Journal of Chemical Ecology

, Volume 33, Issue 7, pp 1405–1420 | Cite as

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

  • Stefano Colazza
  • Gloria Aquila
  • Claudio De Pasquale
  • Ezio Peri
  • Jocelyn G. Millar
Article

Abstract

Contact kairomones from adult southern green stink bugs, Nezara viridula (L.) (Heteroptera: Pentatomidae) that elicit foraging behavior of the egg parasitoid Trissolcus basalis (Wollaston) were investigated in laboratory experiments. Chemical residues from tarsi and scutella of N. viridula induced foraging by gravid female T. basalis. Residues from body parts of female N. viridula elicited stronger responses than those from the corresponding body parts of males. Deproteinized tarsi still elicited searching responses from wasps, indicating that the kairomone was not proteinaceous. Hexane extracts of host cuticular lipids induced searching responses from T. basalis, with a strong preference for extracts from female hosts. Extracts consisted primarily of linear alkanes from nC19 to nC34, with quantitative and qualitative differences between the sexes. Extracts of female N. viridula contained more nC23, nC24, and nC25 than the corresponding extracts from males, whereas nC19 was detected only in extracts from males. Direct-contact solid phase microextraction (DC-SPME) of N. viridula cuticle and of residues left by adult bugs walking on a glass plate confirmed gender-specific differences in nC19. Trissolcus basalis females responded weakly to a reconstructed blend of the straight-chain hydrocarbons, suggesting that minor components other than linear alkanes must be part of the kairomone. Addition of nC19 to hexane extracts of female N. viridula significantly reduced the wasps’ arrestment responses, similar to wasps’ responses to hexane extracts of male hosts. Overall, our results suggest that a contact kairomone that elicits foraging by T. basalis females is present in the cuticular lipids of N. viridula, and that the presence or absence of nC19 allows T. basalis females to distinguish between residues left by male or female hosts. The ecological significance of these results in the host location behavior of scelionid egg parasitoids is discussed.

Keywords

Trissolcus basalis Nezara viridula Egg parasitoid Motivated searching Arrestment response Indirect host-related cue Kairomone Cuticular hydrocarbons Hexane extract Solid-phase microextraction 

Notes

Acknowledgments

We thank Giampiero La Rocca for providing Trypsin-EDTA. This work was financially supported by Miur Cofin 2004. It is part of the European Science Foundation (ESF) Behavioral Ecology of Insect Parasitoids (BEPAR) scientific program.

References

  1. Beevers, M., Lewis, W. J., Gross, H. R., Jr., and Noldus, D. A. 1981. Kairomones and their use for management of entomophagous insects: X. Laboratory studies on manipulation of host-finding behavior of Trichogramma pretiosum Riley with a kairomone extracted from Heliothis zea (Boddie) moth scales. J. Chem. Ecol. 7:635-648.CrossRefGoogle Scholar
  2. Boo, K. S. and Yang, J. P. 2000. Kairomones used by Trichogramma chilonis to find Helicoverpa assulta eggs. J. Chem. Ecol. 26:359–375.CrossRefGoogle Scholar
  3. Borges, M., Colazza, S., Ramirez-Lucas, P., Chauhan, K. R., Kramer, M., Moraes, M. C. B., and Aldrich, J. R. 2003. Kairomonal effect of walking traces from Euschistus heros (Heteroptera: Pentatomidae) on two strains of Telenomus podisi (Hymenoptera: Scelionidade). Physiol. Entomol. 28:349–355.CrossRefGoogle Scholar
  4. Chabi-Olaye, A., Schulthess, F., Poehling, H. M., and Borgemeister, C. 2001. Host location and host discrimination behavior of Telenomus isis, an egg parasitoid of the African cereal stem borer Sesamia calamistis. J. Chem. Ecol. 27:663–678.PubMedCrossRefGoogle Scholar
  5. Colazza, S. and Rosi, M. C. 2001. Difference in the searching behaviors of two strains of the egg parasitoid Telenomus busseolae (Hymenoptera: Scelionidae). Eur. J. Entomol. 98:47–52.Google Scholar
  6. Colazza, S., Peri, D., Salerno, G., Peri, E., Lo pinto, M., and Liotta, G. 1999a. Xbug, a video tracking and motion analysis system for LINUX. XII International Entomophagous Insects Workshop. Pacific Grove, California, September 26–30, 1999.Google Scholar
  7. Colazza, S., Salerno, G., and Wajnberg, E. 1999b. 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.CrossRefGoogle Scholar
  8. Conti, E., Salerno, G., Bin, F., Williams, H. J., and Vinson, S. B. 2003. Chemical cues from Murgantia histrionica eliciting host location and recognition in the egg parasitoid Trissolcus brochymenae. J. Chem. Ecol. 29:115–130.PubMedCrossRefGoogle Scholar
  9. Conti, E., Salerno, G., Bin, F., and Vinson, S. B. 2004. The role of host semiochemicals in parasitoid specificity: a case study with Trissolcus brochymenae and Trissolcus simoni on pentatomid bugs. Biol. Control 29:435–444.CrossRefGoogle Scholar
  10. Eltz, T. 2006. Tracing pollinator footprints on natural flowers. J. Chem. Ecol. 32:907–915.PubMedCrossRefGoogle Scholar
  11. Gardner, S. M. and Van Lenteren, J. C. 1986. Characterization of the arrestment responses of Trichogramma evanescens. Oecologia 68:265–270.CrossRefGoogle Scholar
  12. Ghazi-bayat, A. and Hasenfuss, I. 1980. Zur Herkunft der Adhäsionsflüssigkeit der tarsalen Haftlappen bei den Pentatomide (Heteroptera). Zool. Anz. 204:13–18.Google Scholar
  13. Gibbs, A. G. 1998. Water-proofing properties of cuticular lipids. Am. Zool. 38:471–482.Google Scholar
  14. Godfray, H. C. J. 1994. Parasitoids: Behavioral and Evolutionary Ecology, Princeton Univ. Press, Princeton, NJ, USA.Google Scholar
  15. Grant, L. G. and Barbosa, P. 2006. Effects of leaf epicuticular wax on the movement, foraging behavior, and attack efficacy of Diaretiella rapae. Entomol. Exp. Appl. 121:115–122.CrossRefGoogle Scholar
  16. Hemptinne, J. L., Lognay, G., Doumbia, M., and Dixon, A. F. G. 2001. Chemical nature and persistence of the oviposition deterring pheromone in the tracks of the larvae of the two spot ladybird, Adalia bipunctata (Coleoptera : Coccinellidae). Chemoecology 11:43–47.CrossRefGoogle Scholar
  17. Howard, R. W. and Blomquist, G. J. 2005. Ecological, behavioural, and biochemical aspects of insect hydrocarbons. Annu. Rev. Entomol. 50:371–393.PubMedCrossRefGoogle Scholar
  18. Jones, R. L., Lewis, W. J., Beroza, B. A., and Sparks. A. N. 1973. Host-seeking stimulants (kairomones) for the egg parasite, Trichogramma evanescens. Environ. Entomol. 2:593–596.Google Scholar
  19. Klomp, H. 1981. Parasitic wasps as sleuthhounds. Response of ichneumonid to the trail of its host. Neth. J. Zool. 31:762–772.Google Scholar
  20. Kosaki, A. and Yamaoka, R. 1996. Chemical composition of footprints and cuticular lipids of three species of lady beetles. Jpn. J. App. Entomol. Zool. 40:47–53.Google Scholar
  21. Laing, J. 1937. Host-finding by insect parasites. I. Observations on the finding of host in Alysia manducator, Mormoniella vitripennis and Trichogramma evanescens. J. Anim. Ecol. 6:298–317.CrossRefGoogle Scholar
  22. Lewis, W. J. and Martin, J. 1990. Semiochemicals for use with parasitoids: Status and future. J. Chem. Ecol. 16:3067–3089.CrossRefGoogle Scholar
  23. Lewis, W. J., Nordlund, D. A., Gueldner, R. C., Teal, P. E. A., and Tumlinson, J. N. 1982. Kairomones and their use for management of entomophagous insects XIII. Kairomonal activity for Trichogramma spp of abdominal tips, excretion, and synthetic sex pheromone blend of Heliothis zea (Boddie) moths. J. Chem. Ecol. 9:1323–1331.CrossRefGoogle Scholar
  24. Mattiacci, L., Vinson, S. B., Williams, H. J., Aldrich, J. R., and Bin, F. 1993. A long range attractant kairomone for egg parasitoid Trissolcus basalis, isolated from defensive secretion of its host, Nezara viridula. J. Chem. Ecol. 19:1167–1181.CrossRefGoogle Scholar
  25. Mcauslane, H. J., Simmons, A. M., and Jackson, D. M. 2000. Parasitism of Bemisia argentifolii on collard with reduced or normal leaf wax. Fla. Entomol. 83:428–437.CrossRefGoogle Scholar
  26. Müller, C. and Riederer, M. 2005. Plant surface properties in chemical ecology. J. Chem. Ecol. 31:2621–2651.PubMedCrossRefGoogle Scholar
  27. Nakashima, Y., Birkett, M. A., Pye, B. J., Pickett, J. A., and Powell, W. 2004. The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata, by the aphid parasitoid, Aphidius ervi. J. Chem. Ecol. 30:1103–1116.PubMedCrossRefGoogle Scholar
  28. Powell, W. and Pickett, J. A. 2003. Manipulation of parasitoids for aphid pest management: progress and prospects. Pest Manag. Sci. 59:149–155.PubMedCrossRefGoogle Scholar
  29. 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.PubMedCrossRefGoogle Scholar
  30. Quicke, D. L. J. 1997. Parasitic Wasps. Chapman & Hall, London.Google Scholar
  31. Rani, P. U., Kumari, S. I., Sriramakrishna, T., and Sudhakar, T. R. 2007. Kairomones extracted from rice yellow stem borer and their influence on egg parasitization by Trichogramma japonicum Ashmead. J. Chem. Ecol. 33:59–73.CrossRefGoogle Scholar
  32. Salerno, G., Conti, E., Peri, E., Colazza, S., and Bin, F. 2006. Kairomone involvement in the host specificity of the egg parasitoid Trissolcus basalis. Eur. J. Entomol. 103:311–318.Google Scholar
  33. Schmidt, J. M. and Carter, M. H. 1992. The locomotory response of the egg parasitoid Trichogramma evanescens Westwood to hexane extracts of eastern spruce budworm scales (Choristoneura fumiferana) (Clemens). Can. J. Zool. 70:941–949.CrossRefGoogle Scholar
  34. Todd, J. W. 1989. Ecology and behavior of Nezara viridula. Annu. Rev. Entomol. 34:273–292.CrossRefGoogle Scholar
  35. Vet, L. E. M. 1999. From chemical to population ecology: Infochemical use in an evolutionary context. J. Chem. Ecol. 25:31–49.CrossRefGoogle Scholar
  36. 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
  37. Vinson, S. B. 1984. Parasitoid-host relationships, pp. 205–233, in R. T. Cardé, and W. J. Bell (eds.). Chemical Ecology of Insects. Chapman & Hall, New York.Google Scholar
  38. Vinson, S. B. 1991. Chemical signals used by parasitoids. Redia 74:15–42.Google Scholar
  39. Vinson, S. B. 1998. The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol. Control 11:79–96.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Stefano Colazza
    • 1
  • Gloria Aquila
    • 1
  • Claudio De Pasquale
    • 2
  • Ezio Peri
    • 1
  • Jocelyn G. Millar
    • 3
  1. 1.Department of S.En.Fi.Mi.Zo.Università di PalermoPalermoItaly
  2. 2.Department of C.I.S.A.C.Università di PalermoPalermoItaly
  3. 3.Department of EntomologyUniversity of CaliforniaRiversideUSA

Personalised recommendations