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Theoretical basis for the use of pathogens as biological control agents of pest species

Published online by Cambridge University Press:  06 April 2009

R. M. Anderson
R. M. Anderson
Affiliation:
Department of Pure and Applied Biology, Imperial College, London University, London SW 7 2BB
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Summary

The population dynamics of insect–pathogen interactions are examined with the aid of simple mathematical models. Three concepts of central importance to the interpretation of population behaviour are discussed, namely the ability of the pathogen to persist within its host population, the ability to regulate and depress host population abundance, and the ability to induce non-seasonal cyclic changes in host density. The selection of pathogen species or strains to depress pest population growth is discussed and the optimal characteristics are shown to be intermediate pathogencity combined with an ability to reduce infected host reproduction, high transmission efficiency, including elements of vertical as well as horizontal transmission stages. When the pathogen plays a significant role in the regulation of host population growth, it is argued that many insect–pathogen interactions will exhibit non-seasonal oscilations in host and pathogen abundance. Mathematical models are used to explore the patterns of population behaviour that result from the continual introduction of a pathogen into a target pest population. It is shown that there exists a critical introdution rate, above which the eradication of the pest is theoretically possible. Significant reductions in pest population abundance will not occur until the introduction rate approaches this critical value, whereupon the oscillatory behaviour of the interaction between host and pathogen population will be suppressed.

A general dicussion is given of the problems arising from the combined use of chemical agents and pathogens for the control of pest species, and the evolutionary pressures acting on host and pathogen populations.

Type
Research Article
Information
Parasitology , Volume 84 , Issue 4 , April 1982 , pp. 3 - 33
Copyright
Copyright © Cambridge University Press 1982

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References

Anderson, R. M. (1979 a). The influence of parasitic infection on the dynamics of host population growth. In Population Dynamics (ed. Anderson, R. M., Turner, B. D. and Taylor, L. R.), pp. 245–281. Oxford: Blackwell Scientific Publications.Google Scholar
Anderson, R. M. (1979 b). Parasite pathogenicity and the depression of host population equilibria. Nature, London 279, 150–2.CrossRefGoogle Scholar
Anderson, R. M. (1981). Infectious disease agents and cyclic fluctuations in host abundance. In The Mathematical Theory of the Dynamics of Biological Populations, vol. 2 (ed. Hiorns, R. W. and Cooke, D.), pp. 47–80. London: Academic Press.Google Scholar
Anderson, R. M. (1982). Verterate populations, pathogens and the immune system. In Population and Biology. International Union for the Scientific Study of Population. (In the Press.)Google Scholar
Anderson, R. M. & May, R. M. (1979). Population biology of infectious diseases: I. Nature, London 280, 361–7.CrossRefGoogle Scholar
Anderson, R. M. & May, R. M. (1980). Infectious diseases and population cycles of forest insects. Science 210, 658–61.Google Scholar
Anderson, R. M. & May, R. M. (1981). The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London B 291, 451–524.Google Scholar
Andreadis, T. G. & Hall, D. W. (1979). Significance of transovarial infections of Amnblysopora sp. (Microspora: Thelohaniidae) in relation to parasite maintenance in the mosquito Culex salinarius Coquillett. Journal of Invertebrate Pathology 34, 152–7.CrossRefGoogle Scholar
Auer, C. (1968). Erste Ergebnisse einfacher stochastischer Modelluntersuchungen über die Ursachen der Populations Bewegung des grauen Larchenwicklers Zeiraphera diniana, Gn. (= Z. griseana Hb) im Oberengadin, 1949/66. Zeitschrifi für Angewandte Entomologie 62, 202–35.CrossRefGoogle Scholar
Bang, F. B. (1975). Comparison of immune mechanisms in vertebrates and invertebrates. In Invertebrate Immunity (ed. Maramorosch, K. and Shope, R. E.), pp. 355–7. New York and London: Academic Press.Google Scholar
Baugher, D. G. & Yendol, W. G. (1981). Virulence of Autographa californica baculovirus preparations fed with different food sources to cabbage loopers. Journal of Economic Entomology 74, 309–13.CrossRefGoogle Scholar
Bird, F. T. & Whalen, M. M. (1954). A nuclear and cytoplasmic polyhedral virus disease of the spruce budworm. Canadian Journal of Zoology 32, 83–6.CrossRefGoogle Scholar
Briese, D. T. & Mende, H. A. (1981). Differences in susceptibility to a granulosis virus between field populations of the potato moth, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae). Bulletin of Entomological Research 71, 11–18.CrossRefGoogle Scholar
Burges, H. D., Canning, E. U. & Hurst, J. A. (1971). Morphology, development and pathogenicity of Nosema oryzaephili n.sp. in Oryzaephilus surinamensis and its host range among granivorous insects. Journal of Invertebrate Pathology 17, 419–32.CrossRefGoogle Scholar
Burges, H. D. & Hurst, J. A. (1977). Ecology of Bacillus thuringiensis in storage moths. Journal of Invertebrate Pathology 30, 131–9.Google Scholar
Canning, E. U. (1981). Insect Control with Protozoa. In Biological Control in Crop Production, Beltsville Agricultural Research Center Symposium No. 5, (ed. Papavizas, G. C.) (in press). New Jersey: Allanheld Osmun Company.Google Scholar
Carpenter, S. R. (1981). Effect of control measure on pest populations subject to regulation by parasites and pathogens. Journal of Theoretical Biology 92, 181–9.CrossRefGoogle ScholarPubMed
Cole, R. J. (1970). The application of the ‘triangulation’ method of the purification of Nosema spores from insect tissue. Journal of Invertebrate Pathology 15, 193–5.CrossRefGoogle Scholar
Crawford, A. M. & Kalmakoff, J. (1977). A host–virus interaction in a pasture habitat. Wiseana spp (Lepidoptera: Hepialidae) and its baculoviruses. Journal of Invertebrate Pathology 29, 81–7.CrossRefGoogle Scholar
David, W. A. L. (1965). The granulosis of Pieris brassicae L. in relation to natural limitation and biological control. Annals of Applied Biology 5, 331–4.Google Scholar
David, W. A. L. & Gardiner, D. O. C. (1967). The persistence of a granulosis virus of Pieris brassicae in soil and in sand. Journal of Invertebrate Pathology 9, 342–7.CrossRefGoogle Scholar
Davidson, E. W., Sweeney, A. W. & Cooper, R. (1981). Comparative field trials of Bacillus sphaericus strain 1593 and B. thuringiensis var. israelensis commercial powder formulations. Journal of Economic Entomology 74, 350–4.CrossRefGoogle Scholar
Dietz, K. (1975). Transmission and control of arbovirus diseases. In: Epidemiology (ed. Ludwig, D. and Cooke, K. L.), pp. 104–121. Proceedings of the Society for Industrial and Applied Mathematics, Philadelphia.Google Scholar
Dietz, K. (1976). The incidence of infectious diseases under the influence of seasonal fluctuations. In Mathematical Models in Medicine (ed. Berger, J., Buhler, W., Repges, R. and Tautu, P.), pp. 1–15. Lecture Notes in Biomathematics, vol. 11. Berlin: Springer Verlag.CrossRefGoogle Scholar
Doane, C. C. (1967). Bioassay of nuclear-polyhedrosis virus against larval instars of the Gypsy Moth. Journal of Invertebrate Pathology 9, 376–86.CrossRefGoogle ScholarPubMed
Finlayson, L. H. (1950). Mortality of Laemophloeus (Coleoptera, Cucujidae) injected with Mattesia dispora Naville (Protozoa, Schizogregarinaria). Parasitology 40, 261–4.CrossRefGoogle Scholar
Gilmore, J. E. & Tashiro, H. (1966). Fecundity, longevity and transinfectivity by Citrus Red Mites (Panorychus citri) infected with a noninclusion virus. Journal of Invertebrate Pathology 8, 334–9.Google Scholar
Granados, R. R. (1976). Infection and replication of insect pathogenic viruses in tissue culture. Advances in Virological Research 20, 189–233.CrossRefGoogle ScholarPubMed
Hamm, J. J. (1980). Epizootic of Entomorphthora aulicae in Lepidopterous pests of Sorghum. Journal of Invertebrate Pathology 36, 60–3.CrossRefGoogle Scholar
Harrap, K. A. (1978). The pesticidal use of viruses. Lab-Lore 7, 481–3.Google Scholar
Hembree, S. C., Meisch, M. V. & Williams, D. (1980). Field test of Bacillus thuringiensis var israelensis against Psorophora columbiae larvae in small rice plots. Mosquito News 40, 67–70.Google Scholar
Henry, J. E. (1972). Experimental application of Nosema locustae for control of grasshoppers. Journal of Invertebrate Pathology 18, 389–94.CrossRefGoogle Scholar
Henry, J. E. (1978). Microbial control of grasshoppers with Nosema locustae Canning. Miscellaneous Publications of the Entomological Society of America 11, 85–95.Google Scholar
Henry, J. E. & Oma, E. A. (1974). Effect of prolonged storage of spores on field applications of Nosema locustae (Microsporida: Nosematidae) against grasshoppers. Journal of Invertebrate Pathology 23, 371–7.CrossRefGoogle ScholarPubMed
Ignoffo, C. M., Marston, N. L., Hostetler, D. L., Puttler, B. & Bell, J. V. (1976). Natural and induced epizootics of Nomuraea rileyi in Soybean caterpillars. Journal of Invertebrate Pathology 27, 191–8.CrossRefGoogle Scholar
Ives, W. G. H. & Cunningham, J. C. (1980). Application of nuclear-polyhedrosis virus to control Bruce spanworm (Lepidoptera:geometridae). The Canadian Entomologist 112, 741–4.CrossRefGoogle Scholar
Jaques, R. P. (1967 a). The persistence of a nuclear-polyhedrosis virus in the habitat of the host insect. I. Polyhedra deposited on foliage. Canadian Entomologist 99, 785–94.CrossRefGoogle Scholar
Jaques, R. P. (1967 b). The persistence of a nuclear-polyhedrosis virus in the habitat of the host insect. II. Polyhedra in soil. Canadian Entomologist 99, 820–9.CrossRefGoogle Scholar
Kellen, W. R. & Lindegren, J. E. (1973). Transovarian transmission of Nosema plodiae in the Indian-meal moth, Plodia interpunctella. Journal of Invertebrate Pathology 21, 248–54.Google Scholar
Lacey, L. A. & Mulla, M. S. (1977). Evaluation of Bacillus thuringiensis as a biocide of blackfly larvae (Diptera:Simuliidae). Journal of Invertebrate Pathology 30, 46–9.Google Scholar
Lackie, A. M. (1980). Invertebrate immunity. Parasitology 80, 393–412.Google Scholar
Le Conte, J. L. (1874). Hints for the promotion of economic entomology. American Association for the Advancement of Science Proceedings 22, 10–22.Google Scholar
Lewis, F. B. (1971). Mass propagation of insection viruses with special reference to forest insects. pp. 320–326. In Proceedings of the 4th International Coloquium on Insect Pathology. College Park, Maryland.Google Scholar
Macdonald, G. (1965). The dynamics of helminth infections, with special reference to schistosomes. Transactions of the Royal Society of Tropical Medicine and Hygiene 59, 489–501.CrossRefGoogle ScholarPubMed
Maramorosch, K. & Shope, R. E. (1975). Invertebrate Immunity. New York: Academic Press.Google Scholar
Martignoni, M. E. (1957). Contributo alia conoscenza di una granulosi di Eucosma grieseana (Hubner) (Tortricidae: Lepidoptera) quale fattori limitante il pullulamento dellinsetto nella Engadina alta. Mitteilungen der Schweizerischen (Zentral) anstalt für das forstliche Versuchswesen 32, 371–418.Google Scholar
Martignoni, M. E. & Schmid, P. (1961). Studies on the resistance to virus infections in natural populations of Lepidoptera. Journal of Insect Pathology 3, 62–74.Google Scholar
May, R. M. & Anderson, R. M. (1979). Population biology of infectious diseases Part II. Nature, London 280, 455–61.CrossRefGoogle ScholarPubMed
McGaughey, W. H. (1976). Bacillus thuringiensis for controlling three species of moths in stored grain. Canadian Entomologist 108, 105–12.Google Scholar
McIntyre, T. & Dutky, S. R. (1961). Aerial application of virus for control of a pine sawfly Neodiprion pratti pratti (Dyar). Journal of Economic Entomology 54, 809–10.CrossRefGoogle Scholar
Metchnikoff, E. (1880). Zur Lehre über Insectenkrankheiten. Zoologischer Anzeiger 3, 44–7.Google Scholar
Milner, R. J. (1977). The role of disease during an outbreak of Oncopera alboguttata Tindale and O. rufobrunnae Tindale (Lepidoptera: Heplialidae) in the Ebor/Dorrigo region of N.S.W. Journal of the Australian Entomological Society 16, 21–6.Google Scholar
Milstead, J. E., Odom, D. & Kirby, M. (1980). Control of early larval stages of the California oakworm by low concentrations of Bacillus thuringiensis applied to lower leaf surfaces. Journal of Economic Entomology 73, 344–5.CrossRefGoogle Scholar
Molloy, D. & Jamnback, H. (1981). Field evaluation of Bacillus thuriengiensis var israelensis as a Black fly biocontrol agent and its effect on nontarget stream insects. Journal of Economic Entomology 74, 314–18.Google Scholar
Morris, R. F. (1963). The dynamics of epidemic Spruce Budworm populations. Memoirs of the Entomological Society of Canada 32, 1–332.Google Scholar
Mulligan, F. S., Schaefer, C. H. & Miura, T. (1978). Laboratory and field evaluation of Bacillus sphaericus as a mosquito agent. Journal of Economic Entomology 71, 774–7.Google Scholar
Park, T. (1948). Experimental studies of interspecies competition. I. Competition between populations of the flour beetles Tribolium confusum (Duval) and Tribolium cansteneum (Herbst). Ecological Monographs 18, 207–307.Google Scholar
Pasteur, L. (1870). Etudes sur la maladie des ver a soie, vol. 1. Paris: Gauthier-Villars.Google Scholar
Pinnock, D. E., Garcia, R. & Cubbin, C. M. (1973). Beauveria tenella as a control agent for mosquito larvae Journal of Invertebrate Pathology 22, 143–7.CrossRefGoogle ScholarPubMed
Raun, E. S., Sutter, G. R. & Revelo, M. A. (1966). Ecological factors affecting the pathogenicity of Bacillus thuringiensis var thuringiensis to the European corn borer and Fall armyworm. Journal of Invertebrate Pathology 8, 365–75.CrossRefGoogle Scholar
Shapiro, M., Owens, C. P., Bell, R. A. & Wood, H. A. (1981). Simplified, efficient system for in vivo mass production of Gypsy Moth nucleo polyhedrosis virus. Journal of Economic Entomology 74, 341–3.Google Scholar
Smirnoff, W. A. (1967). Effect of gamma radiation on the larvae and the nuclear polyhedrosis virus of the eastern tent caterpillar, Malacosoma americanium. Journal of Invertebrate Pathology 9, 264–6.CrossRefGoogle Scholar
Smith, K. M. (1976). Virus–insect Relationships. London: Longman.Google Scholar
Stairs, G. (1972). Pathogenic microrganisms in the regulation of forest insect populations. Annual Review of Entomology 17, 355–72.CrossRefGoogle Scholar
Steinhaus, E. A. (1958). Stress as a factor in insect disease. Proceedings of the 10th Interntional Congress of Entomology 4, 725–30.Google Scholar
Summers, M. D., Engler, R., Falcon, L. A. & Vail, P. V. (1975). Baculoviruses for insect pest control: safety considerations. Selected papers from EPA–USDA Working Symposium,Bethesda,American Society for Microbiology.Google Scholar
Tanada, Y. (1964). Epizootiology of insect diseases. In: Biological Control of Insect Pests and Weeds (ed. DeBach, P.), pp. 548–578. London: Chapman and Hall.Google Scholar
Tanada, Y. & Omi, E. M. (1974). Persistence of insect viruses in field populations of alfalfa insects. Journal of Invertebrate Pathology 23, 360–5.CrossRefGoogle ScholarPubMed
Tinsley, T. W. (1979). The potential of insect pathogenic viruses as pesticidal agents. Annual Review of Entomology 24, 63–87.Google Scholar
Thomas, D. E., Reichelderfer, C. F. & Heimpel, A. M. (1972). Accumulation and persistence of a nuclear-polyhedrosis virus of the cabbage looper in the field. Journal of Invertebrate Pathology 20, 157–64.Google Scholar
Thompson, C. G. & Scott, D. W. (1979). Production and persistence of the nuclear-polyhedrosis virus of the Douglas-fir tussock moth, Orgyia pseudotsugata (Lepidoptera: Lymantriidae) in the forest ecosystem. Journal of Invertebrate Pathology 33, 57–65.Google Scholar
Thomson, H. M. (1958). The effect of a microsporidian parasite on the development, reproduction and mortality of the spruce budworm, Choristoneura fumiferana (Clem). Canadian Journal of Zoology 36, 499–511.CrossRefGoogle Scholar
Undeen, A. H. & Nagel, W. L. (1978). The effect of Bacillus thuringiensis ONR-60A strain (Goldberg) on Simulium larvae in the laboratory. Mosquito News 38, 524–7.Google Scholar
Undeen, A., Takaoka, H. & Hansen, K. (1981). A test of Bacillus thuringiensis var. israelensis De Barjac as a larvicide for Simulium ochraceum, the Central American vector of onchocerciasis. Mosquito News 41, 37–40.Google Scholar
Vail, P. V., Seay, R. E. & De Borr, J. (1981). Microbial and chemical control of cabbage looper on fall lettuce. Journal of Economic Entomology 73, 72–5.CrossRefGoogle Scholar
Varley, G. C., Gradwell, G. R. & Hassell, M. P. (1973). Insect Population Ecology: an Analytical Approach. Oxford: Blackwell Scientific Publications.Google Scholar
World Health Organization (1980). The programme of research on the biological control of vectors of diseases of the World Health Organization. Present status and plans for the future. WHO Report, Geneva.Google Scholar
Wraight, S. P., Molloy, D. & Jamnback, H. (1981). Efficacy of Bacillus sphaericus strain 1593 against the four instars of laboratory reared and field collected Culex pipiens pipiens and laboratory reared Culex salinarius. Canadian Entomologist 113, 379–86.Google Scholar
Zelazny, B. (1973). Studies on Rhabdionvirus oryctes. II. Effect on adults oryctes rhinoceros. Journal of Invertebrate Pathology 22, 122–6.Google Scholar
Zethner, O. (1980). Control of Agrotis segetum(Lep.: Noctuidae) root crops by granulosis virus. Entomorphaga 25, 27–35.CrossRefGoogle Scholar