of Invertebrate Pathogenic Fungi 334

9.2.2.1 Patterns of Fungal Abundance and Distribution: Insights from the Use of Molecular Markers 335

9.2.3 Factors Governing Diversity Patterns of Fungal Pathogens 337

9.3 Dynamics of Fungal Pathogens 338

9.3.1 Disease Transmission 338

9.3.2 Fungal Dispersal 341

9.3.3 Fungal Environmental Survival and Persistence 341

9.3.4 Impacts on Host Population Densities over Space and Time 342

9.4 Interactions between Fungal Pathogens and Host Individuals 344

9.4.1 Host Responses to Fungal Pathogens to Prevent or Cure Infections 344

9.5 Impact of Abiotic Factors on Infected Hosts and Pathogen Inocula 347

9.6 Impact of Biotic Factors on Pathogenic Fungi 349

9.6.1 Endophytic and Rhizosphere Associations of Invertebrate Fungal Pathogens 349

9.6.1.1 Natural Occurrence and Distribution of Invertebrate Pathogenic Fungi as Plant Associates 350

9.6.1.2 Experimental Inoculations of Plants with Entomopathogenic Fungi 351

9.6.1.3 Direct and Indirect Fungal Interactions with Insects and Plants 352

9.6.2 Interactions between Host Symbionts and Fungal Pathogens 353

9.6.3 Interactions between Fungal Pathogens and Other Natural Enemies 354

9.6.3.1 Interactions among Co ]infecting Pathogens 355

9.6.3.2 Interactions of Fungal Pathogens with Parasitoids and Predators 356

9.6.4 Mycoparasitism of Fungal Pathogens 357

9.7 Use of Pathogenic Fungi for Biological Control of Invertebrates 358

9.8 Conclusion 361

Acknowledgments 361

References 362

10 Microsporidia 379
Gernot Hoch and Leellen F. Solter

10.1 Introduction 379

10.1.1 Mechanisms of Infection 380

10.1.2 Microsporidian Life Cycles 381

10.1.3 Pathology 381

10.2 Host Population 383

10.2.1 Susceptibility to Microsporidiosis 383

10.2.2 Immune Response 383

10.2.3 Behavioral Response 384

10.3 Pathogen Population 385

10.3.1 Virulence of Microsporidian Pathogens 385

10.3.2 Host Specificity 386

10.3.2.1 Physiological vs. Ecological Host Specificity 386

10.3.2.2 Host Range 386

10.3.2.3 Alternate Hosts 387

10.3.2.4 Microsporidia Crossing the Invertebrate–Vertebrate Barrier 387

10.3.3 Persistence in the Environment 388

10.4 Transmission 390

10.4.1 Horizontal Transmission 390

10.4.1.1 Transmission from Living Hosts 390

10.4.1.2 Transmission after Host Death 392

10.4.1.3 Transmission by Parasitoid Vectors 393

10.4.1.4 Effects of Host Development and Host–Microsporidia Interactions on Transmission 393

10.4.2 Vertical Transmission 394

10.5 Epizootiology 397

10.5.1 Microsporidian Prevalence in Invertebrate Populations and Impact on Host Populations 397

10.5.2 Microsporidia in Cultured Insects 398

10.5.3 Microsporidia as Potential Biological Control Agents 399

References 400

11 Nematodes 415
David I. Shapiro-Ilan, Ivan Hiltpold and Edwin E. Lewis

11.1 Introduction 415

11.1.1 Diversity and Life Histories 415

11.1.2 EPN Distribution 420

11.2 Transmission 421

11.3 Host Population 421

11.4 Pathogen Population 422

11.4.1 Pathogenicity and Virulence 422

11.4.2 Persistence and Recycling 423

11.4.3 Dispersal and Foraging Behavior 423

11.5 Abiotic Environmental Factors 424

11.5.1 Soil Moisture 424

11.5.2 Soil Temperature 425

11.5.3 Soil Characteristics and Chemistry 425

11.5.4 Ultraviolet Light 426

11.6 Biotic Interactions 426

11.6.1 Interactions with Predators and Pathogens, Including Intraguild Competition 426

11.6.2 Cues Used in Host ]Finding and Navigation 427

11.6.3 Tri ]trophic Interactions (Plant, Insect, Nematode) 427

11.7 Applied Ecology and Aspects in Microbial Control 427

11.7.1 Production, Formulation, and Application 427

11.7.2 Approaches to Microbial Control 428

11.8 Conclusion 430

References 431

Section IV Applied Ecology of Invertebrate Pathogens 441

12 Modeling Insect Epizootics and their Population-Level Consequences 443
Bret D. Elderd

12.1 Introduction 443

12.2 The Pathogen and its Hosts 445

12.3 Modeling Disease Transmission: A Single Epizootic 447

12.3.1 Phenomenological and Mechanistic Models 448

12.4 Fitting Models to Data 450

12.4.1 Akaike Information Criterion 451

12.4.2 An Example of the AIC in Action 452

12.5 A Bayesian Approach 453

12.5.1 Fitting a Bayesian Model 454

12.5.2 An Example of the WAIC in Action 456

12.6 Long-Term Dynamics 457

12.6.1 Long ]Term Dynamics: Confronting Models with Data 458

12.6.2 Time ]Series Diagnostics 459

12.7 Modifying and Applying the Model 462

12.8 Conclusion 463

Acknowledgments 463

References 463

13 Leveraging the Ecology of Invertebrate Pathogens in Microbial Control 469
Surendra K. Dara, Tarryn A. Goble and David I. Shapiro-Ilan

13.1 Basics of Microbial Control and Approaches 469

13.1.1 Classical Microbial Control 469

13.1.2 Inoculative Release 471

13.1.3 Inundative Release 472

13.1.4 Conservation/Environmental Manipulation 472

13.2 Ecological Considerations 472

13.2.1 Host Specificity 472

13.2.2 Dispersal Ability 473

13.2.3 Virulence 473

13.2.4 Pathogen Density 473

13.2.5 Host ]Related Factors 474

13.2.6 Transmission 474

13.2.7 Environmental Persistence 475

13.3 Methods to Improve Microbial Control 476

13.3.1 Improving the Organism as a Microbial Control Agent 476

13.3.2 Improving Production Methods 477

13.3.3 Improving Formulation and Application Technologies 478

13.3.4 Improving the Environment 479

13.4 Incorporating Microbial Control into Integrated Pest-Management Systems 480

13.4.1 Regulatory Issues 480

13.4.2 Standalone vs. Integrated Approaches 481

13.4.3 Case Studies 481

13.4.3.1 Orchard Crops 482

13.4.3.2 Row Crops 482

13.4.3.3 Forests 483

13.4.3.4 Greenhouses 483

13.5 Conclusion 484

References 484

14 Prevention and Management of Diseases in Terrestrial Invertebrates 495
Jørgen Eilenberg and Annette Bruun Jensen

14.1 Introduction 495

14.1.1 Types of Production Facilities 496

14.1.2 Transmission of Insect Diseases in Production Facilities 499

14.2 Major uses of Insects and Mites in the Production and Transmission of Insect Pathogens within Production Systems 500

14.2.1 Pollination and Honey Production 500

14.2.2 Silk Production 507

14.2.3 Biological Control 509

14.2.4 Production of Insects for Food and Feed 512

14.3 Status of Diagnostic Services 516

14.4 Ensuring Production of Healthy Insects 516

14.5 Conclusion 519

Acknowledgments 519

References 519

15 Prevention and Management of Infectious Diseases in Aquatic Invertebrates 527
Jeffrey D. Shields

15.1 Scope 527

15.1.1 Myriad Pathogens Infect Aquatic Invertebrates 527

15.1.2 Overview of Disease Issues in Assessing Epidemics in Aquatic Invertebrates 531

15.2 Oyster Diseases 539

15.3 Crustacean Diseases 543

15.3.1 Outbreaks in Shrimp Aquaculture 544

15.3.2 Disease Management in Shrimp Aquaculture 548

15.3.2.1 Switching Species and Specific Pathogen ]Free (SPF) Stocks 549

15.3.2.2 Surveillance 550

15.3.2.3 Development of “Vaccines” 551

15.3.2.4 Ecological and Biological Control 551

15.3.3 Crayfish and Krebspest 552

15.3.4 Disease Emergence in Culture of the Chinese Mitten Crab 553

15.4 Crustacean Fisheries 554

15.4.1 Snow Crabs and Bitter Crab Disease 555

15.4.2 American Lobster and Epizootic Shell Disease 556

15.4.3 Spiny Lobsters and PaV1 559

15.5 Agencies for Disease Management 560

15.6 Conclusion 563

Acknowledgments 563

References 563

16 Ecology of Emerging Infectious Diseases of Invertebrates 587
Colleen A. Burge, Amanda Shore-Maggio and Natalie D. Rivlin

16.1 Introduction 587

16.2 Host–Pathogen Relationships and Anthropogenic Change 593

16.2.1 Ecological Context of Invertebrate Host–Pathogen Relationships 593

16.2.2 Anthropogenic Change and Disease Emergence 594

16.2.2.1 Host Factors 595

16.2.2.2 Pathogen Factors 595

16.2.2.3 Environment Factors 595

16.3 Case Studies of Invertebrate Disease Emergence 596

16.3.1 Molluscan Herpesvirus Infections of Bivalves 597

16.3.1.1 OsHV ]1 Infections of Pacific Oysters and Other Bivalves 598

16.3.2 Acute Hepatopancreatic Necrosis Disease of Shrimp 601

16.3.3 Emerging Densoviruses of Arthropods and Echinoderms 603

16.3.3.1 Acheta domesticus Densovirus 603

16.3.3.2 Sea Star ]Associated Densovirus 604

16.3.4 Emerging Pathogens of Pollinators 605

16.3.4.1 Varroa destructor and Deformed Wing Virus 606

16.3.4.2 Spillover and spread of Nosema ceranae 607

16.3.4.3 Multi ]stressors, Bee Mortalities and Control Measures 608

16.3.5 Emergent Coral Diseases 608

16.3.5.1 Black Band Disease 609

16.3.5.2 Acroporid Serratosis 610

16.3.5.3 Problems Facing Coral Disease Investigations 610

16.4 Conclusion 611

Acknowledgments 612

References 612

17 Conclusions and Future Directions 627
David Shapiro-Ilan and Ann E. Hajek

17.1 The Increasing Urgency of the Study of Invertebrate Pathogen Ecology 627

17.1.1 Food Security and the Role of Microbial Control 627

17.1.2 Conservation of Beneficial Organisms 628

17.2 The Future for Invasive and Native Invertebrate Pathogens 629

17.3 New Directions and Novel Tools for Studying Invertebrate Ecology 630

17.3.1 Molecular Tools 630

17.3.2 Chemical Ecology and Signaling 631

17.3.3 Exploring Other Novel Biotic Associations 632

17.3.4 Interdisciplinary Studies 633

References 634

Index 637

 

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Author Information

ANN E. HAJEK, PHD, is a Professor in the Department of Entomology, Cornell University, Ithaca, New York, US.

DAVID I. SHAPIRO-ILAN, PHD, is a Research Entomologist at USDA-ARS, Byron, Georgia, US.

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