Skip to main content
Log in

Non-additive effects of multiple natural enemies on aphid populations

  • Community Ecology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The question of whether multiple natural enemies often interact to produce lower host mortality than single enemies acting alone has not yet been resolved. We compared the effects of four different combinations of natural enemies-parasitoids, predators, parasitoids plus predators, and no enemies-on caged aphid populations on marsh elder, Iva frutescens, in west-central Florida. Using starting densities of natural enemies commonly found in the field, we showed that parasitoid wasps reduced aphid population densities more than predatory ladybird beetles. The addition of predators to cages containing parasites reduced the ability of parasitoids to decrease aphid population densities. Because the experiments ran only over the course of one generation, such a reduction in the effectiveness of parasites is likely caused by interference of predators with parasitoid behavior. Parasitism in the cages containing both parasitoids and predators was reduced when compared to percent parasitism in parasitoid-only cages, but this could also be due to predation. Our experiments showed that ladybird beetles prey on parasitized aphids. Thus over the long-term, the effectiveness of parasites is impaired by the interference of predators on ovipositing parasitoids and by the predation of parasitized aphids. The effects of natural enemies in this system are clearly non-additive.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bertness MD, Wikler K, Chatkupt T (1992) Flood tolerance and the distribution of Iva frutescens across New England salt marshes. Oecologia 91: 171–178

    Google Scholar 

  • Carroll DP, Hoyt SC (1984) Natural enemies and their effects on apple aphid, Aphis pomi DeGeer (Homoptera: Aphididae), colonies on young apple trees in central Washington. Environ Entomol 13: 469–481

    Google Scholar 

  • Chambers RJ, Sunderland KD, Wyatt IJ, Vickerman GP (1983) The effects of predator exclusion and caging on cereal aphids in winter wheat. J Appl Ecol 20: 209–224

    Google Scholar 

  • Chiverton PA (1986) Predator density manipulation and its effects on populations of Rhopalosiphum padi (Hom.: Aphididae) in spring barley. Ann Appl Biol 109: 49–60

    Google Scholar 

  • Evans EW (1991) Intra versus interspecific interactions of ladybeetles (Coleoptera: Coccinellidae) attacking aphids. Oecologia 87: 401–408

    Google Scholar 

  • Frazer BD, Gilbert N, Nealis V, Raworth DA (1981) Control of aphid density ty a complex of predators. Can Entomol 113: 1035–1041

    Google Scholar 

  • Godfray HCJ, Waage JK (1991) Predictive modelling in biological control: the mango mealybug (Rastrococcus invadens) and its parasitoids. J Appl Ecol 28: 434–453

    Google Scholar 

  • Gutierrez AP, Baumgaertner JU, Summers CG (1984) Multitrophic models of predator prey energetics. III. A case study in an alfalfa ecosystem. Can Entomol 116: 950–963

    Google Scholar 

  • Gutierrez AP, Neuenschwander P, Schulthess F, Herren HR, Baumgaertner JU, Wermelinger B, Lohr B, Ellis CK (1988) Analysis of biological control of cassava pests in Africa. II. Cassava mealybug Phenacoccus manihoti. J Appl Ecol 25: 921–940

    Google Scholar 

  • Hacker SD, Bertness MD (1995) The herbivore paradox: why salt marsh aphids live on poor quality plants. Am Nat 145: 192–210

    Google Scholar 

  • Hagvar EB, Hofsvang T (1988) Interspecific competition between the aphid parasitoids Aphidius colemani Viereck and Ephedrus cerasicola Stáry (Hym., Aphidiidae). J Appl Entomol 106:62–71

    Google Scholar 

  • Hofsvang T (1990) Advantages and disadvantages of parasitoids and predators of aphids when used in biological control. Acta entomol Bohemoslov 87: 401–413

    Google Scholar 

  • Jones RE (1987) Ants, parasitoids, and the cabbage butterfly Pieris rapae J Anim Ecol 56: 739–749

    Google Scholar 

  • Kindlmann P, Ruzicka Z (1992) Possible consequences of a specific interaction between predators and parasites of aphids. Ecol Model 61: 253–265

    Google Scholar 

  • Mackauer M, Volkl W (1993) Regulation of aphid populations by aphidiid wasps: does parasitoid foraging behavior or hyperparasitism limit impact? Oecologia 94: 939–950

    Google Scholar 

  • Mills NJ (1982) Voracity, cannibalism and coccinellid predation. Ann Appl Biol 101: 144–148

    Google Scholar 

  • Prakasan CB, Krishnamoorthy Bhat P (1985) Interference of the predator, Cryptolaemus montrouzieri with the performance of a newly introduced parasite, Leptomastix dactylopii. J Coffee Res 15: 29–32

    Google Scholar 

  • Rosenheim JA, Wilhoit LR, Armer CA (1994) Influence of intraguild predation among generalist insect predators in the suppression of an herbivore population. Oecologia 96: 439–449

    Google Scholar 

  • Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA (1995) Intraguild predation among biological control agents: theory and evidence. Biol Control 5: 303–335

    Google Scholar 

  • Stiling P (1987) The frequency of density dependence in insect-host-parasitoid systems. Ecology 68: 844–856

    Google Scholar 

  • Stiling P, Rossi AM (1994) The window of parasitoid vulnerability to hyperparasitism: template for parasitoid complex structure. In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, London

    Google Scholar 

  • Tscharntke T (1992) Cascade effects among four trophic levels: bird predation on galls affects density-dependent parasitism. Ecology 73: 1689–1698

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ferguson, K.I., Stiling, P. Non-additive effects of multiple natural enemies on aphid populations. Oecologia 108, 375–379 (1996). https://doi.org/10.1007/BF00334664

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00334664

Key words

Navigation