Ecology of Invertebrate Diseases

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.

• List of Contributors xviiPreface xxiSection I Introduction 11 General Concepts in the Ecology of Invertebrate Diseases 3Ann E. Hajek and David I. Shapiro-Ilan1.1 Introduction 31.1.1 What Is Disease? 41.1.2 Terminology and Measurements 51.1.2.1 Prevalence/Incidence 51.1.2.2 Pathogenicity/Virulence 51.1.2.3 Infection/Infectivity 61.1.2.4 Immunity 61.1.2.5 Transmission 71.1.2.6 Epizootic and Enzootic Diseases 71.1.2.7 Cycles of Infection 81.1.2.8 R0 and the Host Density Threshold 101.1.3 Factors Influencing the Ecology of Invertebrate Diseases 111.1.3.1 Host Range 121.2 Types of Studies 131.3 Why Study the Ecology of Invertebrate Diseases? 131.4 What this Book Covers 14Acknowledgments 16References 162 Methods for Studying the Ecology of Invertebrate Diseases and Pathogens 19Raquel Campos-Herrera and Lawrence A. Lacey2.1 Introduction 192.2 Traditional Methods for Studying Diseases 192.2.1 Sampling Goals 192.2.2 Sampling Regimes 202.2.3 Methodologies 202.2.3.1 Searching for Infected Insects Using General Entomological Sampling Methods 232.2.3.2 Selective Media 232.2.3.3 Extraction Methods 242.2.3.4 Airborne Spore Sampling 242.2.3.5 Insect Baiting 242.2.3.6 Dispersal of Entomopathogens: Mark–Release–Recapture Method 252.3 Molecular Tools to Assist in the Detection and Quantification of Pathogens and their Impact on the Host 252.3.1 Employment of Proteins: The Beginning of the Molecular Era in Invertebrate Pathology 262.3.2 Techniques Based on the Nucleic Acids: the “Pre]Omics” Era 272.3.3 Advanced Techniques: qPCR, NGS, and the Arrival of the ]Omics Era 312.4 Traditional Versus Molecular Methods: Advantages and Limitations 332.5 Advancing the Frontiers of Ecology using Pathogens and Diseases 362.6 Conclusion38Acknowledgments 38References 38Section II The Basics of Invertebrate Pathogen Ecology 493 The Pathogen Population 51Leellen F. Solter and James J. Becnel3.1 Introduction 513.2 Characteristics of Pathogens 513.2.1 Invasiveness and Infectivity 523.2.1.1 Routes of Entry 533.2.1.2 Establishment of Infection and Tissue Tropism 543.2.2 Pathogenicity, Virulence, and Pathogen Replication 553.2.2.1 Virulence Factors 573.2.2.2 Attenuation or Enhancement of Virulence 583.2.3 Latency 593.2.4 Obligate, Opportunistic, and Facultative Pathogens 603.2.5 Transmission 613.2.5.1 Horizontal Transmission 613.2.5.2 Vertical Transmission 623.2.5.3 Indirect Transmission 633.2.6 Genetic Variability and Potential for Coevolution with Hosts 643.2.6.1 Species and Strains 643.2.6.2 Host Specificity 653.3 Pathogen Effects on Host Development and Behavior 663.4 Pathogen Populations 673.4.1 Density]Dependent Pathogens 673.4.2 Density]Independent Pathogens 683.4.3 Pathogen Persistence in the Host Population 683.4.3.1 Chronic Infections and Vertical Transmission 693.4.3.2 Alternative and Alternate/Intermediate Hosts 693.4.3.3 Pathogen Survival in Cadavers and in Plant Tissues 703.4.3.4 Latency in Host Populations 703.4.4 Persistence of Pathogen Stages in the Environment 713.5 Dispersal and Spatial Distribution of Pathogens 723.5.1 Physical Factors: Wind and Water Dispersal 733.5.2 Biological Factors 733.5.3 Spatial Distribution 743.6 Pathogen Interactions 753.6.1 Interactions with other Biological Agents 753.6.2 Interactions with Pesticides and other Chemicals 773.6.3 Enhancing Factors 773.7 Conclusion 78References 794 The Host Population 101Louela A. Castrillo4.1 Introduction 1014.2 General Host Factors 1034.2.1 Routes of Pathogen Acquisition 1034.2.2 Insect Species, Life Stage, Age, and Gender 1034.2.3 Population Density 1044.3 Barriers to Microbial Infection 1054.3.1 Insect Integument 1054.3.2 Tracheae 1074.3.3 Insect Gut 1084.3.3.1 Peritrophic Membrane and Basal Lamina 1084.3.3.2 Conditions in the Gut Lumen 1084.3.3.3 Sloughing of Infected Epidermal Cells 1094.4 Defenses against Microbial Infection 1104.4.1 Innate Immune System 1104.4.1.1 Constitutive Innate Immunity: Cellular Immunity 1104.4.1.2 Constitutive Innate Immunity: Phenoloxidase 1134.4.1.3 Induced Innate Immunity: Reactive Oxygen Species 1134.4.1.4 Induced Innate Immunity: Antimicrobial Peptides 1144.4.2 Microbiome]Based Defenses 1174.4.2.1 Gut Microbiota 1174.4.2.2 Intracellular Symbionts 1184.4.3 Behavioral Defenses 1194.4.3.1 Avoidance/Evasion 1204.4.3.2 Grooming and Hygienic Behaviors 1214.4.3.3 Diet]Based Prophylactic and Therapeutic Defenses 1224.4.3.4 Thermoregulation 1234.4.3.5 Deposition of Antimicrobial Compounds 1234.5 Resistance via Priming 1244.6 Conclusion 125Acknowledgments 126References 1265 Abiotic Factors 143Dana Ment, Ikkei Shikano and Itamar Glazer5.1 Introduction 1435.2 The Surviving Unit 1435.2.1 Nematodes 1435.2.2 Fungi 1445.2.3 Viruses 1455.2.4 Bacteria 1465.3 Abiotic Factors Affecting Invertebrate Pathogens 1465.3.1 Temperature 1465.3.1.1 Nematodes 1475.3.1.2 Fungi 1485.3.1.3 Viruses 1505.3.1.4 Bacteria 1525.3.2 Moisture and Humidity 1525.3.2.1 Nematodes 1535.3.2.2 Fungi 1545.3.2.3 Viruses 1555.3.2.4 Bacteria 1565.3.3 Ultraviolet Radiation 1565.3.3.1 Nematodes 1575.3.3.2 Fungi 1575.3.3.3 Viruses 1585.3.3.4 Bacteria 1585.3.4 Chemical Inputs 1595.3.4.1 Nematodes 1595.3.4.2 Fungi 1605.3.4.3 Viruses 1605.3.4.4 Bacteria 1615.3.5 Other Habitat Characteristics 1625.3.5.1 Nematodes 1625.3.5.2 Fungi 1635.3.5.3 Viruses 1645.3.5.4 Bacteria 1655.4 Mechanisms of Survival 1655.4.1 Nematodes 1655.4.2 Fungi 1665.4.3 Viruses 1665.4.4 Bacteria 1675.5 Conclusion 167References 1696 The Biotic Environment 187Jenny S. Cory and Pauline S. Deschodt6.1 Introduction 1876.2 Tritrophic Interactions 1886.2.1 Further Complexity 1906.3 Pathogen– Natural Enemy Interactions 1916.3.1 Entomopathogen–Entomopathogen Interactions 1916.3.2 Entomopathogen–Parasitoid Interactions 1956.3.2.1 Effects of Pathogens on Parasitoids 1956.3.2.2 Effects of Parasitoids on Pathogens 1976.3.2.3 Population Level Effects 1986.3.3 Pathogen–Predator Interactions 1996.3.4 Conclusion 2006.4 Microbe- Mediated Defense 2006.4.1 Heritable Symbionts 2016.4.2 Do Gut Microflora Influence Pathogen Susceptibility? 2026.4.3 Future Directions 2046.5 Conclusion 204Acknowledgments 204References 205Section III Ecology of Pathogen Groups 2137 Viruses 215Trevor Williams7.1 Introduction 2157.2 Diversity of Invertebrate Pathogenic Viruses 2167.3 Distribution of Invertebrate Pathogenic Viruses 2197.4 Key Aspects of Pathogen Ecology 2207.5 Transmission 2217.5.1 Horizontal Transmission 2217.5.1.1 Estimating Horizontal Transmission 2237.5.2 Vertical Transmission 2237.6 Persistence 2257.6.1 Persistence within the Host 2257.6.2 Persistence Outside of the Host 2267.6.2.1 Persistence on Plants 2277.6.2.2 Persistence in Soil 2297.6.2.3 Persistence in Water 2307.7 Dispersal 2317.7.1 Host]Mediated Dispersal 2317.7.2 Environmental Factors Involved in Dispersal 2327.7.3 Biotic Factors that Assist the Dispersal of Viruses 2337.7.3.1 Predators 2337.7.3.2 Parasitoids 2347.7.3.3 Other Organisms 2347.7.4 Agricultural Practices that Affect Dispersal 2347.7.5 Spatial Patterns of Dispersal 2357.8 Genetic Diversity in Viruses 2357.8.1 Genetic Diversity is Pervasive in Virus Populations 2357.8.2 Genetic Diversity Favors Virus Survival 2377.8.3 What Generates So Much Genetic Diversity? 2387.8.4 How Is Genetic Diversity Transmitted? 2397.9 Role of Host Behavior in Virus Ecology 2407.9.1 Foraging Decisions: What and Where to Eat 2407.9.2 The Risks of Cannibalism 2417.9.3 Sexually Transmitted Viral Diseases 2417.9.4 Ecological Consequences of Host Manipulation by Viruses 2427.9.4.1 Molecular Basis for Host Manipulation 2437.10 Dynamics of Viruses in Host Populations 2447.10.1 Pathogenic Viruses Can Regulate Populations 2447.10.2 Ecosystem Characteristics that Favor Virus Transmission 2467.10.3 Climate Change and Insect–Virus Population Dynamics 2477.11 Influence of Abiotic Factors on Viruses 2487.11.1 Effect of Ultraviolet Light on Viruses 2487.11.2 Seasonal Effects on Viruses 2507.11.3 Effect of Temperature on Viruses 2507.11.4 Humidity, Moisture and Precipitation 2517.11.5 Effect of pH on Viruses 2517.12 Biotic Factors that Interact with Virus Populations 2537.12.1 Plant Phenology, Structure, and Nutritional Value 2537.12.2 Phytochemical–Virus Interactions 2537.12.3 Virus Interactions with Alternative Hosts 2547.12.4 Competition and Facilitation in Virus Interactions with Other Organisms 2557.12.4.1 Virus Interactions with Parasitoids 2557.12.4.2 Virus Interactions with Other Pathogens 2577.12.4.3 Virus Interactions with Microbiota 2587.13 Conclusion 258Acknowledgments 259References 2598 Bacteria 287Trevor A. Jackson, Colin Berry and Maureen O’Callaghan8.1 Introduction 2878.2 Bacterial Pathogens and Associations with Insects 2888.3 Pathogenicity and Virulence 2948.3.1 Pathogenicity 2958.3.2 Virulence 2998.4 Disease Transmission 3008.5 Survival in the Environment 3018.5.1 Soil 3028.5.2 Aqueous Environments 3048.5.3 On the Phylloplane and In Planta 3048.6 Population Dynamics: Epizootics and Enzootics 3058.7 Evolution 3088.8 Ecology Guiding Use of Bacterial Entomopathogens in Microbial Control 3098.9 Conclusion 311References 3129 Fungi 327Ann E. Hajek and Nicolai V. Meyling9.1 Introduction 3279.1.1 Fungal Systematics and Taxonomy 3289.1.2 Relevance of Fungal Systematics and Taxonomy in Ecology 3309.2 Fungal Biology and Pathology 3319.2.1 Biology and Pathology of Major Groups of Fungal Pathogens 3319.2.1.1 Entomophthoromycotina, Entomophthorales 3319.2.1.2 Ascomycota, Hypocreales 3339.2.2 Distribution Patterns and Habitat Associations of Invertebrate Pathogenic Fungi 3349.2.2.1 Patterns of Fungal Abundance and Distribution: Insights from the Use of Molecular Markers 3359.2.3 Factors Governing Diversity Patterns of Fungal Pathogens 3379.3 Dynamics of Fungal Pathogens 3389.3.1 Disease Transmission 3389.3.2 Fungal Dispersal 3419.3.3 Fungal Environmental Survival and Persistence 3419.3.4 Impacts on Host Population Densities over Space and Time 3429.4 Interactions between Fungal Pathogens and Host Individuals 3449.4.1 Host Responses to Fungal Pathogens to Prevent or Cure Infections 3449.5 Impact of Abiotic Factors on Infected Hosts and Pathogen Inocula 3479.6 Impact of Biotic Factors on Pathogenic Fungi 3499.6.1 Endophytic and Rhizosphere Associations of Invertebrate Fungal Pathogens 3499.6.1.1 Natural Occurrence and Distribution of Invertebrate Pathogenic Fungi as Plant Associates 3509.6.1.2 Experimental Inoculations of Plants with Entomopathogenic Fungi 3519.6.1.3 Direct and Indirect Fungal Interactions with Insects and Plants 3529.6.2 Interactions between Host Symbionts and Fungal Pathogens 3539.6.3 Interactions between Fungal Pathogens and Other Natural Enemies 3549.6.3.1 Interactions among Co]infecting Pathogens 3559.6.3.2 Interactions of Fungal Pathogens with Parasitoids and Predators 3569.6.4 Mycoparasitism of Fungal Pathogens 3579.7 Use of Pathogenic Fungi for Biological Control of Invertebrates 3589.8 Conclusion 361Acknowledgments 361References 36210 Microsporidia 379Gernot Hoch and Leellen F. Solter10.1 Introduction 37910.1.1 Mechanisms of Infection 38010.1.2 Microsporidian Life Cycles 38110.1.3 Pathology 38110.2 Host Population 38310.2.1 Susceptibility to Microsporidiosis 38310.2.2 Immune Response 38310.2.3 Behavioral Response 38410.3 Pathogen Population 38510.3.1 Virulence of Microsporidian Pathogens 38510.3.2 Host Specificity 38610.3.2.1 Physiological vs. Ecological Host Specificity 38610.3.2.2 Host Range 38610.3.2.3 Alternate Hosts 38710.3.2.4 Microsporidia Crossing the Invertebrate–Vertebrate Barrier 38710.3.3 Persistence in the Environment 38810.4 Transmission 39010.4.1 Horizontal Transmission 39010.4.1.1 Transmission from Living Hosts 39010.4.1.2 Transmission after Host Death 39210.4.1.3 Transmission by Parasitoid Vectors 39310.4.1.4 Effects of Host Development and Host–Microsporidia Interactions on Transmission 39310.4.2 Vertical Transmission 39410.5 Epizootiology 39710.5.1 Microsporidian Prevalence in Invertebrate Populations and Impact on Host Populations 39710.5.2 Microsporidia in Cultured Insects 39810.5.3 Microsporidia as Potential Biological Control Agents 399References 40011 Nematodes 415David I. Shapiro-Ilan, Ivan Hiltpold and Edwin E. Lewis11.1 Introduction 41511.1.1 Diversity and Life Histories 41511.1.2 EPN Distribution 42011.2 Transmission 42111.3 Host Population 42111.4 Pathogen Population 42211.4.1 Pathogenicity and Virulence 42211.4.2 Persistence and Recycling 42311.4.3 Dispersal and Foraging Behavior 42311.5 Abiotic Environmental Factors 42411.5.1 Soil Moisture 42411.5.2 Soil Temperature 42511.5.3 Soil Characteristics and Chemistry 42511.5.4 Ultraviolet Light 42611.6 Biotic Interactions 42611.6.1 Interactions with Predators and Pathogens, Including Intraguild Competition 42611.6.2 Cues Used in Host]Finding and Navigation 42711.6.3 Tri]trophic Interactions (Plant, Insect, Nematode) 42711.7 Applied Ecology and Aspects in Microbial Control 42711.7.1 Production, Formulation, and Application 42711.7.2 Approaches to Microbial Control 42811.8 Conclusion 430References 431Section IV Applied Ecology of Invertebrate Pathogens 44112 Modeling Insect Epizootics and their Population-Level Consequences 443Bret D. Elderd12.1 Introduction 44312.2 The Pathogen and its Hosts 44512.3 Modeling Disease Transmission: A Single Epizootic 44712.3.1 Phenomenological and Mechanistic Models 44812.4 Fitting Models to Data 45012.4.1 Akaike Information Criterion 45112.4.2 An Example of the AIC in Action 45212.5 A Bayesian Approach 45312.5.1 Fitting a Bayesian Model 45412.5.2 An Example of the WAIC in Action 45612.6 Long-Term Dynamics 45712.6.1 Long]Term Dynamics: Confronting Models with Data 45812.6.2 Time]Series Diagnostics 45912.7 Modifying and Applying the Model 46212.8 Conclusion 463Acknowledgments 463References 46313 Leveraging the Ecology of Invertebrate Pathogens in Microbial Control 469Surendra K. Dara, Tarryn A. Goble and David I. Shapiro-Ilan13.1 Basics of Microbial Control and Approaches 46913.1.1 Classical Microbial Control 46913.1.2 Inoculative Release 47113.1.3 Inundative Release 47213.1.4 Conservation/Environmental Manipulation 47213.2 Ecological Considerations 47213.2.1 Host Specificity 47213.2.2 Dispersal Ability 47313.2.3 Virulence 47313.2.4 Pathogen Density 47313.2.5 Host]Related Factors 47413.2.6 Transmission 47413.2.7 Environmental Persistence 47513.3 Methods to Improve Microbial Control 47613.3.1 Improving the Organism as a Microbial Control Agent 47613.3.2 Improving Production Methods 47713.3.3 Improving Formulation and Application Technologies 47813.3.4 Improving the Environment 47913.4 Incorporating Microbial Control into Integrated Pest-Management Systems 48013.4.1 Regulatory Issues 48013.4.2 Standalone vs. Integrated Approaches 48113.4.3 Case Studies 48113.4.3.1 Orchard Crops 48213.4.3.2 Row Crops 48213.4.3.3 Forests 48313.4.3.4 Greenhouses 48313.5 Conclusion 484References 48414 Prevention and Management of Diseases in Terrestrial Invertebrates 495Jørgen Eilenberg and Annette Bruun Jensen14.1 Introduction 49514.1.1 Types of Production Facilities 49614.1.2 Transmission of Insect Diseases in Production Facilities 49914.2 Major uses of Insects and Mites in the Production and Transmission of Insect Pathogens within Production Systems 50014.2.1 Pollination and Honey Production 50014.2.2 Silk Production 50714.2.3 Biological Control 50914.2.4 Production of Insects for Food and Feed 51214.3 Status of Diagnostic Services 51614.4 Ensuring Production of Healthy Insects 51614.5 Conclusion 519Acknowledgments 519References 51915 Prevention and Management of Infectious Diseases in Aquatic Invertebrates 527Jeffrey D. Shields15.1 Scope 52715.1.1 Myriad Pathogens Infect Aquatic Invertebrates 52715.1.2 Overview of Disease Issues in Assessing Epidemics in Aquatic Invertebrates 53115.2 Oyster Diseases 53915.3 Crustacean Diseases 54315.3.1 Outbreaks in Shrimp Aquaculture 54415.3.2 Disease Management in Shrimp Aquaculture 54815.3.2.1 Switching Species and Specific Pathogen]Free (SPF) Stocks 54915.3.2.2 Surveillance 55015.3.2.3 Development of “Vaccines” 55115.3.2.4 Ecological and Biological Control 55115.3.3 Crayfish and Krebspest 55215.3.4 Disease Emergence in Culture of the Chinese Mitten Crab 55315.4 Crustacean Fisheries 55415.4.1 Snow Crabs and Bitter Crab Disease 55515.4.2 American Lobster and Epizootic Shell Disease 55615.4.3 Spiny Lobsters and PaV1 55915.5 Agencies for Disease Management 56015.6 Conclusion 563Acknowledgments 563References 56316 Ecology of Emerging Infectious Diseases of Invertebrates 587Colleen A. Burge, Amanda Shore-Maggio and Natalie D. Rivlin16.1 Introduction 58716.2 Host–Pathogen Relationships and Anthropogenic Change 59316.2.1 Ecological Context of Invertebrate Host–Pathogen Relationships 59316.2.2 Anthropogenic Change and Disease Emergence 59416.2.2.1 Host Factors 59516.2.2.2 Pathogen Factors 59516.2.2.3 Environment Factors 59516.3 Case Studies of Invertebrate Disease Emergence 59616.3.1 Molluscan Herpesvirus Infections of Bivalves 59716.3.1.1 OsHV]1 Infections of Pacific Oysters and Other Bivalves 59816.3.2 Acute Hepatopancreatic Necrosis Disease of Shrimp 60116.3.3 Emerging Densoviruses of Arthropods and Echinoderms 60316.3.3.1 Acheta domesticus Densovirus 60316.3.3.2 Sea Star]Associated Densovirus 60416.3.4 Emerging Pathogens of Pollinators 60516.3.4.1 Varroa destructor and Deformed Wing Virus 60616.3.4.2 Spillover and spread of Nosema ceranae 60716.3.4.3 Multi]stressors, Bee Mortalities and Control Measures 60816.3.5 Emergent Coral Diseases 60816.3.5.1 Black Band Disease 60916.3.5.2 Acroporid Serratosis 61016.3.5.3 Problems Facing Coral Disease Investigations 61016.4 Conclusion 611Acknowledgments 612References 61217 Conclusions and Future Directions 627David Shapiro-Ilan and Ann E. Hajek17.1 The Increasing Urgency of the Study of Invertebrate Pathogen Ecology 62717.1.1 Food Security and the Role of Microbial Control 62717.1.2 Conservation of Beneficial Organisms 62817.2 The Future for Invasive and Native Invertebrate Pathogens 62917.3 New Directions and Novel Tools for Studying Invertebrate Ecology 63017.3.1 Molecular Tools 63017.3.2 Chemical Ecology and Signaling 63117.3.3 Exploring Other Novel Biotic Associations 63217.3.4 Interdisciplinary Studies 633References 634Index 637