Skip to main content
Log in

Virgin Queen Mandibular Gland Signals of Apis mellifera capensis Change with Age and Affect Honeybee Worker Responses

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The mandibular gland secretions of Apis mellifera capensis virgin queens were analyzed by gas chromatography–mass spectroscopy. Changes in the patterns of the mandibular gland volatiles of A. m. capensis virgin queens were followed from emergence until 14-d old. Ontogenetic changes in the mandibular gland secretions were largely quantitative in nature, delineating the age categories (global R = 0.612, P = 0.001), except for 7- and 14-d-old queens, which cannot be separated on their mandibular gland profiles (P = 0.2). (E)-9-Oxodec-2-enoic acid (9ODA) contributes most and most consistently to the dissimilarity between groups as well as the similarity within groups. Worker reactions to introduced virgin queens of various ages were recorded. Workers showed a significant increase in hostile reactions as queens aged (r = 0.615, N = 20, P < 0.05). Consequently, worker reactions and relative 9ODA production exhibit a positive queen age-dependent response.

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

Similar content being viewed by others

References

  • Allsopp, M. H. 1988. Mandibular gland acids and laying workers in African honey bees, pp. 72–79, in G. R. Needham, J. R. Page, M. Delfinado-Baker, and C. E. Bowman (eds.). Africanized Honeybees and Bee Mites. Ellis Horwood Ltd., Chichester.

    Google Scholar 

  • Ambrose, J. T. 1975. Aggressive behaviour of honeybee workers towards foreign queens and an inconsistency with the stress-pheromone hypothesis. Can. J. Zool. 53:69–71.

    Google Scholar 

  • Barbier, M. and Lederer, E. 1960. Structure chemique de la “substance royale” de la reine d'abeille (Apis mellifica). C. R. Acad. Sci. Paris 250:4467–4469.

    CAS  Google Scholar 

  • Barbier, M. and Pain, J. 1960. Étude de la secretion des glandes mandibulaires des reines des ouvrières d'abeilles (Apis mellifera) par chromatographie en phase gazeuse. C. R. Acad. Sci. Paris 250:3740–3742.

    PubMed  CAS  Google Scholar 

  • Boch, R. and Morse, R. A. 1974. Discrimination of familiar and foreign queens by honey bee swarms. Ann. Entomol. Soc. Am. 67:709–711.

    Google Scholar 

  • Boch, R. and Shearer, D. A. 1982. Fatty acids in the heads of worker honeybees of various ages. J. Apic. Res. 21:122–125.

    CAS  Google Scholar 

  • Bray, J. R. and Curtis, J. T. 1957. An ordination of the upland forest communities of Southern Wisconsin. Ecol. Monogr. 27:325–349.

    Article  Google Scholar 

  • Butler, C. G. 1960. Queen substance production by virgin queen honey-bees (Apis mellifera L.). Proc. R. Entomol. Soc. Lond. 35A:170–171.

    Google Scholar 

  • Butler, C. G. and Paton, P. N. 1962. Inhibition of queen rearing by queen honey-bees (Apis mellifera L.) of different ages. Proc. R. Entomol. Soc. Lond. 37A:7–9.

    Google Scholar 

  • Butler, C. G., Callow, R. K., and Johnston, N. C. 1961. The isolation and synthesis of queen substance, 9-oxodec-trans-2-enoic acid, a honeybee pheromone. Proc. R. Soc. Lond. 155B:417–432.

    Google Scholar 

  • Callow, R. K., Chapman, J. R., and Paton, P. N. 1964. Pheromones of the honeybee: Chemical studies of the mandibular gland secretion of the queen. J. Apic. Res. 3:77–89.

    CAS  Google Scholar 

  • Clarke, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18:117–143.

    Article  Google Scholar 

  • Clarke, K. R. and Green, R. H. 1988. Statistical design and analysis for a ‘biological effects’ study. Mar. Ecol., Prog. Ser. 46:213–226.

    Article  Google Scholar 

  • Clarke, K. R. and Warwick, R. M. 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd edition. PRIMER-E, Plymouth.

  • Crewe, R. M. 1982. Compositional variability: The key to the social signals produced by honeybee mandibular glands, pp. 318–322, in M. D. Breed, C.D. Michener, and H. E. Evans (eds.). The Biology of Social Insects. Proc. 9th Congress of IUSSI, Boulder, CO.

  • Crewe, R. M. 1988. Natural history of honey-bee mandibular gland secretions: Development of analytical techniques and the emergence of complexity, pp. 149–158, in G. R. Needham, J. R. Page, M. Delfinado-Baker, and C. E. Bowman (eds.). Africanized Honeybees and Bee Mites. Ellis Horwood Ltd., Chichester.

    Google Scholar 

  • Crewe, R. M. and Moritz, R. F. A. 1989. Variation in the components of head extracts of workers and queens of Apis mellifera intermissa Buttel-Reepen. Z. Naturforsch. 44c:590–596.

    Google Scholar 

  • Crewe, R. M. and Velthuis, H. H. W. 1980. False queens: A consequence of mandibular gland signals in worker honeybees. Naturwissenschaften 67:467–470.

    Article  Google Scholar 

  • Crewe, R. M., Wossler, T., and Allsopp, M. H. 1990. Workers in queens clothing: why capensis workers become pseudoqueens, pp. 83–89, in R. H. Anderson and B. Buys (eds.). Bees and Beekeeping in Southern Africa. Proc. of the Int. Beekeepers' Symp., Stellenbosch, South Africa. University Press, Stellenbosch.

  • De Grandi-Hoffman, G. and Martin, J. H. 1993. Behaviour of egg-laying virgin and mated queen honey bees (Apis mellifera L.) and the composition of brood in their colonies. J. Apic. Res. 32:19–26.

    Google Scholar 

  • De Hazan, M., Lensky, Y., and Cassier, P. 1989a. Effects of queen honeybee (Apis mellifera L.) aging on her attractiveness to workers. Comp. Biochem. Physiol. 93A:777–783.

    Article  Google Scholar 

  • De Hazan, M., Hyams, J., Lensky, Y., and Cassier, P. 1989b. Ultrastructure and ontogeny of the mandibular glands of the queen honey bee, Apis mellifera L. (Hymenoptera: Apidae). Int. J. Insect Morphol. Embryol. 18:311–320.

    Article  Google Scholar 

  • Engels, W., Rosenkranz, P., Adler, A., Taghizadeh, T., Lübke, G., and Francke, W. 1997. Mandibular gland volatiles and their ontogenetic patterns in queen honey bees, Apis mellifera carnica. J. Insect Physiol. 43:307–313.

    Article  PubMed  CAS  Google Scholar 

  • Gary, N. E. 1961. Queen honey bee attractiveness as related to mandibular gland secretion. Science 133:1479–1480.

    Article  PubMed  CAS  Google Scholar 

  • Gehrke, C. W. and Leimer, K. 1971. Trimethylsilylation of amino acids. Derivatization and chromatography. J. Chromatogr. 57:219–238.

    Article  PubMed  CAS  Google Scholar 

  • Keeling, C. I., Slessor, K. N., Higo, H. A., and Winston, M. L. 2003. New components of the honey bee (Apis mellifera L.) queen retinue pheromone. Proc. Natl. Acad. Sci. USA 100:4486–4491.

    Article  PubMed  CAS  Google Scholar 

  • Kruskal, J. B. and Wish, M. 1978. Multidimensional Scaling. Sage Publications, Beverly Hills, CA.

    Google Scholar 

  • Lensky, Y., Cassier, P., Notkin, M., Delorme-Joulie, C., and Levinsohn, M. 1985. Pheromonal activity and fine structure of the mandibular glands of honeybee drones (Apis mellifera L.) (Insecta, Hymenoptera, Apidae). J. Insect Physiol. 31:265–276.

    Article  CAS  Google Scholar 

  • Lensky, Y., Cassier, P., Rosa, S., and Grandperrin, D. 1991. Induction of balling in worker honeybees (Apis mellifera L.) by “stress” pheromone from Koschewnikow glands of queen bees: behavioural, structural, and chemical study. Comp. Biochem. Physiol. 100A:585–594.

    Article  CAS  Google Scholar 

  • Pain, J. and Roger, B. 1976. Variation de la teneur en acide céto-9-décène-2-oïque en function de l'age chez les reines vierges d'abeille (Apis mellifica ligustica S.). C.R. Acad. Sci. Paris 283:797–799.

    CAS  Google Scholar 

  • Pain, J., Hügel, M. F., and Barbier, M. 1960. Sur les constituants du mélange attractif des glandes mandibulaires des reines d'Abeilles (Apis mellifica L.) à différents stades de leur vie. Comptes Rendus 251:1046–1048.

    CAS  Google Scholar 

  • Pain, J., Barbier, M., and Roger, B. 1967. Dosages individuels des acides céto-9-décène-2-oïque et hydroxy-10-décène-2-oïque dans les têtes des reines et des ouvrières d'abeilles. Ann. Abeille 10:45–52.

    Article  CAS  Google Scholar 

  • Pankiw, T., Winston, M. L., Slessor, K. N., Pettis, J. S., and Taylor, O. R. 1996. Mandibular gland components of European and Africanized honey bee queens (Apis mellifera L.). J. Chem. Ecol. 22:605–615.

    Article  CAS  Google Scholar 

  • Pettis, J. S., Westcott, L. V., and Winston, M. L. 1998. Balling behaviour in the honey bee in response to exogenous queen mandibular gland pheromone. J. Apic. Res. 37:125–131.

    CAS  Google Scholar 

  • Plettner, E., Sutherland, G. R. J., Slessor, K. N., and Winston, M. L. 1995. Why not be a queen? Regioselectivity in mandibular secretions of honeybee castes. J. Chem. Ecol. 21:1017–1029.

    Article  CAS  Google Scholar 

  • Plettner, E., Slessor, K. N., Winston, M. L., and Oliver, J. E. 1996. Caste-selective pheromone biosynthesis in honeybees. Science 271:1851–1853.

    Article  CAS  Google Scholar 

  • Plettner, E., Otis, G. W., Wimalaratne, P. D. C., Winston, M. L., Slessor, K. N., Pankiw, T., and Punchihewa, P. W. K. 1997. Species- and caste-determined mandibular gland signals in honeybees (Apis). J. Chem. Ecol. 23:363–377.

    Article  CAS  Google Scholar 

  • Plettner, E., Slessor, K. N., and Winston, M. L. 1998. Biosynthesis of mandibular acids in honey bees (Apis mellifera): De novo synthesis, route of fatty acid hydroxylation and caste selective β-oxidation. Insect Biochem. Mol. Biol. 28:31–42.

    Article  CAS  Google Scholar 

  • Rice, W. R. 1989. Analysing tables of statistical tests. Evolution 43:223–225.

    Article  Google Scholar 

  • Slessor, K. N., Kaminski, L. A., King, G. G. S., Borden, J. H., and Winston, M. L. 1988. Semiochemical basis of the retinue response to queen honey bees. Nature 332:354–356.

    Article  CAS  Google Scholar 

  • Slessor, K. N., Kaminski, L. A., King, G. G. S., and Winston, M. L. 1990. Semiochemicals of the honeybee queen mandibular glands. J. Chem. Ecol. 16:851–860.

    Article  CAS  Google Scholar 

  • Whiffler, L. A., Drusedau, M. U. H., Crewe, R. M., and Hepburn, H. R. 1988. Defensive behaviour and division of labour in the African honeybee (Apis mellifera scutellata). J. Comp. Physiol. 163:401–411.

    Article  Google Scholar 

  • Wossler, T. C. and Crewe, R. M. 1999. Mass spectral identification of the tergal gland secretions of female castes of two African honey bee races (Apis mellifera). J. Apic. Res. 38:137–148.

    CAS  Google Scholar 

  • Yadava, R. P. S. and Smith, M. V. 1971a. Aggressive behaviour of Apis mellifera L. workers towards introduced queens I. Behavioural mechanisms involved in the release of worker aggression. Behaviour 39:212–236.

    Article  PubMed  CAS  Google Scholar 

  • Yadava, R. P. S. and Smith, M. V. 1971b. Aggressive behavior of Apis mellifera L. workers towards introduced queens. II. Role of the mandibular gland contents of the queen in releasing aggressive behavior. Can. J. Zool. 49:1179–1183.

    Article  PubMed  CAS  Google Scholar 

  • Yadava, R. P. S. and Smith, M. V. 1971c. Aggressive behavior of Apis mellifera L. workers towards introduced queens. III. Relationship between the attractiveness of the queen and worker aggression. Can. J. Zool. 49:1359–1362.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the National Research Foundation for funding this project. Thanks are also due to Dr. Arnaud Grégoire for his statistical contribution.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Theresa C. Wossler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wossler, T.C., Jones, G.E., Allsopp, M.H. et al. Virgin Queen Mandibular Gland Signals of Apis mellifera capensis Change with Age and Affect Honeybee Worker Responses. J Chem Ecol 32, 1043–1056 (2006). https://doi.org/10.1007/s10886-006-9053-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-006-9053-8

Keywords

Navigation