Insectes Sociaux

, Volume 64, Issue 4, pp 591–596 | Cite as

Changes in the cuticular hydrocarbon profile associated with the molting cycle correlate with the hydrocarbon profile of the fungus cultivated by the ant Atta sexdens

Research Article

Abstract

Leaf-cutting ants live in obligate mutualism with a basidiomycete fungus that they use as a rearing site and food resource. Chemical analyses of the fungus gardens kept by these ants have revealed the presence of hydrocarbons that also occur in the epicuticle of the ants. However, whether it is the fungus or the ants which are the ultimate producers of these compounds is not yet clear. To shed light on the chemoecological aspects of the symbiotic relationship between ant and fungus, in the present study, we aimed to characterize the changes in the cuticular chemical profiles during larval-to-adult molting of Atta sexdens workers, which allowed us to investigate how these changes were correlated with the chemical profile of fungal cultivars. The results show that cuticular hydrocarbon profiles of ants were comprised of linear and branched alkanes that varied significantly, according to developmental stages, with several ant-specific hydrocarbons being identified as the most representative ones. The chemical profile of symbiotic fungus was predominantly comprised of linear alkanes, which also occurred in the cuticle of the ants. Chemical distances calculated with the chemical profiles of the analyzed groups revealed a great similarity between the hydrocarbon profile of symbiotic fungus and those of the ants, especially at the earliest stages of ants’ development, when mainly linear alkanes were identified. However, as individuals progressed through developmental stages, the chemical profiles increased in difference, due to the fact that several branched alkanes were found in great proportions in the cuticle of the ants. These findings suggest that the intimate relationship between brood and fungus might shape the hydrocarbon profile of both species, and the possible scenarios for the transference of these substances are discussed.

Keywords

Cuticular hydrocarbons Molting cycle Atta sexdens Leucoagaricus gongylophorus 

References

  1. Blomquist GJ (2010) Biosynthesis of cuticular hydrocarbon. In: Blomquist GJ (ed) Insect hydrocarbons. Cambridge University Press, Cambridge, pp 19–34CrossRefGoogle Scholar
  2. Blomquist GJ, Bagnères AG (2010) Structure and analysis of insect hydrocarbons. In: Blomquist GJ (ed) insect hydrocarbons. Cambridge University Press, Cambridge, pp 19–34CrossRefGoogle Scholar
  3. Cassill DL, Tschinkel WR (1996) A duration constant for worker-larva trophallaxis in fire ants. Insectes Soc 43:149–166CrossRefGoogle Scholar
  4. Dani R, Jones GR, Destri S, Spencer SH, Turillazzi S (2001) Deciphering the recognition signature within the cuticular chemical profile of paper wasps. Anim Behav 62:165–171CrossRefGoogle Scholar
  5. Della Lucia TMC (ed) (1993) As Formigas Cortadeiras. Editora Folha de Viçosa, Viçosa, p 262Google Scholar
  6. Dwyer LA, Zamboni AC, Blomquist GJ (1986) Hydrocarbon accumulation and lipid biosynthesis during larval development in the cabbage looper, Trichoplusia ni. Insect Biochem 16:463–469CrossRefGoogle Scholar
  7. Falcón TL, Ferreira-Caliman MJ, Nunes FMF, Tanaka ER, Nascimento FS, Bitondi MMG (2015) Exoskeleton formation in Apis mellifera: cuticular hydrocarbons profiles and expression of desaturase and elongase genes during pupal and adult development. Insect Biochem Mol Biol 50:68–81CrossRefGoogle Scholar
  8. Fedina TY, Kuo TH, Dreisewerd K, Dierick HA, Yew JY, Pletcher SD (2012) Dietary effects on cuticular hydrocarbons and sexual attractiveness in Drosophila. PLoS ONE 7:e49799CrossRefPubMedPubMedCentralGoogle Scholar
  9. Fisher PJ, Stradling DJ, Sutton BC, Petrini LE (1996) Microfungi in the fungus gardens of the leafcutting ant Atta cephalotes: a preliminary study. Mycol Res 100(5):541–546CrossRefGoogle Scholar
  10. Gianoulis TA, Griffin MA, Spakowicz DJ, Dunican BF, Alpha CJ (2012) Genomic analysis of the hydrocarbon-producing, cellulolytic, endophytic fungus ascocoryne sarcoides. PLoS Genet 8:e1002558CrossRefPubMedPubMedCentralGoogle Scholar
  11. Guo L, Blomquist GB (1991) Identification, accumulation and biosynthesis of the cuticular hydrocarbons of the sourthern armyworm Spodoptera eridania (Leptoptera: Noctuidae). Arch Insect Biochem 16:19–30CrossRefGoogle Scholar
  12. Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, CambridgeCrossRefGoogle Scholar
  13. Hunt JH, Napela CA (1994) Nourishment and evolution in insects societies. Westview Press, Boulder, p 449Google Scholar
  14. Ichinose K, Boulay R, Cerdá X, Lenoir A (2009) Influence of queen and diet on nestmate recognition and cuticular hydrocarbon differentiation in a fission-dispersing ant, Aphaenogaster senilis. Zool Sci 10:681–685CrossRefGoogle Scholar
  15. Jandt JM, Gordon DM (2016) The behavioral ecology of variation in social insects. Curr Opin Insect Sci 15:40–44CrossRefPubMedGoogle Scholar
  16. Ladygina N, Dedyukhina EG, Vainshtein MB (2006) A review on microbial synthesis of hydrocarbons. Process Biochem 1001–1014Google Scholar
  17. Lambardi D, Chegia B, Turilazzi S, Boomsma JJ (2004) Diet-induced aggression among colonies of the leafcutter ant Acromyrmex echinatior Forel (Hymenoptera Formicidae). Redia 21:219–221Google Scholar
  18. Liang D, Silverman J (2000) "Your are what you eat": diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87:412–416CrossRefPubMedGoogle Scholar
  19. Martin S, Drijfhout F (2009) A review of ant cuticular hydrocarbons. J Chem Ecol 32:1151–1161CrossRefGoogle Scholar
  20. Otte T, Hilker M, Geiselhardt S (2015) The effect of dietary fatty acids on the cuticular hydrocarbon phenotype of an herbivorous insect and consequences for mate recognition. J Chem Ecol 41:32–43CrossRefPubMedGoogle Scholar
  21. Richard FJ, Hunt JH (2013) Intracolony chemical communication in social insects. Insect Soc 60:275–291CrossRefGoogle Scholar
  22. Richard FJ, Heftz A, Christides JP, Errard C (2004) Food influence on colonial recognition and chemical signature between nestmates in the fungus-growing ant Acromyrmex subterraneus subterraneus. J Chem Ecol 14:9–16Google Scholar
  23. Richard FJ, Poulsen M, Hefetz Errard C, Nash DR, Boomsma JJ (2007a) The origin of the chemical profiles of fungal symbionts and their significance for nestmate recognition in Acromyrmex leaf-cutting ants. Behav Ecol Sociobiol 61(11):1637–1649CrossRefGoogle Scholar
  24. Richard FJ, Poulsen M, Drijfhout F, Jones G, Boomsma JJ (2007b) Specificity in chemical profiles of workers, brood and mutualistic fungi in Atta, Acromyrmex, and Sericomyrmex fungus-growing ants. J Chem Ecol 33(12):2281–2292CrossRefPubMedGoogle Scholar
  25. Schneider MO (2004) Comportamento de cuidado com a prole na saúva-limão Atta sexdens rubropilosa Forel, 1908 (Hymenoptera: Formicidae). MSc Thesis, Universidade Estadual Paulista Júlio de Mesquita Filho, Rio Claro, Brasil, p 86Google Scholar
  26. Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci 14:5435–5440CrossRefGoogle Scholar
  27. Shaw JJ, Spakowicz DJ, Dalal RS, Davis JH, Lehr NA, Dunican BF, Orellana EA, Narváez-Trujillo A, Strobel SA (2015) Biosynthesis and genomic analysis of medium-chain hydrocarbon production by the endophytic fungal isolate Nigrograna mackinnonii E5202H. Appl Microbiol Biotechnol 99:3715–3728CrossRefPubMedPubMedCentralGoogle Scholar
  28. Silva A, Bacci MJR, Siqueira CG, Bueno FC, Pagnocca FC, Hebling MJA (2003) Survival of Atta sexdens workers on different food sources. J Insect Physiol 49:307–313CrossRefPubMedGoogle Scholar
  29. Siqueira CG, Bacci M, Pagnocca FC, Bueno OC, Hebling MJA (1998) Metabolism of plant polysaccharides by Leucoagaricus gongylophorus, the symbiotic fungus of leaf-cutting ant Atta sexdens L. Appl Environ Microbiol 64:4820–4822Google Scholar
  30. Sorvari J, Theodora P, Turillazzi S, Hakkarainen H, Sundström L (2008) Food resources, chemical signalling and nest mate recognition in the ant Formica aquilonia. Behav Ecol 19:441–447CrossRefGoogle Scholar
  31. Spakowicz DJ, Strobel SA (2015) Biosynthesis of hydrocarbons and volatic organic compounds by fungi: bioengineering potential. Appl Microbiol Biotechnol 99:4943–4951CrossRefPubMedPubMedCentralGoogle Scholar
  32. Valadares L, Nascimento FS (2016) Chemical cuticular signature of leafcutter ant Atta sexdens (Hymenoptera, Formicidae) worker subcastes. Rev Bras Entomol 4:308–311CrossRefGoogle Scholar
  33. Valadares L, Nascimento D, Nascimento FS (2015) Foliar substrate affects cuticular hydrocarbon profiles and intraspecific aggression in the leafcutter Ant Atta sexdens. Insects 6:141–151CrossRefPubMedPubMedCentralGoogle Scholar
  34. Vander Meer RK, Morel L (1998) Nestmate recognition in ants. In: Vander Meer RK, Breed M, Wintson M, Espelie KE (eds) Pheromone communication in social insects. Westview Press, Boulder, p 384Google Scholar
  35. Viana AM, Frézard A, Malosse C, Della Lucia TM, Errard C, Lenoir A (2001) Colonial recognition of fungus in the fungus-growing ant Acromyrmex subterraneus subterraneus (Hymenoptera: Formicidae). Chemoecol 11(1):29–36CrossRefGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2017

Authors and Affiliations

  1. 1.Laboratório de Comportamento e Ecologia de Insetos Sociais, Departamento de BiologiaUniversidade de São PauloRibeirão PretoBrazil

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