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Specificity in Chemical Profiles of Workers, Brood and Mutualistic Fungi in Atta, Acromyrmex, and Sericomyrmex Fungus-growing Ants

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Abstract

Neotropical attine ants live in obligatory symbiosis with a fungus that they grow for food on a substrate of primarily plant material harvested by workers. Nestmate recognition is likely based on chemical cues as in most other social insects, but recent studies have indicated that both the ants and their mutualistic fungi may contribute to the recognition templates. To investigate the within-colony variation in chemical profiles, we extracted and identified compounds from the cuticle of workers, the postpharyngeal gland of workers, ant pupae and larvae, and the fungal symbiont of three species of higher attine ants: Atta colombica, Acromyrmex echinatior, and Sericomyrmex amabilis. The relative proportions of identified compounds were compared and represented 11 classes: n-alkanes, alkenes, branched methylalkanes, branched dimethylalkanes, trimethylalkanes, branched alkenes, aldehydes, alcohols, acetates, acids, and esters. The chemical profiles in all three species are likely to be sufficiently different to allow discrimination at the species and colony level and sufficiently similar within colonies to generate a relatively constant colony-specific chemical gestalt. The relative likelihood of individual compounds being derived from the ants, the ant brood, or the fungal symbiont are discussed. We hypothesize that hydrocarbons are particularly important as recognition cues because they appear to simultaneously allow the assessment of developmental stages and the identification of symbiont, colony, and species.

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References

  • Akino, T. and Yamaoka, R. 1998. Chemical mimicry in the root aphid parasitoid Paralipsis eikoae Yasumatsu (Hymenoptera: aphidiidae) of the aphid attending ant Lasius sakagamii Yamauchi and Hayashida (Hymenoptera: Formicidae). Chemoecology 8:153–161.

    Article  CAS  Google Scholar 

  • Beye, M., Neumann, P., and Moritz, R. F. A. 1997. Nestmate recognition and the genetic gestalt in the mound-building ant Formica polyctena. Insectes Soc. 44:49–58.

    Article  Google Scholar 

  • Beye, M., Neumann, P., Chapuisat, M., and Pamilo, P., and Moritz, R. F. A. 1998. Nestmate recognition and the genetic relatedness of nests in the ant Formica pratensis. Behav. Ecol. Sociobiol. 43:67–72.

    Article  Google Scholar 

  • Blomquist, G. J., Howard, R. W., and McDaniel, C. A. 1979. Structures of the cuticular hydrocarbons of the termites Zootermopsis angusticollis (Hagen). Insect Biochem. 9:365–370.

    Article  CAS  Google Scholar 

  • Bonavita-Cougourdan, A., Clément, J., and Lange, C. 1989. The role of cuticular hydrocarbons in the recognition of larvae by workers of the ant Camponotus vagus: changes in the chemical signature in response to social environment (Hymenoptera: Formicidae). Sociobiology 16:49–74.

    Google Scholar 

  • Boomsma, J. J., Nielsen, J., Sundström, L., Oldham, N. J., Tentschert, J., Petersen, H. C., and Morgan, E. D. 2003. Informational contraints on optimal sex allocation in ant. Proc. Natl. Acad. Sci. USA 100:158799–8804.

    Article  PubMed  CAS  Google Scholar 

  • Bot, A. N. M., Rehner, S. A., and Boomsma, J. J. 2001. Partial incompatibility between ants and symbiotic fungi in two sympatric species of Acromyrmex leaf-cutting ants. Evolution 55:1980–1991.

    PubMed  CAS  Google Scholar 

  • Brandão, C. R. F. and Mayhé-Nunes, A. J. 2001. A new fungus-growing genus, Mycetagroicus gen. n., with the description of three new species and comments on the monophyly of the Attini (Hymenoptera: Formicidae). Sociobiology 38:639–665.

    Google Scholar 

  • Breed, M. D. 1983. Nestmate recognition in honey bees. Anim. Behav. 31:86–91.

    Article  Google Scholar 

  • Carlson, D. A., Bernier, U. R., and Sutton, B. C. 1998. Evolution patterns from capillary GC for methyl-branched alkanes. J. Chem. Ecol. 24:1845–1865.

    Article  CAS  Google Scholar 

  • Chapela, I. H., Rehner, S. A., Schultz, T. R., and Mueller, U. G. 1994. Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266:1691–1694.

    Article  PubMed  CAS  Google Scholar 

  • Crosland, M. W. J. 1989. Kin recognition in the ant Rhytidoponera confusa. I. Environmental odour. Anim. Behav. 37:912–919.

    Article  Google Scholar 

  • Currie, C. R., Wong, B., Stuart, A. E., Schultz, T. R., Rehner, S. A., Mueller, U. G., Sung, G. H., Spatafora, J. W., and Straus, N. A. 2003. Ancient tripartite coevolution in the Attine ant–microbe symbiosis. Science 299:386–388.

    Article  PubMed  CAS  Google Scholar 

  • Currie, C. R., Poulsen, M., Mendenhall, J., Boomsma, J. J., and Billen, J. 2006. Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311:81–83.

    Article  PubMed  CAS  Google Scholar 

  • Elmes, G. W., Akino, T., Thomas, J. A., Clarke, R. T., and Knapp, J. J. 2002. Interspecific differences in cuticular hydrocarbon profiles of Myrmica ants are sufficiently consistent to explain host specificity by Maculinea (large blue) butterflies. Oecologia 130:525–535.

    Article  Google Scholar 

  • Heinze, J., Foitzik, S., Hippert, A., and Hölldobler, B. 1996. Apparent dear-enemy phenomenon and environment-based recognition cues in the ant Leptothorax nylanderi. Ethology 102:510–522.

    Article  Google Scholar 

  • Heinze, J., Stengl, B., and Sledge, M. F. 2002. Worker rank, reproductive status and cuticular hydrocarbon signature in the ant, Pachycondyla cf. inversa. Behav. Ecol. Sociobiol. 52:59–65.

    Article  Google Scholar 

  • Hinkle, G., Wetterer, J. K., Schultz, T. R., and Sogin, M. L. 1994. Phylogeny of the attine ant fungi based on analysis of small subunit ribosomal RNA gene sequences. Science 266:1695–1697.

    Article  PubMed  CAS  Google Scholar 

  • Hölldobler, B. and Wilson, E. O. 1990. The ants. 732 pp. Belknap, Cambridge, MA.

    Google Scholar 

  • Howard, R. W. and Blomquist, G. J. 2005. Ecological, behavioral, and biochemical aspects of insect hydrocabons. Annu. Rev. Entomol. 50:371–393.

    Article  PubMed  CAS  Google Scholar 

  • Howard, R. W., Mcdaniel, C. A., and Blomquist, G. J. 1978. Cuticular hydrocarbons of the eastern subterranean termite, Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae). J. Chem. Ecol. 4:233–245.

    Article  CAS  Google Scholar 

  • Howard, R. W., Mcdaniel, C. A., Nelson, D. R., Blomquist, G. J., Gelbaum, L. T., and Zalkow, L. H. 1982. Cuticular hydrocarbons of Reticulitermes virginicus (BANKS) and their role as potential species and caste-recognition cues. J. Chem. Ecol. 8:1227–1239.

    Article  CAS  Google Scholar 

  • Jutsum, A. R., Saunders, T. S., and Cherrett, J. M. 1979. Intraspecific aggression in the leaf-cutting ant Acromyrmex octospinosus. Anim. Behav. 27:839–844.

    Article  Google Scholar 

  • Lahav, S., Soroker, V., Hefetz, A., and Vander Meer, R. K. 1999. Direct behavioral evidence for hydrocarbons as ant recognition discriminators. Naturwissenschaften 86:246–249.

    Article  CAS  Google Scholar 

  • Lambardi, D., Dani, F. R., Turillazzi, S., and Boomsma, J. 2007. Incipient social parasites of Acromyrmex leaf-cutting ants avoid host aggression by being chemically inconspicuous. Behav. Ecol. Sociobiol. 61:843–851.

    Article  Google Scholar 

  • Liang, D. and Silverman, J. 2000. You are what you eat: diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87:412–416.

    Article  PubMed  CAS  Google Scholar 

  • Lommelen, E., Johnson, C. A., Drijfhout, F. P., Billen, J., Wenseleers, T., and Gobin, B. 2006. Cuticular hydrocarbons provide reliable cues of fertility in the ant Gnamptogenys striatula. J. Chem. Ecol. 32:2023–2034.

    Article  PubMed  CAS  Google Scholar 

  • Mikheyev, A. S., Mueller, U. G., and Boomsma, J. J. 2007. Population genetic signatures of diffuse co-evolution between leaf-cutting ants and their cultivar fungi. Mol. Ecol. 16:209–216.

    Article  PubMed  CAS  Google Scholar 

  • Mueller, U. G. 2002. Ant versus fungus versus mutualism: ant cultivar conflict and the deconstruction of the Attine ant–fungus symbiosis. Am. Nat. 160:S67–S98.

    Article  PubMed  Google Scholar 

  • Mueller, U. G., Rehner, S. A., and Schultz, T. R. 1998. The evolution of agriculture in ants. Science 281:2034–2038.

    Article  PubMed  CAS  Google Scholar 

  • Mueller, U. G., Schultz, T. R., Currie, C. R., Adams, R. M. M., and Malloch, D. 2001. The origin of the Attine ant–fungus mutualism. Q. Rev. Biol. 76:169–197.

    Article  PubMed  CAS  Google Scholar 

  • Nielsen, J., Boomsma, J. J., Oldham, N. J., Petersen, H. C., and Morgan, E. D. 1999. Colony-level and season-specific variation in cuticular hydrocarbon profiles of individual workers in the ant Formica truncorum. Insect. Soc. 46:58–65.

    Article  Google Scholar 

  • Obin, M. S. 1986. Nestmate recognition cues in laboratory and field colonies of Solenopsis invicta Buren (Hymenoptera: Formicidae): effect of environment and the role of cuticular hydrocarbons. J. Chem. Ecol. 12:1965–1975.

    Article  CAS  Google Scholar 

  • Poulsen, M. and Boomsma, J. J. 2005. Mutualistic fungi control crop diversity in fungus-growing ants. Science 307:741–744.

    Article  PubMed  CAS  Google Scholar 

  • Richard, F. J., Hefetz, A., Christides, J. P., and Errard, C. 2004. Food influence on colonial recognition and chemical signature between nestmates in the fungus-growing ant Acromyrmex subterraneus. Chemoecology 14:9–16.

    Article  CAS  Google Scholar 

  • Richard, F. J., Mora, P., Errard, C., and Rouland, C. 2005. Digestive capacities of leaf-cutting ants and the contribution of their fungal cultivar to the degradation of plant material. J. Comp. Physiol. B 175:297–303.

    Article  PubMed  Google Scholar 

  • Richard, F. J., Poulsen, M., Hefetz, A., Errard, C., Nash, D. R., and Boomsma, J. J. 2007. The origin of chemical profiles of fungal symbionts and their significance for nestmate recognition in Acromyrmex leaf-cutting ants. Behav. Ecol. Sociobiol. 61:1637–1649.

    Article  Google Scholar 

  • Schultz, T. R. and Meier, R. 1995. A phylogenetic analysis of the fungus-growing ants (Hymenoptera: Formicidae: attini) based on morphological characters of the larvae. Syst. Entomol. 20:337–370.

    Google Scholar 

  • Silverman, J. and Liang, D. 2001. Colony disassociation following diet partitioning in a unicolonial ant. Naturwissenschaften 88:73–77.

    Article  PubMed  CAS  Google Scholar 

  • Singer, T. L. 1998. Roles of hydrocarbons in the recognition systems of insects. Am. Zool. 38:394–405.

    CAS  Google Scholar 

  • Singer, T. L. and Espelie, K. E. 1996. Nest surface hydrocarbons facilitate nestmate recognition for the social wasp, Polistes metricus Say (Hymenoptera, Vespidae). J. Insect Behav. 9:857–870.

    Article  Google Scholar 

  • Soroker, V., Vienne, C., Hefetz, A., and Nowbahari, E. 1994. The postpharyngeal gland as a “Gestalt” organ for nestmate recognition in the ant Cataglyphis niger. Naturwissenschaften 81:510–513.

    CAS  Google Scholar 

  • Soroker, V., Vienne, C., and Hefetz, A. 1995. Hydrocarbon dynamics within and between nestmates in Cataglyphis niger (Hymenoptera: Formicidae). J. Chem. Ecol. 21(3):365–378.

    Article  CAS  Google Scholar 

  • Vander Meer, R. K. and Morel, L. 1998. Nestmate recognition in ants, pp. 79–103, in R. K. Vander Meer, M. Breed, K. E. Espelie, M. Winston, (eds.). Pheromone Communication in Social Insects. Westview, Boulder, CO.

    Google Scholar 

  • Viana, A. M. M., Frézard, A., Malosse, C., Della Lucia, T. M. C., Errard, C., and Lenoir, A. 2001. Colonial recognition of fungus in the fungus-growing ant Acromyrmex subterraneus subterraneus (Hymenoptera: Formicidae). Chemoecology 11:29–36.

    Article  Google Scholar 

  • Wagner, D., Tissot, M., Cuevas, W., and Gordon, D. M. 2000. Harvester ants utilize cuticular hydrocarbons in nestmate recognition. J. Chem. Ecol 26:2245–2257.

    Article  CAS  Google Scholar 

  • Weber, N. A. 1972. Gardening ants, the attines. Memoirs of the American Philosophical Society, Philadelphiap xvii + 146.

    Google Scholar 

  • Wilson, E. O. 1971. The insect societies. 548 pp. Belknap, Cambridge, MA.

    Google Scholar 

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Acknowledgements

We thank the Smithsonian Tropical Research Institute (STRI) for providing logistic help and facilities to work in Gamboa and the Autoridad Nacional del Ambiente y el Mar (ANAM) for permission to sample ant colonies in Panama and export them to Denmark. Fieldwork was supported by grants from the Carlsberg Foundation and the Danish Natural Science Research Council to JJB. All experiments performed in this manuscript comply with current Danish and USA law.

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Correspondence to Freddie-Jeanne Richard.

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Richard, FJ., Poulsen, M., Drijfhout, F. et al. Specificity in Chemical Profiles of Workers, Brood and Mutualistic Fungi in Atta, Acromyrmex, and Sericomyrmex Fungus-growing Ants. J Chem Ecol 33, 2281–2292 (2007). https://doi.org/10.1007/s10886-007-9385-z

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