Spatial aggregation across ephemeral resource patches in insect communities: an adaptive response to natural enemies? (original) (raw)

Abstract

Although an increase in competition is a common cost associated with intraspecific crowding, spatial aggregation across food-limited resource patches is a widespread phenomenon in many insect communities. Because intraspecific aggregation of competing insect larvae across, e.g. fruits, dung, mushrooms etc., is an important means by which many species can coexist (aggregation model of species coexistence), there is a strong need to explore the mechanisms that contribute to the maintenance of this kind of spatial resource exploitation. In the present study, by using Drosophila-parasitoid interactions as a model system, we tested the hypothesis whether intraspecific aggregation reflects an adaptive response to natural enemies. Most of the studies that have hitherto been carried out on Drosophila-parasitoid interactions used an almost two-dimensional artificial host environment, where host larvae could not escape from parasitoid attacks, and have demonstrated positive densitydependent parasitism risk. To test whether these studies captured the essence of such interactions, we used natural breeding substrates (decaying fruits). In a first step, we analysed the parasitism risk of Drosophila larvae on a three-dimensional substrate in natural fly communities in the field, and found that the risk of parasitism decreased with increasing host larval density (inverse density dependence). In a second step, we analysed the parasitism risk of Drosophila subobscura larvae on three breeding substrate types exposed to the larval parasitoids Asobara tabida and Leptopilina heterotoma. We found direct density-dependent parasitism on decaying sloes, inverse density dependence on plums, and a hump-shaped relationship between fly larval density and parasitism risk on crab apples. On crab apples and plums, fly larvae benefited from a density-dependent refuge against the parasitoids. While the proportion of larvae feeding within the fruit tissues increased with larval density, larvae within the fruit tissues were increasingly less likely to become victims of parasitoids than those exposed at the fruit surface. This suggests a facilitating effect of group-feeding larvae on reaching the spatial refuge. We conclude that spatial aggregation in Drosophila communities can at least in part be explained as a predator avoidance strategy, whereby natural enemies act as selective agents maintaining spatial patterns of resource utilisation in their host communities.

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (37)

  1. Alphen JJM van, Galis F (1983) Patch time allocation and parasitization efficiency of Asobara tabida, a larval parasitoid of Drosophila. J Anim Ecol 52:937-952
  2. Alphen JJM van, Nordlander G, Eijs I (1991) Host habitat finding and host selection of the Drosophila parasitoid Leptopilina australis (Hymenoptera, Eucoilidae) with a comparison of the niches of European Leptopilina species. Oecologia 87:324-329
  3. Alphen JJM van, Bernstein C, Driessen G (2003) Information acquisition and time allocation in insect parasitoids. Trends Ecol Evol 18:81-87
  4. Atkinson WD, Shorrocks B (1984) Aggregation of larval diptera over discrete and ephemeral breeding sites: the implications for coexistence. Am Nat 124:336-351
  5. Begon ME, Harper JL, Townsend CR (1996) Ecology-individuals, populations and communities. Blackwell, Oxford
  6. Bernstein C (2000) Host-parasitoid models: the story of a successful failure. In: Hochberg ME, Ives AR (eds) Parasitoid population biology. Princeton University Press, Princeton, N.J., pp 41-57
  7. Carton Y, Boulétreau M, van Alphen JJM, van Lenteren JC (1986) The Drosophila parasitic wasps. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics and biology of Drosophila 3e. Academic Press, London, pp 347-394
  8. Casas J (2000) Host location and selection in the field. In: Hochberg ME, Ives AR (eds) Parasitoid population biology. Princeton University Press, Princeton, N.J., pp 17-26
  9. Ellers J, van Alphen JJM, Sevenster JG (1998) A field study of size- fitness relationships in the parasitoid Asobara tabida. J Anim Ecol 67:318-324
  10. Galis F, van Alphen JJM (1981) Patch time allocation and search intensity of Asobara tabida Nees (Braconidae), a larval parasitoid of Drosophila. Neth J Zool 31:596-611
  11. Hartley S, Shorrocks B (2002) A general framework for the aggregation model of coexistence. J Anim Ecol 71:651-662
  12. Hassell MP (2000) The spatial and temporal dynamics of host- parasitoid interactions. Oxford University Press, Oxford Hawkins BA (1994) Pattern and process in host-parasitoid interactions. Cambridge University Press, Cambridge
  13. Hoffmeister TS, Rohlfs M (2001) Aggregative egg distributions may promote species co-existence-but why do they exist? Evol Ecol Res 3:37-50
  14. Hunter AF (2000) Gregariousness and repellent defences in the survival of phytophagous insects. Oikos 91:213-224
  15. Krebs JR, Davies NB (1996) Introduction to behavioural ecology. Blackwell, Oxford
  16. Krijger CL, Sevenster JG (2001) Higher species diversity is explained by stronger spatial aggregation across six neotropical Drosophila communities. Ecol Lett 4:106-115
  17. Lenteren JC van (1976) The development of host discrimination and the prevention of superparasitism in the parasite Pseudeucoila bochei Weld (Hym.: Cynipidae). Neth J Zool 26:1-83
  18. Lenteren JC van, Bakker K (1978) Behavioural aspects of the functional responses of a parasite (Pseudeucoila bochei Weld) to its host (Drosophila melanogaster). Neth J Zool 28:213-233
  19. Lessells CM (1985) Parasitoid foraging: should parasitism be density dependent? J Anim Ecol 54:27-41
  20. Nunney L (2001) Population Structure. In: Fox CW, Roff DA, Fairbairn DJ (eds) Evolutionary ecology-concepts and case studies. Oxford University Press, Oxford, pp 70-83
  21. Parrish JK, Edelstein-Keshet L (1999) Complexity, pattern, and evolutionary trade-offs in animal aggregation. Science 284:99- 101
  22. Prokopy RJ, Roitberg BD (2001) Joining and avoidance behavior in nonsocial insects. Annu Rev Entomol 46:631-665
  23. Rohlfs M, Hoffmeister TS (2003) An evolutionary explanation of the aggregation model of species coexistence. Proc R Soc Lond B [Suppl] 270:S33-S35
  24. Sevenster JG, van Alphen JJM (1996) Aggregation and coexistence. II. A neotropical Drosophila community. J Anim Ecol 65:308- 324
  25. Shorrocks B (1982) The breeding sites of temperate woodland Drosophila. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics and biology of Drosophila 3b. Academic Press, London, pp 385-428
  26. Shorrocks B, Sevenster JG (1995) Explaining local species diversity. Proc R Soc Lond B 260:305-309
  27. Shorrocks B, Rosewell J, Edwards K, Atkinson, W (1984) Interspecific competition is not a major organizing force in many insect communities. Nature 310:310-312
  28. Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect? Oikos 87:185-190
  29. Stiling PD (1987) The frequency of density dependence in insect host-parasitoid systems. Ecology 68:844-856
  30. Toda M, Kimura M, Tuno N (1999) Coexistence mechanisms of mycophagous drosophilids on multispecies fungal hosts: aggregation and resource partitioning. J Anim Ecol 68:794-803
  31. Vet LEM (2001) Parasitoid searching efficiency links behaviour to population processes. Appl Entomol Zool 36:399-408
  32. Vet LEM, Bakker K (1985) A comparative functional approach to the host detection behaviour of parasitic wasps. 2. A quanti- tative study on eight eucoilid species. Oikos 44:487-498
  33. Walde SJ, Murdoch WW (1988) Spatial density dependence in parasitoids. Annu Rev Entomol 33:441-466
  34. Wertheim B (2001) Ecology of Drosophilaaggregation pheromone: a multitrophic approach. PhD thesis. Wageningen Agricultural University, Wageningen
  35. Wertheim B, Sevenster JG, Eijs IEM, van Alphen JJM (2000) Species diversity in mycophagous insect communities: the case of spatial aggregation vs. resource partitioning. J Anim Ecol 69:335-351
  36. Wertheim B, Vet LEM, Dicke M (2003) Increased risk of parasitism as ecological costs of using aggregation pheromones: labora- tory and field study of Drosophila-Leptopilina interaction. Oikos 100:269-282
  37. Zwölfer H, Arnold-Rinehart J (1994) The evolution of interactions and diversity in plant-insect systems: the Urophora-Eurytoma food web in galls on palearctic cardueae. In: Schulze ED, Mooney HA (eds) Biodiversity and ecosystem function, Springer, Berlin Heidelberg New York, pp 245-233