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Journal of Chemical Ecology

, Volume 42, Issue 5, pp 444–451 | Cite as

Cuticular Hydrocarbon Compounds in Worker Castes and Their Role in Nestmate Recognition in Apis cerana indica

  • Seydur Rahman
  • Sudhanya Ray Hajong
  • Jérémy Gévar
  • Alain Lenoir
  • Eric Darrouzet
Article

Abstract

Differences in cuticular hydrocarbons (CHCs) among worker castes and colonies were examined in Apis cerana indica. The roles of tetracosanoic acid, hexadecanoic acid, pentacosane, and (Z)-9-tricosene in nestmate recognition were studied. The CHC profiles of different castes, i.e., newly emerged bees, nurse bees, and forager bees, were found to differ among colonies. The CHC profiles of nurse bees were similar across different colonies, but forager bees in all colonies had significantly greater amounts of alkanes. In nestmate recognition experiments, guard bees reacted significantly more aggressively to foragers treated with tetracosanoic acid, hexadecanoic acid, and (Z)-9-tricosene. Pentacosane provoked no such effect.

Keywords

Tasks Cuticular hydrocarbons Apis cerana indica Alkanes Fatty acids 

Notes

Acknowledgments

The first author was funded by Maulana Azad National Fellowship (University Grant Commission, New Delhi, India). The GC/MS was obtained thanks to a grant from the PRES Centre Val de Loire University (APR-IA 2012) and the CNRS (INEE).

References

  1. Atchinson J (1986) The statistical analysis of compositional data. Chapman and Hall, LondonCrossRefGoogle Scholar
  2. Bagneres AG, Clement JL, Blum MS, Severson RF, Joulie C, Lange C (1990) Cuticular hydrocarbons and defensive compounds of Reticulitermes flavipes (Kollar) and R. santonensis (Feytaud): Polymorphism and chemotaxonomy. J Chem Ecol 16(12):3213–3244Google Scholar
  3. Bagneres AG, Riviere G, Clement JL (1998) Artificial neural network modeling of caste odor discrimination based on cuticular hydrocarbons in termites. Chemoecology 8:201–209CrossRefGoogle Scholar
  4. Bagneres AG, Darrouzet E, Landre X, Christides JP (2011) Endogenous synchronization of the chemical signature of Reticulitermes (Isoptera: Rhinotermitidae) worker termites. Ann Soc Entomol Fr 47:202–208Google Scholar
  5. Bonavita-Cougourdan A, Clement JL, Lange C (1993) Functional subcaste discrimination (foragers and brood-tenders) in the ant Camponotus vagus Scop: polymorphism of cuticular hydrocarbon patterns. J Chem Ecol 19:1461–1477CrossRefPubMedGoogle Scholar
  6. Bowden RM, Willamson S, Breed MD (1998) Floral oils: their effect on nestmate recognition in the honeybee, Apis mellifera. Insect Soc 45:209–214CrossRefGoogle Scholar
  7. Breed MD (1998) Recognition pheromones of the honey bee. Bioscience 48:463–470CrossRefGoogle Scholar
  8. Breed MD, Stiller TM (1992) Honey bee, Apis mellifera, nestmate discrimination: hydrocarbon effects and the evolutionary implications of comb choice. Anim Behav 43:875–883CrossRefGoogle Scholar
  9. Breed MD, Stiller TM, Moor MJ (1988a) The ontogeny of kin discrimination dues in the honey bee, Apis mellifera. Behav Genet 18:439–448CrossRefPubMedGoogle Scholar
  10. Breed MD, Williams KR, Fewell JH (1988b) Comb wax mediates the acquisition of nest-mate recognition cues in honey bees. Proc Natl Acad Sci U S A 85:8766–8769CrossRefPubMedPubMedCentralGoogle Scholar
  11. Breed MD, Diaz PH, Lucero KD (2004a) Olfactory information processing in honeybee, Apis mellifera, nestmate recognition. Anim Behav 68:921–928CrossRefGoogle Scholar
  12. Breed MD, Perry S, Bjostad LB (2004b) Testing the blank slate hypothesis: why honey bee colonies accept young bees. Insect Soc 51:12–16CrossRefGoogle Scholar
  13. Breed MD, Deng XB, Buchwald R (2007) Comparative nestmate recognition in Asian honey bees, Apis florea, Apis andreniformis, Apis dorsata, and Apis cerana. Apidologie 38:411–418CrossRefGoogle Scholar
  14. Buchwald R, Breed MD (2005) Nestmate recognition cues in a stingless bee, Trigona fulviventris. Anim Behav 70:1331–1337CrossRefGoogle Scholar
  15. Châline N, Sandoz JC, Martin SJ, Ratnieks FLW, Jones GR (2005) Learning and discrimination of individual cuticular hydrocarbons by honeybees (Apis mellifera). Chem Senses 30:327–335CrossRefPubMedGoogle Scholar
  16. Chapman NC, Nanork P, Reddy MS, Bhat NS, Beekman M, Oldroyd BP (2008) Nestmate recognition by guards of the Asian hive bee Apis cerana. Insect Soc 55:382–386CrossRefGoogle Scholar
  17. Chung H, Carroll SB (2015) Wax, sex and the origin of species: dual roles of insect cuticular hydrocarbons in adaptation and mating. Bioessays 37:822–830CrossRefPubMedPubMedCentralGoogle Scholar
  18. Couvillon MJ, Caple JP, Endsor SL, Karcher M, Russell TE, Storey DE, Ratnieks FLW (2007) Nest-mate recognition template of guard honeybees (Apis mellifera) is modified by wax comb transfer. Biol Lett 3:228–230CrossRefPubMedPubMedCentralGoogle Scholar
  19. d’Ettorre P, Wenseleers T, Dawson J, Hutchinson S, Boswell T, Ratnieks FLW (2006) Wax combs mediate nestmate recognition by guard honeybees. Anim Behav 71:773–779CrossRefGoogle Scholar
  20. Dani FR, Jones GR, Destri S, Spencer SH, Turillazzi S (2001) Deciphering the recognition signature within the cuticular chemical profie of paper wasps. Anim Behav 62:165–171CrossRefGoogle Scholar
  21. Dani FR, Jones GR, Corsi S, Beard R, Pradella D, Turillazzi S (2005) Nestmate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes. Chem Senses 30:477–489CrossRefPubMedGoogle Scholar
  22. Darrouzet E, Labédan M, Landré X, Perdereau E, Christidès JP, Bagnères AG (2014) Endocrine control of cuticular hydrocarbon profiles during worker-to-soldier differentiation in the termite Reticulitermes flavipes. J Insect Physiol 61:25–33CrossRefPubMedGoogle Scholar
  23. Deneubourg JL, Lioni A, Detrain C (2002) Dynamics of aggregation and emergence of cooperation. Biol Bull 202:262–267CrossRefPubMedGoogle Scholar
  24. Detrain C, Deneubourg JL (2006) Self-organized structures in a superorganism: do ants “behave” like molecules? Phys Life Rev 3:162–187CrossRefGoogle Scholar
  25. Downs SG, Ratnieks FLW (1999) Recognition of conspecifics by honeybee guards uses nonheritable cues acquired in the adult stage. Anim Behav 58:643–648CrossRefPubMedGoogle Scholar
  26. Downs SG, Ratnieks FLW, Jefferies SL, Rigby HE (2000) The role of floral oils in the nestmate recognition system of honey bees (Apis mellifera L.). Apidologie 31:357–365CrossRefGoogle Scholar
  27. Dyer FC, Seeley TD (1987) Interspecific comparisons of endothermy in honeybees (Apis): deviations from the expected size-related patterns. J Exp Biol 122:1–26Google Scholar
  28. Engel MS (2001) A monography of the Baltic amber bees and evolution of the Apoidea (Hymenoptera). Bull Am Mus Nat Hist 259:5–192CrossRefGoogle Scholar
  29. Ferreira-Caliman MJ, Nascimento FS, Turatti IC, Mateus S, Lopes NP, Zucchi R (2010) The cuticular hydrocarbons profiles in the stingless bee Melipona marginata reflect task-related differences. J Insect Physiol 56:800–804CrossRefPubMedGoogle Scholar
  30. Getz WM, Page RE (1991) Chemosensory kin–communication systems and kin recognition in honeybees. Ethology 87:298–315CrossRefGoogle Scholar
  31. Getz WM, Brückner D, Smith KB (1989) The ontogeny of cuticular chemosensory cues in worker honey bees Apis mellifera. Apidologie 20:105–113CrossRefGoogle Scholar
  32. Gordon DM (1996) The organization of work in social insect colonies. Nature 380:121–124CrossRefGoogle Scholar
  33. Gordon DM (2002) The regulation of foraging activity in red harvester ant colonies. Am Nat 159:509–518CrossRefPubMedGoogle Scholar
  34. Greene MJ, Gordon DM (2003) Social insects: cuticular hydrocarbons inform task decisions. Nature 423:32CrossRefPubMedGoogle Scholar
  35. Greene MJ, Gordon DM (2007) Interaction rate informs harvester ant task decisions. Behav Ecol 18:451–455CrossRefGoogle Scholar
  36. Haverty MI, Grace JK, Nelson LJ, Yamamoto RT (1996) Intercaste, intercolony, and temporal variation in cuticular hydrocarbons of Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). J Chem Ecol 22:1813–1834CrossRefPubMedGoogle Scholar
  37. Hepburn HR, Bernard RTF, Davidson BC, Muller WJ, Lloyd P, Kurstjens SP, Vincent SL (1991) Synthesis and secretion of beeswax in honeybees. Apidologie 22:21–36CrossRefGoogle Scholar
  38. Holldobler B, Wilson EO (2008) The beauty, elegance and strangeness of insect societies. W. W. Norton, New YorkGoogle Scholar
  39. Howard RW, McDaniel CA, Blomquist GJ (1978) Cuticular hydrocarbons of the eastern subterranean termite, Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae). J Chem Ecol 4:233–245CrossRefGoogle Scholar
  40. Howard RW, McDaniel CA, Nelson DR, Blomquist GJ, Gelbaum LT, Zalkow LH (1982) Cuticular hydrocarbons of Reticulitermes virginicus (Banks) and their role as potential species- and caste-recognition cues. J Chem Ecol 8:1227–1239CrossRefPubMedGoogle Scholar
  41. Kaib M, Eisermann B, Schoeters E, Billen J, Franke S, Francke W (2000) Task related variation of postpharyngeal and cuticular hydrocarbon compositions in the ant Myrmicaria eumenoides. J Comp Physiol A 186:939–948CrossRefPubMedGoogle Scholar
  42. Kaib M, Franke S, Francke W, Brandl R (2002) Cuticular hydrocarbons in a termite: phenotypes and a neighbour-stranger effect. Physiol Entomol 27:189–198CrossRefGoogle Scholar
  43. Kather R, Drijfhout FP, Martin SJ (2011) Task group differences in cuticular lipids in the honey bee Apis mellifera. J Chem Ecol 37:205–212CrossRefPubMedGoogle Scholar
  44. Krasnec MO, Breed MD (2013) Colony-specific cuticular hydrocarbon profile in Formica argentea, ants. J Chem Ecol 39:59–66CrossRefPubMedGoogle Scholar
  45. Larsen J, Fouks B, Bos N, D’Ettorre P, Nehring V (2014) Variation in nestmate recognition ability among polymorphic leaf-cutting ant workers. J Insect Physiol 70:59–66CrossRefPubMedGoogle Scholar
  46. Lockey KH (1988) Lipids of the insect cuticle: origin, composition and function. Comp Biochem Physiol 89B:595–645Google Scholar
  47. Martin SJ, Drijfhout FP (2009) Nestmate and task cues are influenced and encoded differently within ant cuticular hydrocarbon profiles. J Chem Ecol 35:368–374CrossRefPubMedGoogle Scholar
  48. Martin SJ, Helantera H, Drijfhout FP (2008) Colony specific hydrocarbons identify nest mates in two species of Formica ant. J Chem Ecol 34:1072–1080CrossRefPubMedGoogle Scholar
  49. Morse RA, Shearer DA, Bosh SR, Benton AW (1967) Observation on alarm substances in the genus Apis. J Apic Res 6:113–118Google Scholar
  50. Murakami ASN, Nunes TM, Desuó IC, Shima SN, Mateus S (2015) The cutiular hydrocarbons profies in the colonial recognitin of the neotropical eusocial wasp, Mischocyttrus cassununga (Hymenoptera: Vespidae). Sociobiology 62:109–115CrossRefGoogle Scholar
  51. Nunes TM, Turatti ICC, Mateus S, Nascimento FS, Lopes NP, Zucchi R (2009) Cuticular hydrocarbons in the stingless bee Schwarziana quadripunctata (Hymenoptera, Apidae, Meliponini): differences between colonies, castes and age. Genet Mol Res 8(2):589–595CrossRefPubMedGoogle Scholar
  52. O’Donnell S, Bulova SJ (2007) Worker connectivity: a review of the design of worker communication systems and their effects on task performance in insect societies. Insect Soc 54:203–210CrossRefGoogle Scholar
  53. Oldroyd BP, Wongsiri S (2006) Asian honey bees: biology, conservation, and human interactions. Harvard University Press, CambridgeGoogle Scholar
  54. Ono M, Okada I, Sasaki M (1987) Heat protection by balling in the Japanese honeybee Apis cerana japonica as a defensive behavior against the hornet, Vespa simillima xanthoptera (Hymenoptera: Vespidae). Experientia 43:1031–1032CrossRefGoogle Scholar
  55. Ono M, Garashi T, Ohno E, Sasaki M (1995) Unusual thermal defence by a honeybee against mass attack by hornets. Nature 377:334–336CrossRefGoogle Scholar
  56. Page RE Jr, Metcalf RA, Metcalf RL, Erickson EH Jr, Lampman RL (1991) Extractable hydrocarbons and kin recognition in the honey bee. J Chem Ecol 17:745–756CrossRefPubMedGoogle Scholar
  57. Pratt S (2005) Quorum sensing by encounter rates in the ant Temnothorax albipennis. Behav Ecol 10:488–496Google Scholar
  58. Scholl J, Naug D (2011) Olfactory discrimination of age-specific hydrocarbons generates behavioral segregation in a honeybee colony. Behav Ecol Sociobiol 65:1967–1973CrossRefGoogle Scholar
  59. Smith RK, Taylor OR (1990) Unsaturated extracted hydrocarbon caste differences between European queen and worker honey bees, Apis mellifera L. (Hymenoptera: Apidae). J Kansas Entomol Soc 63:369–374Google Scholar
  60. Tan K, Wang ZW, Yang M, Hepburn R, Sarah R (2010) Nestmate ecognition differences between honeybee colonies of Apis cerana and Apis mellifera. J Insect Behav 23:381–388CrossRefGoogle Scholar
  61. Torres CW, Brandt M, Tsutsui ND (2007) The role of cuticular hydrocarbons as chemical cues for nestmate recognition in the invasive Argentine ant (Linepithema humile). Insect Soc 54:363–373CrossRefGoogle Scholar
  62. Tulloch AP (1980) Beeswax - Composition and analysis. Bee World 61:47–62Google Scholar
  63. 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
  64. Wagner D, Brown MJF, Broun P, Cuevas W, Moses LE, Chao DL, Gordon DM (1998) Task-related differences in the cuticular hydrocarbon composition of harvester ants, Pogonomyrmex barbatus. J Chem Ecol 24:2021–2037CrossRefGoogle Scholar
  65. Weiss I, Hofferberth J, Ruther J, Stokl J (2015) Varying importance of cuticular hydrocarbons and iridoids in the species-specific mate recognition pheromones of three closely related Leptopilina species. Front Ecol Evol 3:1–12CrossRefGoogle Scholar
  66. Wilson EO (1971) The insect societies. Belknap Press of Harvard University PressGoogle Scholar
  67. Xu P, Shi M, Chen XX (2009) Antimicrobial peptide evolution in the Asiatic honey bee Apis cerana. PLoS ONE 4, e4239CrossRefPubMedPubMedCentralGoogle Scholar
  68. Yamaoka R (1990) Chemical approach to understanding interactions among organisms. Physiol Ecol Jpn 27:31–52Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Seydur Rahman
    • 1
  • Sudhanya Ray Hajong
    • 1
  • Jérémy Gévar
    • 2
  • Alain Lenoir
    • 2
  • Eric Darrouzet
    • 2
  1. 1.North-Eastern Hill UniversityShillong-22India
  2. 2.IRBI UMR CNRS 7261 Université François Rabelais, Faculté des SciencesToursFrance

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