Advertisement

Oecologia

, Volume 137, Issue 1, pp 123–130 | Cite as

Density-dependent foraging behaviors in a parasitoid lead to density-dependent parasitism of its host

  • James UmbanhowarEmail author
  • John Maron
  • Susan Harrison
Behavioural Ecology

Abstract

Empirical studies of spatial heterogeneity in parasitism by insect parasitoids have focused largely on patterns, while the many possible underlying mechanisms have been little studied in the field. We conducted experimental and observational studies on Tachinomyia similis (Diptera: Tachinidae) attacking western tussock moths (Orgyia vetusta; Lepidoptera: Lymantriidae) on lupine bushes at Bodega Bay, Calif., USA. We examined several foraging behaviors that have been hypothesized to create density-dependent variation in parasitism rates, including spatial aggregation of parasitoids to high host density, mutual interference among searching parasitoids and decelerating functional responses of the parasitoid. At the spatial scale of individual bushes, we detected both aggregation to a high density and a decelerating functional response. The resulting spatial pattern of parasitism was best fit by two models; one included an effect of parasitoid aggregation and the other included an effect of aggregation and a decelerating functional response. Most of the variation in parasitism was not correlated with density of O. vetusta.

Keywords

Parasitoid aggregation Functional response Interference Spatial heterogeneity 

Notes

Acknowledgements

We would like to thank P. Chesson, P. de Valpine, A. Hastings, L. Hurd, B. Inouye, J. Rosenheim, and two anonymous reviewers for discussions or comments on the text, M. Greaves, J. Combs, J. Robertson, and the Spatial Group for much needed assistance in the field. This work was sponsored by an NSF grant to S.P. Harrison and an NSF predoctoral fellowship to J. Umbanhowar.

References

  1. Barbour MG, Craig RB, Drysdale FR, Ghiselin MT (1973) Coastal ecology: Bodega Head. University of California Press, BerkeleyGoogle Scholar
  2. Brodman PA, Wilcox CV, Harrison S (1997) Mobile parasitoids may restrict the spatial spread of an insect outbreak. J Anim Ecol 66:65–72Google Scholar
  3. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer, Berlin Heidelberg New YorkGoogle Scholar
  4. Casas J (1989) Foraging behaviour of a leafminer parasitoid in the field. Ecol Entomol 14:257–265Google Scholar
  5. Chesson PL, Murdoch WW (1986) Aggregation of risk: relationships among host-parasitoid models. Am Nat 127:696–715CrossRefGoogle Scholar
  6. Comins HN, Hassell MP (1979) The dynamics of optimally foraging predators and parasitoids. J Anim Ecol 48:335–351Google Scholar
  7. Connor EF, Cargain MJ (1994) Density-related foraging behavior in Closterocerus tricinctus, a parasitoid of the leaf-mining moth, Cameraria hamadryadella. Ecol Entomol 19:327–334Google Scholar
  8. Furniss MM, Knopf JAE (1971) The western tussock moth. (Forest Pest Leaflet no. 120) USDA Forest Service, PortlandGoogle Scholar
  9. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, PrincetonGoogle Scholar
  10. Gross K, Ives AR (1999) Inferring host-parasitoid stability from patterns of parasitism among many patches. Am Nat 154:489–496CrossRefPubMedGoogle Scholar
  11. Harrison S (1994) Resources and dispersal as factors limiting a population of the tussock moth (Orgyia vetusta), a flightless defoliator. Oecologia 99:27–34Google Scholar
  12. Harrison S (1997) Persistent, localized outbreaks in the western tussock moth Orgyia vetusta: the roles of resource quality, predation and poor dispersal. Ecol Entomol 22:158–166Google Scholar
  13. Harrison S, Maron JL (1995) Impacts of defoliation by tussock moths (Orgyia vetusta) on the growth and reproduction of bush lupine (Lupinus arboreus). Ecol Entomol 20:223–229Google Scholar
  14. Harrison S, Wilcox CV (1995) Evidence that predator satiation may restrict the spatial spread of a tussock moth (Orgyia vetusta) outbreak. Oecologia 101:309–316Google Scholar
  15. Hassell MP (1978) The dynamics of arthropod predator-prey systems. Princeton University Press, PrincetonGoogle Scholar
  16. Hassell MP, May RM (1973) Stability in insect host-parasite models. J Anim Ecol 43:693–726Google Scholar
  17. Hassell MP, May RM, Pacala SW, Chesson PL (1991) The persistence of host-parasitoid associations in patchy environments. I. A general criterion. Am Nat 138:568–583CrossRefGoogle Scholar
  18. Hastings A (1997) Population biology, concepts and models. Springer, Berlin Heidelberg New YorkGoogle Scholar
  19. Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398Google Scholar
  20. Hunter AS (2000) Gregariousness and repellent defences in the survival of phytophagous insects. Oikos 91:213–224Google Scholar
  21. Ives AR (1992) Density-dependent and density-independent parasitoid aggregation in host-parasitoid systems. Am Nat 140:912–937CrossRefGoogle Scholar
  22. Ives AR, Schooler SS, Jagar VJ, Knuteson SE, Grbic M, Settle WH (1999) Variability and parasitoid foraging efficiency: a case study of pea aphids and Aphidius ervi. Am Nat 154:652–673CrossRefPubMedGoogle Scholar
  23. Jones TH, Hassell MP, Pacala SW (1993) Spatial heterogeneity and the population dynamics of a host-parasitoid system. J Anim Ecol 62:251–262Google Scholar
  24. Kareiva P, Odell G (1987) Swarms of predator exhibit 'preytaxis' if individual predators use area-restricted search. Am Nat 130:233–270CrossRefGoogle Scholar
  25. Maron JL, Harrison S (1997) Spatial pattern formation in an insect host-parasitoid system. Science 278:1619–1621CrossRefPubMedGoogle Scholar
  26. Maron JL, Harrison S, Greaves M (2001) Origin of an insect outbreak: escape in space or time from natural enemies? Oecologia 126:595–602Google Scholar
  27. McCann K, Hastings A, Harrison S, Wilson W (2000) Population outbreaks in a discrete world. Theor Popul Biol 57:97–108CrossRefPubMedGoogle Scholar
  28. McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall, LondonGoogle Scholar
  29. Murdoch WW, Briggs CJ (1996) Theory for biological control: recent developments. Ecology 77:2001–2013Google Scholar
  30. O'Neil RJ (1997) Functional response and search strategy of Podisus maculiventris (Heteroptera: Pentatomidae) attacking Colorado potato beetle (Coleoptera: Chrysomelidae). Environ Entomol 26:1183–1190Google Scholar
  31. Pacala SW, Hassell MP (1991) The persistence of host-parasitoid associations in patchy environments. II. Evaluation of field data. Am Nat 138:584–605CrossRefGoogle Scholar
  32. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1994) Numerical recipes in C, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  33. Rosenheim JA, Mangel M (1994) Patch-leaving rules for parasitoids with imperfect host discrimination. Ecol Entomol 19:374–380Google Scholar
  34. Rosenheim JA, Heimpel GE, Mangel M (2000) Egg maturation, egg resorption and the costliness of transient egg limitation in insects. Proc R Soc Lond B Biol Sci 267:1565–1573CrossRefPubMedGoogle Scholar
  35. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New YorkGoogle Scholar
  36. Stiling PD (1987) The frequency of density dependence in insect host-parasitoid systems. Ecology 68:844–856Google Scholar
  37. Strong DR, Whipple AV, Child AL, Dennis B (1999) Model selection for a subterranean trophic cascades: root-feeding caterpillars and entomopathogenic nematodes. Ecology 80:2750–2761Google Scholar
  38. Tillman PG (1996) Functional response of Microplitis croceipes and Cardiochiles nigiceps (Hymenoptera: Braconidae) to variation in density of tobacco budworm (Lepidoptera: Noctuidae). Environ Entomol 25:524–528Google Scholar
  39. Turchin P (1987) Population consequences of aggregative movement. J Anim Ecol 58:75–100Google Scholar
  40. Waage J (1983) Aggregation in field parasitoid populations: foraging time allocation in a population of Diadegma (Hymenoptera, Ichneumonidae). Ecol Entomol 8:447–454Google Scholar
  41. Walde SJ, Murdoch WW (1988) Spatial density dependence in parasitoids. Annu Rev Entomol 33:441–466CrossRefGoogle Scholar
  42. Wang B, Ferro DN (1998) Functional responses of Trichogramma ostriniae (Hymenoptera: Pyralidae) under laboratory and field conditions. Environ Entomol 27:752–758Google Scholar
  43. Wilson WG, Harrison SP, Hastings A, McCann K (1998) Exploring spatial pattern formation in models of tussock moth populations. J Anim Ecol 69: 94–107Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Center for Population Biology, Department of Environmental Science and PolicyUniversity of California, DavisDavisUSA
  2. 2.Division of Biological SciencesUniversity of MontanaMissoulaUSA
  3. 3.Department of BiologyMcGill UniversityMontrealCanada

Personalised recommendations