Journal of Chemical Ecology

, Volume 33, Issue 4, pp 767–779 | Cite as

A Comparison of Semiochemically Mediated Interactions Involving Specialist and Generalist Brassica-feeding Aphids and the Braconid Parasitoid Diaeretiella rapae



Diaeretiella rapae, a parasitoid that predominately specializes in the parasitism of Brassica-feeding aphids, attacks Lipaphis erysimi, a specialist feeding aphid of the Brassicaceae and other families in the Capparales, at a greater rate than the generalist-feeding aphid, Myzus persicae. In this study, we investigated the orientation behavior of D. rapae to the volatile chemicals produced when these two aphid species feed on turnip (Brassica rapa var rapifera). We showed no significant preference orientation behavior to either aphid/turnip complex over the other. Isothiocyanates are among the compounds emitted by plants of the Brassicaceae in response to insect feeding damage, including by aphids. We assessed parasitoid orientation behavior in response to laboratory-formulated isothiocyanates. We tested two formulations and discovered significant orientation toward 3-butenyl isothiocyanate. We also assessed plant and aphid glucosinolate content, and showed large levels of glucosinolate concentration in L. erysimi, whereas there was little change in plant content in response to aphid feeding. Our results suggest that during the process of host location, similar cues may be utilized for locating L. erysimi and M. persicae, whereas the acceptance of hosts and their suitability may involve aspects of nonvolatile aphid chemistry.


Glucosinolate Isothiocyanate Lipaphis erysimi Myzus persicae Diaeretiella rapae Volatiles Orientation Behavior 


  1. Aplin, R. T., Darcyward, R., and Rothschild, M. 1975. Examination of large white and small white butterflies (Pieris spp.) for presence of mustard oils and mustard oil glycosides. J. Entomol. Ser A. Physiol. & Behav. 50:73–78.Google Scholar
  2. Bartlet, E., Kiddle, G., Williams, I., and Wallsgrove, R. 1999. Wound-induced increases in the glucosinolate content of oilseed rape and their effect on subsequent herbivory by a crucifer specialist. Entomol. Exp. Appl. 91:163–167.CrossRefGoogle Scholar
  3. Battaglia, D., Pennacchio, F., Marincola, G., and Tranfaglia, A. 1993. Cornicle secretion of Acyrthosiphon-pisum (Homoptera, Aphididae) as a contact kairomone for the parasitoid Aphidius-ervi (Hymenoptera, Braconidae). Eur. J. Entomol. 90:423–428.Google Scholar
  4. Battaglia, D., Poppy, G., Powell, W., Romano, A., Tranfaglia, A., and Pennacchio, F. 2000. Physical and chemical cues influencing the oviposition behavior of Aphidius ervi. Entomol. Exp. Appl. 94:219–227.CrossRefGoogle Scholar
  5. Blande, J. D. 2004. Differential signalling from specialist and generalist Brassica feeding aphids to differentially adapted aphid parasitoids. Ph.D. thesis, University of Southampton, UK.Google Scholar
  6. Blande, J. D., Pickett, J. A., and Poppy, G. M. 2004. Attack rate and success of the parasitoid Diaeretiella rapae on specialist and generalist feeding aphids. J. Chem. Ecol. 30:1781–1795.PubMedCrossRefGoogle Scholar
  7. Bones, A. M., and Rossiter, J. T. 2006. The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry 67:1053–1067.PubMedCrossRefGoogle Scholar
  8. Bradburne, R. P., and Mithen, R. 2000. Glucosinolate genetics and the attraction of the aphid parasitoid Diaeretiella rapae to Brassica. Proc. R. Soc. Lond., Ser. B Biol. Sci. 267:89–95.CrossRefGoogle Scholar
  9. Bridges, M., Jones, A. M. E., Bones, A. M., Hodgson, C., Cole, R., Bartlet, E., Wallsgrove, R., Karapapa, V. K., Watts, N., and Rossiter, J. T. 2002. Spatial organization of the glucosinolate-myrosinase system in brassica specialist aphids is similar to that of the host plant. Proc. R. Soc. Lond., Ser. B Biol. Sci. 269:187–191.CrossRefGoogle Scholar
  10. Carlson, D. G., Daxenbichler, M. E., Vanetten, C. H., and Tookey, H. L. 1981. Glucosinolates in crucifer vegetables—turnips and rutabagas. J. Agric. Food Chem. 29:1235–1239.PubMedCrossRefGoogle Scholar
  11. Carlson, D. G., Daxenbichler, M. E., Tookey, H. L., Kwolek, W. F., Hill, C. B., and Williams, P. H. 1987. Glucosinolates in turnip tops and roots—cultivars grown for greens and or roots. J. Am. Soc. Hortic. Sci. 112:179–183.Google Scholar
  12. Cole, R. 1996. Abiotic induction of changes to glucosinolate profiles in Brassica species and increased resistance to the specialist aphid Brevicoryne brassicae. Entomol. Exp. Appl. 80:228–230.CrossRefGoogle Scholar
  13. Dawson, G. W., Griffiths, D. C., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1987. Plant-derived synergists of alarm pheromone from turnip aphid, Lipaphis (Hyadaphis) erysimi (Homoptera: Aphididae). J. Chem. Ecol. 13:1663–1671.CrossRefGoogle Scholar
  14. Dawson, G. W., Doughty, K. J., Hick, A. J., Pickett, J. A., Pye, B. J., Smart, L. E., and Wadhams, L. J. 1993. Chemical precursors for studying the effects of glucosinolate catabolites on diseases and pests of oilseed rape (Brassica napus) or related plants. Pestic. Sci. 39:271–278.CrossRefGoogle Scholar
  15. De Faris, A. M. I., and Hopper, K. R. 1999. Oviposition behavior of Aphelinus asychis (Hymenoptera: Aphelinidae) and Aphidius matricariae (Hymenoptera: Aphidiidae) and defense behavior of their host Diuraphis noxia (Homoptera: Aphididae). Environ. Entomol. 28:858–862.Google Scholar
  16. De Vos, M., Van Oosten, V. R., Van Poecke, R. M. P., Van Pelt, J. A., Pozo, M. J., Mueller, M. J., Buchala, A. J., Métraux, J-P., Van Loon, L. C., Dicke, M., and Pieterse, C. M. J. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe. Interact. 18:923–937.PubMedGoogle Scholar
  17. Dicke, M., VanBeek, T. A., Posthumus, M. A., Bendom, N., Van Bokhoven, H., and DeGroot, A. E. 1990. Isolation and identification of volatile kairomone that affects acarine predator–prey interactions—involvement of host plant in its production. J. Chem. Ecol. 16:381–396.CrossRefGoogle Scholar
  18. Du, Y. J., Poppy, G. M., and Powell, W. 1996. Relative importance of semiochemicals from first and second trophic levels in host foraging behavior of Aphidius ervi. J. Chem. Ecol. 22:1591–1605.CrossRefGoogle Scholar
  19. Du, Y. J., Poppy, G. M., Powell, W., and Wadhams, L. J. 1997. Chemically mediated associative learning in the host foraging behavior of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae). J. Insect Behav. 10:509–522.Google Scholar
  20. 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
  21. Godfray, H. C. J., and Waage, J. K. 1988. Learning in parasitic wasps. Nature 331:211–211.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. Grubb, C. D., and Abel, S. 2006. Glucosinolate metabolism and its control. Trends Plant Sci. 11:89–100.PubMedCrossRefGoogle Scholar
  24. 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
  25. 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
  26. Guerrieri, E., Poppy, G. M., Powell, W., Tremblay, E., and Pennacchio, F. 1999. Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. J. Chem. Ecol. 25:1247–1261.CrossRefGoogle Scholar
  27. Havill, N. P., and Raffa, K. F. 2000. Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions. Ecol. Entomol. 25:171–179.CrossRefGoogle Scholar
  28. Husebye, H., Arzt, S., Burmeister, W. P., Härtel, F. V., Brandt, A., Rossiter, J. T., and Bones, A. M. 2005. Crystal structure at 1.1 Å resolution of an insect myrosinase from Brevicoryne brassicae shows its close relationship to β-glucosidases. Insect Biochem. Mol. Biol. 35:1311–1320.PubMedCrossRefGoogle Scholar
  29. Jones, A. M. E., Bridges, M., Bones, A. M., Cole, R., and Rossiter, J. T. 2001. Purification and characterisation of a non-plant myrosinase from the cabbage aphid Brevicoryne brassicae (L.). Insect Biochem. Mol. Biol. 31:1–5.PubMedCrossRefGoogle Scholar
  30. Kliebenstein, D. J., Kroymann, J., and Mitchell-Olds, T. 2005. The glucosinolate-myrosinase system in an ecological and evolutionary context. Curr. Opin. Plant Biol. 8:264–271.PubMedCrossRefGoogle Scholar
  31. Koritsas, V. M., Lewis, J. A., and Fenwick, G. R. 1989. Accumulation of indole glucosinolates in Psylliodes chrysocephala L infested, or Psylliodes chrysocephala L-damaged tissues of oilseed rape (Brassica napus L). Experientia 45:493–495.CrossRefGoogle Scholar
  32. MacGibbon, D. B., and Allison, R. M. 1970. A method for the separation and detection of plant glucosinolases (myrosinases). Phytochemistry 9:541–544.CrossRefGoogle Scholar
  33. MacGibbon, D. B., and Beuzenberg, E. J. 1978. Location of glucosinolase in Brevicoryne brassicae and Lipaphis erysimi (Aphididae). N. Z. J. Sci. 21:389–392.Google Scholar
  34. MacKauer, M., Michaud, J. P., and Volkl, W. 1996. Host choice by aphidiid parasitoids (Hymenoptera: Aphidiidae): Host recognition, host quality, and host value. Can. Entomol. 128:959–980.CrossRefGoogle Scholar
  35. Magrath, R., Herron, C., Giamoustaris, A., and Mithen, R. 1993. The inheritance of aliphatic glucosinolates in Brassica napus. Plant Breed. 111:55–72.CrossRefGoogle Scholar
  36. Micha, S. G., Kistenmacher, S., Mölck, G., and Wyss, U. 2000. Tritrophic interactions between cereals, aphids and parasitoids: Discrimination of different plant–host complexes by Aphidius rhopalosiphi (Hymenoptera: Aphidiidae). Eur. J. Entomol. 97:539–543.Google Scholar
  37. Miles, P. W. 1999. Aphid saliva. Biol. Rev. 74:41–85.CrossRefGoogle Scholar
  38. Mölck, G., Micha, S. G., and Wyss, U. 1999. Attraction to odor of infested plants and learning behavior in the aphid parasitoid Aphelinus abdominalis. Z. Pflanzenk. Pflanzens. 106:557–567.Google Scholar
  39. Mölck, G., Pinn, H., and Wyss, U. 2000. Manipulation of plant odor preference by learning in the aphid parasitoid Aphelinus abdominalis (Hymenoptera: Aphelinidae). Eur. J. Entomol. 97:533–538.Google Scholar
  40. Müller, C., Agerbirk, N., Olsen, C. E., Boeve, J. L., Schaffner, U., and Brakefield, P. M. 2001. Sequestration of host plant glucosinolates in the defensive haemolymph of the sawfly Athalia rosae. J. Chem. Ecol. 27:2505–2516.PubMedCrossRefGoogle Scholar
  41. Poppy, G. M., Powell, W., and Pennacchio, F. 1997. Aphid parasitoid responses to semiochemicals—genetic, conditioned or learnt? Entomophaga 42:193–199.Google Scholar
  42. 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
  43. Read, D. P., Feeny, P. P., and Root, R. B. 1970. Habitat selection by aphid parasite Diaeretiella rapae (Hymenoptera: Braconidae) and hyperparasite Charips brassicae (Hymenoptera: Cynipidae). Can. Entomol. 102:1567–1578.Google Scholar
  44. Reed, H. C., Tan, S. H., Haapanen, K., Killmon, M., Reed, D. K., and Elliott, N. C. 1995. Olfactory responses of the parasitoid Diaeretiella rapae (Hymenoptera, Aphidiidae) to odor of plants, aphids, and plant–aphid complexes. J. Chem. Ecol. 21:407–418.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Storeck, A., Poppy, G. M., Van Emden, H. F., and Powell, W. 2000. The role of plant chemical cues in determining host preference in the generalist aphid parasitoid Aphidius colemani. Entomol. Exp. Appl. 97:41–46.CrossRefGoogle Scholar
  47. 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.CrossRefPubMedGoogle Scholar
  48. Van Emden, H. F., Sponagl, B., Baker, T., Ganguly, S., and Douloumpaka, S. 1996. Hopkins ‘host selection principle’, another nail in its coffin. Physiol. Entomol. 21:325–328.Google Scholar
  49. Van Emden, H. F., Eletherianos, I., Rose, J., Douloumpakata, S., and Pettersson, J. 2002. Aphid parasitoids detect that an alien plant was present nearby during their development. Physiol. Entomol. 27:199–205.CrossRefGoogle Scholar
  50. Vaughn, T. T., Antolin, M. F., and Bjostad, L. B. 1996. Behavioral and physiological responses of Diaeretiella rapae to semiochemicals. Entomol. Exp. Appl. 78:187–196.CrossRefGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. Vet, L. E. M., and Groenewold, A. W. 1990. Semiochemicals and learning in parasitoids. J. Chem. Ecol. 16:3119–3135.CrossRefGoogle Scholar
  53. Vinson, S. B. 1976. Host selection by insect parasitoids. Annu. Rev. Entomol. 21:109–133.CrossRefGoogle Scholar
  54. Vinson, S. B. 1985. The behaviour of parasitoids. pp. 417–469, in Kerkut G. A., and L. I. Gilbert, (eds.) Comprehensive Insect Physiology, Biochemistry and Pharmacology. Pergamon Press, Oxford.Google Scholar
  55. Vinson, S. B. 1999. Parasitoid manipulation as a plant defense strategy. Ann. Entomol. Soc. Am. 92:812–828.Google Scholar
  56. Weber, G., Oswald, S., and Zollner, U. 1986. Suitability of rape cultivars with a different glucosinolate content for Brevicoryne brassicae (L) and Myzus persicae (Sulzer) (Hemiptera, Aphididae). Z. Pflanzenk. Pflanzens. 93:113–124.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Rothamsted ResearchHarpendenUK
  2. 2.School of Biological SciencesUniversity of SouthamptonSouthamptonUK
  3. 3.University of KuopioKuopioFinland

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