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Females of the Bumblebee Parasite, Aphomia sociella, Excite Males Using a Courtship Pheromone

Abstract

Aphomia sociella (Lepidoptera: Pyralidae: Galleriinae) is a parasitic moth of bumblebees. Behavioral experiments show that A. sociella females emit semiochemicals that influence male pre-mating behavior and serve as a courtship pheromone. GC/EAD and two-dimensional GC/MS (GCxGC-TOFMS) analyses of extracts of females revealed three antennally active compounds. Comparative GC and GCxGC-TOFMS analyses of extracts and synthetic standards confirmed the identity of the antennally active compounds as hexan-1-ol (1), 6,10,14-trimethylpentadecan-2-one (2), and 6,10,14-trimethylpentadecan-2-ol (3). In laboratory bioassays, alcohol 3 and, at higher doses, ketone 2 initiated male courtship behavior associated with ultrasonic production. Hexan-1-ol (1) and ketone 2 enhanced the activity of alcohol 3. These data suggest that hexan-1-ol, 6,10,14-trimethylpentadecan-2-ol, and 6,10,14-trimethylpentadecan-2-one constitute the female-produced courtship pheromone of A. sociella.

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References

  1. Atkinson, P. R. 1982. Structure of the putative pheromone glands of Eldana saccharina Walker (Lepidoptera: Pyralidae). J Entomol Soc South Afr 45:93–104.

    Google Scholar 

  2. Bennett, A. L., Atkinson, P. R., and la Croix, N. J. S. 1991. On communication in the African sugarcane borer, Eldana saccharina Walker (Lepidoptera: Pyralidae). J Entomol Soc South Afr 54:243–259.

    Google Scholar 

  3. Burger, B. V., Mackenroth, W. M., Smith, D., Spies, H. S. C., and Atkinson, P. R. 1985. Chemical composition of the wing gland and abdominal hair pencil secretions of the male African sugarcane borer, Eldana saccharina (Lepidoptera: Pyralidae). Z Naturforsch C: Biosci 40:847–850.

    Google Scholar 

  4. Burger, B. V., Nell, A. E., Smit, D., Spies, H. S. C., Mackenroth, W. M., Groche, D., and Atkinson, P. R. 1993. Constituents of wing gland and abdominal hairpencil secretions of male African sugarcane borer, Eldana saccharina Walker (Lepidoptera: Pyralidae). J Chem Ecol 19:2255–2277.

    Article  CAS  Google Scholar 

  5. Conner, W. E. 1999. ‘Un chant d’appel amoureux’: acoustic communication in moths. J Exp Biol 202:1711–1723.

    PubMed  Google Scholar 

  6. Farine, J. P. 1983. The exocrine glands of the male of Eldana saccharina Walker (Lepidoptera, Galleriinae): Intervention in precopulatory behavior. J Morphol 178:77–87.

    Article  Google Scholar 

  7. Flint, H. M. and Merkle, J. R. 1983. Mating behavior, sex pheromone responses and radiation sterilization of the greater wax moth (Lepidoptera: Pyralidae). J Econ Entomol 76:467–472.

    CAS  Google Scholar 

  8. Friberg, M., Vongvanich, N., Borg-Karlson, A.-K., Kemp, D. J., Merilaita, S., and Wiklund, C. 2008. Female mate choice determines reproductive isolation between sympatric butterflies. Behav Ecol Sociobiol 62:876–886.

    Article  Google Scholar 

  9. Greenfield, M. D. 2002. Signalers and receivers: Mechanisms and evolution of arthropod communication. Oxford University Press, Oxford.

    Google Scholar 

  10. Greenfield, M. D. and Coffelt, J. A. 1983. Reproductive behaviour of the lesser waxmoth, Achroia grisella (Pyralidae: Galleriinae): signalling, pair formation, male interactions, and mate guarding. Behaviour 84:287–315.

    Article  Google Scholar 

  11. Hall, D. R., Cork, A., Lester, R., Nesbitt, B. F., and Zagatti, P. 1987. Sex pheromones of rice moth, Corcyra cephalonica Stainton II. Identification and role of female pheromone. J Chem Ecol 13:1575–1589.

    Article  CAS  Google Scholar 

  12. Heath, R. R., Landolt, P. J., Dueben, B. D., Murphy, R. E., and Schneider, R. E. 1992. Identification of male cabbage looper sex pheromone attractive to females. J Chem Ecol 18:441–453.

    Article  CAS  Google Scholar 

  13. Hendricks, D. E. and Shaver, T. N. 1975. Tobacco budworm: male pheromne suppressed emission of sex pheromone by the female. Environ Entomol 3:555–558.

    Google Scholar 

  14. Hillier, N. K. and Vickers, N. J. 2004. The role of heliothine hairpencil compounds in female Heliothis virescens (Lepidoptera: Noctuidae) behavior and mate acceptance. Chem Senses 29:499–511.

    PubMed  Article  CAS  Google Scholar 

  15. Huang, Y., Xu, S., Tang, X., Zhao, Z., and Du, J. 1996. Male orientation inhibitor of cotton bollworm: identification of compounds produced by male hairpencil glands. Entomol Sinica 3:172–182.

    Google Scholar 

  16. Jacquin, E., Nagnan, P., and Frerot, B. 1991. Identification of hairpencil secretion from male Mamestra brassicae (L.) (Lepidoptera: Noctuidae) and electroantennogram studies. J Chem Ecol 17:239–247.

    Article  CAS  Google Scholar 

  17. Kalinová, B., Kindl, J., Jiroš, P., Žáček, P., Vašíčková, S., Buděšínský, M., and Valterová, I. 2009. Composition and electrophysiological activity of constituents identified in male wing gland secretion of the bumblebee parasite Aphomia sociella. J Nat Prod 72:8–13.

    PubMed  Article  Google Scholar 

  18. Kindl, J., Kalinová, B., Červenka, M., Jílek, M., and Valterová, I. 2011. Male moth songs tempt female to accept mating: the role of acoustic and pheromonal communication in the reproductive behavior of A. sociella. PlosOne 69:e26476.

    Google Scholar 

  19. Loudon, C. and Koehl, M. A. R. 2000. Sniffing by a silkworm moth: wing fanning enhances air penetration through and pheromone interception by antennae. J Exp Biol 203:2977–2990.

    PubMed  CAS  Google Scholar 

  20. Nieberding, C. M., de Vos, H., Schneider, M. V., Lassance, J.-M., Estramil, N., andersson, J., Bang, J., Hedenstroem, E., Loefstedt, C., and Brakefield, P. M. 2008. The male sex pheromone of the butterfly Bicyclus anynana: towards an evolutionary analysis. PLoS One 3:e2751.

    PubMed  Article  Google Scholar 

  21. Percy, J. E. and Weatherston, J. 1974. Gland structure and pheromone production in insects, pp. 11–34, in M. C. Birch (ed.), Pheromones. North-Holland Publishing Company, Amsterdam.

    Google Scholar 

  22. Percy-Cunningham, J. E. and MacDonald, J. A. 1987. Biology and ultrastructure of sex pheromone-producing glands, pp. 27–75, in G. D. Prestwich and C. J. Blomquist (eds.), Pheromone biochemistry. Academic, London.

    Google Scholar 

  23. Phelan, P. L. and Baker, T. C. 1990. Comparative-study of courtship in 12 Phycitine moths (Lepidoptera, Pyralidae). J Insect Behav 3:303–326.

    Google Scholar 

  24. Phelan, P. L., Silk, P. J., Northcott, C. J., Tan, S. H., and Baker, T. C. 1986. Chemical identification and behavioral characterization of male wing pheromone of Ephestia elutella (Pyralidae). J Chem Ecol 12:135–146.

    Article  CAS  Google Scholar 

  25. Sasaerila, Y., Gries, R., Gries, G., Khaskin, G., King, S., Takacs, S., and Hardi 2003. Sex pheromone components of male Tirathaba mundella (Lepidoptera: Pyralidae). Chemoecology 13:89–93.

    CAS  Google Scholar 

  26. Spangler, H. G. 1985. Sound production and communication by the greater wax moth (Lepidoptera: Pyralidae). Ann Entomol Soc Am 78:54–61.

    Google Scholar 

  27. Spangler, H. G. 1987a. Ultrasonic communication in Corcyra cephalonica (Stainton) (Lepidoptera:Pyralidae). J Stored Prod Res 23:203–211.

    Article  Google Scholar 

  28. Spangler, H. G. 1987b. Acoustically mediated pheromone release in Galleria mellonella (Lepidoptera: Pyralidae). J Insect Physiol 33:465–468.

    Article  Google Scholar 

  29. Spangler, H. G. 1988. Moth hearing, defense and communication. Annu Rev Entomol 33:59–81.

    Article  Google Scholar 

  30. Spangler, H. G., Greenfield, M. D., and Takessian, A. 1984. Ultrasonic mate calling in the lesser wax moth. Physiol Entomol 9:87–95.

    Article  Google Scholar 

  31. Takayoshi, K. and Hiroshi, H. 1999. Identification and possible functions of the hairpencil scent of the yellow peach moth, Conogethes punctiferalis Guenee (Lepidoptera: Pyralidae). Appl Entomol Zool 34:147–153.

    Google Scholar 

  32. Teal, P. E. A., McLauglin, J. R., and Tumlinson, J. H. 1981. Analysis of the reproductive behavior of Heliothis virescens (F.) under laboratory conditions. Ann Entomol Soc Am 74:324–330.

    Google Scholar 

  33. Vendilo, N. V., Lebedeva, K. V., Ponomarev, V. L., and Pletnev, V. A. 1998. Identification of the pheromone of the male of the greater wax moth Galleria mellonella (Lepidoptera: Galleriinae). Agrokhimiya 12:52–56.

    Google Scholar 

  34. Vohringer, K. 1934. Zur Biologie der grossen Wachsmotte (Galleria mellonella L.) III: Morphologische und biologische Untersuchungen am Falter der grossen Wachsmotte (Galleria mellonella). Zool Jahrb (Abt, Anat Ontog Tiere) 58:275–302.

    Google Scholar 

  35. Yildizhan, S., van Loon, J., Sramkova, A., Ayasse, M., Arsene, C., Broeke, C., and Schulz, S. 2009. Aphrodisiac pheromones from the wings of the small cabbage white and large cabbage white butterflies, Pieris rapae and Pieris brassicae. ChemBioChem 10:1666–1677.

    PubMed  Article  CAS  Google Scholar 

  36. Zagatti, P. 1981. Sexual-behavior of the sugarcane borer Eldana saccharina (WLK) due to 2 pheromones emitted by the male. Behaviour 78:81–97.

    Google Scholar 

  37. Zagatti, P., Kunesch, G., Ramiandrasoa, F., Malosse, C., Hall, D. R., Lester, R., and Nesbitt, B. F. 1987. Sex pheromones of rice moth, Corcyra cephalonica Stainton - I. Identification of male pheromone. J Chem Ecol 13:1561–1573.

    Article  CAS  Google Scholar 

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Acknowledgements

The project was supported by research project #Z4-055-905 (Academy of Sciences of the Czech Republic) and by grant #2B06007 (The Ministry of Education, Youth, and Sports of the Czech Republic). We thank Jarmila Titzenthalerova for skillful assistance with the GC-EAD experiments and Marketa Foley for language editing.

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Correspondence to Irena Valterová.

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Jiří Kindl and Pavel Jiroš contributed equally to this work.

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Fig. S1

Mass spectra of TMPD-one (2) and TMPD-ol (3). (PDF 113 kb)

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Kindl, J., Jiroš, P., Kalinová, B. et al. Females of the Bumblebee Parasite, Aphomia sociella, Excite Males Using a Courtship Pheromone. J Chem Ecol 38, 400–407 (2012). https://doi.org/10.1007/s10886-012-0100-3

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Keywords

  • Galleriinae
  • Courtship pheromone
  • Ultrasonic signaling
  • 6,10,14-Trimethylpentadecan-2-ol
  • 6,10,14-Trimethyl-2-pentadecanone
  • Lepidoptera
  • Pyralidae