Microbial Control of Insect and Mite Pests: From Theory to Practice

Microbial Control of Insect and Mite Pests

From Theory to Practice

Editor

Lawrence A. Lacey

IP Consulting International, Yakima, WA, United States

Table of Contents

Cover image

Title page

Copyright

Dedication

List of Contributors

Preface

Part I. Introduction to Insect Pathology and Microbial Control: The Tried and True and Recent Innovations

Chapter 1. Entomopathogens Used as Microbial Control Agents

1.1. Introduction to Entomopathogens Used in the Microbial Control of Insect and Mite Pests

1.2. Entomopathogens Used as MCAs

1.3. Microbial Control Agents and Biological Control

1.4. Advantages and Disadvantages of Microbial Control

Chapter 2. Exploration for Entomopathogens

2.1. Introduction

2.2. General Search for Entomopathogens

2.3. Foreign Exploration for Entomopathogens of Exotic Invertebrate Pests

2.4. Case Studies of Successful Introductions of Nonindigenous Entomopathogens for Control of Insect and Mite Pests and Parasitic Nematodes for Mosquito Control

2.5. Conclusions and Recommendations

Part II. Basic and Applied Research

Chapter 3. Basic and Applied Research: Baculovirus

3.1. Introduction to Entomopathogenic Viruses

3.2. Baculoviridae

3.3. Host Range

3.4. Ecology of Baculoviruses and Microbial Control

3.5. Environmental Factors Affecting Baculovirus Efficacy and Persistence

3.6. Baculovirus Use on Crops and Case Studies of Baculovirus Products

3.7. Overview of Baculovirus Product Development and Commercialization

3.8. Overview of Future Development and Needs

Chapter 4. Basic and Applied Research: Entomopathogenic Bacteria

4.1. Introduction

4.2. Concise History and Key Species Description

4.3. Mode of Action

4.4. Natural Ecology

4.5. Host Susceptibility Range and Efficacy

4.6. Practical Applications and Commercialization

4.7. Environmental and Mammalian Safety

4.8. Registration

4.9. Future

Chapter 5. Basic and Applied Research on Entomopathogenic Fungi

5.1. Introduction

5.2. Entomopathogenic Fungi: Evolutionary Relationships

5.3. Biology of the Two Main Groups of Entomopathogenic Fungi Used as Biological Control Agents of Arthropod Pests: The Hypocreales and the Entomophthoromycota

5.4. Entomopathogenic Fungi: Ecology and Host–Pathogen Interactions

5.5. Entomopathogenic Fungi Life Cycles

5.6. Use of Entomopathogenic Fungi for Arthropod Pest Management

5.7. Future Opportunities and Challenges

Chapter 6. Basic and Applied Research: Entomopathogenic Nematodes

6.1. Introduction and Basic Biology

6.2. Factors Affecting Survival and Efficacy

6.3. Application and Formulation Technology

6.4. Commercialization and Targets

6.5. Methods to Improve Efficacy

6.6. Conclusion: Future Developments and Needs

Part III. Mass Production, Formulationand Quality Control

Chapter 7. Production, Formulation, and Bioassay of Baculoviruses for Pest Control

7.1. Introduction

7.2. Baculovirus Production in Cell Culture

7.3. Baculovirus Production In Vivo

7.4. Quality Control

7.5. Formulation

7.6. Field Production of Baculoviruses

7.7. Overview of Future Developments and Needs

Chapter 8. Entomopathogenic Bacteria: Mass Production, Formulation, and Quality Control

8.1. Introduction

8.2. Mass Production of Bacteria as the Active Ingredients of Biopesticides

8.3. Harvesting

8.4. Formulation of Bacteria for Storage and Application

8.5. Quality Control

8.6. Conclusions and Future Needs

Chapter 9. Mass Production of Fungal Entomopathogens

9.1. Introduction

9.2. Selecting Fungi and Fungal Propagule Development

9.3. Important General Production Parameters

9.4. Solid-State and Biphasic Fermentation

9.5. Liquid Fermentation

9.6. Quality Control

9.7. Formulation of Mycoinsecticides

9.8. Summary

Chapter 10. Production of Entomopathogenic Nematodes

10.1. Introduction

10.2. Biology of Entomopathogenic Nematodes

10.3. Production Methods

10.4. Formulation

10.5. Quality Assurance and Assessment

10.6. Conclusions

Part IV. Applied Research and Implementation of Microbial Control Agents for Pest Control

Chapter 11. Current and Potential Applications of Biopesticides to Manage Insect Pests of Maize

11.1. Introduction

11.2. Fungi

11.3. Entomopathogenic Nematodes

11.4. Baculoviruses

11.5. Bacteria

11.6. Bacillus thuringiensis Maize

11.7. Combining Tactics

11.8. Future Prospects

Chapter 12. Microbial Control of Insect and Mite Pests of Cotton

12.1. Introduction

12.2. Microbial Biopesticides for Use in the Cotton Crop for Resistance Management

12.3. Biopesticides for Use in Non–Bt Refuge Cotton and Alternate Host Plants for Resistance Management

12.4. Potential of EPFs as Root Colonizers and Endophytes – Reduced Rates Required and Alternate Modes of Action

12.5. Conservation Biological Control: Influencing Natural Epizootics

12.6. Other Cotton Pests

12.7. Conclusions

Chapter 13. Microbial Control of Soybean Pest Insects and Mites

13.1. Introduction

13.2. Entomopathogenic Fungi

13.3. Entomopathogenic Baculoviruses

13.4. Entomopathogenic Bacteria

13.5. Genetic Modifications to Enhance Soybean Pest Control

13.6. Conclusions

Chapter 14. Microbial Control of Arthropod Pests in Small Fruits and Vegetables in Temperate Climate

14.1. Introduction

14.2. Microbial Control in Vegetables in Temperate Climate

14.3. Microbial Control in Small Fruits

14.4. Conclusions

Chapter 15. Microbial Control of Insect Pests of Tea and Coffee

15.1. Introduction

15.2. Insect Pests of Tea and Their Microbial Control

15.3. Insect and Mite Pests of Coffee and Their Microbial Control

15.4. Conclusions and Future Development

Chapter 16. Microbial Control of Mite and Insect Pests of Greenhouse Crops

16.1. General Introduction

16.2. Major Groups of Greenhouse Arthropod Pests

16.3. Microbial Biocontrol Agents and Their Use in Greenhouse Pest Management

16.4. Future of Microbial Biological Control of Greenhouse Arthropod Pests

Chapter 17. Microbial Control of Arthropod Pests of Orchards in Temperate Climates

17.1. Introduction

17.2. Pome Fruit

17.3. Stone Fruit

17.4. Nut Crops

17.5. Conclusions and Recommendations

Chapter 18. Entomopathogens Routinely Used in Pest Control Strategies: Orchards in Tropical Climate

18.1. Introduction

18.2. Nut Crops

18.3. Tree Fruits

18.4. Banana

18.5. Papaya

18.6. Other Fruits

18.7. Challenges and Future Prospects

Chapter 19. Microbial Control of Insect and Mite Pests of Citrus

19.1. Introduction

19.2. Microbial Control of Citrus Pests With Entomopathogenic Fungi

19.3. Microbial Control of Citrus Pests Using Entomopathogenic Nematodes

19.4. Baculoviruses for Microbial Control of Lepidoptera in Citrus

19.5. Bacteria for Microbial Control of Citrus Pests

19.6. Perspectives on the Future

Chapter 20. Microbial Control of Sugarcane Insect Pests

20.1. Introduction

20.2. Lepidopteran Stalk Boring Pests

20.3. Hemipteran Sap-Sucking Pests and Their Microbial Control with Entomopathogenic Fungi

20.4. Root-Feeding Pests and Their Microbial Control

20.5. Microbial Control of Other Soil Pests

20.6. Conclusions

Chapter 21. Use of Entomopathogens Against Forest Pests

21.1. Introduction

21.2. Control of Forest Insects Through Classical Biological Control

21.3. Suppression of Forest Insects Through Inoculative Augmentation

21.4. Suppression of Defoliators Through Inundative Release of Pathogens

21.5. Eradication of Invasive Forest Insects With Entomopathogens

21.6. The Future of Microbial Control in Forestry

Chapter 22. Microbial Control of Insect Pests of Turfgrass

22.1. The Turfgrass System

22.2. Important Turfgrass Insect Pests

22.3. Microbial Control Agents of Turfgrass Insect Pests

22.4. Conclusions and Recommendations

Chapter 23. LUBILOSA: The Development of an Acridid-Specific Mycoinsecticide

23.1. History of the LUBILOSA Program

23.2. Developmental Research

23.3. Effects of Humidity and Formulation on Efficacy

23.4. Reasons for Success

23.5. Barriers to Overcome

23.6. Spin-Off/Commercialization

Chapter 24. Microbial Control of Nursery Ornamental and Landscape Plant Pests

24.1. Introduction

24.2. Phytophagous Mites

24.3. Wood Borers

24.4. Root Feeders

24.5. Defoliators

24.6. Sap Feeders

24.7. Conclusions

Chapter 25. Microbial Control of Black Flies (Diptera: Simuliidae) With Bacillus thuringiensis subsp. israelensis

25.1. Introduction

25.2. Pest Status

25.3. Black Fly Biology

25.4. Discovery of Bacillus thuringiensis Subsp. israelensis and Its Development as a Microbial Control Agent of Black Flies

25.5. Prescription Site Applications of Bti-Based Larvicides

25.6. Black Fly Suppression Programs—Overview

25.7. Effects of Bti on Nontarget Aquatic Invertebrates

25.8. Conclusions and Future Directions

Chapter 26. Mosquito Control With Entomopathogenic Bacteria in Europe

26.1. Introduction

26.2. Strategic Considerations of Mosquito Control Programs in Europe

26.3. Control of Mosquitoes With Bacteria

26.4. Suitability of Microbial Control Agent-Integrated Mosquito Control Programs With Community Participation

26.5. Operational Use of Microbial Control Agents

Chapter 27. Microbial Control of Pest and Vector Mosquitoes in North America North of Mexico

27.1. Introduction

27.2. Developmental Research for Use of Bacillus thuringiensis Subsp. israelensis for Control of Mosquito Larvae

27.3. Developmental Research for Use of Lysinibacillus sphaericus for Control of Mosquito Larvae

27.4. Combination of Bacillus thuringiensis Subsp. israelensis and Lysinibacillus sphaericus

27.5. Integrated Mosquito Control

27.6. Future Perspectives

Chapter 28. Microbial Control of Medically Important Mosquitoes in Tropical Climates

28.1. Introduction

28.2. Nematoda: Mermithidae

28.3. Metarhizium anisopliae s.l. and Beauveria bassiana (Fungi: Ascomycota: Hypocreales)

28.4. Bacteria: Bacillales

28.5. Role of Microbial Control Agents in Integrated Vector Management Strategies for the Suppression of Mosquito-Borne Disease

28.6. Conclusions

Chapter 29. Microbial Control of Structural Insect Pests

29.1. Introduction to the Economic Problem Caused by Structural Insect Pests

29.2. Microbial Control of Structural Insect Pests

29.3. Conclusions and Recommendations for Future Development of Microbial Control Agents of Structural Insect Pests

Part V. Registration of MicrobialControl Products: A Comparative Overview

Chapter 30. Registration of Microbial Control Agents (A Comparative Overview)

30.1. Introduction

30.2. Registration Principles: Data Requirements and Processes

30.3. Global Registration and Harmonization Activities for Microorganisms

30.4. Registration Systems Within Individual Countries or Regions

Index

Copyright

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Dedication

This book is dedicated to two of our finest insect pathologists, Sérgio Alves and Flávio Moscardi. Their accomplishments in microbial control and as mentors in insect pathology are detailed here by their friends and colleagues, Roberto Pereira and Pedro Neves.

Lawrence A. Lacey

Sérgio Alves (1944–2008)

If Sérgio was not the Father of Insect Pathology in Brazil, he was certainly a father figure in that he nurtured the science in its humble beginnings in Brazil, being involved in every aspect of insect pathology and microbial control, raising a new generation of insect pathologists, and making sure the science found an application in agriculture and other areas in need of insect control. Sérgio’s was the first university laboratory dedicated to insect pathology and microbial control in Brazil, and he always insisted on dedicating a great portion of his efforts to the development of production systems, formulation, and application of microbial insecticides. His legacy is clearly seen in the number of products and the extensive use of microbial insecticides in Brazil and other countries in Latin America.

Sérgio’s initial studies focused on the use of the fungus Metarhizium anisopliae against spittlebugs in pasture and sugarcane and contributed to the great expansion of microbial control of pests in Brazil and elsewhere in Latin America. His influence expanded to North America through collaboration with researchers at the University of Florida working on control of fire ants by using the fungus Beauveria bassiana. Sérgio’s international reach included collaboration with many other international researchers and assistance in establishing microbial control laboratories and commercial microbial product factories in several countries.

His contributions include more than 180 publications, two books, 40 book chapters, the discovery of numerous insect pathogens, and scientific collaborations all over the globe. The book (S. B. Alves, (ed.) Controle Microbiano de Insetos FEALQ, Piracicaba, Brazil), now in its second edition, has served as the basis for training and development for scientists and practitioners of microbial control of insects. His scientific contribution is further exemplified by his latest book: Controle Micobiano de Pragas na América Latina: avanços e desafios (Alves and Lopes, 2008). Dr. Alves received several awards during his career including the Edilson B. Oliveira Award, the highest honor awarded by the Brazil Entomological Society. As a champion for microbial control of insects, the practical use of insect pathology in solving pest problems, during his career, Sérgio was the face, and heart, of Insect Pathology in Brazil and other countries in Latin America.

Roberto M. Pereira, PhD

University of Florida, Gainesville, FL, United States

Flávio Moscardi (1949–2012)

Flávio was born in Osvaldo Cruz, São Paulo, Brazil. He was one of the principal scientists in charge of the establishment of the biological control program against the soybean caterpillar, using the AgMNPV baculovirus, a technology that was widely implemented and used in Brazil and other Latin America countries. The virus was applied to more than 2  million  ha per year in Brazil, reducing the amount of chemical pesticides used by approximately 25  million liters, and became one of the largest biological control programs worldwide and probably the largest using an entomopathogenic virus.

Moscardi graduated as an agronomic engineer from the Escola Superior deAgricultura Luiz de Queiroz (ESALQ-USP) and obtained his master’s and PhD degrees at the University of Florida, United States. He dedicated 35  years of research with microbial control, mainly with virus in soybean for Embrapa. During his career, he authored more than 200 publications, including scientific articles published in several well-known Brazilian and international journals, book chapters, and technical notes. Moscardi was also the adviser of 23 graduate students, many who continue to work with entomopathogens and microbial control.

A member of the Brazilian Academy of Sciences, he received many awards such as the Commendation of the National Order of Scientific Merit granted by the Brazilian president in August 2002, Agriculture by the Third World Academy of Sciences in 1997, and Distinction by the International Society of Plant Protection in 1995 and the Frederico de Menezes Veiga granted by Embrapa in 1991 and was honored by the Founders’ lecture of the Society for Invertebrate Pathology (SIP) meeting in 2012 as presented by Daniel Sosa-Gomez. Moscardi was a regular attender at SIP meetings and had many friends and collaborators in the Society.

He was a member of the Advisory Board of Agriculture from CNPq, president of the Entomological Society of Brazil from 1998 to 2002, and president of the X CBE (Brazilian Congress of Entomology, 1984), V Siconbiol (Biological Control Symposium in 1996), VII Colloquium of Invertebrate Pathology and Microbial Control (Foz do Iguaçu-PR, 2002), and the Scientific Committee of the XXI International Congress of Entomology (2000). Besides being a great scientist, Moscardi’s other great passion was fishing, where he graduated many fishermen by sharing his knowledge and organizing fishing expeditions.

Prof. Pedro Neves

Universidade Estadual de Londrina, Londrina PR, Brasil

List of Contributors

J. Almeida,     Instituto Biológico, Laboratório de Controle Biológico, Campinas, Brazil

S.P. Arthurs,     University of Florida, Apopka, FL, United States

M.V. Baggio,     UNESP, Jaboticabal, São Paulo, Brazil

R. Bateman,     Imperial College, Ascot, United Kingdom

N. Becker

German Mosquito Control Association (KABS), Speyer, Germany

University of Heidelberg, Heidelberg, Germany

D.J. Bruck,     DuPont Pioneer, Johnston, IA, United States

D. Chandler,     University of Warwick, Wellesbourne, Warwick, United Kingdom

E.H. Clifton,     Iowa State University, Ames, IA, United States

D. Conlong

South African Sugarcane Research Institute, Mount Edgecombe, South Africa

University of KwaZulu-Natal, Pietermaritzburg, South Africa

S.K. Dara,     University of California Cooperative Extension, San Luis Obispo, CA, United States

C. Dolinski,     Universidade Estadual do Norte Fluminense/CCTA/LEF, Rio de Janeiro, Brazil

L.W. Duncan,     University of Florida, Lake Alfred, FL, United States

S. Ekesi,     International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya

M. Faria,     EMBRAPA Genetic Resources and Biotechnology, Brasilia, Federal District, Brazil

R. Fusco,     Valent BioSciences Corporation (Retired), Mifflintown, PA, United States

A.J. Gassmann,     Iowa State University, Ames, IA, United States

T.R. Glare,     Lincoln University, Christchurch, New Zealand

I. Glazer,     ARO, Volcani Center, Israel

T. Goble,     Cornell University, Ithaca, NY, United States

J. Gore,     Mississippi State University, Stoneville, MS, United States

E.W. Gray,     University of Georgia, Athens, GA, United States

D. Grzywacz,     University of Greenwich, Chatham, Kent, United Kingdom

R. Gwynn,     Biorationale Limited, Duns, United Kingdom

A.E. Hajek,     Cornell University, Ithaca, NY, United States

R. Han,     Guangdong Entomological Institute, Guangzhou, Guangdong, China

S. Hazir,     Adnan Menderes University, Aydin, Turkey

T.A. Jackson,     AgResearch, Lincoln Research Center, Christchurch, New Zealand

S.T. Jaronski,     United States Department of Agriculture, Sidney, MT, United States

N. Jenkins,     Pennsylvania State University, University Park, PA, United States

J.-L. Jurat-Fuentes,     University of Tennessee, Knoxville, TN, United States

P.G. Koehler,     University of Florida, Gainesville, FL, United States

C. Kooyman,     Éléphant Vert, Nanyuki, Kenya

A.M. Koppenhöfer,     Rutgers University, New Brunswick, NJ, United States

L.A. Lacey,     IP Consulting International, Yakima, WA, United States

L.G. Leite,     Instituto Biológico, São Paulo, Brazil

J. Leland,     Novozymes BioAg, Salem, VA, United States

R.B. Lopes,     EMBRAPA Genetic Resources and Biotechnology, Brasilia, Federal District, Brazil

P. Lüthy,     Swiss Federal Institute of Technology, ETH Zürich, Zürich, Switzerland

N.K. Maniania,     International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya

G.M. Mascarin,     Embrapa Rice and Beans, Santo Antônio de Goiás, Brazil

D. Moore,     Commonwealth Agricultural Bureaux International Europe – UK, Surrey, United Kingdom

S. Moore

Citrus Research International, Port Elizabeth, South Africa

Rhodes University, Grahamstown, South Africa

S.D. Moore

Citrus Research International, Port Elizabeth, South Africa

Rhodes University, Grahamstown, South Africa

M. Nakai,     Tokyo University of Agriculture and Technology, Tokyo, Japan

M. O’Callaghan

Lincoln University, Christchurch, New Zealand

AgResearch, Christchurch, New Zealand

D.H. Oi,     USDA-ARS, Gainesville, FL, United States

R.M. Pereira,     University of Florida, Gainesville, FL, United States

A. Peters,     e-nema GmbH, Schwentinental, Germany

C. Prior,     Mount Pleasant, Bampton, Devon, United Kingdom

D. Shapiro-Ilan,     USDA-ARS, Southeastern Fruit and Tree Nut Laboratory, Byron, GA, United States

L.F. Solter,     University of Illinois, Champaign, IL, United States

D.R. Sosa-Gómez,     Embrapa Soja, Londrina, Paraná, Brazil

T. Su,     West Valley Mosquito and Vector Control District, Ontario, CA, United States

K. van Frankenhuyzen,     Natural Resources Canada, Sault Ste. Marie, ON, Canada

S.P. Wraight,     USDA-ARS, R. W. Holley Center for Agriculture and Health, Ithaca, NY, United States

S. Wu,     Rutgers University, New Brunswick, NJ, United States

X. Yan,     Guangdong Entomological Institute, Guangzhou, Guangdong, China

Preface

Since the publication of Microbial Control of Pests and Plant Diseases (Burges, 1981) 35 years ago, there have been very few comprehensive books published on microbial control of insect and mite pests. This book was written by an international team of 56 experts from 13 counties with a wealth of experience in a wide variety of fields in order to address the question, which entomopathogens can be successfully employed as significant components of integrated pest management? Although entomopathogens are seldom used as a stand-alone means of control, they have been successfully employed in all of the major types of biological control, including classical, conservation, inoculative and inundation (also referred to as augmentation control). Examples of classical and conservation biological control are presented in the first 6 chapters of the book. Most of the 19 applied chapters focus on inundation application of microbial control agents (MCAs).

The book is intended to serve as a stand-alone resource, designed to provide background on the insect pathology foundations of microbial control and how and where entomopathogens can be used for pest control. However, it is not intended to be an exhaustive review of microbial control in every crop or setting in which MCAs are used. For some of the crops in which MCAs have been applied that are not covered here, the reader is referred to the Field Manual of Techniques in Invertebrate Pathology (Lacey and Kaya, 2007) and Insect Pathology (Vega and Kaya, 2012). This book can also serve as a supplementary resource for courses in insect pathology, biological control, and integrated pest management. It provides information on basic and applied research for each of the major pathogen groups and their mass production. However most of the chapters are devoted to microbial control of a plethora of pests in major crops (corn, soybeans, sugarcane, coffee, cotton), minor crops (fruits, vegetables, tea), landscape and ornamental plants, forestry, turf, rangeland, human health, and structures.

Background on the MCAs that are employed is derived from recent original research and older studies upon which today’s successes are based. The chapters focus primarily on field derived data and, where possible, application rates and efficacy data are provided to be used in implementation of control programs or as starting points for continued research. This data can also be used as the basis for determining the feasibility and cost effectiveness of implementing MCAs for specific control situations.

I sincerely appreciate the efforts and expertise of the 56 authors, 60 reviewers, and a multitude of colleagues who have furnished scientific advice and literature, graphics, and constructive comments. Thank you Cynthia Lacey for your support, grammatical tutoring, and encouragement. I am grateful to the Elsevier editorial staff, especially Pat Gonzalez and Kristi Gomez for their management and editorial skills. Inspiration for this book was provided by Steinhaus (1949, 1956), Burges and Hussey (1971), Burges (1981), Agostino Bassi, and Louis Pasteur.

Lawrence A. Lacey

April, 2016

References

Burges H.D, ed. Microbial Control of Pests and Plant Diseases: 1970–1980. London, UK: Academic Press; 1981:949 pp.

Burges H.D, Hussey N.W, eds. Microbial Control of Insects and Mites. London, UK: Academic Press; 1971:861 pp.

Lacey L.A, Kaya H.K, eds. Field Manual of Techniques in Invertebrate Pathology: Application and Evaluation of Pathogens for Control of Insects and Other Invertebrate Pests. 2nd Edition. Dordrecht, The Netherlands: Springer; 2007:484 pp.

Steinhaus E. Principals of Insect Pathology. Academic Press; 1949:757 pp.

Steinhaus E. Living insecticides. Sci. Am. 1956;195:96–103.

Vega F.E, Kaya H.K, eds. Insect Pathology. 2nd ed. San Diego: Academic Press; 2012:490 pp.

Part I

Introduction to Insect Pathology and Microbial Control: The Tried and True and Recent Innovations

Outline

Chapter 1. Entomopathogens Used as Microbial Control Agents

Chapter 2. Exploration for Entomopathogens

Chapter 1

Entomopathogens Used as Microbial Control Agents

L.A. Lacey     IP Consulting International, Yakima, WA, United States

Abstract

Hundreds of pathogens of arthropods have been reported in the literature. The purpose of this chapter is to provide an overview of those entomopathogens that are used as microbial control agents (MCAs) of insect and mite pests of crops, forests, humans and domesticated animals, and man-made structures. Species of each major group of entomopathogens (ie, virus, bacteria, fungi, and nematodes) have been investigated for their utility as MCAs and for commercial development. Entomopathogens have been successfully used in classic, conservation, and augmentation biological control. Examples of classic biological control include introduction of the Oryctes nudivirus into several islands for control of the coconut rhinoceros beetle and introduction of Steinernema scapterisci for control of exotic mole crickets. Most MCAs are used for augmentative biological control. The best known and most widely used is Bacillus thuringiensis subspp. The most important advantages are the efficacy, specificity, and safety of MCAs. In contrast, the greatest disadvantages include the higher comparative cost, narrower spectrum of insecticidal activity, and reduced persistence relative to conventional chemical insecticides. However, benefits of environmental and food safety are increasingly having a positive effect on the sales and popularity of microbial control. Even though the climate for microbial pesticides is becoming more positive, significant research is still needed to overcome the limitations of current microbial products and expand the range of products available if they are to play a significantly greater role in the next generation of farming and pest control.

Keywords

Augmentative biological control; Bacillus thuringiensis; Baculovirus; Beauveria; Classic biological control; Conservation biological control; Entomopathogenic fungi; Entomopathogenic nematodes; Granulovirus; Lysinibacillus sphaericus; Metarhizium; Neozygites; Nucleopolyhedrovirus; Oryctes nudivirus; Serratia entomophila; Steinernema scapterisci

1.1. Introduction to Entomopathogens Used in the Microbial Control of Insect and Mite Pests

The goal of this book is to provide a current, comprehensive, and enduring reference for microbial control and the underlying principles of insect pathology that determine its success. Central to this must be a clear understanding of the nature and ecology of the microbes that cause diseases in pest species.

1.1.1. A Brief History of Entomopathogens and Their Use as Microbial Control Agents

Diseases of honeybees and silkworms have been recognized for millennia (Davidson, 2012), but the causal agents of insect diseases were not demonstrated until 1835, when Augusto Bassi associated a disease of the silkworm, Bombyx mori, with a fungal pathogen, later named Beauveria bassiana (Bassi, 1835). Bassi is known as the Father of Insect Pathology for demonstrating the transmission of the fungus from larva to larva and from contaminated leaves to larvae (Steinhaus, 1975; Davidson, 2012). Subsequently, a number of entomopathogens have been incriminated as the causal agents of insect disease, including Louis Pasteur’s landmark demonstration of the microsporidium Nosema bombycis as the causal agent of pébrine disease in B. mori (Pasteur, 1870). According to Steinhaus (1949), in solving this problem and another entomopathogen-related silkworm disease (flacherie), Pasteur saved the French silk industry. Metchnikoff was the first to culture an entomopathogen, the fungus Metarhizium anisopliae, on artificial medium after isolation from the wheat cockchafer Anisoplia austriaca and to suggest using it as an applied microbial control agent (MCA) (Metchnikoff, 1879, 1880; Steinhaus, 1975; Lord, 2005). However, it was not until 1888 that M. anisopliae was evaluated as an MCA (Krassilstschik, 1888). Since then, a multitude of entomopathogens have been discovered and developed as MCAs (Steinhaus, 1963, 1975; Lord, 2005; Davidson, 2012; Lacey et al., 2015).

The first commercialization of MCAs began in France in 1938 with Sporeine, a product based on the bacterium Bacillus thuringiensis. The production and use of the product were discontinued, ostensibly due to World War II (Steinhaus, 1949; Davidson, 2012). The first entomopathogenic bacterium to be registered in the United States (1948) was Paenibacillus (Bacillus) popilliae (also known as milky spore) for control of the Japanese beetle, Popillia japonica (Dutky, 1963; Klein, 1981; Federici, 2005; Davidson, 2012). It was applied as an augmentative MCA to larval breeding sites of P. japonica larvae, especially in residential lawns and golf courses. It is no longer commercially produced due in large part to the requirement of in vivo production. Steinhaus stimulated renewed interest in the development of B. thuringiensis and other MCAs with the publication of Living Insecticides (Steinhaus, 1956). Although the first commercial B. thuringiensis product was registered for use in the United States in 1961, it was not until the discovery and commercial development of efficacious strains with greater virulence toward a broader range of pests that microbial control became widely used in agriculture and forestry (Kurstak, 1962; Dulmage, 1970; Glare and O’Callaghan, 2000). More detail on the development of this key MCA leading to its widespread use is presented in Chapter 4 and by Federici (2005) and by Sanchis (2011). Historical accounts of the development of other entomopathogens as MCAs are presented by Steinhaus (1949, 1975), Lord (2005), and Davidson (2012). Several significant advances in microbial control of pest insects and mites have taken place since the comprehensive reviews by Burges and Hussey (1971) and Burges (1981). Glare et al. (2012) and Lacey et al. (2015) reviewed the successes and setbacks for microbial control and made recommendations for improvements of MCAs and their future use.

1.2. Entomopathogens Used as MCAs

1.2.1. Entomopathogenic Viruses

A wide array of viruses have been reported from a broad spectrum of insects and other arthropods (Miller, 1997; Miller and Ball, 1998). These include representatives from at least 16 families of viruses (Possee and King, 2014) including baculoviruses, cytoplasmic polyhedroviruses, entomopoxviruses, nudiviruses, and a variety of lesser known viruses that have been investigated for their potential as MCAs. The most researched for microbial control are the baculoviruses with over 600 species of insects being reported as hosts (Miller, 1997; Szewczy et al., 2006; Cory and Evans, 2007). Inundation augmentative application is the most commonly adopted strategy for their use. Of the four genera of the Baculoviridae, the Alphabaculovirus [nucleopolyhedroviruses (NPVs)] and Betabaculovirus [granuloviruses (GVs)] are the most numerous and most widely used as MCAs (Cory and Evans, 2007; Eberle et al., 2012). NPVs are predominantly found in the Lepidoptera, but also in Diptera, Hymenoptera (Symphyta), and some Crustacea while GVs infect only Lepidoptera (Miller, 1997; Eberle et al., 2012). In addition to host range, the two genera differ mainly in the manner in which virions are embedded in the infectious particles, the proteinaceous occlusion bodies (OBs). In NPVs, several viral rods are embedded together within the same large polyhedral OBs, whereas in GVs only a single virion is embedded singly in smaller OBs, sometimes called a granule. In NPVs, viral rods can be singly enveloped (SNPV) or multiply enveloped (MNPV). Morphology of GVs, MNPVs, and SNPVs is depicted in Chapter 3, Figure 3.2. MNPVs usually have broader host ranges than SNPVs. For example, the Autographa californica MNPV (AucaMNPV) is active against larvae of 95 species in 15 families of Lepidoptera (Vail et al., 1971, 1999; Vail and Jay, 1973; Cory and Evans, 2007). However, it is most efficacious against species in the Noctuidae (Vail et al., 1999). In contrast, another MNPV, Lymantria dispar, is strictly host specific (Barber et al., 1993). Selected NPVs and GVs are presented in Table 1.1, and a more extensive listing is presented in Chapter 3.

With few exceptions, baculovirus OBs must be ingested in order to invade the host insect. Virions enter the host via the midgut epithelium where they initially multiply before spreading and infecting other types of cells (fat body, tracheal matrix, hypodermis) and begin viral replication and occlusion. Detailed descriptions of the infection processes and pathogenesis are presented by Federici (1997) and in Chapter 3. The macroscopic progression of disease signs and symptoms are shown in Chapter 3, Figure 3.1. Among all entomopathogenic viruses, baculoviruses are the only ones to have been mass produced, commercialized, and applied on a widespread basis. The issues and constraints around expanding their use on a broader scale are presented in Chapter 3. Mass production of baculoviruses is covered in Chapter 7.

1.2.2. Bacteria

Although the major volume and market share of commercially produced MCAs that are used for microbial control are bacteria, relatively few species have been developed. These include gram-positive, spore-forming B. thuringiensis subspp. and L. (B.) sphaericus, the gram-negative, non–spore-forming Serratia entomophila, and, most recently, Chromobacterium subtsugae. B. thuringiensis subsp. are the most commonly used of all microbial pesticides worldwide, representing over 50% of all MCA sales (Glare et al., 2012; Lacey et al., 2015). The majority of B. thuringiensis inundative applications are for suppression of lepidopteran pests of crops followed by applications for control of forest pests and then by abatement of mosquitoes and black flies. The insecticidal activity of B. thuringiensis and L. sphaericus is mainly due to protein toxins within parasporal inclusions, which must be ingested to become larvicidal. The toxins become solubilized in the high pH of the midgut and are cleaved to the toxic moieties by gut proteolytic enzymes. These toxins recognize receptors and create pores on enterocytes, with the subsequent osmotic imbalance resulting in cell rupture, compromising integrity of the gut epithelium. Invasion of the main body cavity and subsequent septicemia caused by gut-resident bacteria leads to death of the larva soon afterward. Detailed descriptions of the biochemical nature of the toxins and their modes of action at the molecular level are presented in Chapter 4. Examples of targeted pests for inundative applications include a plethora of lepidopteran pests of field crops, tree fruit, turf, and ornamental plants and forest and dipteran pests and are shown in Table 1.1. The larvicidal activity S. entomophila is due to proliferation of the bacterium in the gut resulting in blockage and lack of nutrient absorption. More details on host range factors affecting larvicidal activity, safety, and production of entomopathogenic bacteria are presented in Chapters 4 and 8.

1.2.3. Fungi

Depending on the scientists reporting, between 700 and 1000 species of fungi are recognized as causal agents of disease in arthropods (Goettel et al., 2010; Vega et al., 2012). The majority of those used for microbial control of insects and mites are in the orders Hypocreales and Entomophthorales. In addition to a broad host range within the Insecta and Acarina, they are the only effective MCAs of sucking insects (Hemiptera). The only commercially produced fungi for microbial control are in the Hypocreales. These include Beauveria bassiana, Metarhizium spp., Isaria fumosorosea, and Lecanicillium spp. and are used against dozens of pests in a variety of crops.

The typical route of invasion of the host is through the cuticle. Once fungal spores have germinated on the surface of the host, the growing tip (appressorium, infection peg, germ tube) penetrates the cuticle through concentrated physical energy and lytic enzymatic activity (Hajek and St. Leger, 1994). Following penetration and growth of hyphae and blastospores within the host, sporulation of the fungus takes place on the surface of the cuticle. Selected examples of the use of entomopathogenic fungi for protection of crops and urban structures are presented in Table 1.1 and in Chapter 5 and several of the applied chapters in the book. Mass production of entomopathogenic fungi is presented in Chapter 9.

Table 1.1

Some Examples of Entomopathogens Used for Microbial Control of Targeted Arthropods

a Insect orders in which naturally occurring EPN infections were found (Peters, 1996). Experimental host ranges can be narrow (H. megidis, S. scapterisci) to very broad (S. carpocapsae, S. feltiae, H. bacteriophora). See also Chapter 6.

1.2.4. Entomopathogenic Nematodes

A huge number of entomogenous nematodes have been reported from insects, (Welch, 1963; Poinar, 1975; Grewal et al., 2005) including those used in classic biological control (Bedding and Akhurst, 1974; Platzer, 2007; Bedding, 2009; Frank, 2009). The only nematodes currently used as MCAs for augmentative biological microbial control are entomopathogenic nematodes (EPNs) in the families Steinernematidae and Heterorhaditidae. Species of EPNs are in mutualistic and obligate associations with bacteria (Xenorhabdis spp. and Photorhabdis spp.) carried inside the gut of infective juveniles (IJs). These IJs wait for or actively seek a host insect. They gain entry into the host insect, per os, via the spiracles or in some cases by penetrating intersegmental membranes. Inside the host, the mutualistic bacteria are liberated, kill the host, and digest host tissues, and the IJs molt and begin feeding. There are normally two to three generations, although if nutrients are low, only one generation may result. Once nutrients are exhausted, IJs are produced and leave the host insect to search for or wait for new hosts. Some examples of EPNs, insect targets, and protected crops are presented in Table 1.1. Detailed information on the life cycle, host ranges, factors that enhance or retard EPN efficacy, and protected crops are given in Chapter 6. Mass production of EPNs is covered in Chapter 10.

1.3. Microbial Control Agents and Biological Control

Entomopathogens used as MCAs fit the three categories of biological control: classic, conservation, and augmentative, as defined by Barbosa (1998), McCrevy (2008) and Hoy (2008a,b) for natural enemies of pest arthropods. Entomopathogens have been successfully used in all three categories. Classic biological control entails introduction of naturally occurring predators, parasitoids, and entomopathogens from the native range of an invasive pest to help bring about its long-term suppression; conservation biological control stresses maintaining a habitat that is conducive to conserving natural enemies of the pest; and augmentative biological control involves enhancing the prevalence of the natural enemies to initiate increased control. In microbial control, this is accomplished with either inoculative or inundative application of MCAs. Eilenberg et al. (2001) proposed replacing augmentative biological control with two separate categories: inoculative biological control and inundative biological control.

1.3.1. Classic Biological Control

There are numerous examples of MCAs used for classic biological control of invasive insects (Hajek et al., 2005, 2007, 2009). These include entomopathogenic viruses (baculovirus, nudivirus), fungi (Entomophthorales), and parasitic and entomopathogenic nematodes (Neotylenchidae, Mermithidae, Steinernematidae). Three noteworthy examples of classical microbial control follow.

1.3.1.1. Case Study: Oryctes Nudivirus for Control of Invasive Coconut Palm Rhinoceros Beetle

One of the most impressive examples of classic biological control with an MCA is that of the Oryctes nudivirus for control of the coconut palm rhinoceros beetle, Oryctes rhinoceros (Hüger, 2005; Jackson et al., 2005; Jackson, 2009). The beetle is a serious exotic pest of coconut and oil palms in the southwest Pacific islands. Adults consume foliage in the crown of the palms and can reduce yield and kill trees (Bedford, 1980). Larvae develop in rotting palm logs, including the tops of standing dead palms, and in organic matter in a diversity of other sites with high organic content (sawdust, manure piles, etc.) (Bedford, 1980). Native to the coconut growing areas of the Asia–west Pacific region, the beetle was accidentally introduced into Samoa and subsequently spread to other islands in the southwest Pacific, where it became a widespread and very serious pest of coconut palms (Bedford, 1980; Jackson, 2009).

The Oryctes virus was originally collected from infected Oryctes rhinoceros in Malaysia by Hüger (1966) and introduced into Samoa and several southwest Pacific islands (Bedford, 1980; Hüger, 2005; Jackson, 2009). Adult beetles become chronically infected and serve as mobile reservoirs of the virus. Aggregations of mating and feeding adults in the palm crowns ensures transmission from infected to uninfected individuals and dispersal of the virus. Larval breeding sites become initially contaminated with virus via ovipositing infected females. Larvae become acutely infected after consuming virus and die within 9–25  days depending on age and temperature (25–32°C) (Hüger, 1966; Zelazny, 1972). The introduced virus has resulted in significant long-term control of the beetle and reduction of foliar damage by causing epizootics that kill larvae, curtail the life span of adults, and reduce fecundity in females (Zelazny, 1972, 1973; Bedford, 1980; Hüger, 2005; Jackson, 2009). Production and application of the virus is reviewed by Bedford (1980) and Jackson (2009). In recent years there are reports of Oryctes virus having become attenuated and therefore less effective on some of the beetle-infested islands (Jackson et al., 2005; Jackson, 2009). Jackson et al. (2005) and Jackson (2009) conclude that selection of more virulent strains of virus and improvements in application methods need to be developed to overcome this problem.

1.3.1.2. Case Study: Entomophaga maimaiga for Classic Biological Control of Gypsy Moth, L. dispar

An example of classic biological control using a fungus as an effective pathogen for long-term control of the gypsy moth, L. dispar, is that of the entomophthoralean E. maimaiga (Hajek et al., 1996; Hajek, 1997; Solter and Hajek, 2009). The moth is a native forest defoliator that outbreaks occasionally from Europe to Asia but was absent from the Western Hemisphere. From its original point of entry into the United States (Boston, Massachusetts) in 1869, it has dispersed annually farther south and west. Larvae of L. dispar feed on a wide range of deciduous trees and during cyclic outbreaks have been responsible for defoliation of trees in up to 2  million ha of forest (Solter and Hajek, 2009).

The fungus originated in Japan and was first released in the United States near Boston in 1910 and 1911 but was not detected in following years (Hajek et al., 1995). It was also collected in Japan in 1984 by Soper et al. (1988), and small field applications of the 1984 isolate in 1985 in New York State and in 1986 in Virginia resulted in few or no infections. It was not until 1989 that significant epizootics caused by E. maimaiga were reported (Andreadis and Weseloh, 1990; Hajek, 1997, 1999). The exact origin of the E. maimaiga causing these outbreaks is not precisely known, but it appears to have originated from areas in Japan different from the 1910–1911 collection sites (Nielsen et al., 2005). Since then, in vivo produced fungal spores (conidia and resting spores) and infected larvae have been introduced into areas on the leading edge of L. dispar dispersal. Subsequent infections indicate that E. maimaiga has become established in and spread from locations where it was not previously observed (Hajek et al., 1996; Weseloh, 2003; Solter and Hajek, 2009). More details on this continuing successful classic microbial control are presented in Chapter 21.

1.3.1.3. Case Study: Steinernema scapterisci for Control of Invasive Mole Crickets

Mole crickets, Scapteriscus spp., expanding northward from their centers of origin in South America, were introduced into the United States in the early 1900s (Frank, 2009). Since introduction, severe damage had been reported in turf infested by the crickets, especially in Florida, where S. vicinus is a serious pest of turf (Frank, 2009). Exploration for EPNs and other natural enemies of Scapteriscus spp. were started in South America. In 1985, an EPN from Uruguay was released in Florida. Initially, the introduction of the EPN, S. scapterisci, for control of the invasive mole crickets in Florida fit the classic biological control paradigm (Parkman et al., 1993). The nematode was collected in Uruguay and introduced into S. vicinus, S. borelli, and S. abbreviatus populations in Florida where it became established (Hudson et al., 1988; Parkman et al., 1993). Additionally, two imported parasitoids, also from South America, were released and became established throughout Florida. By 2000, the combined effort of the three natural enemies reduced the Scapteriscus populations by 95% (Frank and Walker, 2006). Since then the EPN has been applied to infestations of the cricket in several sites in Florida (Frank, 2009).

Numerous additional examples of classic microbial control are found throughout the literature; some of which are examined in this book. These include importation and establishment of the nematode Deladenus siricidicola (Tylenchida: Neotylenchidae) for control of the Sirex woodwasp, Sirex noctilio (Chapter 21); importation and establishment the of nematode Romanomermis iyengari (Nematoda: Mermithidae) for control of mosquitoes (Chapter 28); development of Neozygites tanajoae (Entomophthorales) for control of cassava greenmite in Brazil and Chapter 2 Chapter 21 Benin (Chapter 2); baculoviruses in forestry (Chapter 21); and agriculture (Chapters 14 and 17). A catalog of imported exotic entomopathogens used as classic biological control agents was compiled by Hajek et al. (2005).

1.3.2. Conservation Biological Control

Epizootics caused by naturally occurring viral and fungal pathogens are often responsible for spectacular crashes of insect pest populations and are often credited with eliminating the need for further interventions (Harper, 1987; Steinkraus, 2007; Shapiro-Ilan et al., 2012). Conservation biological control relies on the protection of and improving conditions for naturally occurring MCAs to enable induction of high rates of infection in pest populations. Reliance on the natural occurrence of entomopathogens for pest management, however, can be risky due to the unpredictability of factors that govern epizootics. Because many pathogens are host-density dependent, epizootics often occur after economic injury levels have been surpassed (Odindo, 1983; Harper, 1987; Rose et al., 2000). However, agricultural practices that foster their conservation and increase their prevalence should nevertheless be considered.

A demonstration of the conservation microbial control strategy is that reported by Steinkraus (2007). By not treating cotton with broad-spectrum insecticides, populations of the cotton aphid, Aphis gossypii, were allowed to develop, which in turn encouraged epizootics of the fungus Neozygites fresenii. Conservation of naturally occurring MCAs can also be disrupted by the effect of pesticides directly on the MCAs. For example, application of fungicides and nematicides can drastically curtail the insecticidal activity of entomopathogenic fungi and EPNs, respectively.

In addition to pesticide type and timing of application, other agricultural practices [type of tillage (conventional versus conservation), irrigation, fertilizer (chemical versus organic) crop rotation, type of ground cover, etc.] can have a marked effect on the survival and pathogenicity of MCAs. Hummel et al. (2002) and Millar and Barbercheck (2002) found that tillage practices can significantly affect the survival and abundance of entomopathogenic fungi and EPNs. Hummel et al. (2002) demonstrated that detection of entomopathogens was significantly higher in conservation tilling compared with conventional tillage systems. They reported that conservation tilling (strip-till) did not affect levels of detection of Steinernema carpocapsae, but pesticide use significantly reduced detection of entomopathogenic fungi. Millar and Barbercheck (2002) demonstrated that tillage versus no tillage resulted in a significant negative effect of detection of S. carpocapsae but a positive effect on detection of S. riobrave. The authors surmised that the different sensitivities of the EPNs could be partly explained by differences in environmental tolerances of the two species and tendencies to disperse deeper into the soil. A number of other examples of the role of conserved EPN and fungal MCAs in microbial control are presented by Lewis et al. (1998), Ekesi et al. (2005), Meyling and Eilenberg (2007), Nielsen et al. (2007), Steinkraus (2007), Pell et al. (2010), and Campos-Herrera et al. (2010).

1.3.3. Augmentative Biological Control

Augmentation of naturally occurring MCAs can be accomplished with either inoculative or inundative applications depending on the pathogen and crop that requires protection. Inoculative microbial control is the application of smaller amounts of inoculum with the goal that the MCA will increase in the host population on its own (Eilenberg et al., 2001). This could result in outbreaks of disease earlier in the season than would otherwise occur. Examples include limited applications of P. popilliae and Heterorhabditis bacteriophora for control of Popillia japonica (Dutky, 1963; Klein, 1981; Klein and Georgis, 1992).

The more common strategy is the inundative application of larger amounts of MCAs to initiate widespread infections and provide immediate control of targeted pests (Steinhaus, 1949, 1963; Burges and Hussey, 1971; Burges, 1981; Lacey et al., 2001, 2015; Kaya and Lacey, 2007). In the inundative approach, the main route of infection is through the pests picking up the applied MCA rather than through secondary infections. Depending on the number of generations of the pest insect or mite and the impact of adverse environmental factors on MCA persistence, especially exposure to ultraviolet-B radiation, one to several applications of the MCA may be required throughout the growing season.

There are scores of commercially produced microbial pesticides used for augmentative control of pest insects and mites worldwide (Glare and O’Callaghan, 2000; Federici, 2005; Alves and Lopes, 2008; Kabaluk and Gazdik, 2005; Faria and Wraight, 2007; Gwynn, 2014; Lacey et al., 2015). Some examples of the augmentative use of entomopathogenic viruses, bacteria, fungi, and nematodes are presented in Table 1.1. B. thuringiensis is the most widely used MCA for control of hundreds of species of insect pests (Glare and O’Callaghan, 2000; Federici, 2005; see Chapter 4). The use of MCAs against insects and mites is the predominant theme of Chapters 11–29.

1.4. Advantages and Disadvantages of Microbial Control

Table 1.2 presents several advantages and disadvantages of microbial control as compiled from Steinhaus (1949), Burges and Hussey (1971), Tanada and Kaya (1993), Alves (1998), Kaya and Lacey (2007) and Kaya and Vega (2012). The most important advantages are the efficacy, specificity, and safety of MCAs. In contrast, the greatest disadvantages include the higher comparative cost, narrower spectrum of insecticidal activity, and reduced persistence relative to conventional chemical insecticides. However, benefits of environmental and food safety are increasingly having a positive effect on the sales and popularity of microbial control. Numerous studies attest to the safety of MCAs for applicators and other vertebrates, most nontarget organisms, especially honeybees and predators and parasitoids (Hokkanen and Hajek, 2003). There could be indirect effects on other natural enemies if the host insect is killed before parasitoids emerge or host and prey are significantly removed from the food chain. However, natural enemy vagility and alternative hosts and prey minimize this effect so that the overall positive effect of arthropod natural enemies on pests outweighs any potential negative effects. Publication of studies on the safety of MCAs have been reviewed by Laird et al. (1990), Glare and O’Callaghan (2000), Lacey and Siegel (2000), Goettel et al. (2001), and Hokkanen and Hajek (2003). MCAs may not always provide a stand-alone means for total pest control, yet they can be invaluable components of integrated pest management working in concert with other natural enemies, resistant plant varieties, agricultural practices, the judicious use of selective and soft pesticides (avermectin, spinosad, etc.), mating disruption, and environmental manipulation and modification (Gurr et al., 2004; Radcliffe et al., 2009; Wraight and Hajek, 2009).

Table 1.2

Advantages and Disadvantages of Using Microbial Control Agents (MCAs)

Information compiled from Steinhaus, E., 1949. Insect Pathology, Academic Press, 757 pp.; Burges, H.D., Hussey, N.W., 1971. Microbial Control of Insects and Mites. Academic Press, London, UK, 861 pp.; Tanada, Y., Kaya, H.K., 1993. Insect Pathology. Academic Press, San Diego, 666 pp.; Alves, S.B. (Ed.), 1998. Controle Microbiano de Insetos, second ed. Fundação de Estudos Agrários Luiz de Queiroz, Piracicaba, Brasil, 1163 pp.; Kaya, H.K., Lacey, L.A., 2007. Introduction to microbial control. In: Lacey, L.A., Kaya, H.K. (Eds.), Field Manual of Techniques in Invertebrate Pathology: Application and Evaluation of Pathogens for Control of Insects and Other Invertebrate Pests, second ed. Springer, Dordrecht, The Netherlands, pp. 3–7; Kaya, H.K., Vega, F.E., 2012. Scope and basic principles of insect pathology. In: Vega, F.E., Kaya, H.K. (Eds.), Insect Pathology, second ed. Academic Press, San Diego, pp. 1–12.

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Chapter 2

Exploration for Entomopathogens

L.F. Solter¹, A.E. Hajek²,  and L.A. Lacey³     ¹University of Illinois, Champaign, IL, United States     ²Cornell University, Ithaca, NY, United States     ³IP Consulting International, Yakima, WA, United States

Abstract

Foreign and domestic exploration for entomopathogens continues to provide candidate species for microbial control with environmental tolerances and host ranges that are appropriate for the systems in which they are used, as well as greater virulence and other beneficial traits. Pathogens that are useful as biological control agents have been discovered by fortuitous accident infecting insect colonies and in field collections, and in purposeful searches of exotic hosts and their