Journal of Chemical Ecology

, Volume 38, Issue 4, pp 331–339 | Cite as

Stereoselective Chemical Defense in the Drosophila Parasitoid Leptopilina heterotoma is Mediated by (−)-Iridomyrmecin and (+)-Isoiridomyrmecin

  • Johannes Stökl
  • John Hofferberth
  • Maria Pritschet
  • Michael Brummer
  • Joachim Ruther


Chemical defense mechanisms are widespread among insects but have rarely been demonstrated in parasitoid wasps. Here, we show that the Drosophila parasitoid Leptopilina heterotoma (Hymenoptera, Figitidae) produces (−)-iridomyrmecin and (+)-isoiridomyrmecin in a cephalic gland, and that these chemicals have a highly repellent effect on ants. Stereoselective synthesis of 4 stereoisomers of iridomyrmecin allowed us to demonstrate that the repellent effect of iridomyrmecins depends on the stereochemistry. Potential food items impregnated with natural doses of (−)-iridomyrmecin were avoided by ants much longer than those impregnated with (+)-iridomyrmecin, (+)-isoiridomyrmecin, or (−)-isoiridomyrmecin, respectively. Quantitative headspace analyses revealed furthermore that females and males of L. heterotoma released iridomyrmecins in higher amounts when confronted with ants. This is the first time, that (−)-iridomyrmecin and (+)-isoiridomyrmecin are reported as natural products. Females synthesize more iridomyrmecins than males, and the most active (−)-iridomyrmecin is produced by females only. We, therefore, hypothesize that this defense mechanism is used mainly by female wasps when foraging for Drosophila larvae on rotten fruits, but also may protect male wasps during dispersal.


Leptopilina Drosophila Iridomyrmecin Isoiridomyrmecin Chemical defense 



The authors thank Prof. Dr. Thomas Hoffmeister, University of Bremen, for sending us a starter culture of L. heterotoma and two anonymous reviewers for their comments on the manuscript. This study was funded by the German Research Council (Deutsche Forschungsgemeinschaft, DFG; STO 996/1-1).

Supplementary material

10886_2012_103_MOESM1_ESM.docx (2.4 mb)
ESM 1 (DOCX 2427 kb)


  1. Beckett, J. S., Beckett, J. D., and Hofferberth, J. E. 2010. A divergent approach to the diastereoselective synthesis of several ant-associated iridoids. Org. Lett. 12:1408–1411.PubMedCrossRefGoogle Scholar
  2. Bettelli, E., Cherubini, P., D’andrea, P., Passacantilli, P., and Piancatelli, G. 1998. Mercuration-reductive demercuration of glycals: A mild and convenient entry to 2-deoxy-sugars. Tetrahedron 54:6011–6018.CrossRefGoogle Scholar
  3. Blum, M. S. 1996. Semiochemical parsimony in the arthropoda. Annu. Rev. Entomol. 41:353–374.PubMedCrossRefGoogle Scholar
  4. Brenna, E., Fuganti, C., and Serra, S. 2003. Enantioselective perception of chiral odorants. Tetrahedron-Asymmetry 14:1–42.CrossRefGoogle Scholar
  5. Byers, J. and Levi-Zada, A. 2011. Individual variation of (S)-4-methyl-3-heptanone in heads of braconid wasp, Leiophron uniformis, and Pogonomyrmex ants indicates costs of semiochemical production. Chemoecology 21:35–44.CrossRefGoogle Scholar
  6. Cavill, G. W. K. and Clark, D. V. 1971. Ant secretions and cantharidin, pp. 271–305, in M. Jacobson and D. G. Crosby (eds.), Naturally Occurring Insecticides. Marcel Dekker Inc, New York.Google Scholar
  7. Cavill, G. W. K. and Houghton, E. 1974. Volatile constituents of the Argentine ant, Iridomyrmex humilis. J. Insect Physiol. 20:2049–2059.PubMedCrossRefGoogle Scholar
  8. Cavill, G. W. and Locksley, H. D. 1957. The chemistry of ants. II. Structure and configuration of Iridolactone (Isoiridomyrmecin). Aust. J. Chem. 10:352–358.CrossRefGoogle Scholar
  9. Cavill, G. W. K., Houghton, E., Mcdonald, F. J., and Williams, P. J. 1976. Isolation and characterization of dolichodial and related compounds from the argentine ant, Iridomyrmex humilis. Insect Biochem. 6:483–490.CrossRefGoogle Scholar
  10. Choe, D.-H., Millar, J. G., and Rust, M. K. 2009. Chemical signals associated with life inhibit necrophoresis in Argentine ants. Proc. Natl. Acad. Sci. U.S.A. 106:8251–8255.PubMedCrossRefGoogle Scholar
  11. Dettner, K. 2010. Chemical defense and toxins of lower terrestrial and freshwater animals, pp. 387–410 in: Mander L. and Liu H.-W. (eds.), Comprehensive Natural Products II: Chemistry and Biology. Elsevier, Amsterdam.Google Scholar
  12. Dobler, S., Petschenka, G., and Pankoke, H. 2011. Coping with toxic plant compounds—The insect’s perspective on iridoid glycosides and cardenolides. Phytochemistry 72:1593–1604.PubMedCrossRefGoogle Scholar
  13. Francke, W. and Dettner, K. 2005. Chemical signalling in beetles, pp. 85–166, in S. Schulz (ed.), The Chemistry of Pheromones and Other Semiochemicals II. Springer, Berlin/Heidelberg.Google Scholar
  14. Goubault, M., Batchelor, T. P., Romani, R., Linforth, R. S. T., Fritzsche, M., Francke, W., and Hardy, I. C. W. 2008. Volatile chemical release by bethylid wasps: Identity, phylogeny, anatomy and behaviour. Biol. J. Linnean Soc. 94:837–852.CrossRefGoogle Scholar
  15. Hammer, Ø., Harper, D. A. T., and Ryan, P. D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4:9.Google Scholar
  16. Hedlund, K., Vet, L. E. M., and Dicke, M. 1996. Generalist and specialist parasitoid strategies of using odours of adult drosophilid flies when searching for larval hosts. Oikos 77:390–398.CrossRefGoogle Scholar
  17. Heimpel, G. E., Rosenheim, J. A., and Mangel, M. 1997. Predation on adult Aphytis parasitoids in the field. Oecologia 110:346–352.CrossRefGoogle Scholar
  18. Hilgraf, R. 1997. Stereoselektive Synthese trans-verknüpfter Iridomyrmecine und deren Vorkommen in Alloxysta victrix. (Diploma thesis). Universität Hamburg, Hamburg.Google Scholar
  19. Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6:65–70.Google Scholar
  20. Hübner, G. and Dettner, K. 2000. Hyperparasitoid defense strategies against spiders: The role of chemical and morphological protection. Entomol. Exp. Appl. 97:67–74.CrossRefGoogle Scholar
  21. Hübner, G., Völkl, W., Francke, W., and Dettner, K. 2002. Mandibular gland secretions in alloxystine wasps (Hymenoptera, Cynipoidea, Charipidae): Do ecological or phylogenetical constraints influence occurrence or composition? Biochem. Syst. Ecol. 30:505–523.CrossRefGoogle Scholar
  22. Huth, A. and Dettner, K. 1990. Defense chemicals from abdominal glands of 13 rove beetle species of subtribe staphylinina (Coleoptera: Staphylinidae, Staphylininae). J. Chem. Ecol. 16:2691–2711.CrossRefGoogle Scholar
  23. Ibarra-Wiltschek, D. 1995. Identifizierung und Synthese mono- und sesquiterpenoider Inhaltsstoffe aus Hymenopteren. (PhD Thesis) Universität Hamburg, Hamburg, Germany.Google Scholar
  24. Jefson, M., Meinwald, J., Nowicki, S., Hicks, K., and Eisner, T. 1983. Chemical defense of a rove beetle (Creophilus maxillosus). J. Chem. Ecol. 9:159–180.CrossRefGoogle Scholar
  25. Jenni, W. 1951. Beitrag zur Morphologie und Biologie der Cynipide Pseudeucoila bochei Weld, eines Larvenparasiten von Drosophila melanogaster Meig. Acta Zool. 32:177–254.CrossRefGoogle Scholar
  26. Kindle, H., Winistörfer, M., Lanzrein, B., and Mori, K. 1989. Relationship between the absolute configuration and the biological activity of juvenile hormone III. Cell. Mol. Life Sci. 45:356–360.CrossRefGoogle Scholar
  27. Kuwahara, Y. 1984. Identification of Skatole from a Bethylid Wasp, Cephalonomia gallicola (Ashmead)(Hymenoptera; Bethylidae). Agric. Biol. Chem. 48:2371–2372.CrossRefGoogle Scholar
  28. Mori, K. 2007. Significance of chirality in pheromone science. Bioorg. Med. Chem. 15:7505–7523.PubMedCrossRefGoogle Scholar
  29. Nordlander, G. 1980. Revision of the genus Leptopilina Förster, 1869, with notes on the status of some other genera (Hymenopter, Cynipoideam, Eucoilidae). Entomol. Scand. 11:428–453.CrossRefGoogle Scholar
  30. Pasteels, J. M., Grégoire, J. C., and Rowell-Rahier, M. 1983. The chemical ecology of defense in arthropods. Annu. Rev. Entomol. 28:263–289.CrossRefGoogle Scholar
  31. Pasteels, J. M., Braekman, J.-C., and Daloze, D. 1988. Chemical defense in the Chrysomelidae, pp. 233–252, in P. Jolivet, E. Petitpierre, and T. H. Hsiao (eds.), Biology of Chrysomelidae. Kluwer Academic Publishers, Dordrecht.CrossRefGoogle Scholar
  32. Pavan, M. 1949. Ricerche sugli antibiotici di origine animale. Nota riassuntiva. (Researches on antibiotic substances of animal origin). Ricerca scientifica e riconstruzione 19:1011–1017.Google Scholar
  33. Pavan, M. 1952. Iridomyrmecin as insecticide. Trans. IXth Int. Congr. Entomol. 1:321–327.Google Scholar
  34. Petersen, G. 2000. Signalstoffe in der innerartlichen Kommunikation des Hyperparasitoiden Alloxysta victrix (Hymenoptera: Cynipidae) und ihre Wirkung auf den Primärparasitoiden Aphidius uzbekistanicus und die Große Getreideblattlaus Sitobion avenae. (PhD Thesis) University of Kiel, Kiel, Germany.Google Scholar
  35. Reddy, I. K. and Mehvar, R. 2004. Chirality in Drug Design and Development. CRC Press, Boca Raton/London.CrossRefGoogle Scholar
  36. Ruther, J., Reinecke, A., Tolasch, T., and Hilker, M. 2001. Make love not war: a common arthropod defence compound as sex pheromone in the forest cockchafer Melolontha hippocastani. Oecologia 128:44–47.CrossRefGoogle Scholar
  37. Sakurai, S., Ohtaki, T., Mori, H., Fujiwhara, M., and Mori, K. 1990. Biological activity of enantiomerically pure forms of insect juvenile hormone I and III in Bombyx mori. Cell. Mol. Life Sci. 46:220–221.CrossRefGoogle Scholar
  38. Schöllhorn, B. and Mulzer, J. 2006. Stereocontrolled formation of three contiguous stereogenic centers by free radical cyclization—Synthesis of (+)-Iridomyrmecin and (−)-Iso-iridomyrmecin—formal synthesis of δ-Skythantine. Eur. J. Org. Chem. 2006:901–908.CrossRefGoogle Scholar
  39. Schultz, G., Simbro, E., Belden, J., Zhu, J., and Coats, J. 2004. Catnip, Nepeta cataria (Lamiales: Lamiaceae)—A closer look: Seasonal occurrence of nepetalactone isomers and comparative repellency of three terpenoids to insects. Environ. Entomol. 33:1562–1569.CrossRefGoogle Scholar
  40. Tomalski, M. D., Blum, M. S., Jones, T. H., Fales, H. M., Howard, D. F., and Passera, L. 1987. Chemistry and functions of exocrine secretions of the ants Tapinoma melanocephalum and T. erraticum. J. Chem. Ecol. 13:253–263.CrossRefGoogle Scholar
  41. Van den Dool, H. and Kratz, P. D. 1963. A generalization of the retention index system including linear temperature programmed gas—liquid partition chromatography. J. Chromatogr. A 11:463–471.CrossRefGoogle Scholar
  42. Völkl, W. 1992. Aphids or their parasitoids: Who actually benefits from ant-attendance? J. Anim. Ecol. 61:273–281.CrossRefGoogle Scholar
  43. Völkl, W., Hübner, G., and Dettner, K. 1994. Interactions between Alloxysta brevis (Hymenoptera, Cynipoidea, Alloxystidae) and honeydew-collecting ants: How an aphid hyperparasitoid overcomes ant aggression by chemical defense. J. Chem. Ecol. 20:2901–2915.CrossRefGoogle Scholar
  44. Weisser, W. W. and Völkl, W. 1997. Dispersal in the aphid parasitoid, Lysiphlebus cardui (Marshall) (Hym., Aphidiidae). J. Appl. Entomol. 121:23–28.CrossRefGoogle Scholar
  45. Weldon, P. J., Kramer, M., Gordon, S., Spande, T. F., and Daly, J. W. 2006. A common pumiliotoxin from poison frogs exhibits enantioselective toxicity against mosquitoes. Proc. Natl. Acad. Sci. U.S.A. 103:17818–17821.PubMedCrossRefGoogle Scholar
  46. Wheeler, J. W., Olagbemiro, T., Nash, A., and Blum, M. S. 1977. Actinidine from the defensive secretions of dolichoderine ants. J. Chem. Ecol. 3:241–244.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Johannes Stökl
    • 1
  • John Hofferberth
    • 2
  • Maria Pritschet
    • 1
  • Michael Brummer
    • 1
  • Joachim Ruther
    • 1
  1. 1.University of Regensburg, Institute for ZoologyRegensburgGermany
  2. 2.Department of ChemistryKenyon CollegeGambierUSA

Personalised recommendations