Insectes Sociaux

, Volume 58, Issue 4, pp 513–518 | Cite as

Workers do not mediate the inhibitory power of queens in a termite, Reticulitermes speratus (Isoptera, Rhinotermitidae)

Research Article

Abstract

In social insects, the caste systems are based on reproductive division of labor; queens specialize in reproduction and workers primarily maintain the colony. Recently, a volatile pheromone containing n-butyl-n-butyrate and 2-methyl-1-butanol was identified as a termite queen pheromone that inhibits the differentiation of female neotenic reproductives (secondary queens). Although this volatile inhibitory pheromone regulates caste differentiation directly, the method by which it reaches members without direct contact with the queen in large colonies is not well understood. Therefore, additional mechanisms of indirect communication must exist, such as worker-mediated queen signal transport. We found that workers exposed to female reproductives did not mediate queens’ inhibitory signal in a termite Reticulitermes speratus. The experiment assessed worker transfer from direct to indirect contact groups and determined that the differentiation of new female reproductives in the indirect contact groups was not influenced by the direct contact groups, whereas direct contact with functional female reproductives and artificial queen pheromone did suppress neotenic differentiation. This suggests that worker transfer of the queen signal is unlikely and that for colony-wide inhibition direct contact by the majority of infertile members with reproductives or eggs, which emit the same volatiles as female reproductives, is necessary within a certain time interval.

Keywords

Queen pheromone Caste differentiation Inhibitory pheromone Social insects Reproductive conflict 

References

  1. Afzal M. 1983. Radioisotope studies of trophallaxis in the drywood termite Bifiditermes beesoni (Gardner) (Isoptera). I: effect of group size on the rate of food exchange. Mater. Org. 18: 51-63Google Scholar
  2. Arnold G., Leconte Y., Trouiller J., Hervet H., Chappe B. and Masson C. 1994. Inhibition of worker honeybee ovaries development by a mixture of fatty-acid esters from larvae. C.R. Acad. Sci. Paris Sci. Vie 317: 511-515Google Scholar
  3. Brian M. and Rigby C. 1978. The trophic eggs of Myrmica rubra L. Insect. Soc. 25: 89-110.Google Scholar
  4. Butler C.G., Callow R.K. and Johnston N.C. 1959. Extraction and purification of ‘queen substance’ from queen bees. Nature 184: 1871Google Scholar
  5. Endler A., Liebig J., Schmitt T., Parker J.E., Jones G.R., Schreier P. and Hölldobler B. 2004. Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc. Natl Acad. Sci. USA 101: 2945-2950. doi:10.1073/pnas.0308447101 Google Scholar
  6. Fletcher D.J.C. and Ross K.G. 1985. Regulation of reproduction in eusocial Hymenoptera. Annu. Rev. Entomol. 30: 319-343. doi:doi:10.1146/annurev.en.30.010185.001535 Google Scholar
  7. Fujita A. and Watanabe H. 2010. Inconspicuous matured males of worker form are produced in orphaned colonies of Reticulitermes speratus (Isoptera: Rhinotermitidae) and participate in reproduction. J. Insect Physiol. 56: 1510-1515Google Scholar
  8. Hanus R., Vrkoslav V., Hrdý I., Cvačka J. and Šobotník J. 2010. Beyond cuticular hydrocarbons: evidence of proteinaceous secretion specific to termite kings and queens. Proc. R. Soc. Lond. B 277: 995-1002. doi:10.1098/rspb.2009.1857 Google Scholar
  9. Holman L., Jørgensen C.G., Nielsen J. and d’Ettorre P. 2010. Identification of an ant queen pheromone regulating worker sterility. Proc. R. Soc. Lond. B 277: 3793-3800. doi:10.1098/rspb.2010.0984
  10. Jay S.C. 1970. The effect of various combinations of immature queen and worker bees on the ovary development of worker honeybees. Can. J. Zool. 48: 169-173Google Scholar
  11. Kawabata S. and Tsuji K. 2005. The policing behavior ‘immobilization’ towards ovary-developed workers in the ant, Diacamma sp. from Japan. Insect. Soc. 52: 89-95. doi:10.1007/s00040-004-0778-5
  12. Keller L. and Nonacs P. 1993. The role of queen pheromones in social insects: queen control or queen signal? Anim. Behav. 45: 787-794Google Scholar
  13. Kikuchi T., Suwabe M. and Tsuji K. 2010. Durability of information concerning the presence of a gamergate in Diacamma sp. from Japan. Physiol. Entomol. 35: 93-97. doi:10.1111/j.1365-3032.2009.00710.x
  14. Kindl J. and Hrdý I. 2005. Development of neotenics induced by a temporary absence of functional reproductives in Kalotermes flavicollis (Isoptera: Kalotermitidae). Eur. J. Entomol. 102: 307-311Google Scholar
  15. Lenz M. 1994. Food resources, colony growth and caste development in wood-feeding termites. In: Nourishment and Evolution in Insect Societies (Hunt J.H. and Nalepa C.A., Eds), Westview Press, Boulder, Colorado, pp 159-210Google Scholar
  16. Liebig J., Eliyahu D. and Brent C.S. 2009. Cuticular hydrocarbon profiles indicate reproductive status in the termite Zootermopsis nevadensis. Behav. Ecol. Sociobiol. 63: 1799-1807. doi:10.1007/s00265-009-0807-5 Google Scholar
  17. Liebig J., Monnin T. and Turillazzi S. 2005. Direct assessment of queen quality and lack of worker suppression in a paper wasp. Proc. R. Soc. Lond. B 272: 1339-1344. doi:10.1098/rspb.2005.3073
  18. Liebig J., Peeters C. and Hölldobler B. 1999. Worker policing limits the number of reproductives in a ponerine ant. Proc. R. Soc. Lond. B 266: 1865-1870Google Scholar
  19. Lüscher M. 1960. Hormonal control of caste differentiation in termites. Annals N.Y. Acad. Sci. 89: 549-563Google Scholar
  20. Lüscher M. 1952. Die Produktion und Elimination von Ersatzgeschlechtstieren bei der Termite Kalotermes flavicollis Fabr. Z. Vergl. Physiol. 34: 123-141Google Scholar
  21. Markin G.P. 1970. Food distribution within laboratory colonies of the Argentine ant, Iridomyrmex humilis (Mayr). Insect. Soc. 17: 127-158Google Scholar
  22. Matsuura K. 2010. Sexual and asexual reproduction in termites. In: Biology of Termites: a Modern Synthesis (Bignell D.E., Roisin Y. and Lo N., Eds), Springer, Dordrecht, pp 255-277Google Scholar
  23. Matsuura K., Himuro C., Yokoi T., Yamamoto Y., Vargo E.L. and Keller L. 2010. Identification of a pheromone regulating caste differentiation in termites. Proc. Natl Acad. Sci. USA 107: 12963-12968. doi:10.1073/pnas.1004675107 Google Scholar
  24. Matsuura K., Kobayashi N. and Yashiro T. 2007. Seasonal patterns of egg production in field colonies of the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Pop. Ecol. 49: 179-183. doi:10.1007/s10144-006-0030-4
  25. Matsuura K., Vargo E.L., Kawatsu K., Labadie P.E., Nakano H., Yashiro T. and Tsuji K. 2009. Queen succession through asexual reproduction in termites. Science 323: 1687. doi:10.1126/science.1169702
  26. Mohammedi A., Paris A., Crauser D. and Le Conte Y. 1998. Effect of aliphatic esters on ovary development of queenless bees (Apis mellifera L.). Naturwissenschaften 85: 455-458. doi:10.1007/s001140050531
  27. Naumann K., Winston M.L., Slessor K.N., Prestwich G.D. and Webster F.X. 1991. Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone. Behav. Ecol. Sociobiol. 29: 321-332. doi:10.1007/bf00165956 Google Scholar
  28. Pamilo P. 1991. Evolution of colony characteristics in social insects. II. Number of reproductive individuals. Am. Nat. 138: 412-433. doi:doi:10.1086/285224 Google Scholar
  29. Pettis J.S., Higo H.A., Pankiw T. and Winston M.L. 1997. Queen rearing suppression in the honey bee evidence for a fecundity signal. Insect. Soc. 44: 311-322Google Scholar
  30. Ratnieks F.L.W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132: 217-236Google Scholar
  31. Rosengaus R.B., Traniello J.F.A. and Levy C.K. 1986. Social transfer, elimination, and biological half-life of gamma-emitting radionuclides in the termite Reticulitermes flavipes Kol. J. Appl. Entomol. 101: 287-294Google Scholar
  32. Seeley T.D. 1979. Queen substance dispersal by messenger workers in honeybee colonies. Behav. Ecol. Sociobiol. 5: 391-415. doi:10.1007/bf00292527
  33. Shellman-Reeve J.S. 1997. The spectrum of eusociality in termites. In: The Evolution of Social Behaviour in Insects and Arachnids (Choe J.C. and Crespi B.J., Eds), Cambridge University Press, Cambridge, UK, pp 52-93Google Scholar
  34. Springhetti A. 1972. I reali nella differenziazione delle caste di Kalotermes flavicollis (Fabr.) (Isoptera). Boll. Zool. 39: 83-87Google Scholar
  35. Stuart A.M. 1979. The determination and regulation of the neotenic reproductive caste in the lower termites (Isoptera): with special reference to the genus Zootermopsis (Hagen). Sociobiology 4: 223-237Google Scholar
  36. Suárez M.E. and Thorne B.L. 2000. Rate, amount, and distribution pattern of alimentary fluid transfer via trophallaxis in three species of termites (Isoptera: Rhinotermitidae, Termopsidae). Ann. Entomol. Soc. Am. 93: 145-155Google Scholar
  37. Traniello J.F.A. 1977. Recruitment behavior, orientation, and the organization of foraging in the carpenter ant Camponotus pennsylvanicus DeGeer (Hymenoptera: Formicidae). Behav. Ecol. Sociobiol. 2: 61-79. doi:10.1007/bf00299289
  38. Traniello J.F.A., Rosengaus R.B. and Levy C.K. 1985. Single and double isotope labeling of social insect colonies: gamma-emitting radionuclides as individually identifiable markers. Entomol. Exper. Appl. 38: 87-92Google Scholar
  39. Tsuji K., Egashira K. and Hölldobler B. 1999. Regulation of worker reproduction by direct physical contact in the ant Diacamma sp. from Japan. Anim. Behav. 58: 337-343Google Scholar
  40. Tsunoda K., Matsuoka H., Yoshimura T. and Tokoro M. 1999. Foraging populations and territories of Reticulitermes speratus (Isoptera: Rhinotermitidae). J. Econ. Entomol. 92: 604-609Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2011

Authors and Affiliations

  1. 1.Graduate School of Environmental ScienceOkayama UniversityOkayamaJapan

Personalised recommendations