Advertisement

Insectes Sociaux

, Volume 56, Issue 2, pp 157–170 | Cite as

Smelling like resin: terpenoids account for species-specific cuticular profiles in Southeast-Asian stingless bees

  • S. D. Leonhardt
  • N. Blüthgen
  • T. SchmittEmail author
Research Article

Abstract

Insects may be unique in having a cuticle with a species-specific chemical profile. In social insects, colony survival depends not only on species-specific but also on colony-specific cuticular compounds with hydrocarbons playing an important role in the communication systems of ants, termites, wasps and bees. We investigated inter- and intraspecific differences in the composition of compounds found on the body surface of seven paleotropical stingless bee species (Apidae: Meliponini) at two different sites in Borneo (Sabah, Malaysia). Besides hydrocarbons, the body surface of all seven stingless bee species comprised terpenoid compounds, a substance class that has not been reported for chemical profiles of any social insect so far. Moreover, the chemical profile of some species differed fundamentally in the composition of terpenoids with one group (e.g. sesquiterpenes) being present in one species, but missing in another. Chemical profiles of different colonies from the same species showed the same hydrocarbon- and terpenoid compounds over different regions, as tested for Tetragonilla collina and Tetragonula melanocephala. However, chemical profiles differed quantitatively between the different colonies especially in T. melanocephala. It is likely that the terpenoids are derived from plant resins because stingless bees are known to collect and use large amounts of resins for nest construction and defence, suggesting an environmental origin of the terpenoids in the chemical profile of paleotropical stingless bees.

Keywords

Stingless bees Trigona Cuticular profiles Terpenoids Resins 

Notes

Acknowledgments

We thank the Royal Society as well as the staff from DVC and KSR for their support, and the Economic Planning Unit (EPU) for giving us permission to perform research in Malaysia. Chey Vun Khen and Arthur Chung (Forestry Research Centre, Sandakan) kindly supported this project. We further thank Dylan Burge for proof-reading the first draft of this manuscript and Gunnar Knobloch for help with data collection as well as Florian Menzel for help with the statistical analyses. The comments of two anonymous reviewers greatly improved this manuscript. SDL was supported by a grant of the German Excellence Initiative to the Graduate School of Life Science, University of Würzburg, NB and TS by the Sonderforschungsbereich ‘Mechanisms and Evolution of Arthropod Behaviour’ (SFB 554) of the German Research Foundation (DFG).

References

  1. Abdalla F.C., Jones G.R., Morgan E.D. and da Cruz-Landim C. 2003. Comparative study of the cuticular hydrocarbon composition of Melipona bicolor Lepeletier, 1836 (Hymenoptera, Meliponini) workers and queens. Gen. Molec. Res. 2: 191–199Google Scholar
  2. Ayasse M., Engels W., Lübke G., Taghizadeh T. and Francke W. 1999. Mating expenditures reduced via female sex pheromone modulation in the primitively eusocial halictine bee, Lasioglossum (Evylaeus) malachurum (Hymenoptera : Halictidae). Behav. Ecol. Sociobiol. 45: 95–106CrossRefGoogle Scholar
  3. Ayasse M., Marlovits T., Tengö J., Taghizadeh T. and Francke W. 1995. Are there pheromonal dominance signals in the bumblebee Bombus hypnorum L (Hymenoptera, Apidae). Apidologie 26: 163–180CrossRefGoogle Scholar
  4. Bagnères A.G., Clement J.L., Blum M.S., Severson R.F., Joulie C. and Lange C. 1990. Cuticular hydrocarbons and defensive compounds of Reticulitermes flavipes (Kollar) and R. santonensis (Feytaud) - polymorphism and chemotaxonomy. J. Chem. Ecol. 16: 3213–3244CrossRefGoogle Scholar
  5. Blomquist G.J., Chu A.J. and Remaley S. 1980. Biosynthesis of wax in the honeybee, Apis mellifera L. Insect Biochemistry 10: 313–321CrossRefGoogle Scholar
  6. Blum M.S. and Brand J.M. 1972. Social insect pheromones - their chemistry and function. Am. Zool. 12: 553–576Google Scholar
  7. Bowden R.M., Garry M.F. and Breed M.D. 1994. Discrimination of conspecific and heterospecific bees by Trigona (Tetragonisca) angustula guards. J. Kans. Entomol. Soc. 67: 137–139Google Scholar
  8. Breed M.D., Leger E.A., Pearce A.N. and Wang Y.J. 1998. Comb wax effects on the ontogeny of honey bee nestmate recognition. Anim. Behav. 55: 13–20PubMedCrossRefGoogle Scholar
  9. Breed M.D. and Page R.E. 1991. Intraspecific and interspecific nestmate recognition in Melipona workers (Hymenoptera, Apidae). J. Insect Behav. 4: 463–469CrossRefGoogle Scholar
  10. Breed M.D., Smith T.A. and Torres A. 1992. Role of guard honey bees (Hymenoptera, Apidae) in nestmate discrimination and replacement of removed guards. Ann. Entomol. Soc. 85: 633–637Google Scholar
  11. Breed M.D. and Stiller T.M. 1992. Honey bee, Apis mellifera, nestmate discrimination - hydrocarbon effects and the evolutionary implications of comb choice. Anim. Behav. 43: 875–883Google Scholar
  12. Breed M.D., Stiller T.M. and Moor M.J. 1988a. The ontogeny of kin discrimination cues in the honey bee, Apis mellifera. Behav. Genet. 18: 439–448PubMedCrossRefGoogle Scholar
  13. Breed M.D., Williams K.R. and Fewell J.H. 1988b. Comb wax mediates the acquisition of nest-mate recognition cues in honey bees. Proc. Natl. Acad. Sci. U.S.A. 85: 8766–8769PubMedCrossRefGoogle Scholar
  14. Buckner J.L. 1993. Cuticular polar lipids in insects. Insect Lipids: Chemistry, Biochemistry and Biology (Stanley-Samuelson D.W. and Nelson D.R., Eds), University of Nebraska Press, Lincoln, Nebraska. pp 227–270Google Scholar
  15. Cane J.H. 1986. Predator deterrence by mandibular gland secretions of bees (Hymenoptera, Apoidea). J. Chem. Ecol. 12: 1295–1309CrossRefGoogle Scholar
  16. Cruz-Lopez L., Malo E.A., Morgan E.D., Rincon M., Guzman M. and Rojas J.C. 2005. Mandibular gland secretion of Melipona beecheii: chemistry and behavior. J. Chem. Ecol. 31: 1621–1632PubMedCrossRefGoogle Scholar
  17. Cruz-Lopez L., Patricio E. and Morgan E.D. 2001. Secretions of stingless bees: The Dufour gland of Nannotrigona testaceicornis. J. Chem. Ecol. 27: 69–80PubMedCrossRefGoogle Scholar
  18. Downs S.G., Ratnieks F.L.W., Jefferies S.L. and Rigby H.E. 2000. The role of floral oils in the nestmate recognition system of honey bees (Apis mellifera L.). Apidologie 31: 357–365CrossRefGoogle Scholar
  19. Eisner T., Johnesse J., Carrel J., Hendry L.B. and Meinwald J. 1974. Defensive use by an insect of a plant resin. Science 184: 996–999PubMedCrossRefGoogle Scholar
  20. Espelie K.E., Gamboa G.J., Grudzien T.A. and Bura E.A. 1994. Cuticular hydrocarbons of the paper wasp, Polistes fuscatus - a search for recognition pheromones. J. Chem. Ecol. 20: 1677–1687CrossRefGoogle Scholar
  21. Fletcher D.J.C. and Michener C.D. 1987. Kin Recognition in Animals, John Wiley & Sons, Chichester. 465 ppGoogle Scholar
  22. Fox J.D. 1973. A Handbook to Kabili-Sepilok Forest Reserve., Sandakan, Malaysia. 102 ppGoogle Scholar
  23. Francis B.R., Blanton W.E., Littlefield J.L. and Nunamaker R.A. 1989. Hydrocarbons of the cuticle and hemolymph of the adult honey bee (Hymenoptera, Apidae). Ann. Entomol. Soc. 82: 486–494Google Scholar
  24. Francis B.R., Blanton W.E. and Nunamaker R.A. 1985. Extractable surface hydrocarbons of workers and drones of the genus Apis. J. Apic. Res. 24: 13–26Google Scholar
  25. Francke W., Lübke G., Schröder W., Reckziegel A., Imperatriz-Fonseca A., Kleinert A., Hartfelder K., Radtke R. and Engels W. 2000. Identification of oxygen containing volatiles in cephalic secretions of workers of Brazilian stingless bees. J. Braz. Chem. Soc. 11: 562–571CrossRefGoogle Scholar
  26. Fröhlich B., Riederer M. and Tautz J. 2001. Honeybees discriminate cuticular waxes based on esters and polar components. Apidologie 32: 265–274CrossRefGoogle Scholar
  27. Fröhlich B., Tautz J. and Riederer M. 2000. Chemometric classification of comb and cuticular waxes of the honeybee Apis mellifera carnica. J. Chem. Ecol. 26: 123–137CrossRefGoogle Scholar
  28. Gamboa G.J., Reeve H.K., Ferguson I.D. and Wacker T.L. 1986. Nestmate recognition in social wasps - the origin and acquisition of recognition odors. Anim. Behav. 34: 685–695CrossRefGoogle Scholar
  29. Ghisalberti E.L. 1979. Propolis: a review. Bee World 60: 59–84Google Scholar
  30. Hick A.J., Luszniak M.C. and Pickett J.A. 1999. Volatile isoprenoids that control insect behaviour and development. Natural Product Reports 16: 39–54CrossRefGoogle Scholar
  31. Hölldobler B. 1995. The chemistry of social regulation - multicomponent signals in ant societies. Proc. Natl. Acad. Sci. U.S.A. 92: 19–22PubMedCrossRefGoogle Scholar
  32. Howard J.J. 1985. Observations on resin collecting by six interacting species of stingless bees (Apidae, Meliponinae). J. Kans. Entomol. Soc. 58: 337–345Google Scholar
  33. Howard R.W. 1993. Cuticular hydrocarbons and chemical communication. Insects Lipids: Chemistry, Biochemistry and Biology (Stanley-Samuelson D.W. and Nelson D.R., Eds), University of Nebraska Press, Lincoln, Nebraska. pp 179–226Google Scholar
  34. 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)1 and their role as potential species- and caste-recognition cues. J. Chem. Ecol. 8: 1227–1239CrossRefGoogle Scholar
  35. Inoue T. and Roubik D.W. 1990. Kin recognition of the stingless bee Melipona fasciata. Social Insects and the Environment (Veeresh G.K., Mallik R. and Viraktamath C.A., Eds), Oxford & IBH Publishing Co, New Delhi. pp 517–518Google Scholar
  36. Inoue T., Roubik D.W. and Suka T. 1999. Nestmate recognition in the stingless bee Melipona panamica (Apidae, Meliponini). Insect. Soc. 46: 208–218CrossRefGoogle Scholar
  37. Inoue T., Sakagami S.F., Salmah S. and Yamane S. 1984. The process of colony multiplication in the Sumatran stingless bee Trigona (Tetragonula) laeviceps. Biotropica 16: 100–111CrossRefGoogle Scholar
  38. Jungnickel H., da Costa A.J.S., Tentschert J., Patricio E., Imperatriz-Fonseca V.L., Drijfhout F. and Morgan E.D. 2004. Chemical basis for inter-colonial aggression in the stingless bee Scaptotrigona bipunctata (Hymenoptera : Apidae). J. Insect Physiol. 50: 761–766PubMedCrossRefGoogle Scholar
  39. Kaib M., Jmhasly P., Wilfert L., Durka W., Franke S., Francke W., Leuthold R.H. and Brandl R. 2004. Cuticular hydrocarbons and aggression in the termite Macrotermes subhyalinus. J. Chem. Ecol. 30: 365–385PubMedCrossRefGoogle Scholar
  40. Kerr W.E., Jungnickel H. and Morgan E.D. 2004. Workers of the stingless bee Melipona scutellaris are more similar to males than to queens in their cuticular compounds. Apidologie 35: 611–618CrossRefGoogle Scholar
  41. Kirchner W.H. and Friebe R. 1999. Nestmate discrimination in the African stingless bee Hypotrigona gribodoi Magretti (Hymenoptera : Apidae). Apidologie 30: 293–298CrossRefGoogle Scholar
  42. Langenheim J.H. 2003. Plant Resins: Chemistry, Evolution, Ecology and Ethnobotany, Timber Press, Portland. 586 ppGoogle Scholar
  43. Laurent P., Braekman J.-C., Daloze D. and Pasteels J. 2003. Biosynthesis of defensive compounds from beetles and ants. Eur. J. Org. Chem. 15: 2733–2743CrossRefGoogle Scholar
  44. Lehmberg L., Dworschak K. and Blüthgen N. 2008. Stingless bees (Meliponini: Trigona) - chemical and behavioral defenses against ants. J. Apic. Res. 47: 17–21Google Scholar
  45. Leonhardt S.D. and Blüthgen N. 2009. A sticky affair: resin collection by Bornean stingless bees. Biotropica (in press)Google Scholar
  46. Leonhardt S.D., Dworschak K., Eltz T. and Blüthgen N. 2007. Foraging loads of stingless bees and utilisation of stored nectar for pollen harvesting. Apidologie 38: 125–135CrossRefGoogle Scholar
  47. Lockey K.H. 1988. Lipids of the insect cuticle: origin, composition and function. Comp. Biochem. Physiol. B-Biochem. Mol. Biol. 89B: 595–645CrossRefGoogle Scholar
  48. Mant J., Brändli C., Vereecken N.J., Schulz C.M., Francke W. and Schiestl F.P. 2005. Cuticular hydrocarbons as sex pheromone of the bee Colletes cunicularius and the key to its mimicry by the sexually deceptive orchid, Ophrys exaltata. J. Chem. Ecol. 31: 1765–1787PubMedCrossRefGoogle Scholar
  49. Marsh C.W. and Greer A.G. 1992. Forest land-use in Sabah, Malaysia: an introduction to Danum Valley. Phil. Trans. R. Soc. Lond. B 335: 331–339CrossRefGoogle Scholar
  50. McDaniel C.A., Howard R.W., Blomquist G.J. and Collins A.M. 1984. Hydrocarbons of the cuticle, sting apparatus, and sting shaft of Apis mellifera L - identification and preliminary evaluation as chemotaxonomic characters. Sociobiology 8: 287–298Google Scholar
  51. Messer A.C. 1985. Fresh dipterocarp resins gathered by megachilid bees inhibit growth of pollen-associated fungi. Biotropica 17: 175–176CrossRefGoogle Scholar
  52. Michener C.D. 1974. The Social Behavior of the Bees, Harvard University Press, Harvard. 404 ppGoogle Scholar
  53. Michener C.D. 2000. The Bees of the World, John Hopkins University Press, Baltimore & London. 953 ppGoogle Scholar
  54. Morgan E.D., Jungnickel H., Keegans S.J., Do Nascimento R.R., Billen J., Gobin B. and Ito F. 2003. Comparative survey of abdominal gland secretions of the ant subfamily Ponerinae. J. Chem. Ecol. 29: 95–114PubMedCrossRefGoogle Scholar
  55. Nagamitsu T. and Inoue T. 1997. Aggressive foraging of social bees as a mechanism of floral resource partitioning in an Asian tropical rainforest. Oecologia 110: 432–439CrossRefGoogle Scholar
  56. Nunes T.M., Nascimento F.S., Turatti I.C., Lopes N.P. and Zucchi R. 2008. Nestmate recognition in a stingless bee: does the similarity of chemical cues determine guard acceptance? Anim. Behav. 75: 1165–1171CrossRefGoogle Scholar
  57. Page R.E., Metcalf R.A., Metcalf R.L., Erickson E.H. and Lampman R.L. 1991. Extractable hydrocarbons and kin recognition in honeybee (Apis mellifera L). J. Chem. Ecol. 17: 745–756CrossRefGoogle Scholar
  58. Patricio E., Cruz-Lopez L., Maile R., Tentschert J., Jones G.R. and Morgan E.D. 2002. The propolis of stingless bees: terpenes from the tibia of three Frieseomelitta species. J. Insect Physiol. 48: 249–254PubMedCrossRefGoogle Scholar
  59. Patricio E., Lopez L.C., Maile R. and Morgan E.D. 2003. Secretions of stingless bees: the Dufour glands of some Frieseomelitta species (Apidae, Meliponinae). Apidologie 34: 359–365CrossRefGoogle Scholar
  60. Paulmier I., Bagnères A.G., Afonso C.M.M., Dusticier G., Riviere G. and Clément J.L. 1999. Alkenes as a sexual pheromone in the alfalfa leaf-cutter bee Megachile rotundata. J. Chem. Ecol. 25: 471–490CrossRefGoogle Scholar
  61. Roubik D.W. 1983. Nest and colony characteristics of stingless bees from Panama (Hymenoptera, Apidae). J. Kans. Entomol. Soc. 56: 327–355Google Scholar
  62. Roubik D.W. 1989. Ecology and Natural History of Tropical Bees, Cambridge University Press, New York. 514 ppGoogle Scholar
  63. Roubik D.W. 2006. Stingless bee nesting biology. Apidologie 37: 124–143CrossRefGoogle Scholar
  64. Sakagami S.F. and Camargo J.F.M. 1964. Cerumen collection accompanied by thieving and attacking in a stingless bee, Nannotrigona (Scaptotrigona) postica (Latreille), with a consideration on territoriality in social insects. Rev. Biol. Trop. 12: 197–207Google Scholar
  65. St. Leger R.J. 1995. Integument as a barrier to microbial infections. Physiology of the Insect Epidermis (Binnington K. and Retnakaran I., Eds), CSIRO Publications, Melbourne. pp 284–306Google Scholar
  66. Suka T. and Inoue T. 1993. Nestmate recognition of the stingless bee Trigona (Tetragonula) minangkabau (Apidae, Meliponinae). J. Ethol. 11: 141–147CrossRefGoogle Scholar
  67. Suka T., Inoue T. and Roubik D.W. 1994. Worker oviposition and kin recognition of the stingless bee Scaptotrigona barrocoloradensis. Les Insectes Sociaux (Lenoir A., Arnold G. and Lepage M., Eds), Universite Paris Nord, Villetaneuse. pp 338Google Scholar
  68. Velikova M., Bankova V., Marcucci M.C., Tsvetkova I. and Kujumgiev A. 2000. Chemical composition and biological activity of propolis from Brazilian Meliponinae. Z. Naturforsch. C 55: 785–789PubMedGoogle Scholar
  69. Wheeler J.W., Blum M.S., Daly H.V., Kislow C.J. and Brand J.M. 1977. Chemistry of mandibular gland secretions of small Carpenter bees (Ceratina spp) (Hymenoptera - Anthophoridae). Ann. Entomol. Soc. 70: 635–636Google Scholar
  70. Wilson E.O. 1971. The Insect Societies, Belknap Press of the Harvard University Press, 560 ppGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  1. 1.Department of Animal Ecology and Tropical BiologyUniversity of WürzburgWürzburgGermany
  2. 2.Department of Evolutionary Biology and Animal EcologyUniversity of FreiburgFreiburgGermany

Personalised recommendations