Abstract
The signalling functions of cuticular lipids, particularly cuticular hydrocarbons, have gained considerable attention in social insect communication. Information transfer between individuals by means of these substances has been examined extensively. However, communication with cuticular lipids is not limited to inter-individual recognition. Cuticular compounds can also have a signalling function in the nest environment. Workers of the bumblebee Bombus terrestris leave cuticular lipid traces, so-called footprints, that mark their nest entrance. In addition, there is evidence that bumblebees sense nesting material to identify their colony. In this study, we examined the signalling potential of bumblebee wax, and tested if bumblebee workers are able to identify their colony with the help of wax scent. Chemical analyses of wax extracts using coupled gas chromatography–mass spectrometry showed that wax from colonies of the bumblebee B. terrestris contained a complex blend of cuticular lipids, dominated by hydrocarbons and wax esters. Comparing the relative compound amounts of wax samples from different colonies, we found that wax scent patterns varied with nest identity. Olfactometer bioassays showed that bumblebees were able to discriminate between wax scents from their own and a foreign colony. Our findings suggest that wax emits characteristic olfactory profiles that are used by workers to recognize their colony.
Similar content being viewed by others
References
Ayasse, M., Birnbaum, J., Tengö, J., van Doorn, A., Taghizadeh, T., and Francke, W. 1999. Caste- and colony-specific chemical signals on eggs of the bumble bee, Bombus terrestris L. (Hymenoptera: Apidae). Chemoecology 9:119–126.
Ayasse, M., Marlovits, T., Tengo, J., Taghizadeh, T., and Francke, W. 1995. Are there pheromonal dominance signals in the bumblebee Bombus hypnorum L (Hymenoptera, Apidae)? Apidologie 26:163–180.
Benjamini, Y. and Hochberg, Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. Roy. Stat. Soc. Ser. B 57:289–300.
Billen, J. and Morgan, E. D. 1998. Pheromone communication in social insects: Sources and secretions, pp. 3–33, in R. K. Vander Meer, M. D. Breed, K. E. Espelie, and M. L. Winston (eds.), Pheromone Communication in Social Insects. Westview Press, Boulder.
Blomquist, G. J. and Bagnères, A. G. 2010. Insect hydrocarbons: Biology, Biochemistry, and Chemical Ecology. Cambridge University Press, Cambridge.
Blomquist, G. J., Chu, A. J., and Remaley, S. 1980. Biosynthesis of wax in the honeybee, Apis mellifera L. Insect Biochem 10:313–321.
Breed, M. D. 1998. Recognition pheromones of the honey bee: The chemistry of nestmate recognition. BioScience 48:463–470.
Breed, M. D., Page, R. E., Hibbard, B. E., and Bjostad, L. B. 1995. Interfamily variation in comb wax hydrocarbons produced by honey bees. J. Chem. Ecol. 21:1329–1338.
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. 43:875–883.
Breed, M. D., Williams, K. R., and Fewell, J. H. 1988. Comb wax mediates the acquisition of nest-mate recognition cues in honey bees. Proc. Natl. Acad. Sci. U. S. A 85:8766–8769.
Brüschweiler, H., Felber, H., and Schwager, F. 1989. Bienenwachs—Zusammensetzung und Beurteilung der Reinheit durch gaschromatographische Analyse. Eur. J. Lipid Sci. Technol 91:73–79.
Bunk, E., Sramkova, A., and Ayasse, M. 2010. The role of trail pheromones in host nest recognition of the social parasitic bumblebees Bombus bohemicus and Bombus rupestris (Hymenoptera: Apidae). Chemoecology 20:189–198.
Cederberg, B. 1977. Evidence for trail marking in Bombus terrestris workers (Hymenoptera, Apidae). Zoon 5:143–146.
Chittka, L., Williams, N. M., Rasmussen, H., and Thomson, J. D. 1999. Navigation without vision: Bumblebee orientation in complete darkness. Proc. R. Soc. Lond. Ser. B 266:45–50.
Couvillon, M. J., Caple, J. P., Endsor, S. L., Kärcher, M., Russell, T. E., Storey, D. E., and Ratnieks, F. L. 2007. Nest-mate recognition template of guard honeybees (Apis mellifera) is modified by wax comb transfer. Biol. Lett 3:228–230.
Crozier, R. H. and Dix, M. W. 1979. Analysis of two genetic models for the innate components of colony odor in social Hymenoptera. Behav. Ecol. Sociobiol. 4:217–224.
Dani, F. R., Jones, G. R., Corsi, S., Beard, R., Pradella, D., and Turillazzi, S. 2005. Nestmate recognition cues in the honey bee: Differential importance of cuticular alkanes and alkenes. Chem. Senses 30:477–489.
Da Cruz Landim, C. 1963. Evaluation of the wax and scent glands in the Apinae (Hymenoptera: Apidae). J. N. Y. Entomol. Soc. 21:2–13.
D’Ettorre, P. and Moore, A. J. 2008. Chemical communication and the coordination of social interactions in insects, pp. 81–96, in P. D’Ettorre and D. P. Hughes (eds.), Sociobiology of Communication: An Interdisciplinary Perspective. Oxford University Press, Oxford.
D’Ettorre, P., Wenseleers, T., Dawson, J., Hutchinson, S., Boswell, T., and Ratnieks, F. L. W. 2006. Wax combs mediate nestmate recognition by guard honeybees. Anim. Behav. 71:773–779.
Espelie, K. E., Wenzel, J. W., and Chang, G. 1990. Surface lipids of social wasp Polistes metricus Say and its nest and nest pedicel and their relation to nestmate recognition. J. Chem. Ecol. 16:2229–2242.
Ferguson, D., Gamboa, G. J. J., and Julia, K. 1987. Discrimination between natal and non-natal nests by the social wasps Dolichovespula maculata and Polistes fuscatus (Hymenoptera: Vespidae). J. Kansas Entomol. Soc. 60:65–69.
Foster, R. L. and Gamboa, G. J. 1989. Nest entrance marking with colony specific odors by the bumble bee Bombus occidentalis (Hymenoptera: Apidae). Ethology 81:273–278.
Francke, W. and Schulz, S. 2010. Pheromones of terrestrial invertebrates, pp. 153–224, in L. Mander and H.-W. Liu (eds.), Comprehensive Natural Products Chemistry II, Vol. 4. Elsevier, Oxford.
Free, J. B. 1987. Pheromones of Social Bees. Comstock Pub. Associates, Ithaca.
Fröhlich, B., Riederer, M., and Tautz, J. 2001. Honeybees discriminate cuticular waxes based on esters and polar components. Apidologie 32:265–274.
Fröhlich, B., Tautz, J., and Riederer, M. 2000. Chemometric classification of comb and cuticular waxes of the honeybee Apis mellifera carnica. J. Chem. Ecol. 26:123–137.
Gamboa, G. J. 2004. Kin recognition in eusocial wasps. Ann. Zool. Fenn. 41:789–808.
Gamboa, G. J., Foster, R. L., and Richards, K. W. 1987. Intraspecific nest and brood recognition by queens of the bumble bee, Bombus occidentalis (Hymenoptera: Apidae). Can. J. Zool. 65:2893–2897.
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 odours. Anim. Behav. 34:685–695.
Greene, M. 2010. Cuticular hydrocarbon cues in the formation and maintenance of insect social groups, pp. 244–253, in G. J. Blomquist and A. G. Bagnères (eds.), Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. Cambridge University Press, Cambridge.
Greene, M. J. and Gordon, D. M. 2003. Cuticular hydrocarbons inform task decisions. Nature 423:32.
Hadley, N. 1994. Water Relations of Terrestrial Arthropods. Academic, San Diego.
Hannonen, M., Sledge, M. F., Turillazzi, S., and Sundstrom, L. 2002. Queen reproduction, chemical signalling and worker behaviour in polygyne colonies of the ant Formica fusca. Anim. Behav. 64:477–485.
Hefetz, A. 1998. Exocrine glands and their products in non-Apis bees: Chemical, functional and evolutionary perspectives, pp. 236–256, in R. K. Vander Meer, M. D. Breed, K. E. Espelie, and M. L. Winston (eds.), Pheromone Communication in Social Insects. Westview Press, Boulder.
Hefetz, A., Taghizadeh, T., and Francke, W. 1996. The exocrinology of the queen bumble bee Bombus terrestris (Hymenoptera: Apidae, Bombini). Z. Naturforsch. 51:409–422.
Hölldobler, B. and Wilson, E. O. 2008. The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies. Norton, New York.
Hölldobler, B. and Michener, C. D. 1980. Mechanisms of identification and discrimination in social Hymenoptera, pp. 35–58, in H. Markl (ed.), Evolution of Social Behaviour: Hypotheses and Empirical Tests. Weinheim, Verlag Chemie.
Howard, R. W. and Blomquist, G. J. 2005. Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu. Rev. Entomol. 50:371–393.
Kreuter, K., Bunk, E., Lückemeyer, A., Twele, R., Francke, W., and Ayasse, M. 2012. How the social parasitic bumblebee Bombus bohemicus sneaks into power of reproduction. Behav. Ecol. Sociobiol. 66:475–486.
Kreuter, K., Twele, R., Francke, W., and Ayasse, M. 2010. Specialist Bombus vestalis and generalist Bombus bohemicus use different odour cues to find their host Bombus terrestris. Anim. Behav. 80:297–302.
Kukuk, P. F., Breed, M. D., Sobti, A., and Bell, W. J. 1977. The contributions of kinship and conditioning to nest recognition and colony member recognition in a primitively eusocial bee, Lasioglossum zephyrum (Hymenoptera: Halictidae). Behav. Ecol. Sociobiol. 2:319–327.
Kurstjens, S., Hepburn, H., Schoening, F., and Davidson, B. 1985. The conversion of wax scales into comb wax by African honeybees. J. Comp. Physiol. B. 156:95–102.
le Conte, Y. and Hefetz, A. 2008. Primer pheromones in social hymenoptera. Annu. Rev. Entomol. 53:523–542.
Liebig, J. 2010. Hydrocarbon profiles indicate fertility and dominance status in ant, bee, and wasp colonies, pp. 254–281, in G. J. Blomquist and A. G. Bagnères (eds.), Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. Cambridge University Press, Cambridge.
Lopez-Vaamonde, C., Koning, J. W., Brown, R. M., Jordan, W. C., and Bourke, A. F. G. 2004. Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557–560.
McLafferty, F. W. and Turecek, F. 1993. Interpretation of Mass Spectra, 4th ed. University Science, Mill Welley.
Menzel, R., DE Marco, R., and Greggers, U. 2006. Spatial memory, navigation and dance behaviour in Apis mellifera. J. Comp. Physiol. A. 192:889–903.
Michener, C. D. 1969. Evolution of the nests of bees. Am. Zool. 4:227–239.
Monnin, T. 2006. Chemical recognition of reproductive status in social insects. Ann. Zool. Fenn. 43:515–530.
Ramsay, J. 1935. The evaporation of water from the cockroach. J. Exp. Biol. 12:373–383.
Saleh, N., Scott, A., Bryning, G., and Chittka, L. 2007. Distinguishing signals and cues: Bumblebees use general footprints to generate adaptive behaviour at flowers and nest. Arthropod-Plant Interactions 1:119–127.
Singer, T. and Espelie, K. 1996. Nest surface hydrocarbons facilitate nestmate recognition for the social wasp, Polistes metricus Say (Hymenoptera: Vespidae). J. Insect Behav. 9:857–870.
Snodgrass, R. E. 1956. Anatomy of The Honey Bee. Cornell University Press, London.
Sramkova, A., Schulz, C., Twele, R., Francke, W., and Ayasse, M. 2008. Fertility signals in the bumblebee Bombus terrestris. Naturwissenschaften 95:515–522.
Schulz, S. 2001. Composition of the silk lipids of the spider Nephila clavipes. Lipids 36:637–647.
Tengö, J., Hefetz, A., Bertsch, A., Schmitt, U., Lübke, G., and Francke, W. 1991. Species specificity and complexity of Dufour’s gland secretion of bumble bees. Comp. Biochem. Physiol. B 99:641–646.
van Zweden, J. S. and D’Ettorre, P. 2010. Nestmate recognition in social insects and the role of hydrocarbons, pp. 222–243, in G. J. Blomquist and A. G. Bagnères (eds.), Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. Cambridge University Press, Cambridge.
Velthuis, H. H. W. and van Doorn, A. 2006. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37:421–451.
von Frisch, K. 1967. The Dance Language and Orientation of Bees. Harvard University Press, Cambridge.
Wcislo, W. T. 1992. Nest localization and recognition in a solitary bee, Lasioglossum (Dialictus) figueresi Wcislo (Hymenoptera: Halictidae), in relation to sociality. Ethology 92:108–123.
Wilson, E. O. and Bossert, W. H. 1963. Chemical communication among animals. Recent Prog. Horm. Res. 19:673–716.
Witjes, S. and Eltz, T. 2009. Hydrocarbon footprints as a record of bumblebee flower visitation. J. Chem. Ecol. 35:1320–1325.
Acknowledgments
This study was funded by the German Research Foundation (AY 12/3-1) and the PhD program of the Carl Zeiss Foundation.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 147 kb)
Rights and permissions
About this article
Cite this article
Rottler, AM., Schulz, S. & Ayasse, M. Wax Lipids Signal Nest Identity in Bumblebee Colonies. J Chem Ecol 39, 67–75 (2013). https://doi.org/10.1007/s10886-012-0229-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-012-0229-0