Ecological theory and biological control

  • William W. Murdoch
Part of the Monographiae Biologicae book series (MOBI, volume 67)


Successful classical biological control in long-lived ecosystems occurs when an imported natural enemy keeps the density of the alien pest insect below the density at which it causes economic damage. It has been generally accepted for some 75 years that such enemies establish a low stable equilibrium pest density and maintain it by imposing density-dependent mortality on the pest. In recent years it has been suggested that success typically involves aggregation by the enemy, perhaps to those patches that contain more pests. This theory is embodied in Nicholson-Bailey models of the parasitoid-host interaction.

This chapter reviews this body of theory and compares it with real systems. It appears, at least in some cases, that the basic premise of the theory — a stable interaction on the small scale — does not hold. In the few examples studied, it also appears that the mechanisms proposed in the models, including aggregation, do not account for control. In the one apparently stable system studied — red scale on citrus controlled by the parasitoid Aphytis — a refuge may be the key stabilizing factor; otherwise this interaction also has features implying instability. In another case the maintenance of a pest weed (ragwort) in the face of enemies driving it extinct may depend upon an invulnerable pest stage (the seed bank).

Few real systems have been analyzed and it should not be assumed that the above results hold in general. Stability may be common in some circumstances, and it seems likely that aggregation to local pest density will be important in some instances.

There is a strong trade-off between stability and degree of pest suppression in the Nicholson-Bailey models discussed. The trade-off is associated with the lack of within-generation dynamics in these models: stability arises from density dependence in the parasitoid (decreasing efficiency with increasing parasitoid density) rather than in the pest. This process operates and the trade-off is severe even when the parasitoid aggregates to patches that (initially) contain more pests. By contrast, such aggregation in a model that allows the parasitoids to redistribute themselves in response to the continually-changing pest distribution results in better control, but can also be destabilizing.

The consequences of these results for biological control in theory and practice are discussed. More work is needed to expose the mechanisms operating in real examples of successful control. For systems in which control involves local instability, further modeling of ensemble dynamics should help pinpoint possible key features that may allow both regional persistence of the system and consistently low pest densities.


Biological Control Natural Enemy Density Dependence Ecological Theory Pest Population 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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Literature cited

  1. Bailey, V. A., A. J. Nicholson, and E. J. Williams. 1962. Interactions between hosts and parasites when some host individuals are more difficult to find than others. J. Theor. Biol. 3:1–18.Google Scholar
  2. Banks, C. J. 1957. The behaviour of individual coccinellid larvae on plants. British J. Anim. Behav. 5:12–24.CrossRefGoogle Scholar
  3. Beddington, J. R., C. A. Free, and J. H. Lawton. 1978. Characteristics of successful enemies in models of biological control of insect pests. Nature 273:513–519.PubMedCrossRefGoogle Scholar
  4. Chesson, P. L. 1978. Predator-prey theory and variability. Ann. Rev. Ecol. Syst. 9: 323–347.CrossRefGoogle Scholar
  5. Chesson, P. L. 1984a. The storage effect in stochastic population models. In Lecture Notes in Biomathematics (Ed. by S. A. Levin and T. G. Hallam), 54: 76–89. Springer-Verlag, New York.Google Scholar
  6. Chesson, P. L. 1984b. Persistence of a markovian population in a patchy environment. Z. Wahrscheinlichkeitstheorie und verwandte Gebiete 66: 97–107.CrossRefGoogle Scholar
  7. Chesson, P. L. and W. W. Murdoch. 1986. Aggregation of risk: relationships among host-parasitoid models. Amer. Nat. 127: 696–715.CrossRefGoogle Scholar
  8. Clausen, C. P. (ed.) 1978. Introduced parasites and predators of arthropods and weeds: a world review. U.S.D.A. Agricultural Handbook No. 480.Google Scholar
  9. Comins, H. N. and M. P. Hassell. 1979. The dynamics of optimally foraging predators and parasitodis. J. Anim. Ecol. 48: 335–351.CrossRefGoogle Scholar
  10. Crowley, P. H. 1981. Dispersal and the stability of predator-prey interactions. Amer. Nat. 118: 673–701.CrossRefGoogle Scholar
  11. Dempster, J. P. 1982. The ecology of the cinnabar moth, Tyria Jacobaeae L. (Lepidoptera: Arctiidae). Advances in Ecological Research 12: 1–36.Google Scholar
  12. Embree, D. G. 1966. The role of introduced parasites in the control of the winter moth in Nova Scotia. Can. Ent. 98:1159–1168.CrossRefGoogle Scholar
  13. Free, C. A., J. R. Beddington, and J. H. Lawton. 1977. On the inadequacy of simple models of mutual interference for parasitism and predation. J. Anim. Ecol. 46: 543–554.CrossRefGoogle Scholar
  14. Goh, B. S. 1980. Management and Analysis of Biological Populations. Elsevier, New York.Google Scholar
  15. Hassell, M. P. 1978. The Dynamics of Anthropod Predator-Prey Systems. Princeton University Press, Princeton.Google Scholar
  16. Hassell, M. P. 1984. Parasitism in patchy environments: inverse density dependence can be stabilizing. IMA J. Math. Appl. Med. Biol. 1:123–133.PubMedCrossRefGoogle Scholar
  17. Hassell, M. P. and R. M. May. 1973. Stability in insect host-parasite models. J. Anim. Ecol. 43: 567–594.Google Scholar
  18. Hassell, M. P. and R. M. May. 1974. Aggregation in predators and insect parasites and its effect on stability. J. Anim. Ecol. 42:693–736.Google Scholar
  19. Hassell, M. P. and G. C. Varley. 1969. New inductive population model for insect parasites and its bearing on biological control. Nature 223:1133–1136.PubMedCrossRefGoogle Scholar
  20. Hassell, M. P., J. K. Waage, and R. M. May. 1983. Variable parasitoid sex ratios and their effect on host-parasitoid dynamics. J. Anim. Ecol. 52: 889–904.CrossRefGoogle Scholar
  21. Hastings, A. 1977. Spatial heterogeneity and the stability of predator-prey systems. Theor. Pop. Biol. 12:37–48.CrossRefGoogle Scholar
  22. Hastings, A. 1983. Age-dependent predation is not a simple process. I. Continuous time models. Theor. Popul. Biol. 23: 347–362.CrossRefGoogle Scholar
  23. Hastings, A. 1984. Delays in recruitment at different trophic levels: effects on stability. J. Math. Biol. 21: 35–44.PubMedGoogle Scholar
  24. Howard, L. O. and W. F. Fiske. 1911. The importation into the United States of the parasites of the gipsy-moth and the brown-tail moth. Bull, of Bureau of Ent., U.S. Dept. of Agriculture 91:1–312.Google Scholar
  25. Kareiva, P. 1984. Predator-prey dynamics in spatially structured populations: manipulating dispersal in a coccinellid-aphid interaction. In Lecture Notes in Biomathematics (ed. by S. A. Levin and T. G. Hallam), 54: 368–389. Springer-Verlag, New York.Google Scholar
  26. May, R. M. 1978. Host-parasitoid systems in patchy environments: a phenomenological model. J. Anim. Ecol. 47: 833–844.CrossRefGoogle Scholar
  27. McEvoy, P. B. 1987. Depression in ragwort Senecio jacobaea abundance following introduction of Tyria jacobaca and Longitarsus jacobaea on the central coast of Oregon. Proc. VI Int. Symp. Biol. Contr. Weeds, Vancouver.Google Scholar
  28. McNair, J. N. 1986. The effects of refuges on predator-prey interactions: a reconsideration. Theor. Pop. Bio. 29: 38–63.CrossRefGoogle Scholar
  29. Murdoch, W. W. 1979. Predation and the dynamics of prey populations. Fortschritte der Zoologie 25: 295–310.Google Scholar
  30. Murdoch, W. W. and A. Oaten. 1975. Predation and population stability. Advances in Ecological Research 9: 1–131.CrossRefGoogle Scholar
  31. Murdoch, W. W. and A. Stewart-Oaten. 1989. Aggregation by parasitoids and predators: effects on equilibrium and stability. Amer. Nat. 134: 288–310.CrossRefGoogle Scholar
  32. Murdoch, W. W., J. D. Reeve, C. B. Huffaker, and C. E. Kennett. 1984. Biological control of scale insects and ecological theory. Amer. Nat. 123: 371–392.CrossRefGoogle Scholar
  33. Murdoch, W. W., J. Chesson, and P. L. Chesson. 1985. Biological control in theory and practice. Amer. Nat. 125: 344–366.CrossRefGoogle Scholar
  34. Murdoch, W. W., R. M. Nisbet, W. S. C. Gurney, and J. D. Reeve. 1987. An invulnerable age class and stability in delay-differential parasitoid-host models. Amer. Nat. 129: 263–282.CrossRefGoogle Scholar
  35. Nachman, G. 1987a. Systems analysis of acarine predator-prey interactions. I. A stochastic simulation model of spatial processes. J. Anim. Ecol. 56: 247–265.CrossRefGoogle Scholar
  36. Nachman, G. 1987b. Systems analysis of acarine predator-prey interactions. II. The role of spatial processes in system stability. J. Anim. Ecol. 56: 267–281.CrossRefGoogle Scholar
  37. Nicholson, A. J. and V. A. Bailey. 1935. The balance of animal populations. Proc. Zool. Soc. Lond.: 551–598.Google Scholar
  38. Oaten, A. 1977. Transit time and density dependent predation in a patchily distributed prey. Amer. Nat. 111:1061–1075.CrossRefGoogle Scholar
  39. Reeve, J. D. 1988. Environmental variability, migration, and persistence in host-parasitoid systems. Amer. Nat. 132: 810–836.CrossRefGoogle Scholar
  40. Reeve, J. D. and W. W. Murdoch. 1985. Aggregation by parasitoids in the successful control of the California red scale: A test of theory. J. Anim. Ecol. 54: 797–816.CrossRefGoogle Scholar
  41. Reeve, J. D. and W. W. Murdoch. 1986. Biological control by the parasitoid Aphytis melinus, and population stability of the California red scale. J. Anim. Ecol.Google Scholar
  42. Sabelis, M. W. and W. E. M. Laane. 1986. Regional dynamics of spider-mite populations that become extinct locally because of food source depletion and predation by phytoseiid mites (Acarina: Tatranychidae, Phytoseiidae). In J. A. J. Metz and O. Diekmann (Eds). Dynamics of Physiologically Structured Populations. Springer-Verlag, Berlin.Google Scholar
  43. Smith, A. D. M. and D. A. Maelzer. 1987. Aggregation of parasitoids and density independence of parasitism in filed populations of the wasp Aphytis melinus and its host, the red scale Aonidiella aurantii. Eco. Entomol., in press.Google Scholar
  44. Smith, H. S. 1935. The role of biotic factors in the determination of population densities. J. Econ. Ent. 28: 873–898.Google Scholar
  45. Strong, D. R. 1984. Density-vague ecology and liberal population regulation in insects. Pp. 313–329. In P.W. Price, C.N. Slobodchikoff and W. S. Gaud (eds.). A New Ecology: Novel Approaches to Interactive Systems. Wiley, New York.Google Scholar
  46. Taylor, A. D. 1988. Parasitoid competition and the dynamics of host-parasitoid models. Amer. Nat. 132:417–436.CrossRefGoogle Scholar
  47. Varley, G. C, G. R. Gradwell and M. P. Hassell. 1973. Population dynamics and pest control. In D. Price Jones and M. E. Solomon (eds.), Biology in Pest and Disease Control.Google Scholar
  48. Walde, S. J. and W. W. Murdoch. 1988. Spatial density — dependence in parasitoids. Ann. Rev. Ent. 33:441–446.CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1992

Authors and Affiliations

  • William W. Murdoch
    • 1
  1. 1.Department of Biological SciencesUniversity of CaliforniaSanta BarbaraUSA

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