Skip to main content
Log in

Response of the Aphid Parasitoid Aphidius funebris to Volatiles from Undamaged and Aphid-infested Centaurea nigra

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

Abstract

Two issues have hindered the understanding of the ecology and evolution of volatile-mediated tritrophic interactions: few studies have addressed noncrop systems; and few statistical techniques have been applied that are suitable for the analysis of complex volatile blends. In this paper, we addressed both of these issues by studying the noncrop system involving the plant Centaurea nigra, the specialist aphid Uroleucon jaceae, and the parasitoid Aphidius funebris. In a Y-tube olfactometer, A. funebris was attracted to the odor from undamaged C. nigra, but preferred the plant–host complex (PHC) after 3 d of feeding by 200 U. jaceae over the undamaged plant, but not after three or 5 d of feeding by 50 U. jaceae. When aphids were removed, the initial preference for the damaged plant remained, but the final preference was not greater than for the undamaged plant. No qualitative differences were detected between the headspaces of C. nigra and the C. nigraU. jaceae PHC. For quantitative analysis, we used a compositional approach, which treats each compound produced as part of a blend, and not as a compound released in isolation, thus allowing analysis of the relative contribution of each compound to the blend as a whole. With this approach, subtle increases and decreases of some green leaf volatiles and monoterpenoids on the third day of aphid infestation were detected. Mechanically damaged C. nigra had a volatile profile that differed from undamaged C. nigra and the PHC. One and 10 ng of (Z)-3-hexenyl acetate, and 10 or 100 ng of 6-methyl-5-hepten-2-one were attractive to the parasitoid when placed in solution on filter paper. A. funebris appears to be using a combination of chemical cues to locate host-infested plants.

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

Similar content being viewed by others

References

  • Aitchison, J. 1986. The Statistical Analysis of Compositional Data. Chapman & Hall, Inc., Bristol.

    Google Scholar 

  • Bernays, E. A. and Funk, D. J. 2000. Electrical penetration graph analysis reveals population differentiation of host-plant probing behaviors within the aphid species Uroleucon ambrosiae. Entomol. Exp. Appl. 97:183–191.

    Article  Google Scholar 

  • Blackman, R. L. and Eastop, V. F. 2000. Aphids on the World’s Crops. John Wiley and Sons Ltd., New York.

    Google Scholar 

  • Bostock, R. M. 2005. Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu. Rev. Phytopathol. 43:545–580.

    Article  PubMed  CAS  Google Scholar 

  • Bronstein, J. L. and Barbosa, P. 2002. Multitrophic/multispecies mutualistic interactions: the role of non-mutualists in shaping and mediating mutualisms. in T. Tscharntke and B. A. Hawkins (eds.). Multitrophic level interactions pp. 44–66. Cambridge: Cambridge University Press.

    Google Scholar 

  • Bukovinszky, 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 (Hellén). J. Chem. Ecol. 31:461–480.

    Article  PubMed  CAS  Google Scholar 

  • Colazza, S., Fucarino, A., Peri, E., Salerno, G., Conti, E., and Bin, F. 2004a. Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J. Exp. Biol. 207:47–53.

    Article  PubMed  Google Scholar 

  • Colazza, S., Mcelfresh, J. S., and Millar, J. G. 2004b. Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J. Chem. Ecol. 30:945–964.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Dicke, M., Van Poecke, R. M. P., and De Boer, J. G. 2003. Inducible defense of plants: from mechanisms to ecological functions. Basic Appl. Ecol. 4:27–42.

    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., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1998. Identification of semiochemicals released during aphid feeding that attract the parasitoid Aphidius ervi. J. Chem. Ecol. 24:1355–1368.

    Article  CAS  Google Scholar 

  • Fäldt, J., Arimura, G.-I., Gershenzon, J., Takabayashi, J., and Bohlmann, J. 2003. Functional identification of AtTPS03 as (E)-β-ocimene synthase: a monoterpene synthase catalyzing jasmonate- and wound-induced volatile formation in Arabidopsis thaliana. Planta 216:745–751.

    PubMed  Google Scholar 

  • Feeny, P. 1976. Plant apparency and chemical defense. Recent Adv. Phytochem. 10:1–40.

    CAS  Google Scholar 

  • Geervliet, J. B. F., Verdel, M. S. W., Snellen, H., Schaub, J., Dicke, M., and Vet, L. E. M. 2000. Coexistence and niche segregation by field populations of the parasitoids Cotesia glomerata and C. rubecula in the Netherlands: predicting field performance from laboratory data. Oecologia 124:55–63.

    Article  Google Scholar 

  • Gouinguené, S., Degen, T., and Turlings, T. C. J. 2001. Variability in herbivore-induced odor emissions among maize cultivars and their wild ancestors. Chemoecology 11:9–16.

    Article  Google Scholar 

  • Gouinguené, S., Pickett, J. A., Wadhams, L. J., Birkett, M. A., and Turlings, T. C. J. 2005. Antennal electrophysiological responses of three parasitic wasps to caterpillar-induced volatiles from maize (Zea mays mays), cotton (Gossypium herbaceum), and cowpea (Vigna unguiculata). J. Chem. Ecol. 31:1023–1038.

    Article  PubMed  CAS  Google Scholar 

  • Greenhouse, S. W. and Geisser, S. 1959. On methods in the analysis of profile data. Psychometrika 24:95–112.

    Article  Google Scholar 

  • Guerrieri, E., Poppy, G. M., Powell, W., Tremblay, E., and Penacchio, 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 

  • Heidel, A. J. and Baldwin, I. T. 2004. Microarray analysis of salicylic acid- and jasmonic acid-signalling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant Cell Environ. 27:1362–1373.

    Article  CAS  Google Scholar 

  • Hoballah, M. E. and Turlings, T. C. J. 2005. The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J. Chem. Ecol. 31:2003–2018.

    Article  PubMed  CAS  Google Scholar 

  • Kaloshian, I. and Walling, L. L. 2005. Hemipterans as plant pathogens. Annu. Rev. Phytopathol. 43:491–521.

    Article  PubMed  CAS  Google Scholar 

  • Kessler, A. and Baldwin, I. T. 2002. Plant responses to insect herbivores: the emerging molecular analysis. Annu. Rev. Plant Biol. 53:299–328.

    Article  PubMed  CAS  Google Scholar 

  • Lo Pinto, M., Wajnberg, E., Colazza, S., Curty, C., and Fauvergue, X. 2004. Olfactory response of two aphid parasitoids, Lysiphlebus testaceipes and Aphidius colemani, to aphid-infested plants from a distance. Entomol. Exp. Appl. 110:159–164.

    Article  Google Scholar 

  • Martinez De Ilarduya, O., Xie, Q., and Kaloshian, I. 2003. Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol. Plant-Microb. Interact. 16:699–708.

    CAS  Google Scholar 

  • Mattiacci, L., Ambühl Rocca, B., Scascighini, N., D’alessandro, M., Hern, A., and Dorn, S. 2001. Systemically induced plant volatiles emitted at the time of “danger”. J. Chem. Ecol. 27:2233–2252.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Moraes, M. C. B., Laumann, R., Sujii, E. R., Pires, C., and Borges, M. 2005. Induced volatiles in soybean and pigeon pea plants artificially infested with the neotropical brown stink bug, Euschistus heros, and their effect on the egg parasitoid, Telenomus podisi. Entomol. Exp. Appl. 115:227–237.

    Article  CAS  Google Scholar 

  • Moran, N. A. 1986. Morphological adaptation to host plants in Uroleucon (Homoptera: Aphididae). Evolution 40:1044–1050.

    Article  Google Scholar 

  • Moran, P. J. and Thompson, G. A. 2001. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 125:1074–1085.

    Article  PubMed  CAS  Google Scholar 

  • Ngi-Song, A. J., Njagi, P. G. N., Torto, B., and Overholt, W. A. 2000. Identification of behaviorally active components from maize volatiles for the stemborer parasitoid Cotesia flavipes Cameron (Hymenoptera: Braconidae). Insect Sci. Appl. 20:181–189.

    CAS  Google Scholar 

  • Paré, P. W. and Tumlinson, J. H. 1997. De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol. 114:1161–1167.

    PubMed  Google Scholar 

  • Pareja, M. F. 2006. Tritrophic interactions and chemical ecology of a non-crop plant-aphid-parasitoid system. PhD dissertation. University of Reading, Reading, UK.

  • Pauw, B. and Memelink, J. 2004. Jasmonate-responsive gene expression. J. Plant Growth Regul. 23:200–210.

    Article  CAS  Google Scholar 

  • Payne, R. W., Harding, S. A., Murray, D. A., Soutar, D. M., Baird, D. B., Welham, S. J., Kane, A. F., Gilmour, A. R., Thompson, R., Webster, R., et al. 2005. GenStat Release 8 Reference Manual. Part 3: Procedure Library PL16. VSN International, Oxford.

    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 

  • Roßbach, A., Löhr, B., and Vidal, S. 2005. Generalism vesus specialism: responses of Diadegma mollipla (Holmgren) and Diadegema semiclausum (Hellen), to the host shift of the diamondback moth (Plutella xylostella L.) to peas. J. Insect Behav. 18:491–503.

    Article  Google Scholar 

  • Röse, U. S. R., Lewis, W. J., and Tumlinson, J. H. 1998. Specificity of systemically released cotton volatiles as attractants for specialist and generalist parasitic wasps. J. Chem. Ecol. 24:303–319.

    Article  Google Scholar 

  • Shiojiri, K., Takabayashi, J., Yano, S., and Takafuji, A. 2001. Infochemically mediated tritrophic interaction webs on cabbage plants. Popul. Ecol. 43:23–29.

    Article  Google Scholar 

  • Shiojiri, K., Ozawa, R., Matsui, K., Kishimoto, K., Kugimiya, S., and Takabayashi, J. 2006. Role of the lipoxygenase/lyase pathway of host-food plants in the host searching behavior of two parasitoid species, Cotesia glomerata and Cotesia plutellae. J. Chem. Ecol. 32:969–979.

    Article  PubMed  CAS  Google Scholar 

  • Smid, H. M., Van Loon, J. J. A., Posthumus, M. A., and Vet, L. E. M. 2002. GC-EAG-analysis of volatiles from Brussels sprouts plants damaged by two species of Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid wasp species. Chemoecology 12:169–176.

    Article  CAS  Google Scholar 

  • Takabayashi, J., Noda, T., and Takahashi, S. 1991. Plants produce attractants for Apanteles kariyai, a parasitoid of Pseudaletia separata; cases of ‘communication’ and ‘misunderstanding’ in parasitoid-plant interactions. Appl. Entomol. Zool. 26(2):237–243.

    Google Scholar 

  • Tjallingii, W. F. 2006. Salivary secretions by aphids interacting with proteins of phloem wound responses. J. Exp. Bot. 57:739–745.

    Article  PubMed  CAS  Google Scholar 

  • Turlings, T. C. J., Tumlinson, J. H., Eller, F. J., and Lewis, W. J. 1991. Larval-damaged plants: source of volatile synomones that guide the parasitoid Cotesia marginiventris to the micro-habitat of its hosts. Entomol. Exp. Appl. 58:75–82.

    Article  Google Scholar 

  • Turlings, T. C. J., Lengwiler, U. B., Bernasconi, M. L., and Weschler, D. 1998. Timing of induced volatile emissions in maize seedlings. Planta 207:146–152.

    Article  CAS  Google Scholar 

  • Van Poecke, R. M. P., Roosjen, M., 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.

    Article  Google Scholar 

  • Vet, L. E. M. 1996. Parasitoid foraging: the importance of variation in individual behaviour for population dynamics. in R. B. Floyd, A. W. Sheppard, and P. J. De Barro (eds.). Frontiers of population ecology pp. 245–256. Melbourne: CSIRO Publishing.

    Google Scholar 

  • Vet, L. E. M. 1999. From chemical to population ecology: infochemical use in an evolutionary context. J. Chem. Ecol. 25:31–49.

    Article  CAS  Google Scholar 

  • Vet, L. E. M. and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tritophic context. Annu. Rev. Entomol. 37:141–172.

    Article  Google Scholar 

  • Vinson, S. B. 1976. Host selection by insect parasitoids. Annu. Rev. Entomol. 21:109–134.

    Article  Google Scholar 

  • Völkl, W., Kranz, P., Weisser, W., and Hübner, G. 1995. Patch time allocation and resource exploitation in aphid primary parasitoids and hyperparasitoids searching simultaneously within aphid colonies. J. Appl. Entomol. 119:399–404.

    Article  Google Scholar 

  • Walling, L. L. 2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19:195–216.

    PubMed  CAS  Google Scholar 

  • Weisser, W. W. 1995. Within-patch foraging behaviour of the aphid parasitoid Aphidius funebris: plant architecture, host behaviour, and individual variation. Entomol. Exp. Appl. 76:133–141.

    Article  Google Scholar 

  • Whitman, D. W. and Eller, F. J. 1992. Orientation of Microplitis croceipes (Hymenoptera: Braconidae) to green leaf volatiles: dose–response curves. J. Chem. Ecol. 18:1743–1753.

    CAS  Google Scholar 

  • Will, T. and Van Bel, A. J. E. 2006. Physical and chemical interactions between aphids and plants. J. Exp. Bot. 57:729–737.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to K. Chamberlain, L. Wadhams, and M. Borges for providing help with the chemical analyses, J. Aldrich for providing synthetic standards, V. Brown for advice on the experiments, G. Piaggio for statistical advice and comments on previous versions of the manuscript, and M. Torrance and K. Plumb for help in rearing. We thank two anonymous reviewers and M. Hilker for valuable comments during the review process. This work was funded by a Lawes Trust–University of Reading award to MP. Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council (BBSRC) of the United Kingdom.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martín Pareja.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pareja, M., Moraes, M.C.B., Clark, S.J. et al. Response of the Aphid Parasitoid Aphidius funebris to Volatiles from Undamaged and Aphid-infested Centaurea nigra . J Chem Ecol 33, 695–710 (2007). https://doi.org/10.1007/s10886-007-9260-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-007-9260-y

Keywords

Navigation