Skip to main content

Entomopathogenic Fungi as Classical Biological Control Agents

  • Chapter
Environmental Impacts of Microbial Insecticides

Part of the book series: Progress in Biological Control ((PIBC,volume 1))

Abstract

Classical biological control has been defined as the intentional introduction of an exotic biological control agent for permanent establishment and long-term pest control’ (Eilenberg et al., 2001). This technique has most often been used to target arthropod pests and weeds that have been introduced to new areas. It has predominantly focussed on use of herbivores or arthropod parasitoids and predators while it has been used relatively rarely for entomopathogens. Classical biological control releases using parasitoids and predators between 1888 and 1992 included 5500 programs (Greathead, 1995) while the last estimate for classical biological control using pathogens was only 50 programs prior to 1987 (Fuxa, 1987). Perhaps pathogens have been used little due to lack of microbiological training among practitioners and lack of knowledge regarding both the endemic and exotic pathogenic microbiota.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Anonymous 1919. Notes on insects in Seychelles. Review of Applied Entomology, Ser. A 7: 483–484.

    Google Scholar 

  • Bidochka, M. J. 2001. Monitoring the fate of biocontrol fungi. In Fungal Biocontrol Agents: Progress, Problems and Potential. T. Butt, C. Jackson, & N. Magan (Eds.), CABI Publ., Wallingford, UK, pp. 193–218.

    Google Scholar 

  • Bidochka, M. J., Walsh, S. R. A., Ramos, M. E., St. Leger, R. J., Silver, J. C., & Roberts, D. W. 1995. Pathotypes of the Entomophaga grylli species complex of grasshopper pathogens differentiated with random amplification of polymorphic DNA and cloned-DNA probes. Applied and Environmental Microbiology 61: 556–560.

    PubMed  CAS  Google Scholar 

  • Boucias, D. G., & Pendland, J. C. 1998. Principles of Insect Pathology. Kluwer Acad. Publ., Boston.

    Google Scholar 

  • Butler, L., Chrislip, G. A., Kondo, V. A., & Townsend, E. C. 1997. Effect of diflubenzuron on nontarget canopy arthropods in closed, deciduous watersheds in a central Appalachian forest. Journal of Economic Entomology 90: 784–794.

    CAS  Google Scholar 

  • Carruthers, R. J., & Onsager, J. A. 1993. Perspective on the use of exotic natural enemies for biological control of pest grasshoppers (Orthoptera: Acrididae). Environmental Entomology 22: 885–903.

    Google Scholar 

  • Delalibera Jr., I. 2002. Investigations toward implementation of Neozygites tanajoae sp. nov. as a classical biological control agent against the cassava green mite in Africa. Ph.D. Thesis, Cornell University.

    Google Scholar 

  • Delalibera Jr., I., Gomez, D. R. S., Moraes, G. J. de, Alencar, J. A. de, & Araujo W. F. 1992. Infection of Mononychellus tanajoa (Acari Tetranychidae) by the fungus Neozygites sp. (Entomophthorales) in northeastern Brazil. Florida Entomologist 75: 145–147.

    Article  Google Scholar 

  • DeLoach, C. J. 1976. Considerations in introducing foreign biotic agents to control native weeds of rangelands. In Proceedings of the 4th International Symposium, Biological Control of Weeds, Gainesville, FL, USA, pp. 39–50.

    Google Scholar 

  • Eilenberg, J., Hajek, A. E., & Lomer, C. 2001. Suggestions for unifying the terminology in biological control. BioControl 46: 387–400.

    Article  Google Scholar 

  • Fetter-Lasko, J. L., & Washino, R. K. 1977. A three year study of the ecology of Lagenidium giganteum, infections of Culex tarsalis in California. Proceedings and Papers of the Annual Conference of the California Mosquito and Vector Control Association 45: 106.

    Google Scholar 

  • Federici, B. A. 1981. Mosquito control by the fungi Culicinomyces, Lagenidium and Coelomomyces. In Microbial Control of Pests and Plant Diseases, 1970–1980. H. D. Burges (Ed.), Academic Press, London, pp. 555–572.

    Google Scholar 

  • Ferguson, D. C. 1978. Noctuoidea (in part), Lymantriidae. In The Moths of North America. Fasc. 22.2. R. B. Dominick, et al. (Eds.), E. B. Classey, London and The Wedge Entomological Research Foundation, pp. 1–110.

    Google Scholar 

  • Follett, P. A., & Duan, J. J. 2000. Nontarget Effects of Biological Control. Kluwer Acad. Publ., Dordrecht, NL.

    Book  Google Scholar 

  • Fuxa, J. R. 1987. Ecological considerations for the use of entomopathogens in IPM. Annual Review of Entomology 32: 225–251.

    Article  Google Scholar 

  • Glare, T. R., & Milner, R. J. 1991. Ecology of entomopathogenic fungi. In Handbook of Applied Mycology, vol. 2. D. K. Arora, L. Ajello & K. G. Mukerji (Eds.), Dekker, New York, pp. 547–612.

    Google Scholar 

  • Goettel, M. S., & Hajek, A. E. 2001. Evaluation of non-target effects of pathogens used for management of arthropods. In Evaluating Indirect Ecological Effects of Biological Control. E. Wajnberg, J. K. Scott, & P. C. Quimby (Eds.), CABI Publ., Wallingford, UK, pp. 81–97.

    Google Scholar 

  • Goettel, M. S., Hajek, A. E., Siegel, J. P., & Evans, H. D. 2001. Safety of fungal biocontrol agents. In Fungi as Biocontrol Agents: Progress, Problems and Potential. T. M. Butt, C. W. Jackson, & N. Magan (Eds.), CABI Publ., Wallingford, UK, pp. 347–375.

    Google Scholar 

  • Greathead, D. J. 1995. Benefits and risks of classical biological control. In Biological Control: Benefits and Risks. H. M. T. Hokkanen, & J. M. Lynch (Eds.), Cambridge Univ. Press, Cambridge, UK, pp. 53–63.

    Chapter  Google Scholar 

  • Hajek, A. E. 1999. Pathology and epizootiology of the lepidoptera-specific mycopathogen Entomophaga maimaiga. Microbiology and Molecular Biology Reviews 63: 814–835.

    PubMed  CAS  Google Scholar 

  • Hajek, A. E. 2001. Larval behavior in Lymantria dispar increases risk of fungal infection. Oecologia 126: 285–291.

    Article  Google Scholar 

  • Hajek, A.E., & Butler, L. 2000. Predicting the host range of entomopathogenic fungi. In Nontarget Effects of Biological Control. P. A. Follett, & J. J. Duan (Eds.), Kluwer Acad. Publ., Dordrecht, NL, Pp. 263–276.

    Chapter  Google Scholar 

  • Hajek, A. E., & Goettel, M. S. 2000. Guidelines for evaluating effects of entomopathogens on non-target organisms. In Field Manual of Techniques in Invertebrate Pathology, L. A. Lacey & H. K. Kaya (Eds.), Kluwer Acad. Publ., Dordrecht, NL, pp. 847–868.

    Google Scholar 

  • Hajek, A. E., Butler, L., & Wheeler, M. M. 1995. Laboratory bioassays testing the host range of the gypsy moth fungal pathogen Entomophaga maimaiga. Biological Control 5: 530–544.

    Article  Google Scholar 

  • Hajek, A. E., Butler, L., Walsh, S. R. A., Silver, J. C., Hain, F. P., Hastings, F. L., ODell, T. M., and Smitley, D. R. 1996. Host range of the gypsy moth (Lepidoptera: Lymantriidae) pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) in the field versus laboratory. Environmental Entomology 25: 709–721.

    Google Scholar 

  • Hajek, A. E., Butler, L., Liebherr, J. K., & Wheeler, M. M. 2000. Risk of infection by the fungal pathogen Entomophaga maimaiga among Lepidoptera on the forest floor. Environmental Entomology 29: 645–650.

    Article  Google Scholar 

  • Hajek, A. E., Delalibera Jr., I., & McManus, M. L. 2000. Introduction of exotic pathogens and documentation of their establishment and impact. In Field Manual of Techniques in Invertebrate Pathology, L. A. Lacey & H. K. Kaya (Eds.), Kluwer Acad. Publ., Dordrecht, NL, pp. 339–369.

    Google Scholar 

  • Hajek, A. E., Hodge, K. T., Liebherr, J. K., Day, W. H., & Vandenberg, J. D. 1996. Use of RAPD analysis to trace the origin of the weevil pathogen Zoophthora phytonomi in North America. Mycological Research 100: 349–355.

    Article  Google Scholar 

  • Harper, J. 1978. Introduction and colonization of entomopathogens. In Microbial Control of Insect Pests: Future Strategies in Pest Management Systems. G. E. Allen, C. M. Ignoffo & R. P. Jaques (Eds.), NSF-USDA-Univ. Florida Workshop, pp. 3–13.

    Google Scholar 

  • Hodge, K. T., Sawyer, A. J., & Humber, R. A. 1995. RAPD-PCR for identification of Zoophthora radicans isolates in biological control of potato leafhopper. J. Invertebrate Pathology 65: 1–9.

    Article  CAS  Google Scholar 

  • Hountondji, F. C., De Nardo, E. A. B. & Tamai, M. A. 1995. Nâo susceptibilidade de abelhas a infecçâo pelo fungo Neozygites sp. agente de controle do acaro verde da mandioca. In Anais do 15 Congresso de Entomologia. Caxambu, MG, Brazil, p. 610.

    Google Scholar 

  • Hountondji, F. C. C., Yaninek, J. S., Moraes, G. J. d., & Oduor, G. J. 2002. Host specificity of the cassava green mite pathogen Neozygites floridana. BioControl 47: 61–66

    Article  Google Scholar 

  • Humber, R. A. 1999. USDA-ARS Collection of Entomopathogenic Fungal Cultures (ARSEF ). http://www.ppru.cornell.edu/Mycology/ARSEF_Culture_Collection.htm.

  • Humber, R. A. 2000. Fungal pathogens and parasites of insects. In Applied Microbial Systematics F.G. Priest & M. Goodfellow (Eds.), Kluwer Acad. Publ., Dordrecht, NL, pp. 203–230.

    Google Scholar 

  • Jones, W. O. 1959. Manioc in Africa. Stanford Univ. Press, California.

    Google Scholar 

  • Laird, M. 1967. A coral island experiment: A new approach to mosquito control. World Health Organization Chronicles 21: 18.

    CAS  Google Scholar 

  • Laird, M. 1971. Microbial control of arthropods of medical importance. In Microbial Control of Insects and Mites. H.D. Burges & N.W. Hussey (Eds.), Academic Press, London, pp. 387–406.

    Google Scholar 

  • Lockwood, J. A. 2000. Nontarget effects of biological control: What are we trying to miss? In Nontarget Effects of Biological Control. P. A. Follett & J. J. Duan (Eds.), Kluwer Acad. Publ., Dordrecht, NL, pp. 15–30.

    Chapter  Google Scholar 

  • Lockwood, J. A., Howarth, F. G., & Purcell, M. F. 2001. Balancing Nature: Assessing the Impact of Importing Non-native Biological Control Agents (An International Perspective). Entomol. Soc. Amer., Lanham, MD.

    Google Scholar 

  • Maddox, J. V., McManus, M. L., Jeffords, M. R., & Webb, R. E. 1992. Exotic insect pathogens as classical biological control agents with an emphasis on regulatory considerations. In Selection Criteria and Ecological Consequences of Importing Natural Enemies. W.C. Kauffmann, & J.E. Nechols (Eds.), Entomol. Soc. Amer., Lanham, MD, pp. 27–39.

    Google Scholar 

  • Malakar, R, Elkinton, J. S., Carroll, S. D., & D’Amico, V. (1999a) Interactions between two gypsy moth (Lepidoptera: Lymantriidae) pathogens: Nucleopolyhedrovirus and Entomophaga maimaiga (Zygomycetes: Entomophthorales): Field studies and a simulation model. Biological Control 16: 189–198.

    Article  Google Scholar 

  • Malakar, R., Elkinton, J. S., Hajek, A. E., & Burand, J. P. (1999b) Within-host interactions of Lymantria dispar (Lepidoptera: Lymantriidae) nucleopolyhedrosis virus and Entomophaga maimaiga (Zygomycetes: Entomophthorales). Journal of Invertebrate Pathology 73: 91–100.

    Article  PubMed  Google Scholar 

  • McCray Jr., E. M. Womeldorf, D. J., Husbands, R. C., & Eliason, D. A. 1973. Laboratory observations and field tests with Lagenidium against California mosquitoes. Proceedings and Papers of the Annual Conference of the California Mosquito and Vector Control Association 41: 123–128.

    Google Scholar 

  • McGuire, M.R., Maddox, J.V., & Armbrust, E.J. 1987a. An epizootic caused by Erynia radicans (Zygomycetes: Entomophthoraceae) isolated from Empoasca fabae (Homoptera: Cicadellidae). Journal of Invertebrate Pathology 50: 78–80.

    Article  Google Scholar 

  • McGuire, M.R., Maddox, J.V., & Armbrust, E.J. 1987b. Host range studies of an Erynia radicans strain (Zygomycetes: Entomophthorales) isolated from Empoasca fabae (Homoptera: Cicadellidae). Journal of Invertebrate Pathology 50: 75–77.

    Article  Google Scholar 

  • Miller, J. C. 2000. Monitoring the effects of Bacillus thuringiensis kurstaki on nontarget Lepidoptera in woodlands and forests in western Oregon. In Nontarget Effects of Biological Control. P. A. Follett, & J. J. Duan (Eds.), Kluwer Acad. Publ., Dordrecht, NL, pp. 277–286.

    Chapter  Google Scholar 

  • Moraes, G. J. de., & Delalibera Jr., I. 1992. Specificity of a strain of Neozygites sp. (Zygomycetes: Entomophthorales) to Mononychellus tanajoa (Acari: Tetranychidae). Experimental & Applied Acarology 14: 89–94.

    Article  Google Scholar 

  • Moraes, G. J. de, Alencar, J. A., Wenzel Neto, F., & Mergulhao, S. M. R. 1990. Explorations for natural enemies of the cassava green mite in Brazil. In Symposium of the International Society of Tropical Root Crops. R. H. Howeler ( Ed. ), Bangkok, pp. 351–353.

    Google Scholar 

  • Moraes, G. J. de., Mesa, N. C., & Braun, A. 1991. Some phytoseiid mites of Latin America (Acari: Phytoseiidae). International Journal of Acarology 17: 117–139.

    Article  Google Scholar 

  • Moraes, G. J. de, Alencar, J. A., Lima, J. L. S. de, Yaninek, J. S., & Delalibera Jr., I. 1993. Alternative plant habitats for common phytoseiid predators of the cassava green mite (Acari: Phytoseiidae, Tetranychidae) in northeast Brazil. Experimental & Applied Acarology 17: 77–90.

    Google Scholar 

  • Papierok, B., Valadâo, B., Tôrres, L., & Arnault, M. 1984. Contribution to the study of the specificity of the entomopathogenic fungus Zoophthora radicans (Zygomycetes: Entomophthorales). Entomophaga 29: 109–119.

    Article  Google Scholar 

  • Parker, M. A. 1984. Local food depletion and the foraging behavior of a specialist grasshopper, Hesperotettix viridis. Ecology 65: 824–835.

    Article  Google Scholar 

  • Pell, J., Eilenberg, J., Hajek, A. E., & Steinkraus, D. C. 2001. Exploring the potential of Entomophthorales in integrated crop management. In Fungal Biocontrol Agents: Progress, Problems and Potential. T. Butt, C. Jackson, & N. Magan (Eds.), CABI Publ., Wallingford, UK, pp. 71–153.

    Google Scholar 

  • Ramoska, W. A., Hajek, A. E., Ramos, M. E., & Soper, R. S. 1988. Infection of grasshoppers (Orthoptera: Acrididae) by members of the Entomophaga grylli species complex (Zygomycetes: Entomophthorales). Journal of Invertebrate Pathology 52: 309–313.

    Article  Google Scholar 

  • Shimazu, M., Sato, H., & Maehara, N. 2002. Density of the entomopathogenic fungus, Beauveria bassiana Vuillemin (Deuteromycotina: Hyphomycetes) in forest air and soil. Applied Entomology and Zoology 37: 19–26.

    Article  Google Scholar 

  • Soper, R. S., Shimazu, M., Humber, R. A., Ramos, M. E., & Hajek, A. E. 1988. Isolation and characterization of Entomophaga maimaiga sp. nov., a fungal pathogen of gypsy moth, Lymantria dispar, from Japan. Journal of Invertebrate Pathology, 51: 229–241.

    Article  Google Scholar 

  • Speare, A. T., & Colley, R. H. 1912. The Artificial Use of the Brown-tail Fungus in Massachusetts, with Practical Suggestions for Private Experiment, and a Brief Note on a Fungous Disease of the Gypsy Caterpillar. Wright & Potter, Boston.

    Google Scholar 

  • Squibbs, F. L. 1935. Work connected with insect pests and fungus diseases. Review of Applied Entomology, Ser. A 23: 241.

    Google Scholar 

  • Steinkraus, D. C., & Kramer, J. P. 1987. Susceptibility of sixteen species of Diptera to the fungal pathogen Entomophthora muscae (Zygomycetes: Entomophthoraceae). Mycopathologia 100: 55–63.

    Article  Google Scholar 

  • Stiling, P. 1990. Calculating the establishment rates of parasitoids in classical biological control. American Entomologist 36: 225–229.

    Google Scholar 

  • Valenti, M. A. (1998) Entomophaga maimaiga: Salvation from gypsy moth or fly in the ointment. American Entomologist 44: 20–22.

    Google Scholar 

  • Wajnberg, E., Scott, J. K., & Quimby, P. C. (Eds.) 2001. Evaluating Indirect Ecological Effects of Biological Control. CABI Publ., Wallingford, UK.

    Google Scholar 

  • Washino, R. K., Fetter, J. L., Fukushima, C. K., & Gonot, K. 1976. The establishment of Lagenidium giganteum, an aquatic fungal parasite of mosquitoes, three years after field introduction. Proceedings and Papers of the Annual Conference of the California Mosquito and Vector Control Association 44: 52.

    Google Scholar 

  • Yaninek, J. S., & Herren, H. R. 1988. Introduction and spread of the cassava green mite Mononychellus tanajoa (Bondar) (Acari: Tetranychidae) an exotic pest in Africa and the search for appropriate control methods: a review. Bulletin of Entomological Research 78: 1–13.

    Article  Google Scholar 

  • Yaninek, J. S., Moraes, G. J. de, & Markham, R. H. 1989. Handbook on the Cassava Green Mite (Mononychellus tanajoa) in Africa. Alphabyte, Rome.

    Google Scholar 

  • Yaninek, J. S., & Schulthess, F. 1993. Developing an environmentally sound plant protection for cassava in Africa. Agriculture, Ecosystems and Environment 46: 305–324.

    Article  Google Scholar 

  • Yaninek, J. S., Saizonou, S., Onzo, A., Zannou, I., & Gnanvossou, D. 1996. Seasonal and habitat variability in the fungal pathogens, Neozygites cf. floridana and Hirsutella thompsonii, associated with cassava mites in Benin, West Africa. Biocontrol Science and Technology 6: 23–33.

    Article  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2003 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Hajek, A.E., Junior, I.D., Butler, L. (2003). Entomopathogenic Fungi as Classical Biological Control Agents. In: Hokkanen, H.M.T., Hajek, A.E. (eds) Environmental Impacts of Microbial Insecticides. Progress in Biological Control, vol 1. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-1441-9_2

Download citation

  • DOI: https://doi.org/10.1007/978-94-017-1441-9_2

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-90-481-6100-3

  • Online ISBN: 978-94-017-1441-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics