Skip to main content

Advertisement

SpringerLink
Log in

Host Sex Discrimination by an Egg Parasitoid on Brassica Leaves

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

Abstract

Egg parasitoids are able to find their hosts by exploiting their chemical footprints as host location cues. In nature, the apolar epicuticular wax layer of plants that consists of several classes of hydrocarbons serves as the substrate that retains these contact kairomones. However, experiments on chemical footprints generally have used filter paper as substrate to study insect behavior. Here, we explored the ability of Trissolcus basalis (Scelionidae) females to discriminate between footprint cues left by male and female Nezara viridula (Pentatomidae) on leaves of their host plant Brassica oleracea (broccoli). Furthermore, we analyzed the chemical composition of the outermost wax layer of broccoli leaves to evaluate the degree of overlap in insect and plant cuticular hydrocarbons that could lead to masking effects in the detection of footprint cues. Our results showed that B. oleracea epicuticular wax retains the chemical footprints of adult bugs and allows T. basalis females to differentiate hosts of different sex. Traces of female bugs elicited more extensive searching behavior in egg parasitoids than traces of males. The application of n-nonadecane, a compound specific to male N. viridula, on the tarsi of female bugs prevented parasitoid females from distinguishing between host male and host female footprints. Analyses of B. oleracea leaves revealed that epicuticular waxes were mainly composed of linear alkanes, ketones, and secondary alcohols. Alkanes were dominated by n-nonacosane (nC29) and n-hentriacontane (nC31), while male-specific n-nonadecane (nC19) was absent. The ecological significance of these results for parasitoid host location behavior is discussed.

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

Access this article

Log in via an institution

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

  • Aldrich, J. R. 1996. Sex pheromones in Homoptera and Heteroptera, pp. 188–233, in C. W. Schafer (ed.) Studies on Hemipteran Phylogeny. Proceedings Thomas Say Publications in Entomology, Entomol. Soc. Am., Lanham, MD.

    Google Scholar 

  • Aldrich, J. R., Lusby, W. R., Kochansky, J. P., and Lockwood, J. A. 1987. Pheromone strains of the cosmopolitan pest, Nezara viridula (Heteroptera: Pentatomidae). J. Exp. Zool. 244:171–175.

    Article  CAS  Google Scholar 

  • Baker, E. 1974. Influence of environment on leaf wax development in Brassica oleracea var Gemmifera. New Phytol. 73:955–966.

    Article  CAS  Google Scholar 

  • Boo, K. S., and Yang, J. P. 2000. Kairomones used by Trichogramma chilonis to find Helicoverpa assulta eggs. J. Chem. Ecol. 26:359–375.

    Article  CAS  Google Scholar 

  • Bown, A. W., Hall, D. E., and Macgregor, K. B. 2002. Insect footsteps on leaves stimulate the accumulation of 4-aminobutyrate and can be visualized through increased chlorophyll fluorescence and superoxide production. Plant Physiology. 129:1430–1434.

    Article  PubMed  CAS  Google Scholar 

  • Chabi-olaye, A., Schulthess, F., Poehling, H. M., and Borgemeister, C. 2001. Host location and host dis- crimination behavior of Telenomus isis, an egg parasitoid of the African cereal stem borer Sesamia calamistis. J. Chem. Ecol. 27:663–678.

    Article  PubMed  CAS  Google Scholar 

  • Colazza, S., Rosi, C. M., and Clemente, A. 1997. Response of egg parasitoid Telenomus busseolae to sex pheromone of Sesamia nonagrioides. J. Chem. Ecol. 23:2437–2444.

    Article  CAS  Google Scholar 

  • Colazza, S., Salerno, G., and Wajnberg, E. 1999. Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol. Control. 16:310–317.

    Article  Google Scholar 

  • Colazza, S., Aquila, G., De Pasquale, C., Peri, E., and Millar, J. 2007. The egg parasitoid Trissolcus basalis uses n-nonadecane, a cuticular hydrocarbon from its stink bug host Nezara viridula, to discriminate between female and male hosts. J. Chem. Ecol. 33:1405–1420.

    Article  PubMed  CAS  Google Scholar 

  • Colazza, S., Lo Bue, M., Lo Giudice, D., and Peri, E. 2009. The response of Trissolcus basalis to footprint contact kairomones from Nezara viridula females is mediated by leaf epicuticular waxes. Naturwissenschaften 96:975–981.

    Article  PubMed  CAS  Google Scholar 

  • Colazza, S., Peri, E., Salerno, G., and Conti, E. 2010. Host searching by egg parasitoids: exploitation of host chemical cues, pp 97–147, in F. L. Cônsoli, J. R. P. Parra, R. A. Zucchi (eds.). Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Springer London New York.

    Google Scholar 

  • Conti, E., Salerno, G., Leombruni, B., Frati, F., and Bin, F. 2010. Short-range allelochemicals from a plant-herbivore association: a singular case of oviposition-induced synomone for an egg parasitoid. J. Exp. Biol. 213:3911–3919.

    Article  PubMed  CAS  Google Scholar 

  • Durak, D. 2008. Morphology and chemical composition of metathoracic scent glands in Dolycoris baccarum (Linnaeus, 1758) (Heteroptera: Pentatomidae). Acta Zool. 89:193–199.

    Article  Google Scholar 

  • Durak, D., and Kalender, Y. 2007. Fine structure and chemical analysis of the metathoracic scent gland of Eurygaster maura (Linnaeus, 1758) (Heteroptera: Scutelleridae). Folia Biol. 55:133–141.

    Article  CAS  Google Scholar 

  • Eigenbrode, S. D., and Espelie K. E. 1995. Effects of plant epicuticular lipids on insect herbivores. Annu. Rev. Entomol. 40:171–194.

    Article  Google Scholar 

  • Fatouros, N. E., Bukovinszkine’kiss, G., Dicke, M., and Hilker, M. 2007. The response specificity of Trichogramma egg parasitoids towards infochemicals during host location. J. Insect Behav. 20:53–6.

    Article  Google Scholar 

  • Fatouros, N. E., Dicke, M., Mumm, R., Meiners, T., and Hilker, M. 2008. Foraging behavior of egg parasitoids exploiting chemical information. Behav. Ecol. 19:677–689.

    Article  Google Scholar 

  • Gniwotta, F., Vogg, G., Gartmann, V., Carver, T. L. W., Riederer, M., and Jetter, R. 2005. What do microbes encounter at the plant surface? Chemical composition of pea leaf cuticular waxes. Plant Physiol. 139:519–530.

    Article  PubMed  CAS  Google Scholar 

  • Howard, R. W., and Blomquist, G. J. 2005. Ecological, behavioral, and biochemical aspects of insect hydrocarbons Annu. Rev. Entomol. 50:371–393.

    Article  CAS  Google Scholar 

  • Huigens, M. E., Woelke, J. B., Pashalidou, F. G., Bukovinszky, T., Smid, H. M., and Fatouros, N. E. 2010. Chemical espionage on species-specific butterfly anti-aphrodisiacs by hitchhiking Trichogramma wasps. Behav. Ecol. 21:470–478.

    Article  Google Scholar 

  • Hunsche, M., Bringe, K., Schmitz-eiberger, M., and Noga, G. 2006. Leaf surface characteristics of apple seedlings, bean seedlings and kohlrabi plants and their impact on the retention and rainfastness of mancozeb. Pest Man. Sci. 62:839–847.

    Article  CAS  Google Scholar 

  • Kim, K. S., Park, S. H., Kim, D. K., and Jenks, M. A. 2007. Influence of water deficit on leaf cuticular waxes of soybean (Glycine max [L.] Merr.). Int. J. Plant Sci. 168:307–316.

    Article  CAS  Google Scholar 

  • Klomp, H. 1981. Parasitic wasps as sleuthhounds: Response of an ichneumon wasp to the trail of its host. Neth. J. Zool. 31:762–772.

    Article  Google Scholar 

  • Lewis, W. J., Nordlund, D. A., Gueldner, R. C., Teal, P. E. A., and Tumlinson, J. H. 1982. Kairomones and their use for management of entomophagous insects. XIII. Kairomonal activity for Trichogramma spp. of abdominal tips, excretion and a synthetic sex pheromone blend of Heliothis zea (Boddie) moths. J. Chem. Ecol. 8:1323–1331.

    Article  CAS  Google Scholar 

  • Lo Giudice, D. 2009. Contact chemo-orientation in insect parasitoids: the case study of mate-finding in Metaphycus luteolus and host-finding in Trissolcus basalis. PhD dissertation. University of Palermo, Palermo, Italy.

  • Müller, C., and Riederer, M. 2005. Plant surface properties in chemical ecology. J. Chem. Ecol. 31:2621–2651.

    Article  PubMed  Google Scholar 

  • Peri, E., Sole, M. A., Wajnberg, E., and Colazza, S. 2006. Effect of host kairomones and oviposition experience on the arrestment behavior of an egg parasitoid. J. Exp. Biol. 209:3629–3635.

    Article  PubMed  Google Scholar 

  • Powell, G., Maniar, S. P., Pickett, J. A., and Hardie, J. 1999. Aphid responses to non-host epicuticular lipids. Entom. Exp. App. 91:115–123.

    Article  Google Scholar 

  • Purdy, S. J. and Truter E. V. 2010. Constitution of the surface lipid from the leaves of Brassica oleracea (var. capitata (winnigstadt)). iii. nonacosane and its derivatives. Proc. R. Soc. Lond. B 1963 158:553–565.

    Article  Google Scholar 

  • Riedel, M., Eichner, A., and Jetter, R. 2003. Slippery surfaces of carnivorous plants: composition of epicuticular wax crystals in Nepenthes alata Blanco pitchers. Planta 218:87–97.

    Article  PubMed  CAS  Google Scholar 

  • Rostás, M., and Wölfling, M. 2009. Caterpillar footprints as host location kairomones for Cotesia marginiventris: persistence and chemical nature. J. Chem Ecol. 35: 20–27.

    Article  PubMed  Google Scholar 

  • Rostás, M., Ruf, D., Zabka, V., and Hildebrandt, U. 2008. Plant surface wax affects parasitoid’s response to host footprints. Naturwissenschaften 95:997–1002.

    Article  PubMed  Google Scholar 

  • Salerno, G., Conti, E., Peri, E., Colazza, S., and Bin, F. 2006. Kairomone involvement in the host speci- ficity of the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Eur. J. Entomol. 103:311–318.

    Google Scholar 

  • Salerno, G., Frati, F., Conti, E., De Pasquale, C., Peri, E., and Colazza, S. 2009. A finely tuned strategy adopted by an egg parasitoid to exploit chemical traces from host adults. J. Exp. Biol. 212:1825–1831.

    Article  PubMed  CAS  Google Scholar 

  • Szafranek, B. M., and Synak, E. E. 2006. Cuticular waxes from potato (Solanum tuberosum) leaves. Phytochemistry 67:80–90.

    Article  PubMed  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 

  • Witjes, S., and Eltz, T. 2009. Hydrocarbon footprints as a record of bumblebee flower visitation. J. Chem. Ecol. 35:1320–1325.

    Article  PubMed  CAS  Google Scholar 

  • Zygadlo, J., Maestri, D., and Grosso, N. 1994. Alkane distribution in epicuticular wax of some Solanaceae species. Biochem. System. Ecol. 22:203–209.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Mauro Lo Bue for assistance in the behavioral bioassays run at University of Palermo, Paolo Lucido for help in the collections of N. viridula from fields, Olga Frank for technical assistance with the GC analysis, and John Marris for constructive comments on the manuscript. The work was partially supported by the German DAAD and the Italian CRUI within the German-Italian bilateral program “VIGONI 2009”.

Author information

Authors and Affiliations

  1. Dipartimento DEMETRA, Università degli Studi di Palermo, Palermo, Italy

    Daniela Lo Giudice, Ezio Peri & Stefano Colazza

  2. Department of Botany II, University of Würzburg, Würzburg, Germany

    Michael Riedel & Michael Rostás

  3. Bio-Protection Research Centre, Lincoln University, Lincoln, 7647, New Zealand

    Michael Rostás

Authors
  1. Daniela Lo Giudice
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Riedel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Rostás
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ezio Peri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stefano Colazza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stefano Colazza.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lo Giudice, D., Riedel, M., Rostás, M. et al. Host Sex Discrimination by an Egg Parasitoid on Brassica Leaves. J Chem Ecol 37, 622–628 (2011). https://doi.org/10.1007/s10886-011-9957-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-011-9957-9

Key Words

Search

Navigation