Host recognition by the specialist hoverfly Microdon mutabilis, a social parasite of the ant Formica lemani

Journal of Chemical Ecology

Volumn 34, Issue 2, 2008, Pages 168-178

  Schönrogge, Karsten ^a   Napper, Emma K V ^a,b   Birkett, Michael A ^b   Woodcock, Christine M ^b   Pickett, John A ^b   Wadhams, Lester J ^b   Thomas, Jeremy A ^c  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^b ROTHAMSTED RESEARCH   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

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

Indexed keywords

PHEROMONE;

ANT; BIOASSAY; CHEMICAL CUE; FLY; GAS CHROMATOGRAPHY; HABITAT USE; HOST LOCATION; HOST-PARASITE INTERACTION; HYPOTHESIS TESTING; LOCAL ADAPTATION; MASS SPECTROMETRY; OVIPOSITION; PHYSIOLOGICAL RESPONSE; RECOGNITION; SOCIAL INSECT; SOCIAL PARASITISM; SPECIALIST; SURVIVAL; VOLATILE SUBSTANCE; WORKER CASTE;

ANIMAL; ANT; ARTICLE; EGG LAYING; ELECTROPHYSIOLOGY; FEMALE; FLY; HOST PARASITE INTERACTION; ODOR; PARASITOLOGY; PHYSIOLOGY; SENSE ORGAN;

ANIMALS; ANTS; DIPTERA; ELECTROPHYSIOLOGY; FEMALE; HOST-PARASITE INTERACTIONS; ODORS; OVIPOSITION; PHEROMONES; SENSE ORGANS;

EURASIA; EUROPE; IRELAND; WESTERN EUROPE;

FORMICA LEMANI; FORMICIDAE; HEXAPODA; MICRODON (DIPTERAN FLY); MICRODON MUTABILIS; MYRMICA SCABRINODIS; SYRPHIDAE;

EID: 39149127563     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-007-9417-8     Document Type: Article

References (43)

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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
16. Godfray, H. C. J. 1994. Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, New Jersey.
17. Griffith, D. C., and Pickett, J. A. 1980. A potential application of aphid alarm pheromones. Entomol. Exp. Appl. 27:199-201.
18. Hölldobler, B. 1969. Host Finding by odor in the myrmecophilic beetle Atemeles pubicollis Bris.(Staphylinidae). Science. 166:757-758.
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.
20. Hölldobler, B., and Wilson, E. O. 1990. The ants. Springer Verlag, Berlin.
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.
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.
23. Morehead, S. A. 2001. Geographic variation in host location cues for a dipteran parasitoid of Paraponera clavata. Biotropica. 33:495-501.
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.
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.
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.
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.
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.
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.
30. Powell, W., and Pickett, J. A. 2003. Manipulation of parasitoids for aphid pest management: progress and prospects. Pest Manag. Sci. 59:149-155.
31. Sadeghi, H., and Gilbert, F. 2000. Oviposition preferences of aphidophagous hoverflies. Ecol. Entomol. 25:91-100.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.