Skip to main content
Log in

Fertility signals in the bumblebee Bombus terrestris (Hymenoptera: Apidae)

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

In eusocial Hymenoptera, queen control over workers is probably inseparable from the mechanism of queen recognition. In primitively eusocial bumblebees (Bombus), worker reproduction is controlled not only by the presence or absence of a dominant queen but also by other dominant workers. Furthermore, it was shown that the queen dominance is maintained by pheromonal cues. We investigated whether there is a similar odor signal released by egg-laying queens and workers that may have a function as a fertility signal. We collected cuticular surface extracts from nest-searching and breeding Bombus terrestris queens and workers that were characterized by their ovarian stages. In chemical analyses, we identified 61 compounds consisting of aldehydes, alkanes, alkenes, and fatty acid esters. Nest-searching queens and all groups of breeding females differed significantly in their odor bouquets. Furthermore, workers before the competition point (time point of colony development where workers start to develop ovaries and lay eggs) differed largely from queens and all other groups of workers. Breeding queens showed a unique bouquet of chemical compounds and certain queen-specific compounds, and the differences toward workers decrease with an increasing development of the workers’ ovaries, hinting the presence of a reliable fertility signal. Among the worker groups, the smallest differences were found after the competition point. Egg-laying females contained higher total amounts of chemical compounds and of relative proportions of wax-type esters and aldehydes than nest-searching queens and workers before the competition point. Therefore, these compounds may have a function as a fertility signal present in queens and workers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ayasse M, Marlovits TC, Tengö J, Taghizadeh T, Francke W (1995) Are there pheromonal dominance signals in the bumblebee Bombus hypnorum L (Hymenoptera, Apidae). Apidologie 26(1):163–180

    Article  CAS  Google Scholar 

  • Ayasse M, Birnbaum J, Tengö J, van Doorn A, Taghizadeh T, Francke W (1999) Caste- and colony-specific chemical signals on eggs of the bumble bee, Bombus terrestris L. (Hymenoptera: Apidae). Chemoecology 9(3):119–126

    Article  CAS  Google Scholar 

  • Backhaus K, Erichson B, Flinke W, Schuchard-Ficher C, Weiber R (1987) Multivariate Analysemethoden. Springer, New York, p 404

    Google Scholar 

  • Bloch G (1999) Regulation of queen–worker conflicts in bumble-bee (Bombus terrestris) colonies. Proc R Soc Lond B 266:2465–2469

    Article  Google Scholar 

  • Bloch G, Hefetz A (1999) Reevaluation of the role of mandibular glands in regulation of reproduction in bumblebee colonies. J Chem Ecol 25:881–896

    Article  CAS  Google Scholar 

  • Buckle GR (1982) Queen-worker behavior and nestmate interactions in young colonies of Lasioglossum zephyrum. Insect Soc 29:125–137

    Article  Google Scholar 

  • Buser H-R, Arn H, Guerin P, Rauscher S (1983) Determination of double bond position in mono-unsaturated acetates by mass spectrometry of dimethyl disulfide adducts. Anal Chem 55:818–822

    Article  CAS  Google Scholar 

  • Cahlíková L, Hovorka O, Ptáček V, Valterová I (2004) Exocrine gland secretions of virgin queens of five bumblebee species (Hymenoptera: Apidae, Bombini). Z Naturforsch C 59(7–8):582–589

    PubMed  Google Scholar 

  • D’Ettorre P, Heinze J, Schulz C, Francke W, Ayasse M (2004) Does she smell like a queen? Chemoreception of a cuticular hydocarbon signal in the ant Pachycondyla inversa. J Exp Biol 207:1085–1091

    Article  PubMed  CAS  Google Scholar 

  • D’Etorre P, Tofilski A, Heinze J, Ratnieks FLW (2006) Non-transferable signal on ant queen eggs prevent policing evasion by cue scrambling. Naturwissenschaften 93(3):136–140

    Article  Google Scholar 

  • Fletcher DJC, Ross KG (1985) Regulation of reproduction in eusocial Hymenoptera. Annu Rev Entomol 30:319–343

    Article  Google Scholar 

  • Hefetz A, Tengö J, Lübke G, Francke W (1993) Inter-colonial and intra-colonial variations in Dufour’s gland secretion in the bumble bee species Bombus hypnorum (Hymenoptera: Apidae). In: Weise K, Gribakin FG, Renninger G (eds) Sensory systems of arthropods. Birkhauser, Basel, pp 469–480

    Google Scholar 

  • Hefetz A, Taghizadeh T, Francke W (1996) The exocrinology of the queen bumble bee Bombus terrestris (Hymenoptera:Apidae, Bombini). Z Naturforsch 51c:409–422

    Google Scholar 

  • Hölldobler B, Michener CD (1980) Mechanisms of identification and discrimination in social hymenoptera. In: Markl H (ed) Evolution of social behaviour hypotheses and empirical tests. Verlag Chemie GmbH, Weinheim, pp 35–58

    Google Scholar 

  • Katayama E (1974) Egg-laying habits and brood development in Bombus hypocrita (Hymenoptera, Apidae), 1 egg-laying habits of queens and workers. Kontyû 42(4):416–438

    Google Scholar 

  • Katzav-Gozansky T, Soroker V, Hefetz A (2002) Honeybees Dufour’s gland—idiosyncrasy of a new queen signal. Apidologie 33:525–537

    Article  CAS  Google Scholar 

  • Katzav-Gozansky T, Boulay R, Soroker V, Hefetz A (2004) Queen-signal modulation of worker pheromonal composition in honeybees. Proc R Soc Lond B 271:2065–2069

    Article  Google Scholar 

  • Katzav-Gozansky T, Boulay R, Soroker V, Hefetz A (2006) Queen pheromones affecting the production of queen-like secretion in workers. J Comp Physiol 192:737–742

    Article  Google Scholar 

  • Keller L, Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signalling? Anim Behav 45:787–794

    Article  Google Scholar 

  • Liebig J, Peeters C, Oldham NJ, Markstädter C, Hölldobler B (2000) Are variations in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator? Proc Natl Acad Sci USA 97:4124–4131

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AF (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Lett Nat 430:557–560

    Article  CAS  Google Scholar 

  • Malka O, Shnieor S, Hefetz A, Katzav-Gozansky T (2006) Reversible royalty in worker honeybees under the queen influence. Behav Ecol Sociobiol 61:465–473

    Article  Google Scholar 

  • McLafferty FW, Stauffer DB (1989) The Wiley NBS registry of mass spectral data. Wiley, New York

    Google Scholar 

  • Michener CD (1974) The social behavior of the bees. Harvard University Press, Cambrige, UK, p 404

    Google Scholar 

  • Norusis MJ (1993a) SPSS for Windows: base system user’s guide, release 6.0. SPSS, Chicago, IL

    Google Scholar 

  • Norusis MJ (1993b) SPSS for Windows: professional statistics, release 6.0. SPSS, Chicago, IL

    Google Scholar 

  • Plettner E, Slessor KN, Winston ML, Robinson GE, Page RE (1993) Mandibular gland components and ovarian development as measures of caste differentiation in the honey bee (Apis mellifera L.). J Insect Physiol 39(3):235–240

    Article  Google Scholar 

  • Röseler PF (1985) A technique for year-round rearing of Bombus terrestris (Apidae, Bombini) colonies in captivity. Apidologie 16:165–169

    Article  Google Scholar 

  • Röseler PF, Röseler I (1977) Dominance in bumblebees. In: Proc Int IUSSI Congr, vol 8, Wageningen, pp 232–235

  • Röseler PF, van Honk CGJ (1990) Castes and reproduction in bumblebees. In: Engels W (ed) Social insects, an evolutionary approach to castes and reproduction. Springer, Berlin, pp 147–166

    Google Scholar 

  • Röseler PF, Röseler I, van Honk CGJ (1981) Evidence for inhibition of corpora allata activity in workers of Bombus terrestris by a pheromone from the queen’s mandibular glands. Experientia 37:348–351

    Article  Google Scholar 

  • Seeley TD (1979) Queen substance dispersal by messenger workers in honeybee colonies. Behav Ecol Sociobiol 5:391–415

    Article  Google Scholar 

  • Slessor KN, Kaminski L-A, King GGS, Borden JH, Winston ML (1988) Semiochemical basis of the retinue response to queen honey bees. Nature 332:354–356

    Article  CAS  Google Scholar 

  • Tengö J, Hefetz A, Bertsch A, Schmitt U, Lübke G, Francke W (1991) Species specificity and complexity of Dufour’s gland secretion of bumble bees. Comp Biochem Physiol 99B:641–646

    Google Scholar 

  • van Doorn A (1988) Reproductive dominance in bumble-bees: an etho-physiological study. Thesis, University of Utrecht, The Netherlands

  • van Doorn A (1989) Factors influencing dominance behaviour in queenless bumblebee workers (Bombus terrestris). Physiol Entomol 14:211–221

    Article  Google Scholar 

  • van Doorn A, Heringa J (1986) The ontogeny of a dominance hierarchy in colonies of the bumblebee Bombus terrestris (Hymenoptera, Apidae). Insect Soc 33:3–25

    Article  Google Scholar 

  • van Honk CGJ, Velthuis HHW, Röseler P-F, Malotaux ME (1980) The mandibular glands of Bombus terrestris queens as a source of queen pheromones. Entomol Exp Appl 28:191–198

    Article  Google Scholar 

  • van Honk CG, Röseler PF, Velthuis HHW, Hoogeveen JC (1981) Factors influencing the egg laying of workers in a captive Bombus terrestris colony. Behav Ecol Sociobiol 9:9–14

    Article  Google Scholar 

  • Velthuis HHW (1976) Egg laying, aggression and dominance in bees. In: Proc XI Int Congr Entomol Washington DC, pp. 436–449

  • Winston ML, Higo HA, Slessor KN (1990) Effect of various dosages of queen mandibular gland pheromone on the inhibition of queen rearing in the honey bee (Hymenoptera: Apidae). Ann Entomol Soc Am 83(2):234–238

    Google Scholar 

Download references

Acknowledgments

We wish to thank the German Research Foundation (DFG) for financial support (AY 12/2-1). A. Sramkova would like to thank the Friedrich Naumann Stiftung for financial support. W. Francke likes to thank the Fonds der Chemischen Industrie for financial support. All experiments comply with the current laws of the country in which they were performed: in this case, Germany.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Ayasse.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sramkova, A., Schulz, C., Twele, R. et al. Fertility signals in the bumblebee Bombus terrestris (Hymenoptera: Apidae). Naturwissenschaften 95, 515–522 (2008). https://doi.org/10.1007/s00114-008-0353-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-008-0353-4

Keywords

Navigation