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Models of intermediate complexity in insect-pathogen interactions: population dynamics of the microsporidian pathogen, Nosema pyrausta, of the European corn borer, Ostrinia nubilalis

Published online by Cambridge University Press:  06 April 2009

C. J. Briggs  and
H. C. J. Godfray
C. J. Briggs
Affiliation:
Department of Biology and NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire SLS 7P Y, UK
H. C. J. Godfray
Affiliation:
Department of Biology and NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire SLS 7P Y, UK
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Summary

Nosema pyrausta is an important microsporidian pathogen of the European corn-borer, Ostrinia nubilalis (Pyralidae), a major pest of corn (maize). The population dynamics of the interaction between the moth and its pathogen have been studied previously using simple models phrased as coupled differential equations, and using large simulation models containing over 150000 coupled equations. A middle approach is adopted here and the interaction studied using an age-structured model written as a system of delay-differential equations. Although the model contains twenty four parameters, estimates for twenty of these were available in the literature. Our model provides a good qualitative match to observed within and between season dynamics and suggests which aspects of the interaction are most important in determining the nature of the system's population dynamics. More generally, we argue that in the absence of better data on insect-disease interactions in natural habitats, valuable insights can be gained by studying equivalent systems in agro-ecosystems. We also argue that models of intermediate complexity that incorporate considerable detail about the natural history of individual interactions, but which are derived from the classical models of animal ecology and epidemiology, offer the most profitable way of modelling insect-pathogen interactions in the wild.

Keywords

Population dynamicsage-structurepathogeninsectOstrinia nubilalisNosema pyrausta
Type
Research Article
Information
Parasitology , Volume 111 , Supplement S1: Ecology of wildlife host-parasite interactions , January 1995 , pp. S71 - S89
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Anderson, R. M. & May, R. M. (1980). Infectious diseases and population cycles of forest insects. Science 210, 658–61.CrossRefGoogle ScholarPubMed
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
Anderson, R. M. & May, R. M. (1991). Infectious Diseases of Humans. Oxford: Oxford University Press.CrossRefGoogle Scholar
Andreadis, T. G. (1980). Nosema pyrausta infection in Macrocentrus grandii, a braconid parasite of the European corn borer, Ostrinia nubilalis. Journal of Invertebrate Pathology 35, 229–33.CrossRefGoogle Scholar
Andreadis, T. G. (1984). Epizootiology of Nosema pyrausta in field populations of the European corn borer (Lepidoptera: Pyralidae). Environmental Entomology 13, 882–7.CrossRefGoogle Scholar
Andreadis, T. G. (1986). Dissemination of Nosema pyrausta in feral populations of the European corn borer, Ostrinia nubilalis. Journal of Invertebrate Pathology 48, 335–43.CrossRefGoogle Scholar
Andreadis, T. G. (1987). Horizontal transmission of Nosema pyrausta (Microsporida: Nosematidae) in the European corn borer, Ostrinia nubilalis (Lepidoptera Pyralidae). Environmental Entomology 16, 1124–9.CrossRefGoogle Scholar
Begon, M. & Bowers, R. G. (1995). Beyond host-pathogen dynamics. In Population Biology of Infectious Diseases in Natural Populations (ed. Grenfell, B. & Dobson, A. P.), Cambridge: Cambridge University Press (1996).Google Scholar
Begon, M., Bowers, R. C., Kadianakis, N. & Hodgkinson, D. E. (1992). Disease and community Structure: the importance of host self-regulation in a host-host-pathogen model. American Naturalist 139, 1131–50.CrossRefGoogle Scholar
Blythe, S. P. & Anderson, R. M. (1988). Heterogeneous sexual-activity models of HIV transmission in male homosexual populations. IMA Journal of Mathematics Applied in Medicine and Biology 5, 237–60.CrossRefGoogle ScholarPubMed
Bottger, G. T. & Kent, V. F. (1931). Seasonal-history studies on the European corn borer in Michigan. Journal of Economic Entomology 24, 372–9.CrossRefGoogle Scholar
Bowers, R. G. & Begon, M. (1991). A host-host-pathogen model with free-living infective stages, applicable to microbial pest control. Journal of Theoretical Biology 148, 305–29.CrossRefGoogle ScholarPubMed
Bowers, R. G., Begon, M. & Hodgkinson, D. E. (1993). Host-pathogen population cycles in forest insects? Lessons from simple models reconsidered. Oikos 67, 529–38.CrossRefGoogle Scholar
Briggs, C. J. (1993). Competition among parasitoid species on a stage-structured host and its effect on host suppression. American Naturalist 141, 372–97.CrossRefGoogle Scholar
Briggs, C. J. & Godfray, H. C. J. (1995). The dynamics of insect-pathogen interactions in stage-structured populations. American Naturalist 145, 855–87.CrossRefGoogle Scholar
Briggs, C. J. & Godfray, H. C. J. (1996). The dynamics of insect-pathogen interactions in seasonal environments. Theoretical Population Biology (In Press).CrossRefGoogle ScholarPubMed
Briggs, C. J., Nisbet, R. M. & Murdoch, W. W. (1993). Coexistence of competing parasitoids on a host With a variable life cycle. Theoretical Population Biology 44, 341–73.CrossRefGoogle Scholar
Brindley, T. A. & Dicke, F. F. (1963). Significant developments in European corn borer research. Annual Review of Entomology 8, 155–76.CrossRefGoogle Scholar
Brindley, T. A., Sparks, A. N., Showers, W. B. & Guthrie, W. D. (1975). Recent research advances on the European corn borer in North America. Annual Review of Entomology 20, 221–39.CrossRefGoogle ScholarPubMed
Brown, G. C. (1984). Stability in an insect-pathogen model incorporating age-dependent immunity and seasonal host reproduction. Bulletin of Mathematical Biology 46, 139–53.CrossRefGoogle Scholar
Caffrey, D. J. & Worthley, L. H. (1927). A progress report on the investigations of the European corn borer. USDA Bulletin 1476.Google Scholar
Canning, E. U. (1982). An evaluation of protozoal characteristics in relation to biological control of pests. Parasitology 84, 119–49.CrossRefGoogle Scholar
Carruthers, R. I., Whitfield, G. H., Tummala, R. L. & Haynes, D. L. (1986). A systems-approach to research and simulation of insect pest dynamics in the onion agro-ecosystem. Ecological Modelling 33, 101–21.CrossRefGoogle Scholar
Cavalieri, L. F. & Koçak, H. (1994). Chaos in biological control systems. Journal of Theoretical Biology 169, 179–87.CrossRefGoogle Scholar
Chaing, H. C. (1964). Overwintering corn borer larvae in storage cribs. Journal of Economic Entomology 57, 666–9.CrossRefGoogle Scholar
Dwyer, G. (1994). Density-dependence and spatial structure in the dynamics of insect pathogens. American Naturalist 143, 533–62.CrossRefGoogle Scholar
Dwyer, G. & Elkinton, J. S. (1993). Using simple models to predict virus epizootics in gypsy moth populations. Journal of Animal Ecology 62, 1–11.CrossRefGoogle Scholar
Godfray, H. C. J. (1995). Field experiments with genetically manipulated insect viruses: ecological issues. Trends in Ecology and Evolution 16, 1124–29.Google Scholar
Godfray, H. C. J. & Briggs, C. J. (1995). The population dynamics of pathogens that control insect outbreaks. Journal of Theoretical Biology 176, 125–36.CrossRefGoogle Scholar
Godfray, H. C. J. & Chan, M. S. (1990). How insecticides trigger single-stage outbreaks in tropical pests. Functional Ecology 4, 329–37.CrossRefGoogle Scholar
Godfray, H. C. J. & Hassell, M. P. (1987). Natural enemies may be a cause of discrete generations in tropical insects. Nature 327, 144–7.CrossRefGoogle Scholar
Godfray, H. C. J. & Hassell, M. P. (1989). Discrete and continuous insect populations in tropical environments. Journal of Animal Ecology 58, 153–74.CrossRefGoogle Scholar
Godfray, H. C. J., Hassell, M. P. & Holt, R. D. (1994). The population dynamic consequences of phenological asynchrony between parasitoids and their hosts. Journal of Animal Ecology 62, 1–10.CrossRefGoogle Scholar
Godfray, H. C. J. & Waage, J. K. (1991). Predictive modelling in biological control: the Mango Mealy Bug (Rastrococcus invadens) and its parasitoids. Journal of Applied Ecology 28, 434–53.CrossRefGoogle Scholar
Gordon, D. M., Nisbet, R. M., De Roos, A., Gurney, W. S. C. & Stewart, R. K. (1991). Discrete generations in host-parasitoid models With contrasting life cycles. Journal of Animal Ecology 60, 295–308.CrossRefGoogle Scholar
Gurney, W. S. C., Nisbet, R. M. & Lawton, J. H. (1983). The systematic formulation of tractable single-species population models incorporating age structure. Journal of Animal Ecology 52, 479–96.CrossRefGoogle Scholar
Gurney, W. S. C. & Tobia, s. (1994). Solver Rev. 4.41, A program template for initial value problems expressible as sets of coupled ordinary or delay differential equations. STAMS, University of Strathclyde, Glasgow.Google Scholar
Hassell, M. P. (1978). The Dynamics of Arthropod Predator-Prey Systems. Princeton: Princeton University Press.Google ScholarPubMed
Hill, H. E. & Gary, W. J. (1979). Effects of the Microsporidium, Nosema pyrausta, on field populations of European corn borer in Nebraska. Environmental Entomology 8, 91–5.CrossRefGoogle Scholar
Hochberg, M. E. (1989). The potential role of pathogens in biological control. Nature 337, 262–5.CrossRefGoogle ScholarPubMed
Hochberg, M., Hassell, M. P. & May, R. M. (1990). The dynamics of host-parasitoid-pathogen interactions. American Naturalist 135, 74–94.CrossRefGoogle Scholar
Hochberg, M. E. & Holt, R. D. (1990). The coexistence of competing parasites: I. The role of cross-species infection. American Naturalist 136, 517–41.CrossRefGoogle Scholar
Holt, R. D. & Pickering, J. (1985). Infectious disease and species coexistence: a model of Lotka–Volterra form. American Naturalist 126, 196–211.CrossRefGoogle Scholar
Jarvis, J. L. & Guthrie, W. D. (1987). Ecological studies of the European corn borer (Lepidoptera: Pyralidae) in Boone county, Iowa. Environmental Entomology 16, 50–8.CrossRefGoogle Scholar
Kramer, J. P. (1959 a). Observations on the seasonal incidences of microsporidiosis in European corn borer populations in Illinois. Entomophaga 4, 37–42.CrossRefGoogle Scholar
Kramer, J. p (1959 b). Some relationships between Perezia pyraustae Paillot (Sporozoa, Nosematidae) and Perezia nubilalis (Hübner) (Lepidoptera, Pyralidae). Journal of Insect Pathology 1, 25–33.Google Scholar
Lewis, L. C. & Lynch, R. E. (1976). Influence on the European corn borer on Nosema pyrausta and resistance in maize to leaf feeding?. Environmental Entomology 5, 139–46.CrossRefGoogle Scholar
Matteson, J. W. & Decker, G. C. (1965). Development of the European corn borer at controlled constant and variable temperatures. Journal of Economic Entomology 58, 344–9.CrossRefGoogle Scholar
Murdoch, W. W., Nisbet, R. M., Gurney, W. S. C. & Reeve, J. D. (1987). An invulnerable age class and stability in delay-differential parasitoid-host models. American Naturalist 129, 263–82.CrossRefGoogle Scholar
Murdoch, W. W., Nisbet, R. M., Luck, R. F., Godfray, H. C. J. & Gurney, W. S. C. (1992). Size-selective sex-allocation and host feeding in a parasitoid-host model. Journal of Animal Ecology 61, 533–41.CrossRefGoogle Scholar
Nisbet, H. M. & Gurney, W. S. C. (1983). The systematic formulation of population models for insects With dynamically varying instar duration. Theoretical Population Biology 23, 114–35.CrossRefGoogle Scholar
Onstad, D. W. & Carruthers, R. I. (1990). Epizootiological models of insect diseases. Annual Review of Entomology 35, 399–419.CrossRefGoogle Scholar
Onstad, D. W. & Maddox, J. V. (1989). Modelling the effects of the microsporidium, Nosema pyrausta, on the population dynamics of the insect, Ostrinia nubilalis. Journal of Invertebrate Pathology 53, 410–21.CrossRefGoogle Scholar
Onstad, D. W., Maddox, J. V., Cox, D. J. & Kornkven, E. A. (1990). Spatial and temporal dynamics of animals and the host-density threshold in epizootiology. Journal of Invertebrate Pathology 55, 76–84.CrossRefGoogle Scholar
Onstad, D. W., Siegel, J. P. & Maddox, J. V. (1991). Distribution of parasitism by Macrocentrus grandii (Hymenoptera: Braconidae) in maize infected by Ostrinia nubilalis (Lepidoptera: Pyralidae). Environmental Entomology 20, 156–9.CrossRefGoogle Scholar
Régnière, J. (1984). Vertical transmission of diseases and population dynamics of insects With discrete generations: a model. Journal of Theoretical Biology 107, 287–301.CrossRefGoogle Scholar
Rohani, P., Godfray, H. C. J. & Hassell, M. P. (1994). Aggregation and the dynamics of host-parasitoid systems: a discrete generation model with within generation redistribution. American Naturalist 144, 491–509.CrossRefGoogle Scholar
Sajap, A. S. & Lewis, L. C. (1988). Histopathology of trans-ovarial transmission of Nosema pyrausta in the European corn borer, Ostrinia nubilalis. Journal of Invertebrate Pathology 52, 147–53.CrossRefGoogle Scholar
Sajap, A. S. & Lewis, L. C. (1992). Chronology of infection of European corn borer (Lepidoptera: Pyralidae) With the microsporidium Nosema pyrausta: effects of development and vertical transmission. Environmental Entomology 21, 178–82.CrossRefGoogle Scholar
Showers, W. B., Rozari, M. B., Reed, G. L. & Shaw, R. H. (1978). Temperature-related climatic effects on survival of the European corn borer. Environmental Entomology 7, 717–23.CrossRefGoogle Scholar
Siegel, J. P., Maddox, J. V. & Ruesink, W. G. (1986 a). Impact of Nosema pyrausta on a Braconid, Macrocentrus grandii, in Central Illinois. Journal of Invertebrate Pathology 47, 271–6.CrossRefGoogle Scholar
Siegel, J. P., Maddox, J. V. & Ruesink, W. G. (1986 b). Lethal and sublethal effects of Nosema pyrausta on the European corn borer (Ostrinia nubilalis) in Central Illinois. Journal of Invertebrate Pathology 48, 167–73.CrossRefGoogle Scholar
Siegel, J. P., Maddox, J. V. & Ruesink, W. G. (1988). Seasonal progress of Nosema pyrausta in the European corn borer, Ostrinia nubilalis. Journal of Invertebrate Pathology 52, 130–6.CrossRefGoogle Scholar
Solter, L. F., Onstad, D. W. & Maddox, J. V. (1990). Timing of disease-induced processes in the life cycle of Ostrinia nubilalis infected With Nosema pyrausta. Journal of Invertebrate Pathology 55, 337–41.CrossRefGoogle Scholar
Vezina, S. A. & Peterman, R. M. (1985). Tests of the role of a nuclear polyhedrosis virus in the population dynamics of its host, Douglas-fir tussock moth, Orgyia pseudotsugata (Lepidoptera: Lymantriidae. Oecologia 67, 260–6.CrossRefGoogle ScholarPubMed
Windels, M. B., Chiang, H. C. & Furgala, B. (1976). Effects of Nosema pyrausta on pupal and adult stages of the European corn borer, Ostrinia nubilalis. Journal of Invertebrate Pathology 27, 239–42.CrossRefGoogle Scholar
Zimmack, H. L., Arbuthnot, K. D. & Brindley, T. A. (1954). Distribution of the European corn borer parasite, Perezia pyraustae, and its effect on the host. Journal of Economic Entomology 20, 637–40.Google Scholar