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Journal of Chemical Ecology

, 34:179 | Cite as

Protected by Fumigants: Beetle Perfumes in Antimicrobial Defense

  • Jürgen Gross
  • Kerstin Schumacher
  • Henrike Schmidtberg
  • Andreas Vilcinskas
Article

Abstract

Beetles share with other eukaryotes an innate immune system that mediates endogenous defense against pathogens. In addition, larvae of some taxa produce fluid exocrine secretions that contain antimicrobial compounds. In this paper, we provide evidence that larvae of the brassy willow leaf beetle Phratora vitellinae constitutively release volatile glandular secretions that combat pathogens in their microenvironment. We identified salicylaldehyde as the major component of their enveloping perfume cloud, which is emitted by furrow-shaped openings of larval glandular reservoirs and which inhibits in vitro the growth of the bacterial entomopathogen Bacillus thuringiensis. The suggested role of salicylaldehyde as a fumigant in exogenous antimicrobial defense was confirmed in vivo by its removal from glandular reservoirs. This resulted in an enhanced susceptibility of the larvae to infection with the fungal entomopathogens Beauveria bassiana and Metarhizium anisopliae. Consequently, we established the hypothesis that antimicrobial defense in beetles can be expanded beyond innate immunity to include external disinfection of their microenvironment, and we report for the first time the contribution of fumigants to antimicrobial defense in animals.

Keywords

Phratora vitellinae Beauveria bassiana Metarhizium anisopliae Bacillus thuringiensis Fumigants Antimicrobial activity Glandular secretion Salicylaldehyde 

Notes

Acknowledgments

We thank Gisbert Zimmermann (BBA Darmstadt, Germany) for providing the different strains of entomopathogenic bacteria and fungi and Monika Hilker (Berlin, Germany) for providing the GC-MS for analysis of headspace samples. The authors are indebted to Rod Snowdon (Giessen, Germany) for editing the manuscript.

References

  1. Altincicek B., Knorr E., and Vilcinskas A. 2007. Beetle immunity: Identification of immune-inducible genes from the model insect Tribolium castaneum. Dev. Comp. Immunol., DOI  10.1016/j.dci.2007.09.005.
  2. Bärlocher, F. 1999. Biostatistik. Thieme Publ., Stuttgart, Germany.Google Scholar
  3. Blum, M. S., Brand, J. M., Wallace, J. B., and Fales, H. M. 1972. Chemical characterisation of the defensive secretion of a chrysomelid larva. Life Sci. 11:525–531.CrossRefGoogle Scholar
  4. Clarkson, J. M., and Charnley, A. K. 1996. New insights into the mechanisms of fungal pathogenesis in insects. Trends Microbiol. 4:197–203.PubMedCrossRefGoogle Scholar
  5. Dettner, K. 1985. Ecological and phylogenetic significance of defensive compounds from pygidial glands of Hydradephaga (Coleoptera). Proc. Acad. Nat. Sci. Philadelphia 137:156–171.Google Scholar
  6. Dettner, K., Fettköther, R., Ansteeg, O., Deml, R., Liepert, C., Petersen, B., Haslinger, E., and Francke, W. 1992. Insecticidal fumigants from defensive glands of insects—a fumigant test with adults of Drosophila melanogaster. J. Appl. Entomol. 113:128–137.CrossRefGoogle Scholar
  7. Freitak, D., Wheat, C. W., Heckel, D. G., and Vogel, H. 2007. Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biology, DOI  10.1186/1741-7007-5-56.
  8. Garb, G. 1915. The eversible glands of a chrysomelid larva, Melasoma lapponica. J. Entomol. Zool. 7:87–97.Google Scholar
  9. Gillespie, J. P., Bailey, A. M., Cobb, B., and Vilcinskas, A. 2000. Fungi as elicitors of insect immune responses. Arch. Insect Biochem. Physiol. 44:49–68.PubMedCrossRefGoogle Scholar
  10. Grégoire, J.-C. 1988. Larval gregariousness in the Chrysomelidae, pp. 253–260, in P. H., Jolivet, E., Petitpierre, T. H., and Hsiao (eds.). Biology of ChrysomelidaeKluwer Academic Publisher, Dordrecht, The Netherlands.Google Scholar
  11. Gross, J., and Hilker, M. 1995. Chemoecological studies of the exocrine glandular larval secretions of two chrysomelid species (Coleoptera): Phaedon cochleariae and Chrysomela lapponica. Chemoecology 5/6:185–189.CrossRefGoogle Scholar
  12. Gross, J., Müller, C., Vilcinskas, A., and Hilker, M. 1998. Antimicrobial activity of the exocrine glandular secretions, hemolymph and larval regurgitate of the mustard leaf beetle Phaedon cochleariae. J. Invertebr. Pathol. 72:296–303.PubMedCrossRefGoogle Scholar
  13. Gross, J., Podsiadlowski, L., and Hilker, M. 2002. Antimicrobial activity of exocrine glandular secretion of Chrysomela larvae. J. Chem. Ecol. 28:317–331.PubMedCrossRefGoogle Scholar
  14. Gross, J., Fatouros, N. E., Neuvonen, S., and Hilker, M. 2004. The importance of specialist natural enemies for Chrysomela lapponica in pioneering a new hostplant. Ecol. Entomol. 29:584–593.CrossRefGoogle Scholar
  15. Herzner, G., and Strohm, E. 2007. Fighting fungi with physics: Food wrapping by a solitary wasp prevents water condensation. Curr. Biol. 17:R46–R47.PubMedCrossRefGoogle Scholar
  16. Herzner, G., Schmitt, T., Peschke, K., Hilpert, A., and Strohm, E. 2007. Food wrapping with the postpharyngeal gland secretion by females of the European beewolf Philanthus triangulum. J. Chem. Ecol. 33:849–859.PubMedCrossRefGoogle Scholar
  17. Hilker, M., and Schulz, S. 1994. Composition of larval secretion of Chrysomela lapponica (Coleoptera, Chrysomelidae) and its dependence on host plant. J. Chem. Ecol. 20:1075–1093.CrossRefGoogle Scholar
  18. Hinton, H. E. 1951. On a little-known protective device of some chrysomelid pupae (Coleoptera). Proc. R. Entomol. Soc. Lond. 26:67–73.Google Scholar
  19. Hoffmann, J. A. 2003. The immune response of Drosophila. Nature 426:33–38.PubMedCrossRefGoogle Scholar
  20. Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6:65–70.Google Scholar
  21. Humber, R. A. 1996. Fungal pathogens of the Chrysomelidae and prospects of their use in biological control, pp. 93–115, in P. H., Jolivet, M. L., and Cox (eds.). Chrysomelidae Biology, SPB Academic Publ., Amsterdam, The Netherlands.Google Scholar
  22. Köpf, A., Rank, N. E., Roininen, H., and Tahvanainen, J. 1997. Defensive larval secretions of leaf beetles attract a specialist predator Parasyrphus nigritarsis. Ecol. Entomol. 22:176–183.CrossRefGoogle Scholar
  23. Kovac, D., and Maschwitz, U. 1990. Secretion-grooming in aquatic beetles (Hydradephaga): A chemical protection against contamination of the hydrofuge respiratory region. Chemoecology 1:131–138.CrossRefGoogle Scholar
  24. Kuhn, J., Pettersson, E. M., Feld, B., Burse, A., Termonia, A., Pasteels, J. M., and Boland, W. 2004. Selective transport systems mediate sequestration of plant glucosides in leaf beetles: A molecular basis for adaptation and evolution. Proc. Natl. Acad. Sci. U. S. A. 101:13808–13813.PubMedCrossRefGoogle Scholar
  25. Nahrung, H. F., Dunstan, P. K., and Allen, G. R. 2001. Larval gregariousness and neonate establishment of the eucalypt-feeding beetle Chrysophtharta agricola (Coleoptera: Chrysomelidae: Paropsini). Oikos 94:358–364.CrossRefGoogle Scholar
  26. Oldham, N. J., Veith, M., and Boland, W. 1996. Iridoid monoterpene biosynthesis in insects: evidence for a de novo pathway occurring in the defensive glands of Phaedon armoraciae (Chrysomelidae) leaf beetle larvae. Naturwissenschaften 83:470–473.Google Scholar
  27. Pasteels, J. M., Braekman, J.-C., Daloze, D., and Ottinger, R. 1982. Chemical defence in chrysomelid larvae and adults. Tetrahedron 38:1891–1897.CrossRefGoogle Scholar
  28. Pasteels, J. M., Daloze, D., and Rowell-Rahier, M. 1986. Chemical defence in chrysomelid eggs and neonate larvae. Physiol. Entomol. 11:29–37.Google Scholar
  29. Pasteels, J. M., Braekman, J.-C., and Daloze, D. 1988. Chemical defence in the Chrysomelidae, pp. 233–252, in P. H. Jolivet, E. Petitpierre, and T. H. Hsiao (eds.). Biology of ChrysomelidaeKluwer Academic Publ., Dordrecht, The Netherlands.Google Scholar
  30. Rosengaus, R. B., Lefebvre, M. L., and Traniello, J. F. A. 2000. Inhibition of fungal spore germination by Nasutitermes: Evidence for a possible antiseptic role of soldier defensive secretions. J. Chem. Ecol. 26:21–39.CrossRefGoogle Scholar
  31. Rostás, M., and Hilker, M. 2002. Feeding damage by larvae of the mustard leaf beetle deters conspecific females from oviposition and feeding. Entomol. Exp. Appl. 103:267–277.CrossRefGoogle Scholar
  32. Rowell-Rahier, M., and Pasteels, J. M. 1986. Economics of chemical defense in Chrysomelinae. J. Chem. Ecol. 12:1189–1203.CrossRefGoogle Scholar
  33. Royet, J., Reichhart, J. M., and Hoffmann, J. A. 2005. Sensing and signaling during infection in Drosophila. Curr. Opin. Immunol. 17:11–17.PubMedCrossRefGoogle Scholar
  34. StatSoft I. 1999. STATISTICA for Windows users manual, version 5.5.Google Scholar
  35. Traniello, J. F., Rosengaus, R. B., and Savoie, K. 2002. The development of immunity in a social insect: Evidence for the group facilitation of disease resistance. Proc. Natl. Acad. Sci. U. S. A. 99:6838–6842.PubMedCrossRefGoogle Scholar
  36. Tribolium Genome Sequencing Consortium 2008. The genome of the developmental model beetle and pest Tribolium castaneum. Nature: in press Google Scholar
  37. Vilcinskas, A., and Götz, P. 1999. Parasitic fungi and their interactions with the insect immune system. Adv. Parasitol. 43:268–313.Google Scholar
  38. Vilcinskas, A., and Gross, J. 2005. Drugs from bugs: The use of insects as a valuable source of transgenes with potential in modern plant protection strategies. Journal of Pest Science 78:187–191.CrossRefGoogle Scholar
  39. Wain, R. L. 1943. The secretion of salicylaldehyde by the larvae of the brassy willow beetle (Phyllodecta vitellinae L.). Ann. Rep. Agric. Horticult. Res. Stat. 108–110.Google Scholar
  40. Wallace, J. B., and Blum, M. S. 1969. Refined defensive mechanisms in Chrysomela scripta. Ann. Entomol. Soc. Am. 62:503–506.Google Scholar
  41. Wilson, K., Knell, R., Boots, M., and Koch-Osborne, J. 2003. Group living and investment in immune defence: an interspecific analysis. J. Anim. Ecol. 72:133–143.CrossRefGoogle Scholar
  42. Zvereva, E. L., and Rank, N. E. 2004. Fly parasitoid Megaselia opacicornis uses defensive secretions of the leaf beetle Chrysomela lapponica to locate its host. Oecologia 140:516–522.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Jürgen Gross
    • 1
  • Kerstin Schumacher
    • 2
  • Henrike Schmidtberg
    • 1
  • Andreas Vilcinskas
    • 1
  1. 1.Institute of Phytopathology and Applied ZoologyJustus-Liebig University GiessenGiessenGermany
  2. 2.Institute for Integrated Plant ProtectionFederal Biological Research Centre for Agriculture and ForestryKleinmachnowGermany

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