Skip to main content
Log in

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

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Bones, A. M., and Rossiter, J. T. 2006. The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry 67:1053–1067.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • Godfray, H. C. J., and Waage, J. K. 1988. Learning in parasitic wasps. Nature 331:211–211.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Grubb, C. D., and Abel, S. 2006. Glucosinolate metabolism and its control. Trends Plant Sci. 11:89–100.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • MacGibbon, D. B., and Allison, R. M. 1970. A method for the separation and detection of plant glucosinolases (myrosinases). Phytochemistry 9:541–544.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Magrath, R., Herron, C., Giamoustaris, A., and Mithen, R. 1993. The inheritance of aliphatic glucosinolates in Brassica napus. Plant Breed. 111:55–72.

    Article  CAS  Google Scholar 

  • 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 

  • Miles, P. W. 1999. Aphid saliva. Biol. Rev. 74:41–85.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • Poppy, G. M., Powell, W., and Pennacchio, F. 1997. Aphid parasitoid responses to semiochemicals—genetic, conditioned or learnt? Entomophaga 42:193–199.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Vet, L. E. M., and Groenewold, A. W. 1990. Semiochemicals and learning in parasitoids. J. Chem. Ecol. 16:3119–3135.

    Article  CAS  Google Scholar 

  • Vinson, S. B. 1976. Host selection by insect parasitoids. Annu. Rev. Entomol. 21:109–133.

    Article  Google Scholar 

  • 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 

  • Vinson, S. B. 1999. Parasitoid manipulation as a plant defense strategy. Ann. Entomol. Soc. Am. 92:812–828.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

Download references

Acknowledgements

We thank Julietta Marquez for her work on the glucosinolate analysis. J. Blande was supported by a Biotechnology and Biological Sciences Research Council of the United Kingdom (BBSRC) Quota studentship. Funding for this work was provided in part by the Department of the Environment, Food and Rural Affairs. Rothamsted Research receives grant-aided support from the BBSRC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. D. Blande.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blande, J.D., Pickett, J.A. & Poppy, G.M. 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 (2007). https://doi.org/10.1007/s10886-007-9264-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-007-9264-7

Keywords

Navigation