Protected by Fumigants: Beetle Perfumes in Antimicrobial Defense
- 304 Downloads
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.
KeywordsPhratora vitellinae Beauveria bassiana Metarhizium anisopliae Bacillus thuringiensis Fumigants Antimicrobial activity Glandular secretion Salicylaldehyde
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.
- 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.
- Bärlocher, F. 1999. Biostatistik. Thieme Publ., Stuttgart, Germany.Google Scholar
- 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
- 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.
- Garb, G. 1915. The eversible glands of a chrysomelid larva, Melasoma lapponica. J. Entomol. Zool. 7:87–97.Google Scholar
- 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
- 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
- Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6:65–70.Google Scholar
- 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
- 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
- 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
- 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
- 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
- StatSoft I. 1999. STATISTICA for Windows users manual, version 5.5.Google Scholar
- Tribolium Genome Sequencing Consortium 2008. The genome of the developmental model beetle and pest Tribolium castaneum. Nature: in press Google Scholar
- Vilcinskas, A., and Götz, P. 1999. Parasitic fungi and their interactions with the insect immune system. Adv. Parasitol. 43:268–313.Google Scholar
- 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
- Wallace, J. B., and Blum, M. S. 1969. Refined defensive mechanisms in Chrysomela scripta. Ann. Entomol. Soc. Am. 62:503–506.Google Scholar