Journal of Chemical Ecology

, Volume 33, Issue 12, pp 2229–2235 | Cite as

Effect of the Presence of a Nonhost Herbivore on the Response of the Aphid Parasitoid Diaeretiella rapae to Host-infested Cabbage Plants



The vast majority of studies of plant indirect defense strategies have considered simple tritrophic systems that involve plant responses to attack by a single herbivore species. However, responses by predators and parasitoids to specific, herbivore-induced, volatile blends could be compromised when two or more different herbivores are feeding on the same plant. In Y-tube olfactometer studies, we investigated the responses of an aphid parasitoid, Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae), to odors from cabbage plants infested with the peach-potato aphid Myzus persicae (Sulzer) (Homoptera: Aphididae), in both the presence and absence of a lepidopteran caterpillar, Plutella xylostella L. (Lepidoptera: Plutellidae). Female parasitoids chose aphid-infested plants over uninfested plants but did not distinguish between caterpillar-infested and uninfested plants. When given a choice between odors from an aphid-infested plant and those from a plant infested with diamondback moth larvae, they significantly chose the former. Furthermore, the parasitoids responded equally to odors from a plant infested with aphids only and those from a plant infested with both aphids and caterpillars. The results support the hypothesis that the aphid and the caterpillar induce different changes in the volatile profile of cabbage plants and that D. rapae females readily distinguish between the two. Furthermore, the changes to the plant volatile profile induced by the caterpillar damage did not hinder the responses of the parasitoid to aphid-induced signals.


Parasitoid Aphid Plant volatiles Plant signaling Herbivore-induced volatiles Myzus persicae Plutella xylostella Brassica Y-tube olfactometer 



The first author is indebted to the Biotechnology and Biological Sciences Research Council (BBSRC) of the UK for financial support via the Underwood Fund and to The British Council for sponsoring the academic link with Rothamsted Research. Rothamsted Research receives grant-aided support from the BBSRC.


  1. Agelopoulos, N. G., and Keller, M. A. 1994a. Plant natural enemy association in the tritrophic system, Cotesia rubecula—Pieris rapae—Brassicaceae (Cruciferae). 1. Sources of infochemicals. J.Chem.Ecol. 20:1725–1734.CrossRefGoogle Scholar
  2. Agelopoulos, N. G., and Keller, M. A. 1994b. Plant natural enemy association in the tritrophic system, Cotesia rubecula—Pieris rapae—Brassicaceae (Cruciferae). 3. Collection and identification of plant and frass volatiles. J. Chem. Ecol. 20:1955–1967.CrossRefGoogle Scholar
  3. Bartlet, E., Blight, M. M., Lane, P., and Williams, I. H. 1997. The responses of the cabbage seed weevil Ceutorhynchus assimilis to volatile compounds from oilseed rape in a linear track olfactometer. Entomol. Exp. Appl. 85:257–262.CrossRefGoogle Scholar
  4. Blande, J. D., Pickett, J. A., and Poppy, G. M. 2007. A comparison of semiochemically mediated interactions involving specialist and generalist Brassica-feeding aphids and the braconid parasitoid Diaeretiella rapae. J. Chem. Ecol. 33:767–779.PubMedCrossRefGoogle Scholar
  5. Blight, M. M., and Smart, L. E. 1999. Influence of visual cues and isothiocyanate lures on capture of the pollen beetle, Meligethes aeneus in field traps. J. Chem. Ecol. 25:1501–1516.CrossRefGoogle Scholar
  6. Bradburne, R. P., and Mithen, R. 2000. Glucosinolate genetics and the attraction of the aphid parasitoid Diaeretiella rapae to Brassica. Proc. R. Soc. Lond. B 267:89–95.CrossRefGoogle Scholar
  7. Bukovinsky, T., Gols, R., Posthumus, M. A., Vet, L. E. M., and Van Lenteren, J. C. 2005. Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellen). J. Chem. Ecol. 31:461–480.CrossRefGoogle Scholar
  8. Cook, S. M., Smart, L. E., Martin, J. L., Murray, D. A., Watts, N. P., and Williams, I. H. 2006. Exploitation of host plant preferences in pest management strategies for oilseed rape (Brassica napus). Entomol. Exp. Appl. 119:221–229.CrossRefGoogle Scholar
  9. De, Boer, J. G., Snoeren, T. A. L., and Dicke, M. 2005. Predatory mites learn to discriminate between plant volatiles induced by prey and nonprey herbivores. Anim. Behav. 69:869–879.CrossRefGoogle Scholar
  10. De, Moraes, C. M., Lewis, W. J., Paré, P. W., Alborn, H. T., and Tumlinson, J. H. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573.CrossRefGoogle Scholar
  11. Dicke, M. 1999. Evolution of induced indirect defense of plants. The Ecology and Evolution of Inducible Defenses. pp. 62–88, in R. Tollrian, and C. J. Harevell (eds.). Princeton University Press, Princeton, NJ.Google Scholar
  12. Dicke, M., Sabelis, M. W., Takabayashi, J., Bruin, J., and Posthumus, M. A. 1990. Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. J. Chem. Ecol. 16:3091–3118.CrossRefGoogle Scholar
  13. Du, Y.-J., Poppy, G. M., and Powell, W. 1996. Relative importance of semiochemicals from first and second trophic level in host foraging behavior of Aphidius ervi. J. Chem. Ecol. 22:1591–1606.CrossRefGoogle Scholar
  14. Du, Y.-J., Poppy, G. M., Powell, W., and Wadhams, L. J. 1997. Chemically mediated associative learning in the host foraging behaviour of the aphid parasitoid Aphidius ervi (hymenoptera: Braconidae). J. Insect Behav. 10:509–522.CrossRefGoogle Scholar
  15. Du, Y.-J., Poppy, G. M., Powell, W., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1998. Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J. Chem. Ecol. 24:1355–1368.CrossRefGoogle Scholar
  16. Futuyma, D. J., and Gould, F. 1979. Association of plants and insects in a deciduous forest. Ecol. Monogr. 49:33–50.CrossRefGoogle Scholar
  17. Geervliet, J. B. F., Vreugdenhil, A. I., Dicke, M., and Vet, L. E. M. 1998. Learning to discriminate between infochemicals from different plant–host complexes by the parasitoids Cotesia glomerata and C. rubecula. Entomol. Exp. Appl. 86:241–252.CrossRefGoogle Scholar
  18. Girling, R. D., Hassall, M., Turner, J. G., and Poppy, G. M. 2006. Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabipdopsis thaliana induced by Myzus persicae. Entomol. Exp. Appl 120:1–9.CrossRefGoogle Scholar
  19. Grasswitz, T. R. 1998. Effect of adult experience on the host-location behaviour of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Biol. Control 12:177–181.CrossRefGoogle Scholar
  20. Guerrieri, E., Pennacchio, F., and Tremblay, E. 1997. Effect of adult experience on in-flight orientation to plant and plant-host complex volatiles in Aphidius ervi Haliday (Hymenoptera, Braconidae). Biol. Control 10:159–165.CrossRefGoogle Scholar
  21. Ibrahim, M. A., Nissinen, A., and Holopainen, J. K. 2005. Response of Plutella xylostella and its parasitoid Cotesia plutellae to volatile compounds. J. Chem. Ecol. 31:1969–1984.PubMedCrossRefGoogle Scholar
  22. Potting, R. P. J., Poppy, G. M., and Schuler, T. H. 1999. The role of volatiles from cruciferous plants and pre-flight experience in the foraging behaviour of the specialist parasitoid Cotesia plutellae. Entomol. Exp. Appl. 93:87–95.CrossRefGoogle Scholar
  23. Powell, W., Pennacchio, F., Poppy, G. M., and Tremblay, E. 1998. Strategies involved in the location of hosts by the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae). Biol. Control 11:104–112.CrossRefGoogle Scholar
  24. Rodriguez-Saona, C., Crafts-Brandner, S. J., and Cañas, L. A. 2003. Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J. Chem. Ecol. 29:2539–2550.PubMedCrossRefGoogle Scholar
  25. Rostás, M., Ton, J., Mauch-Manni, B., and Turlings, T. C. J. 2006. Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naïve parasitoids. J. Chem. Ecol. 32:1897–1909.PubMedCrossRefGoogle Scholar
  26. Shiojiri, K., Takabayashi, J., Yano, S., and Takafuji, A. 2000. Flight response of parasitoids toward plant-herbivore complexes: a comparative study of two parasitoid–herbivore systems on cabbage plants. Appl. Entomol. Zool. 35:87–92.CrossRefGoogle Scholar
  27. Shiojiri, K., Takabayashi, J., Yano, S., and Takafuji, A. 2001. Infochemically mediated tritrophic interaction webs on cabbage plants. Popul. Ecol. 43:23–29.CrossRefGoogle Scholar
  28. Takabayashi, J., and Dicke, M. 1996. Plant–carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci. 1:109–113.CrossRefGoogle Scholar
  29. Takabayashi, J., Sabelis, M. W., Janssen, A., Shiojiri, K., and Van, Wijk, M. 2006. Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks. Ecol. Res. 21:3–8.CrossRefGoogle Scholar
  30. Thompson, J. N. 1998. Coping with multiple enemies: 10 years of attack on Lomatium dissectum plants. Ecology 79:2550–2554.Google Scholar
  31. Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J. 1990. Exploitation of herbivore-induced plant odors by host seeking parasitic wasps. Science 250:1251–1253.PubMedCrossRefGoogle Scholar
  32. Turlings, T. C. J., Wäckers, F. L., Vet, L. E. M., Lewis, W. J., and Tumlinson, J. H. 1993. Learning of host finding cues by hymenopterous parasitoidsInsect Learning. pp. 51–78, in D.R., Papaj, A.C., and Lewis (eds.). Chapman & Hall, London.Google Scholar
  33. Turlings, T. C. J., Bernasconi, M. L., Bertossa, R., Bigler, F., Caloz, G., and Dorn, S. 1998. The induction of volatile emissions in maize by three herbivore species with different feeding habits—possible consequences for their natural enemies. Biol. Control 11:122–129.CrossRefGoogle Scholar
  34. Van Roosjen, P. R. M. P., Pumarino, L., and Dicke, M. 2003. Attraction of the specialist parasitoid Cotesia rubecula to Arabidopsis thaliana infested by host or non-host herbivore species. Entomol. Exp. Appl. 107:229–236.CrossRefGoogle Scholar
  35. Vet, and L. E. M. 1999. From chemical to population ecology: infochemical use in an evolutionary context. J. Chem. Ecol. 25:31–49.CrossRefGoogle Scholar
  36. Vet, L. E. M., and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Ecol. Syst. 37:141–172.Google Scholar
  37. Vos, M., Berrocal, S. M., Karamaouna, F., Hemerik, L., and Vet, L. E. M. 2001. Plant-mediated indirect effects and the persistence of parasitoid-herbivore communities. Ecol. Lett. 4:38–45.CrossRefGoogle Scholar
  38. Yan, Z. G., and Wang, C. Z. 2006. Similar attractiveness of maize volatiles induced by Helicoverpa armigera and Pseudaletia separate to the generalist parasitoid Campoletis chlorideae. Entomol. Exp. Appl. 118:87–96.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Department of Animal Biology, Faculty of ScienceUniversity C.A. Diop de DakarDakarSenegal
  2. 2.Plant and Invertebrate Ecology DepartmentRothamsted ResearchHarpendenUK

Personalised recommendations