Journal of Chemical Ecology

, Volume 34, Issue 2, pp 168–178 | Cite as

Host Recognition by the Specialist Hoverfly Microdon mutabilis, a Social Parasite of the Ant Formica lemani

  • Karsten Schönrogge
  • Emma K. V. Napper
  • Michael A. Birkett
  • Christine M. Woodcock
  • John A. Pickett
  • Lester J. Wadhams
  • Jeremy A. Thomas


The larva of the hoverfly Microdon mutabilis is a specialist social parasite of the ant Formica lemani that is adapted to local groups of F. lemani colonies but mal-adapted to colonies of the same species situated only a few hundred meters away. At a study site in Ireland, F. lemani shares its habitat with four other ant species. All nest under stones, making the oviposition choice by M. mutabilis females crucial to offspring survival. In this study, we tested the hypothesis that, as an extreme specialist, M. mutabilis should respond to cues derived from its host rather than from its microenvironment, a phenomenon that has hitherto only been addressed in the context of herbivorous insects and their parasitoids. In behavioral assays, M. mutabilis females reacted to volatiles from F. lemani colonies by extending their ovipositors, presumably probing for an oviposition substrate. This behavior was not observed toward negative controls or volatiles from colonies of Myrmica scabrinodis, the host ant of the closely related Microdon myrmicae. Coupled gas chromatography-electroantennography (GC-EAG) that used antennal preparations of M. mutabilis located a single physiologically active compound within an extract of heads of F. lemani workers. Coupled GC-mass spectrometry (GC-MS) tentatively identified the compound as a methylated methylsalicylate. GC co-injection of the extract with authentic samples showed that of the four possible isomers (methyl 3-, 4-, 5-, and 6-methylsalicylate), only methyl 6-methylsalicylate co-eluted with the EAG-active peak. Furthermore, the response to methyl 6-methylsalicylate was four times higher than to those of the other isomers. Coupled GC-EAG and GC-MS also revealed physiological responses to two constituents, 3-octanone and 3-octanol, of the M. scabrinodis alarm pheromone. However, the behavioral trials did not reveal any behavior that could be attributed to these compounds. Results are discussed in the context of four phases of host location behavior, and of the characteristics, which volatile cues should provide to be useful for an extreme specialist such as M. mutabilis.


Host/parasite interactions Host recognition behavior Syrphidae Formicidae EAG GC Methyl 6-methylsalicylate 



We thank Judith Wardlaw for help with rearing and maintenance of ant colonies, and two anonymous referees for helpful comments. This work was partly funded by NERC (GR3/12662) and partly by the EU FP V project MacMan (EVK2-CT-2001-00126). Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council of the UK.


  1. Al Abassi, S., Birkett, M. A., Petterson, J., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 2001. Response of the ladybird parasitoid Dinocampus coccinellae to toxic alkaloids from the seven-spot ladybird, Coccinella septempunctata. J. Chem. Ecol. 27:33–43.PubMedCrossRefGoogle Scholar
  2. Attygalle, A. B., Billen, J. P. J., Jackson, B. D., and Morgan, E. D. 1990. Morphology and Chemical Contents of Dufour Glands of Pseudomyrmex Ants (Hymenoptera, Formicidae). Z. Naturforsch. 45:691–697.Google Scholar
  3. Cammerts, M. C., Attygalle, A. B., Evershed, R. P., and Morgan, E. D. 1985. The pheromonal activity of chiral 3-Octanol for Myrmica ants. Physiol. Ent. 10:33–36.Google Scholar
  4. Cammerts, M. C., Evershed, R. P., and Morgan, E. D. 1981. Comparative study of the mandibular gland secretion of 4 species of Myrmica ants. J. Insect Physiol. 27:225–231.CrossRefGoogle Scholar
  5. Cammerts, M. C., Evershed, R. P., and Morgan, E. D. 1982. Mandibular gland secretions of workers of Myrmica rugulosa and Myrmica schencki—Comparison with 4 other Myrmica species. Physiol. Ent. 7:119–125.Google Scholar
  6. Cammerts, M. C., Evershed, R. P., and Morgan, E. D. 1983. The volatile components of the mandibular gland secretion of workers of the ants Myrmica lobicornis and Myrmica sulcinodis. J. Insect Physiol. 29:659–664.CrossRefGoogle Scholar
  7. Cortesero, A. M., De Moraes, C. M., Stapel, J. O., Tumlinson, J. H., and Lewis, W. J. 1997. Comparisons and contrasts in host-foraging strategies of two larval parasitoids with different degrees of host specificity. J. Chem. Ecol. 23:1589–1606.CrossRefGoogle Scholar
  8. De Moraes, C. M., and Mescher, M. C. 2005. Intrinsic competition between larval parasitoids with different degrees of host specificity. Ecol. Ent. 30:564–570.CrossRefGoogle Scholar
  9. Dicke, M., Lenteren, J. C., Boskamp, G. J. F., and Voorst, R. 1985. Intensification and prolongation of host searching in Leptopilina heterotoma (Thomson)(Hymenoptera: Eucoilidae) through a kairomone produced by Drosophila melanogaster. J. Chem. Ecol. 11:125–136.CrossRefGoogle Scholar
  10. Du, Y., Poppy, G. M., Powell, W., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1998. Identification of semiochemicals released during aphid feeding that attract the parasitoid Aphidius ervi. J. Chem. Ecol. 24:1355–1368.CrossRefGoogle Scholar
  11. Duffield, R. M., and Blum, M. S. 1975. Methyl 6-methyl salicylate: Identification and function in a ponerine ant (Gnamptogenys pleurodon). CMLS. 31:466–466.Google Scholar
  12. Elmes, G. W., Barr, B., Thomas, J. A., and Clarke, R. T. 1999. Extreme host specificity by Microdon mutabilis (Diptera: Syrphidae), a social parasite of ants. Proc. R. Soc. Lond. B. 266:447–453.CrossRefGoogle Scholar
  13. Elmes, G. W., Thomas, J. A., and Wardlaw, J. C. 1991. Larvae of Maculinea rebeli, a Large Blue Butterfly, and their Myrmica host ants—Wild adoption and behavior in ant nests. J. Zool. 223:447–460.CrossRefGoogle Scholar
  14. Feener, D. H., Jacobs, L. F., and Schmidt, J. O. 1996. Specialized parasitoid attracted to a pheromone of ants. Anim. Behav. 51:61–66.CrossRefGoogle Scholar
  15. Gardner, M. G., Schönrogge, K., Elmes, G. W., and Thomas, J. A. 2007. Increased genetic diversity as a defence against parasites is undermined by social parasites: Microdon mutabilis hoverflies infesting Formica lemani ant colonies. Proc. R. Soc. Lond.B. 274:103–110.CrossRefGoogle Scholar
  16. Godfray, H. C. J. 1994. Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, New Jersey.Google Scholar
  17. Griffith, D. C., and Pickett, J. A. 1980. A potential application of aphid alarm pheromones. Entomol. Exp. Appl. 27:199–201.CrossRefGoogle Scholar
  18. Hölldobler, B. 1969. Host Finding by odor in the myrmecophilic beetle Atemeles pubicollis Bris.(Staphylinidae). Science. 166:757–758.PubMedCrossRefGoogle Scholar
  19. Hölldobler, B. 1970. Zur Physiologie der Gast-Wirt-Beziehungen (Myrmecophilie) bei Ameisen. II. Das Gastverhäiltnis des imaginalen Atemeles pubicollis Bris.(Col, Staphylinidae) zu Myrmica und Formica (Hym. Formicidae). Z. Vergl. Physiol. 66:176–189.CrossRefGoogle Scholar
  20. Hölldobler, B., and Wilson, E. O. 1990. The ants. Springer Verlag, Berlin.Google Scholar
  21. Jaffe, K., and Sanchez, C. 1984. On the nestmate recognition system and territorial marking behavior in the ant Camponotus rufipes. Insectes Soc. 31:302–315.CrossRefGoogle Scholar
  22. Maddrell, S. H. P. 1969. Secretion by the malpighian tubules of Rhodnius. The movements of ions and water. J. Exp. Biol. 51:71–97.Google Scholar
  23. Morehead, S. A. 2001. Geographic variation in host location cues for a dipteran parasitoid of Paraponera clavata. Biotropica. 33:495–501.Google Scholar
  24. Morehead, S. A., and Feener, D. H. 2000. Visual and chemical cues used in host location and acceptance by a dipteran parasitoid. J. Insect Behav. 13:613–625.CrossRefGoogle Scholar
  25. Morehead, S. A., Seger, J., Feener, D. H., and Brown, B. V. 2001. Evidence for a cryptic species complex in the ant parasitoid Apocephalus paraponerae (Diptera: Phoridae). Evol. Ecol. Res. 3:273–284.Google Scholar
  26. Morgan, E. D., Inwood, M. R., and Cammerts, M. C. 1978. Mandibular gland secretion of the ant Myrmica scabrinodis. Physiol. Entomol. 3::107–114.Google Scholar
  27. Musche, M., Anton, C., Worgan, A., and Settele, J. 2006. No experimental evidence for host ant related oviposition in a parasitic butterfly. J. Insect Behav. 19:631–643.CrossRefGoogle Scholar
  28. Orr, M. R., De Camargo, R. X., and Benson, W. W. 2003. Interactions between ant species increase arrival rates of an ant parasitoid. Anim. Behav. 65:1187–1193.CrossRefGoogle Scholar
  29. Pickett, J. A. 1990. GC-MS in insect pheromone identification: three extreme case histories, pp. 299–309, in A. R. McCaffery, and I.D. Wilson (eds.). Chromatography and Isolation of Insect Hormones and PheromonesPlenum Press, New York and London.Google Scholar
  30. 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
  31. Sadeghi, H., and Gilbert, F. 2000. Oviposition preferences of aphidophagous hoverflies. Ecol. Entomol. 25:91–100.CrossRefGoogle Scholar
  32. Schönrogge, K., Wardlaw, J. C., Thomas, J. A., and Elmes, G. W. 2000. Polymorphic growth rates in myrmecophilous insects. Proc. R. Soc. Lond. B. 267:771–777.CrossRefGoogle Scholar
  33. Schönrogge, K., Barr, B., Wardlaw, J. C., Napper, E. K. V., Gardner, M. G., Breen, J., Elmes, G. W., and Thomas, J. A. 2002. When rare species become endangered: cryptic speciation in myrmecophilous hoverflies. Biol. J. Linn. Soc. 75:291–300.CrossRefGoogle Scholar
  34. Schönrogge, K., Gardner, M. G., Elmes, G. W., Napper, E. K. V., Simcox, D. J., Wardlaw, J. C., Breen, J., Knapp, J. J., Pickett, J. A., and Thomas, J. A. 2006. Host propagation permits extreme local adaptation in a social parasite of ants. Ecol. Lett. 9:1032–1040.PubMedCrossRefGoogle Scholar
  35. Sutherland, J. P., Sullivan, M. S., and Poppy, G. M. 2001. Oviposition behavior and host colony size discrimination in Episyrphus balteatus (Diptera: Syrphidae). Bull. Entomol. Res. 91:411–417.PubMedCrossRefGoogle Scholar
  36. Thomas, J. A., and Elmes, G. W. 2001. Food-plant niche selection rather than the presence of ant nests explains oviposition patterns in the myrmecophilous butterfly genus Maculinea. Proc. R. Soc. Lond. B. 268:471–477.CrossRefGoogle Scholar
  37. Torres, J. A., Snelling, R. R., Blum, M. S., Flournoy, R. C., Jones, T. H., and Duffield, R. M. 2001. Mandibular gland chemistry of four Caribbean species of Camponotus (Hymenoptera: Formicidae). Biochem. Syst. Ecol. 29:673–680.PubMedCrossRefGoogle Scholar
  38. Van Alphen, J. J. M., and Visser, M. E. 1990. Superparasitism as an adaptive strategy for insect parasitoids. Annu. Rev. Entomol. 35:59–79.PubMedCrossRefGoogle Scholar
  39. Van Dyck, H., Oostermeijer, J. G. B., Talloen, W., Feenstra, V., Van der HiddeA., and Wynhoff, I. 2000. Does the presence of ant nests matter for oviposition to a specialized myrmecophilous Maculinea butterfly. Proc. R. Soc. Lond. B. 267:861–866.CrossRefGoogle Scholar
  40. 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
  41. Vet, L. E. M., Sokolowski, M. B., Macdonald, D. E., and Snellen, H. 1993. Responses of a generalist and a specialist parasitoid (Hymenoptera, Eucoilidae) to drosophilid larval kairomones. J. Insect Behav. 6:615–624.CrossRefGoogle Scholar
  42. Wadhams, L. J., Angst, M. E., and Blight, M. M. 1982. Responses of the olfactory receptors of Scolytus scolytus to the stereoisomeres of 4-methyl-3-heptanol. J. Chem. Ecol. 8:477–492.CrossRefGoogle Scholar
  43. Wadhams, L. J. 1990. The use of coupled gas chromatography: electrophysiological techniques in the identification of insect pheromones, pp, pp. 289–298, in A.R. McCaffery, and I. D. Wilson (eds.). Chromatography and Isolation of Insect Hormones and PheromonesPlenum Press, New York and London.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Karsten Schönrogge
    • 1
  • Emma K. V. Napper
    • 1
    • 2
  • Michael A. Birkett
    • 2
  • Christine M. Woodcock
    • 2
  • John A. Pickett
    • 2
  • Lester J. Wadhams
    • 2
  • Jeremy A. Thomas
    • 3
  1. 1.Centre for Ecology and HydrologyCEH WallingfordWallingfordUK
  2. 2.Biological Chemistry DivisionRothamsted ResearchHarpendenUK
  3. 3.Department of ZoologyUniversity of OxfordOxfordUK

Personalised recommendations