Preface

xiii

Foreword

xv

Contributors

xvii

1

Scope and Basic Principles of Insect Pathology   Harry K. Kaya and Fernando E. Vega

1

1.1

Introduction

1

1.2

Categories of Disease

3

1.3

Basic Principles in Insect Pathology

3

1.3.1

Entomopathogens

4

1.3.2

Some Major Classification and Taxonomic Changes

4

1.3.3

Portal of Entry

5

1.3.4

Microbia! Toxins

5

1.3.5

Infectivity

7

1.3.6

Pathogenicity and Virulence

7

1.3.7

Dosage

8

1.3.8

Signs, Symptoms, and Syndromes

8

1.3.9

Course of Infection

8

1.3.10

Acute, Chronic, and Latent Infections

9

1.3.11

Koch’s Postulates

10

1.3.12

Diagnosis

11

References

11

2

History of Insect Pathology   Elizabeth W. Davidson

13

2.1

Introduction

13

2.2

Early History of the Discovery of Insect Pathogens

13

2.2.1

Honey Bees

13

2.2.2

Silkworms

17

2.3

Early Discoveries of Other Pathogens

17

2.3.1

Viruses

17

2.3.2

Bacteria

18

2.3.3

Fungi

18

2.3.4

Microsporidia

19

2.3.5

Nematodes

19

2.4

Development of Insect Pathogens for Biological Control

19

2.4.1

Viruses

19

2.4.2

Bacteria

20

Bacillus (Paenibacillus) popilliae

20

Bacillus thuringiensis

20

Bacillus sphaericus

21

2.4.3

Fungi

21

2.4.4

Microsporidia

21

2.4.5

Nematodes

22

2.5

Events that Brought Scientists Together and Advanced the Field

22

2.6

Unexpected Products of Research on Insect Pathogens

22

2.7

Conclusions

23

References

23

3

Principles of Epizootiology and Microbial Control   David I. Shapiro-llan, Denny J. Bruck, and Lawrence A. Lacey

29

3.1

Introduction

29

3.2

Epizootiology: Basic Principles

30

3.2.1

The Pathogen Population

31

Pathogen Density

31

Dispersal

32

Infectivity and Latency

32

Virulence

32

Strain Effects and Genetics

33

3.2.2

The Host Population

34

Genetic Resistance

34

Behavioral Resistance

35

Host Associations

35

3.2.3

Transmission

36

Methods of Transmission

36

Modes of Dissemination

38

3.2.4

The Environment

38

Aerial and Aquatic Environments

39

Edaphic Environment

39

Interactions among Trophic Levels

40

3.2.5

Modeling Epizootics

41

General Concepts in Epizootiological Modeling

41

Examples of Epizootiological Models

42

3.3

Microbial Control (Applied Epizootiology)

43

3.3.1

Basic Concepts in Microbial Control

43

3.3.2

Factors Affecting Efficacy in Microbial Control

44

3.3.3

Improving Efficacy in Microbiai Control

46

Improving the Entomopathogen

46

Improving Production and Application Methods

48

Improving the Environment

50

3.3.4

Approaches to Microbial Control

50

Case Studies: Classical Biological Control

51

Case Studies: Inoculation

52

Case Studies: Inundation

53

Case Studies: Conservation

55

3.4

Future Research Directions

55

References

56

4

Baculoviruses and Other Occluded Insect Viruses   Robert Harrison and Kelli Hoover

73

4.1

Introduction

74

4.2

Classification and Phylogerty

75

4.2.1

General Characteristics

75

Morphology: Virions, Occlusion Bodies, and Genomes

75

Genetic Definition of a Baculovirus: The Core Genes

79

4.2.2

Organization of Baculoviridae

79

Current Classification Scheme: Four Genera

79

Phylogeny and Evolution

81

4.2.3

Other Occluded Viruses and Nudiviruses

81

Entomopoxviruses

81

Cypoviruses

84

Nudiviruses

84

4.3

Baculovirus Infection, Replication, Pathology, and Transmission

85

4.3.1

Primary Infection

85

Solubilization of Occlusions

85

Penetration of the Peritrophic Matrix and Midgut Cell Entry

86

Transport and Entry into the Nucleus

87

4.3.2

Replication and Virion Assembly

87

Viral DNA Uncoating

87

Temporally Regulated Virai Gene Expression

87

Virogenic Stroma and Peristromal Region Formation, and DNA Replication

89

Virion Assembly and Budded Virion Egress

91

4.3.3

Secondary Infection

92

Route of Infection; Penetration of Basement Membranes

92

Tissue Tropism

93

Cell Entry

93

Occlusion-Derived Virion Occlusion and Morphogenesis

93

4.3.4

Host Response and Pathology

95

Developmental Resistance Between and Within Instars

95

Apoptosis

95

Immune Responses

96

Behavioral and Developmental Effects

97

Cytopathology, Tissue Liquefaction, and Cuticular Weakening

98

4.3.5

Ecology

98

Transmission

98

Host Resistance and Specificity

99

Genetic Variation

100

Multitrophic Interactions

101

4.4

Use of Baculoviruses for Insect Pest Control

102

4.4.1

Factors Involved in Controlling Pests with Baculoviruses

102

Host Range

102

Survival Time

102

Mass Production

103

Formulation

103

4.4.2

Case Studies from the Field

104

Helicoverpa zea/Helicoverpa armigera SNPVs

104

Lymantria dispar MNPV

105

Anticarsia gemmatalis MNPV

106

Neodiprion spp. NPVs

106

Cydia pomonella GV

107

4.4.3

Recombinant Baculoviruses

107

4.5

Future Research Directions

109

Acknowledgments

110

References

110

5

RNA Viruses Infecting Pest Insects   Van Ping Chen, James J. Becnel, and Steven M. Valles

133

5.1

Introduction

133

5.2

Classification, Phylogeny, Structure, and Genome Organization

135

5.2.1

Alphanodaviruses

136

5.2.2

Dicistroviruses

136

5.2.3

Flaviviruses

141

5.2.4

Iflaviruses

141

5.2.5

Tetraviruses

142

5.2.6

Cypoviruses

142

5.3

Infection, Replication, Pathology, Transmission, and Host Range

144

5.3.1

Alphanodaviruses

144

5.3.2

Dicistroviruses

145

5.3.3

Flaviviruses

150

5.3.4

Iflaviruses

151

5.3.5

Tetraviruses

154

5.3.6

Cypoviruses

156

5.4

Future Research Directions

159

References

160

6

Fungal Entomopathogens   Fernando E. Vega, Nicolai V. Meyling, Janet Jennifer Luangsa-ard, and Meredith Blackwell

171

6.1

Introduction

172

6.2

Classification and Phylogeny

172

6.2.1

Classification of Fungi and Fungus-like Organisms

172

6.2.2

An Overview of Fungal Entomopathogens in a Phylogenetic Context

174

Stramenopiles (Oomycetes)

174

Phylum Microsporidia

175

Zoosporic Fungi

175

Zygosporic Fungi

175

Phylum Ascomycota

176

Phylum Basidiomycota

180

6.3

Biology

181

6.3.1

Reproduction

182

6.3.2

Types of Infective Propagules and Cell Wall Surface Properties

182

6.3.3

The Infection Process

184

Attachment to the Cuticle

184

Spore Germination

185

Cuticle Penetration

186

Insect Responses to Infection

186

6.3.4

Secondary Metabolites

187

6.3.5

Environmental Factors Influencing Stability

188

Ultraviolet Light

188

Temperature

189

Humidity

189

6.4

Ecology

189

6.4.1

Host Range of Fungal Entomopathogens

190

Narrow and Broad Host Ranges: Specialist and Generalist Entomopathogens

190

Cryptic Species and the Use of Molecular Methods for Ecological Studies

191

Host Range Beyond Insects

192

6.4.2

Distribution and Abundance of Fungal Entomopathogens

192

Distribution Patterns of Generaiist Fungal Entomopathogens

193

Linking Below- and Above-ground Distribution of Fungal E ntomopath oge ns

195

Are Fungal Entomopathogens Only Associated with Arthropods? 196 Distribution of Specialist Fungal Entomopathogens

196

6.4.3

Trophic Interactions Involving Fungal Entomopathogens

198

Community Modules Including Arthropod—Fungus Interactions: Tritrophic Context

198

Effects of Interactions Among Plants and Fungal Entomopathogens

199

Fungal Entomopathogens as Part of Natural Enemy Communities

201

6.5

Use of Fungal Entomopathogens as Biological Control Agents

202

6.5.1

Pathogenicity, Virulence, and Bioassays

202

6.5.2

Production, Formulation, and Application

203

6.5.3

Some Important Case Studies

204

Gypsy Moth in the USA

204

Locusts and Grasshoppers

205

Spittlebugs in Brazil

205

6.5.4

Commercial Products

205

6.5.5

Genetic Modification of Fungal Entomopathogens

205

6.6

Future Research Directions

206

Acknowledgments

206

References

206

7

Microsporidran Entomopathogens   Leellen F Softer, James J. Becnel, and David H. Oi

221

7.1

Introduction

221

7.2

Classification and Phylogeny

222

7.2.1

Overview of Microsporidian Entomopathogens in a Phylogenetic Context

223

Amblyospora/Parathelohania Clade

223

Nosema/Vairlmorpha Clade

225

7.2.2

Genera! Characteristics of Microsporidia

226

Morphology

226

Genetic Characters

227

7.3

Life History

229

7.3.1

Infection and Replication

229

7.3.2

Pathology

229

7.3.3

Transmission

230

7.3.4

Environmental Persistence

231

7.3.5

Life Cycles

231

Life Cycles of Microsporidia in the NosemaA/airimorpha Clade

231

Life Cycle of Vavraia cut ids

233

Life Cycle of Edhazardia aedis

233

7.3.6

Epizootiology and Host

Population Effects

234

7.3.7

Host Specificity

234

7.4

Biological Control Programs: Case Histories

235

7.4.1

Use of Microsporidia in Biological Control Programs

235

7.4.2

Aquatic Diptera

236

Edhazardia aedis

237

Amblyospora connecticus

238

Life-cycle Based Management Strategies

238

7.4.3

Lepidopteran Pests in Row Crop Systems

239

7.4.4

Grasshoppers and Paranosema locustae

240

7.4.5

Fire Ants in Urban Landscapes

242

Kneallhazia solenopsae

242

Vairimorpha invictae

245

7.4.6

Control of Forest Insect Pests

246

Impacts of Naturally Occurring Microsporidia on Forest Pests

247

Spruce Budworm Microsporidia

247

Microsporidian Pathogens of Gypsy Moth

249

7.4.7

Microsporidia Infecting Biological Control Agents

250

7.5

Future Research Directions

251

References

252

8

Bacterial Entomopathogens   Juan Luis Jurat-Fuentes and Trevor A, Jackson

265

8.1

Introduction

266

8.2

Classification and Phylogeny

267

8.2.1

General Characteristics

268

8.2.2

Classification of Bacterial Entomopathogens

268

8.3

Infection, Replication, Pathology, and Transmission

269

8.3.1

Portals of Entry

269

8.3.2

Pathologies, Symptoms, and Factors Influencing Host Susceptibility

271

8.3.3

Host Response to Infection

272

8.4

Gram-Positive Entomopathogens: Phylum Firmicutes, Class Bacilli, Order Bacillales

272

8.4.1

Family Bacillaceae, Genus Bacillus

272

Bacillus cereus (sensu stricto)

274

Bacillus thuringiensis: Characteristics and Classification

275

Bacillus thuringiensis Ecology, Biology, and Infection

278

General Characteristics of Bacillus thuringiensis Crystal Toxins

281

Regulation of Cry Gene Expression

282

Structure and Classification of Crystal Toxins

283

Crystal Toxin Structure—Function

287

Midgut Proteins Interacting with Crystal Toxins and Toxin Receptors

288

Crystal Intoxication Process

289

Cytolytic Toxins: Description, Regulation, and Classification

293

Structure—Function Relationship in Cytolytic Toxins

294

Non-Crystal Toxins: Vegetative Insecticidal Proteins

295

Exotoxins

295

Other Bacillus thuringiensis Virulence Factors

296

Host Range

297

Improvement of Bacillus thuringiensis Activity

298

Formulation, Delivery Systems, and Enhancers

298

Safety of Bacillus thuringiensis Pesticides and Crops

300

8.4.2

Family Bacillaceae, Genus Lysinibacillus

301

Binary Toxin

302

Crystal Toxins of Bacillus sphaericus

303

Mosquitocidal Toxins

304

Other Toxins in Bacillus sphaericus

304

Formulation, Improvement, and Safety

304

8.4.3

Family Paenibacillaceae

305

Genus Paenibacillus

305

Genus Brevibacillus

307

8.4.4

Other Entomopathogenic Bacteria in the Order Bacillales

307

8.5

Gram-Negative Bacteria

308

8.5.1

General Introduction to the Group

308

8.5.2

Family Enterobacteriaceae

309

Serratia spp

309

Serratia Virulence Factors: Sep and Tc Toxins

309

Host Range and Ecology

311

Yersinia spp

311

8.5.3

Family Pseudomonadaceae: Pseudomonas spp

312

8.5.4

Family Coxiellaceae: Rickettsiella spp

312

8.5.5

New Pathologies from Other Genera313

8.5.6

Safety and Registration of Non-spore-forming Bacteria

313

8.6

Other Potentially Pathogenic Bacteria: Infection by Mollicutes

314

8.7

Field use: Examples, Success, and Constraints

314

8.8

Future Research Directions

316

References

317

9

Wolbachia Infections in Arthropod Hosts   Grant L Hughes and Jason L Rasgon

351

9.1

Introduction

351

9.2

Classification and Phylogeny

351

9.3

Pathogen Versus Mutualist

352

9.4

Historical Overview of Wolbachia and Vector Control

352

9.5

Reproductive Manipulations

353

9.5.1

Cytoplasmic Incompatibility

353

Case Study: Drosophila

354

Case Studies: Aedes and Culex

354

9.5.2

Sex Ratio Distorters

356

Male Killing

356

Feminization

357

9.5.3

Parthenogenesis

357

9.6

Pathogen Interference and

Pathogen Protection

358

9.7

Applied Use of Wolbachia

359

9.8

Future Research Directions

360

References

360

10

Protistan Entomopathogens   Carlos E. Lange and Jeffrey C. Lord

367

10.1

Introduction

367

10.2

Classification and Phylogeny

368

10.3

Associations, Signs, and Symptoms

368

10.4

Amoebozoa

368

10.5

Apicomplexa

372

10.5.1

Eugregarinorida

372

10.5.2

Neogregarinorida

376

10.5.3

Coccidia

379

10.6

Ciliophora

381

10.7

Euglenozoa

384

10.8

Helicosporidia

385

10.9

Future Research Directions

387

References

387

11

Nematode Parasites and Entomopathogens   Edwin E. Lewis and David J. Clarke

395

11.1

Introduction

395

11.2

Classification and Phylogeny

396

11.2.1

Insect-parasitic Nematodes

396

11.2.2

Entomopathogenic Nematodes and Symbiotic Bacteria

396

11.3

Insect-Parasitic Nematodes

398

11.3.1

Facultative Parasite: Beddingia siricidicola

398

11.3.2

Monoxenous Obligate Parasites: No Symbionts

399

Romanomermis culicivorax: Obligate, Lethal Parasite

399

Paraiotonchium autumnale: Obligate, Non-lethal Parasite

400

11.4

Entomopathogenic Nematodes: Monoxenous, Lethal Parasites with Symbionts

400

11.4.1

Life Cycle

401

11.4.2

History

402

11.4.3

Symbiotic Relationship

402

11.4.4

Sampling

402

11.5

Biodiversity

402

11.5.1

Entomopathogenic Nematodes

402

11.5.2

Symbiotic Bacteria

403

11.6

Infective Stage Juvenile and Bacteria Storage

403

11.7

Infection

404

11.7.1

Infective Stage Juvenile Host Finding, Recognition, and Penetration

404

11.7.2

Release of Bacteria

407

11.7.3

Overcoming the Insect Immune System

408

Nematode Contribution

408

Bacterial Contribution

408

11.8

Nutrition Within the Insect

409

11.9

Natural Populations and Host Associations

410

11.9.1

Natural Host Affiliations

410

11.9.2

Population Structure in Nature

412

11.10

Aging and Lifespan

413

11.11

Survival Mechanisms

415

11.11.1

Desiccation

415

11.11.2

Osmotic Stress

416

11.11.3

Temperature Extremes

416

11.12

Future Research Directions

417

References

417

12

From Silkworms to Bees: Diseases of Beneficial Insects   Rosalind R. James and Zengzhi Li

425

12.1

Introduction

425

12.2

Diseases of Silkworms

426

12.2.1

Viruses

427

12.2.2

Bacteria

431

12.2.3

Fungi: Filamentous

432

12.2.4

Fungi: Microsporidia

433

12.2.5

Protists

435

12.2.6

Non-infectious Biotic Agents

435

12.2.7

Abiotic Agents

436

12.2.8

Disease Control Methods for Sericulture

437

12.3

Diseases of Bees

438

12.3.1

Viruses

439

12.3.2

Bacteria

439

12.3.3

Fungi: Filamentous

444

12.3.4

Fungi: Microsporidia

446

12.3.5

Protists

446

12.3.6

Non-infectious Biotic Agents

447

12.3.7

Abiotic Agents

448

12.3.8

Colony Collapse Disorder

448

12.3.9

Disease Control Methods for Managed Bees

449

12.4

Future Research Directions

453

References

454

13

Physiology and Ecology of Host Defense Against Microbial invaders   Jonathan G. Lundgren and Juan Luis Jurat-Fuentes

461

13.1

Introduction

461

13.2

Behavioral and Physical Barriers to Infection

462

13.2.1

Behavioral Avoidance of Pathogens

462

Avoidance Behavior

462

Antiseptic Behavior

463

13.2.2

Morphological Barriers lo Infections

463

Cuticle

464

Digestive and Tracheal Systems

464

13.3

Physiological Response to Infections

465

13.3.1

Distinguishing Self from Non-self from Altered Self

465

13.3.2

Humoral Response System

466

Antimicrobial Peptides

466

Regulation of Humoral Defenses

467

13.3.3

Cellular Response System

467

Hemocytes

467

Phagocytosis

468

Nodulation and Encapsulation

468

13.3.4

Melanization

469

13.3.5

Intracellular Defenses

469

Involvement of the Extracellular Immune Systems Against Intracellular Pathogens

469

RNA Interference

470

Xenophagy

470

Resistance Against Intracellular Host Defenses

470

13.4

Managing Resistance to Entomopathogens

470

13.4.1

Resistance Mechanisms to Bacillus tnuringiensis

471

13.4.2

Managing Resistance to Bacillus thuringiensis

472

Delaying the Evolution of Resistance and Slowing its Spread

473

Fitness Costs Associated with Resistance

473

13.5