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Chemically Mediated Intraguild Predator Avoidance by Aphid Parasitoids: Interspecific Variability in Sensitivity to Semiochemical Trails of Ladybird Predators

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Abstract

The avoidance responses of aphid parasitoids with varying host ranges (Aphidius eadyi, Aphidius ervi, and Praon volucre) to chemical trails deposited by intraguild predatory ladybirds, Coccinella septempunctata and Adalia bipunctata, were investigated. Females of all three parasitoid species avoided leaves previously visited by C. septempunctata or A. bipunctata adults. The avoidance responses shown by the two Aphidius species were stronger to trails of C. septempunctata than to those of A. bipunctata. However, P. volucre avoided trails of both ladybird species to a similar degree. Dose responses of these three parasitoid species to the hydrocarbons n-tricosane (C23H48), n-pentacosane (C25H52), and n-heptacosane (C27H56), which are components of the trails of both C. septempunctata and A. bipunctata, were evaluated. Dual-choice bioassays indicated the following: (1) A. eadyi showed more sensitive avoidance responses to n-tricosane than did the other two parasitoid species, (2) all three species showed similar responses to n-pentacosane across a range of doses, and (3) only P. volucre showed avoidance responses to n-heptacosane. Quantitative analyses of each hydrocarbon in the trails of the two ladybird species showed that n-pentacosane and n-heptacosane occur in significantly greater amounts in C. septempunctata trails than in those of A. bipunctata. The trails of the two species also differ qualitatively in the other hydrocarbons present.

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References

  • Agarwala, B. K., Yasuda, H., and Kajita Y. 2003. Effect of conspecifics and heterospecific feces on foraging and oviposition of two predatory ladybirds: role of fecal cues in predator avoidance. J. Chem. Ecol. 29:357–376.

    Article  PubMed  CAS  Google Scholar 

  • Colfer, R. G. and Rosenheim, J. A. 1995. Intraguild predation by coccinellid beetles on an aphid parasitoid, Lysiphlebus testaceipes, pp. 1033–1036, in Proc. Beltwide Cotton Conference.

  • Dixon, A. F. G. 2000. Insect Predator–Prey Dynamics: Ladybird Beetles & Biological Control. Cambridge University Press, UK.

    Google Scholar 

  • Doumbia, M., Hemptinne, J. L., and Dixon, A. F. G. 1998. Assessment of patch quality by ladybirds: role of larval tracks. Oecologia 113:197–202.

    Article  Google Scholar 

  • Ekbom, B. 1994. Arthropod predators of the pea aphid, Acyrthosiphon pisum Harr. (Hom., Aphididae) in peas (Pisum sativum L.), clover (Trifolium pratense L.) and alfalfa (Medicago sativa L.). J. Appl. Entomol. 117:469–476.

    Article  Google Scholar 

  • Ferguson, K. I. and Stiling, P. 1996. Non-additive effects of multiple natural enemies on aphid populations. Oecologia 108:375–379.

    Google Scholar 

  • Hemptinne, J. L., Lognay, G., Doumbia, M., and Dixon, A. F. G. 2001. Chemical nature and persistence of the oviposition deterring pheromone in the tracks of the two spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Chemoecology 11:43–47.

    Article  CAS  Google Scholar 

  • Honek, A. 1985. Habitat preferences of aphidophagous coccinellids [Coleoptera]. Entomophaga 30:253–264.

    Article  Google Scholar 

  • Kosaki, A. and Yamaoka, R. 1996. Chemical composition of footprints and cuticular lipids of three species of lady beetles. Jpn. J. Appl. Entomol. Zool. 40:47–53.

    Google Scholar 

  • Lucas, E., Coderre, D., and Brodeur, J. 1998. Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092.

    Google Scholar 

  • Mackauer, M. and Finlayson, T. 1967. The hymenopterous parasites (Hymenoptera: Aphidiidae et Aphelinidae) of the pea aphid in eastern North America. Can. Entomol. 99:1081–1082.

    Google Scholar 

  • Nakashima, Y. and Akashi, M. 2005. Seasonal and within-plant distribution of the predator and parasitoid complexes associated with Acyrthosiphon pisum and A. kondoi. (Homoptera: Aphididae) on alfalfa in Japan. Appl. Entomol. Zool. 40:137–144.

    Article  Google Scholar 

  • Nakashima, Y. and Senoo, N. 2003. Avoidance of ladybird trails by an aphid parasitoid Aphidius ervi: Active period and effects of prior oviposition experience. Entomol. Exp. Appl. 109:163–166.

    Article  Google Scholar 

  • Nakashima, Y., Birkett, M. A., Pye, B. J., Pickett, J. A., and Powell. W. 2004. The role of semiochemicals in the avoidance of the seven-spot ladybird Coccinella septempunctata (Coleoptera: Coccinellidae) by the aphid parasitoid, Aphidius ervi (Hymenoptera: Braconidae). J. Chem. Ecol. 30:1103–1115.

    Article  PubMed  CAS  Google Scholar 

  • Nist 2002. Standard Reference Data Base (Version 3.0.1). Office of the Standard Reference Data Base. National Institute of Standards and Technology, Gaithersburg, MD.

    Google Scholar 

  • Pennacchio, F. 1989. The Italian species of the genus Aphidius Nees (Hymenoptera, Braconidae, Aphidiinae). Boll. Lab. Entomol. Agr. “Fillippo Silvestri.” 46:75–106.

    Google Scholar 

  • Pickett, J. A. 1990. Gas chromatography-mass spectrometry in insect pheromone identification: three extreme cases, pp. 209–309, in A. R. McCaffery and I. D. Wilson (eds.). Chromatography and Isolation of Insect Hormones and Pheromones. Plenum Press, New York.

    Google Scholar 

  • Raymond, B. Darby, A. C., and Douglas, A. E. 2000. Intraguild predators and the spatial distribution of a parasitoid. Oecologia 124:367–372.

    Article  Google Scholar 

  • Rosenheim, J. A. 1998. Higher-order predators and the regulation of insect herbivore populations. Annu. Rev. Entomol. 43:421–447.

    Article  PubMed  CAS  Google Scholar 

  • Rosenheim, J. A. Wilholt, L. R., and Armer, C. A. 1993. Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia 96:439–449.

    Article  Google Scholar 

  • Ruzicka, Z. 1998. Further evidence of oviposition-deterring allomone in chrysopids (Neuroptera: Chrysopidae). Eur. J. Entomol. 95:35–39.

    Google Scholar 

  • Ruzicka, Z. 2001. Oviposition responses of aphidophagous coccinellids to tracks of ladybird (Coleoptera: Coccinellidae) and lacewing (Neuroptera: Chrysopidae) larvae. Eur. J. Entomol. 98:183–188.

    Google Scholar 

  • Snyder, W. E. and Ives, A. R. 2001. Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82:705–716.

    Article  Google Scholar 

  • Stary, P. 1976. Aphid Parasites (Hymenoptera, Aphidiidae) of the Mediterranean Area. Academia, Prague.

    Google Scholar 

  • Takada, H. 1968. Aphidiidae of Japan (Hymenoptera). Insec. Matsu. 30:67–124.

    Google Scholar 

  • Taylor, A. J., Muller, C. B., and Godfray, H. C. J. 1998. Effect of aphid predators on oviposition behavior of aphid parasitoids. J. Insect. Behav. 11:297–302.

    Article  Google Scholar 

  • Wheeler, A. G. 1977. Studies on the arthropod fauna of alfalfa. Predaceus insects. Can. Entomol. 109:423–427.

    Article  Google Scholar 

  • Wratten, S. D. and Powell, W. 1991. Cereal aphids and their natural enemies, pp. 223–257, in L. G. Firbank, J. F. Darbyshire, and G. R. Potts (eds.). The Ecology of Temperate Cereal Fields. Blackwell Scientific Publications, London, UK.

    Google Scholar 

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Acknowledgments

We thank Martin Torrance for assistance with insect rearing. This work was supported by a Research Fellowship (to Y.N.) through the Japan Society for the Promotion of Science, and by the United Kingdom Department for Food, Environment, and Rural Affairs. Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council of the United Kingdom.

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Correspondence to Wilf Powell.

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Nakashima, Y., Birkett, M.A., Pye, B.J. et al. Chemically Mediated Intraguild Predator Avoidance by Aphid Parasitoids: Interspecific Variability in Sensitivity to Semiochemical Trails of Ladybird Predators. J Chem Ecol 32, 1989–1998 (2006). https://doi.org/10.1007/s10886-006-9123-y

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  • DOI: https://doi.org/10.1007/s10886-006-9123-y

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