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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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.
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.
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.
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.
Ferguson, K. I. and Stiling, P. 1996. Non-additive effects of multiple natural enemies on aphid populations. Oecologia 108:375–379.
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.
Honek, A. 1985. Habitat preferences of aphidophagous coccinellids [Coleoptera]. Entomophaga 30:253–264.
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.
Lucas, E., Coderre, D., and Brodeur, J. 1998. Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092.
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.
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.
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.
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.
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.
Pennacchio, F. 1989. The Italian species of the genus Aphidius Nees (Hymenoptera, Braconidae, Aphidiinae). Boll. Lab. Entomol. Agr. “Fillippo Silvestri.” 46:75–106.
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.
Raymond, B. Darby, A. C., and Douglas, A. E. 2000. Intraguild predators and the spatial distribution of a parasitoid. Oecologia 124:367–372.
Rosenheim, J. A. 1998. Higher-order predators and the regulation of insect herbivore populations. Annu. Rev. Entomol. 43:421–447.
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.
Ruzicka, Z. 1998. Further evidence of oviposition-deterring allomone in chrysopids (Neuroptera: Chrysopidae). Eur. J. Entomol. 95:35–39.
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.
Snyder, W. E. and Ives, A. R. 2001. Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82:705–716.
Stary, P. 1976. Aphid Parasites (Hymenoptera, Aphidiidae) of the Mediterranean Area. Academia, Prague.
Takada, H. 1968. Aphidiidae of Japan (Hymenoptera). Insec. Matsu. 30:67–124.
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.
Wheeler, A. G. 1977. Studies on the arthropod fauna of alfalfa. Predaceus insects. Can. Entomol. 109:423–427.
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.
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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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