Journal of Chemical Ecology

, Volume 24, Issue 8, pp 1355–1368 | Cite as

Identification of Semiochemicals Released During Aphid Feeding That Attract Parasitoid Aphidius ervi

  • Yongjun Du
  • Guy M. Poppy
  • Wilf Powell
  • John A. Pickett
  • Lester J. Wadhams
  • Christine M. Woodcock


Herbivore induced release of plant volatiles mediating the foraging behavior of the aphid parasitoid Aphidius ervi was investigated using the pea aphid, Acyrthosiphon pisum, feeding on broad bean, Vicia faba. Behavioral responses were studied using an olfactometer and a wind tunnel. Volatiles obtained by air entrainment of aphid infested plants were more attractive to A. ervi than those from uninfested plants, in both behavioral bioassays. GC-EAG of both extracts showed a number of peaks associated with responses by A. ervi, but with some differences between extracts. Compounds giving these peaks were tentatively identified by GC-MS and confirmed by comparison with authentic samples on GC, using two columns of different polarity. The activity of pure compounds was further investigated by EAG and wind tunnel assays. Results showed that, of the compounds tested, 6-methyl-5-hepten-2-one was the most attractive for A. ervi females, with linalool, (Z)-3-hexen-1-yl acetate, (E)-β-ocimene, (Z)-3-hexen-1-ol, and (E)-β-farnesene all eliciting significantly more oriented flight behavior than a solvent control. Foraging experience significantly increased parasitoid responses to these compounds, with the exception of (E)-β-farnesene. Time-course GC analysis showed that feeding of A. pisum on V. faba induced or increased the release of several compounds. Release of two of these compounds (6-methyl-5-hepten-2-one and geranic acid) was not induced by the nonhost black bean aphid, Aphis fabae. During the analysis period, production of (E)-β-ocimene remained constant, but 6-methyl-5-hepten-2-one, linalool, geranic acid, and (E)-β-farnesene appeared during the first day after A. pisum infestation and increased in concentration with increasing time of aphid feeding.

Homoptera Aphididae Hymenoptera Braconidae tritrophic interactions host foraging plant volatiles semiochemicals induction synomones wind tunnel GC-EAG Acyrthosiphon pisum Aphidius ervi Vicia faba Aphis fabae 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949.Google Scholar
  2. Blight, M. M. 1990. Techniques for isolation and characterization of volatile semiochemicals of phytophagous insects, pp. 281–288, in A. R. McCaffery and I. D. Wilson (eds.). Chromatography and Isolation of Insect Hormones and Pheromones. Plenum Press, New York.Google Scholar
  3. Bruin, J., Dicke, M., and Sabelis, M. W. 1992. Plants are better protected against spider–mites after exposure to volatiles from infested conspecifics. Experientia 48:525–529.Google Scholar
  4. Bruin, J., Sabelis, M. W., and Dicke, M. 1995. Do plants tap SOS signals from their infested neighbours? TREE 10:167–170.Google Scholar
  5. Buttery, R. G., and Ling, L. C. 1984. Corn leaf volatiles: Identification using Tenax trapping for possible insect attractants. J. Agric. Food Chem. 32:1104–1106.Google Scholar
  6. Dawson, G. W., Griffiths, D. C., Pickett, J. A., Smith, M. C., and Woodcock, C. M. 1982. Improved preparation of (E)–β–farnesene and its activity with economically important aphids. J. Chem. Ecol. 8:1111–1117.Google Scholar
  7. Dicke, M., and Sabelis, M. W. 1988. How plants obtain predatory mites as bodyguards. Neth. J. Zool. 38:148–165.Google Scholar
  8. Dicke, M., Van Beek, T. A., Posthumus, M. A., Ben Dom, N., Van Bokhoven, H., and De Groot, A. 1990a. Isolation and identification of volatile kairomone that affects acarine predator prey interactions. Involvement of host plant in its production. J. Chem. Ecol. 16:381–395.Google Scholar
  9. Dicke, M., Sabelis, M. W., Takabayashi, J., Bruin, J., and Posthumus, M. A. 1990b. Plant strategies of manipulating predator–prey interactions through allelochemicals: Prospects for application in pest control. J. Chem. Ecol. 16:3091–3117.Google Scholar
  10. Dicke, M., Van Baarlen, P., Wessels, R., and Dijkman, H. 1993. Herbivory induces systemic production of plant volatiles that attract herbivore predators: Extraction of endogenous elicitor. J. Chem. Ecol. 19:581–599.Google Scholar
  11. Du, Y.–J., Poppy, G. M., and Powell, W. 1996. Relative importance of semiochemicals from the first and second trophic level in host foraging behavior of Aphidius ervi. J. Chem. Ecol. 22:1591–1605.Google Scholar
  12. 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.Google Scholar
  13. Genstat 5 Committee. 1993. Genstat 5 Release 3 Reference Manual. Clarendon Press, Oxford.Google Scholar
  14. Grasswitz, T. R., and Paine, T. D. 1993. Effect of experience on in–flight orientation to host–associated cues in the generalist parasitoid Lysiphlebus testaceipes. Entomol. Exp. Appl. 68:219–229.Google Scholar
  15. Guerrieri, E., Pennacchio, F. and Tremblay, E. 1993. Flight behavior of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae) in response to plant and host volatiles. Eur. J. Entomol. 90:415–421.Google Scholar
  16. Guerrieri, E., Du, Y.–J., Poppy, G., Powell, W., Pennacchio, F., and Tremblay, E. 1996. The role of host–induced plant synomones on in–flight orientation of the aphid parasitoid Aphidius ervi Haliday (Hymenopter, Braconidae). Proceedings, XX International Congress on Entomology, Firenze, Italy, August 1996, p. 647.Google Scholar
  17. 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.Google Scholar
  18. Johnson, A. E., Nursten, H. E., and Williams, A. A. 1971. Vegetable volatiles: A survey of components identified—Part 1. Chem. Ind. 1971:556–565.Google Scholar
  19. Maddrell, S. H. P. 1969. Secretion by the Malpighian tubules of Rhodnius. The movement of ions and water. J. Exp. Biol. 51:71–97.Google Scholar
  20. Mattiacci, L., Dicke, M., and Posthumus, M. A. 1995. β–Glucosidase: An elicitor of herbivore–induced plant odor that attracts host–searching parasitic wasps. Proc. Natl. Acad. Sci. U.S.A. 92:2036–2040.Google Scholar
  21. ParÉ, P. W., and Tumlinson, J. H. 1997. Induced synthesis of plant volatiles. Nature 385:30–31.Google Scholar
  22. Pickett, J. A. 1990. Gas chromatography–mass spectrometry in insect pheromone identification: Three extreme case histories, pp. 299–309, in A. R. McCaffery and I. D. Wilson (eds.). Chromatography and Isolation of Insect Hormones and Pheromones. Plenum Press, New York.Google Scholar
  23. Pickett, J. A., and Griffiths, D. C. 1980. Composition of aphid alarm pheromones. J. Chem. Ecol. 6:349–360.Google Scholar
  24. Pickett, J. A., Powell, W., Wadhams, L. J., Woodcock, C. M., and Wright, A. F. 1991. Biochemical interactions between plant–herbivore–parasitoid, pp. 1–14, in F. Bin (ed) Insect Parasitoids, 4th European Workshop, Perugia. (REDIA, Vol. LXXIV, n. 3, Appendice)Google Scholar
  25. Powell, W., and Wright, A. F. 1992. The influence of host food plants on host recognition by four aphidine parasitoids (Hymenoptera: Braconidae). Bull. Entomol. Res. 74:153–161.Google Scholar
  26. Powell, W., and Zhang, Z. L. 1983. The reactions of two cereal aphid parasitoids, Aphidius uzbeckistanicus and A. ervi to host aphids and their food plants. Physiol. Entomol. 8:439–443.Google Scholar
  27. 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.Google Scholar
  28. Price, P. W. 1981. Semiochemicals in evolutionary time, pp. 251–272, in D. A. Nordlund, R. L. Jones, and W. J. Lewis (eds.). Semiochemicals: Their role in pest control. John Wiley, New York.Google Scholar
  29. Read, D. P., Feeny, P. P., and Root, R. B. 1970. Habitat selection by the aphid parasite Diaeretiella rapae (Hymenoptera: Braconidae) and hyperparasite Charips brassicae (Hymenoptera: Cynipidae). Can. Entomol. 102:1567–1578.Google Scholar
  30. Sheehan, W., and Shelton, A. M. 1989. The role of experience in plant foraging by the aphid parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae). J. Insect Behav. 2:743–759.Google Scholar
  31. Takabayashi, J., Dicke, M., and Posthumus, M. A. 1994. Volatile herbivore–induced terpenoids in plant–mite interactions: Variation caused by biotic and abiotic factors. J. Chem. Ecol. 20:1329–1354.Google Scholar
  32. Tumlinson, J. H., Turlings, T. C. J., and Lewis, W. J. 1992. The semiochemical complexes that mediate insect parasitoid foraging. Agric. Zool. Rev. 5:221–252.Google Scholar
  33. Tumlinson, J. H., Lewis, W. J., and Vet, L. E. M. 1993. How parasitic wasps find their hosts. Sci. Am. 268:101–105.Google Scholar
  34. Turlings, T. C. J., and Tumlinson, J. H. 1992. Systemic release of chemical signals by herbivore–injured corn. Proc. Natl. Acad. Sci. U.S.A. 89:8399–8402.Google Scholar
  35. Turlings, T. C. J., Scheepmaker, J. W. A., Vet, L. E. M., Tumlinson, J. H., and Lewis, W. J. 1990a. How contact foraging experiences affect preferences for host–related odors in the larval parasitoid Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae). J. Chem. Ecol. 16:1577–1589.Google Scholar
  36. Turlings, T. C. J., Tumlinson, J. H., Eller, F. J., and Lewis, W. J. 1990b. Exploitation of herbivore–induced plant odors by host–seeking parasitic wasps. Science 250:1251–1253.Google Scholar
  37. Turlings, T. C. J., Tumlinson, J. H., Heath, R. R., Proveaus, A. T., and Doolittle, R. E. 1991. Isolation and identification of allelochemicals that attract the larval parsitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts. J. Chem. Ecol. 17:2235–2251.Google Scholar
  38. Turlings, T. C. J., McCall, P. J., Alborn, H. T., and Tumlinson, J. H. 1993. An elicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps. J. Chem. Ecol. 19:411–425.Google Scholar
  39. Vet, L. E. M. 1996. Parasitoid foraging: the importance of variation in individual behavior for population dynamics, pp. 245–256, in R. B. Floyd and A. W. Sheppard (eds.). Frontiers of Population Ecology. CSIRO Publications, Melbourne, Australia.Google Scholar
  40. Vet, L. E. M., and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37:141–172.Google Scholar
  41. Vet, L. E. M., Lewis, W. J., Papaj, D. R., and van Lenteren, J. C. 1990. A variable–response model for parasitoid foraging behaviour. J. Insect. Behav. 3:471–489.Google Scholar
  42. Vinson, S. B. 1985. The behavior of parasitoids, pp. 417–469, in G. A. Kerkut and L. I. Gilbert (eds.). Comprehensive Insect Physiology Biochemistry and Pharmacology, Vol. 9. Pergamon Press, Oxford.Google Scholar
  43. Visser, J. H. 1983. Differential sensory perceptions of plant compounds by insects, pp. 215–230, in P. A. Hedin (ed.). Plant Resistance to Insects. ACS Symposium Series, American Chemical Society, Washington, DC.Google Scholar
  44. Visser, J. H. 1986. Host odor perception in phytophagous insects. Annu. Rev. Entomol. 31:121–144.Google Scholar
  45. Wadhams, L. J. 1990. The use of coupled gas chromatography:electrophysiological techniques in the identification of insect pheromones, pp. 289–298, in A. R. McCaffery and I. D. Wilson (eds.). Chromatography and Isolation of Insect Hormones and Pheromones. Plenum Press, New York.Google Scholar
  46. Wadhams, L. J., Angst, M. E., and Blight, M. M. 1982. Responses of the olfactory receptors of Scolytus scolytus (F.) (Coleoptera: Scolytidae) to the stereoisomers of 4–methyl–3–heptanol. J. Chem. Ecol. 8:477–492.Google Scholar
  47. Wickremasinghe, M. G. V., and Van Emden, H. F. 1992. Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile cues from the host plants of their aphid prey. Physiol. Entomol. 17:297–304.Google Scholar

Copyright information

© Plenum Publishing Corporation 1998

Authors and Affiliations

  • Yongjun Du
    • 1
  • Guy M. Poppy
    • 1
  • Wilf Powell
    • 1
  • John A. Pickett
    • 2
  • Lester J. Wadhams
    • 2
  • Christine M. Woodcock
    • 2
  1. 1.Entomology and Nematology Department, IACR-Rothamsted, HarpendenHertsUK
  2. 2.Biological and Ecological Chemistry Department, IACR-Rothamsted, HarpendenHertsUK

Personalised recommendations