Journal of Chemical Ecology

, Volume 31, Issue 11, pp 2731–2745 | Cite as

Pheromone Communication in the Honeybee (Apis mellifera L.)

  • Keith N. Slessor
  • Mark L. Winston
  • Yves Le ConteEmail author


Recent studies have demonstrated a remarkable and unexpected complexity in social insect pheromone communication, particularly for honeybees (Apis mellifera L.). The intricate interactions characteristic of social insects demand a complex language, based on specialized chemical signals that provide a syntax that is deeper in complexity and richer in nuance than previously imagined. Here, we discuss this rapidly evolving field for honeybees, the only social insect for which any primer pheromones have been identified. Novel research has demonstrated the importance of complexity, synergy, context, and dose, mediated through spatial and temporal pheromone distribution, and has revealed an unprecedented wealth of identified semiochemicals and functions. These new results demand fresh terminology, and we propose adding “colony pheromone” and “passenger pheromone” to the current terms sociochemical, releaser, and primer pheromone to better encompass our growing understanding of chemical communication in social insects.

Key Words

Apis mellifera honeybee social insect chemical communication pheromone chemoecology 



We appreciate the continued financial support of Natural Science and Engineering Research Council of Canada (K.S., M.W.) and of I.N.R.A., S.P.E. Department and Beekeeper associations in France (Y.L.C.). We acknowledge the hard work and insights of our students, employees, and colleagues in our pursuit to better understand these animals. We thank C. Brillet, H.A. Higo, C.I. Keeling, M. Ono, T. Pankiw, E. Plettner, and anonymous reviewers for their critical readings of this manuscript.


  1. Arnold, G., Conte, Y., Trouiller, J., Hervet, H., Chappe, B., Masson, C. 1994Inhibition of worker honeybee ovaries development by a mixture of fatty acid esters from larvaeC. R. Acad. Sci., Ser. 3 Sci. vie317511515Google Scholar
  2. Avitabile, A. R., Morse, R. E., Boch, R. 1975Swarming honeybees guided by pheromonesAnn. Entomol. Soc. Am.6810791082Google Scholar
  3. Barbier, J., Lederer, E. 1960Structure chimique de la substance royale de la reine d'abeille (Apis mellifera L.)C. R. Acad. Sci., Ser. 3 Sci. vie25111311135Google Scholar
  4. Bell, W. J., Cardé, R. T. 1984Bell, W. J.Cardé, R. T. eds. Chemical Ecology of InsectsChapman and HallLondonGoogle Scholar
  5. Breed, M. D., Stiller, T. M., Blum, M. S., Page, R. E. 1992Honeybee nestmate recognition—effects of queen fecal pheromonesJ. Chem. Ecol.1816331640CrossRefGoogle Scholar
  6. Breed, M. D., Garry, M. F., Pearce, A. N., Hibbard, B. E., Bjostad, L. B., Page, R. E. 1995The role of wax comb in honey bee nestmate recognitionAnim. Behav.50489496CrossRefGoogle Scholar
  7. Breed, M. D., Leger, E. A., Pearce, A. N., Wang, Y. J. 1998Comb wax effects on the ontogeny of honey bee nestmate recognitionAnim. Behav.551320CrossRefPubMedGoogle Scholar
  8. Breed, M. D., Guzman-Novoa, E., Hunt, G. J. 2004Defensive behavior of honey bees: organization, genetics, and comparisons with other beesAnnu. Rev. Entomol.49271298CrossRefPubMedGoogle Scholar
  9. Brillet, C., Robinson, G. E., Bues, R., Conte, Y. 2002Racial differences in division of labor in colonies of the honey bee (Apis mellifera)Ethology108115126CrossRefGoogle Scholar
  10. Butler, C. G., Fairey, E. M. 1963The role of the queen in preventing oogenesis in worker honey beesJ. Apic. Res.21418Google Scholar
  11. Butler, C. G., Callow, R. K., Johnston, N. C. 1961The isolation and synthesis of queen substance, 9-oxodec-trans-2-enoic acid, a honeybee pheromoneProc. R. Soc. Lond., B Biol. Sci.155417432Google Scholar
  12. Groot, A. P., Voogd, A. 1954On the ovary development in queenless worker bees (Apis mellifera L.)Experientia10384385CrossRefPubMedGoogle Scholar
  13. Free, J. B. 1987Pheromones of Social BeesChapman and HallLondonGoogle Scholar
  14. Gary, N. E. 1962Chemical mating attractants in the queen honey beeScience136773774Google Scholar
  15. Grozinger, C. M., Sharabash, N. M., Whitfield, C. W., Robinson, G. E. 2003Pheromone-mediated gene expression in the honey bee brainProc. Natl. Acad. Sci. USA1001451914525CrossRefPubMedGoogle Scholar
  16. Higo, H. A., Winston, M. L., Slessor, K. N. 1992Mechanisms by which honey bee (Hymenoptera: Apidae) queen pheromone sprays enhance pollinationAnn. Entomol. Soc. Am.88366373Google Scholar
  17. Hoover, S. E. R., Keeling, C. I., Winston, M. L., Slessor, K. N. 2003The effect of queen pheromones on worker honey bee ovary developmentNaturwissenschaften90477480CrossRefPubMedGoogle Scholar
  18. Huang, Z. Y., Robinson, G. E. 1996Regulation of honey bee division of labor by colony age demographyBehav. Ecol. Sociobiol.39147158CrossRefGoogle Scholar
  19. Hunt, G. J., Wood, K. V., Guzman-Novoa, E., Lee, H. D., Rothwell, A. P., Bonham, C. C. 2003Discovery of 3-methyl-2-buten-1-yl acetate, a new alarm component in the sting apparatus of Africanized honeybeesJ. Chem. Ecol.29453463CrossRefPubMedGoogle Scholar
  20. Jay, S. C. 1968Factors influencing ovary development of worker honeybees under natural conditionsCan. J. Zool.46345347Google Scholar
  21. Jay, S. C. 1972Ovary development of worker honeybees when separated from worker brood by various methodsCan. J. Zool.50661664Google Scholar
  22. Kaatz, H. H., Hildebrandt, H., Engels, W. 1992Primer effect of queen pheromone on juvenile hormone biosynthesis in adult worker honey beesJ. Comp. Physiol., B162588592Google Scholar
  23. Katzav-Gozansky, T., Soroker, V., Hefetz, A., Cojocaru, M., Erdmann, D. H., Francke, W. 1997Plasticity of caste-specific Dufour's gland secretion in the honey bee (Apis mellifera L.)Naturwissenschaften84238241CrossRefGoogle Scholar
  24. Katzav-Gozansky, T., Soroker, V., Ionescu, A., Robinson, G. E., Hefetz, A. 2001aTask-related chemical analysis of labial gland volatile secretion in worker honeybees (Apis mellifera ligustica)J. Chem. Ecol.27919926CrossRefGoogle Scholar
  25. Katzav-Gozansky, T., Soroker, V., Ibarra, F., Francke, W., Hefetz, A. 2001bDufour's gland secretion of the queen honeybee (Apis mellifera): an egg discriminator pheromone or a queen signal?Behav. Ecol. Sociobiol.517686CrossRefGoogle Scholar
  26. Keeling, C. I., 2001. Isolation and identification of new components of the honey bee (Apis mellifera) queen retinue pheromone. PhD Dissertation, Simon Fraser University, Vancouver.Google Scholar
  27. Keeling, C. I., Slessor, K. N., Higo, H. A., Winston, M. L. 2003New components of the honey bee (Apis mellifera L.) queen retinue pheromoneProc. Natl. Acad. Sci. USA10044864491CrossRefPubMedGoogle Scholar
  28. Conte, Y., Arnold, G., Trouiller, J., Masson, C., Chappe, B., Ourisson, G. 1989Attraction of the parasitic mite Varroa to the drone larvae of honey bees by simple aliphatic estersScience245638639Google Scholar
  29. Conte, Y., Arnold, G., Trouiller, J., Masson, C., Chappe, B. 1990Identification of a brood pheromone in honeybeesNaturwissenschaften77334336CrossRefGoogle Scholar
  30. Conte, Y., Sreng, L., Trouiller, J. 1994The recognition of larvae by worker honeybeesNaturwissenschaften81462465CrossRefGoogle Scholar
  31. Conte, Y., Sreng, L., Sacher, N., Trouiller, J., Dusticier, G., Poitout, S. H. 1994/1995Chemical recognition of queen cells by honey bee workers Apis mellifera (Hymenoptera: Apidae)Chemoecology5/6612CrossRefGoogle Scholar
  32. Conte, Y., Sreng, L., Poitout, S. H. 1995Brood pheromone can modulate the feeding behavior of Apis mellifera workers (Hymenoptera: Apidae)J. Econ. Entomol.88798804Google Scholar
  33. Conte, Y., Mohammedi, A., Robinson, G. E. 2001Primer effects of a brood pheromone on honeybee behavioural developmentProc. R. Soc. Lond., B Biol. Sci.268163168Google Scholar
  34. Ledoux, M. N., Winston, M. L., Higo, H., Keeling, C. I., Slessor, K. N., Conte, Y. 2001Queen pheromonal factors influencing comb construction by simulated honey bee (Apis mellifera L.) swarmsInsectes Soc.481420Google Scholar
  35. Leoncini, I., 2002. Phéromones et régulation sociale chez l'abeille, Apis mellifera L.: Identification d'un inhibiteur du développement comportemental des ouvrières. PhD. Dissertation, Institut National Agronomique Paris-Grignon, Paris.Google Scholar
  36. Leoncini, I., Conte, Y., Costagliola, G., Plettner, E., Toth, A. L., Wang, M., Huang, Z., Bécard, J., Crauser, D., Slessor, K. N., Robinson, G. E. 2004Regulation of behavioral maturation by a primer pheromone produced by adult worker honey beesProc. Natl. Acad. Sci. USA1011755917564CrossRefPubMedGoogle Scholar
  37. Lindauer, M. 1953Division of labour in the honeybee colonyBee World346373Google Scholar
  38. Martin, S. J., Jones, G. R. 2004Conservation of biosynthetic pheromone pathways in honeybees ApisNaturwissenschaften91232236CrossRefPubMedGoogle Scholar
  39. Mohammedi, A., Crauser, D., Paris, A., Conte, Y. 1996Effect of a brood pheromone on honeybee hypopharyngeal glandsC. R. Acad. Sci. Paris, Sci. Vie/Life Sci.319769772Google Scholar
  40. Mohammedi, A., Paris, A., Crauser, D., Conte, Y. 1998Effect of aliphatic esters on ovary development of queenless bees (Apis mellifera L.)Naturwissenschaften85455458CrossRefGoogle Scholar
  41. Naumann, K., Winston, M. L., Slessor, K. N., Prestwich, G. D., Webster, F. X. 1991Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromoneBehav. Ecol. Sociobiol.29321332CrossRefGoogle Scholar
  42. Naumann, K., Winston, M. L., Slessor, K. N. 1993Movement of honey bee (Apis mellifera L.) queen mandibular gland pheromone in populous and unpopulous coloniesJ. Insect Behav.6211223CrossRefGoogle Scholar
  43. Pain, J. 1961Sur la phéromone des reines d'abeilles et ses effets physiologiquesAnn. Abeille473152Google Scholar
  44. Pankiw, T. 2004Cued in: honey bee pheromones as information flow and collective decision-makingApidologie35217226CrossRefGoogle Scholar
  45. Pankiw, T., Page, R. E. 2001Brood pheromone modulates honeybee (Apis mellifera L.) sucrose response thresholdsBehav. Ecol. Sociobiol.49206213CrossRefGoogle Scholar
  46. Pankiw, T., Huang, Z. Y., Winston, M. L., Robinson, G. E. 1998Queen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) foraging ontogeny and juvenile hormone titersJ. Insect Physiol.44685692CrossRefPubMedGoogle Scholar
  47. Pankiw, T., Winston, M. L., Fondrk, M. K., Slessor, K. N. 2000Selection on worker honeybee responses to queen pheromone (Apis mellifera L.)Naturwissenschaften87487490CrossRefPubMedGoogle Scholar
  48. Pankiw, T., Roman, R., Sagili, R., Zhu-Salzman, K. 2004Pheromone-modulated behavioral suites influence colony growth in the honey bee (Apis mellifera)Naturwissenschaften91575578CrossRefPubMedGoogle Scholar
  49. Pickett, J. A., Williams, I. H., Smith, M. C., Martin, A. P. 1980Nasonov pheromone of honey bee, Apis mellifica L. (Hymenoptera Apidae). Part I. Chemical characterizationJ. Chem. Ecol.6425434CrossRefGoogle Scholar
  50. Plettner, E., Slessor, K. N., Winston, M. L., Oliver, J. E. 1996Caste-selective pheromone biosynthesis in honeybeesScience27118511853Google Scholar
  51. Ratnieks, F. L. W. 1995Evidence for a queen-produced egg-marking pheromone and its use in worker policing in the honey beeJ. Apic. Res.343137Google Scholar
  52. Ratnieks, F. L. W., Visscher, P. K. 1989Workers policing in the honeybeeNature342796797CrossRefGoogle Scholar
  53. Robinson, G. E. 1992Regulation of division of labor in insect societiesAnnu. Rev. Entomol.37637665CrossRefPubMedGoogle Scholar
  54. Robinson, G. E., Page, R. E.,Jr., Strambi, C., Strambi, A. 1989Hormonal and genetic control of behavioral integration in honey bee coloniesScience246109112Google Scholar
  55. Seeley, T. D. 1979Queen substance dispersal by messenger workers in honeybee coloniesBehav. Ecol. Sociobiol.5391415CrossRefGoogle Scholar
  56. Slessor, K. N. 2003Sociochemicals: more complicated than expectedKikuchi, T.Azuma, N.Higashi, S. eds. Genes, Behaviors and Evolution of Social InsectsHokkaido University PressSapporo5577Google Scholar
  57. Slessor, K. N., Kaminski, L. A., King, G. G. S., Borden, J. H., Winston, M. L. 1988Semiochemical basis of the retinue response to queen honey beesNature332354356CrossRefGoogle Scholar
  58. Frisch, K. 1967The Dance Language and Orientation of BeesThe Belnap Press of Harvard University PressCambridge, MA578Google Scholar
  59. Whitfield, C. W., Band, M. R., Bonaldo, M. F., Kumar, C. G., Liu, L., Pardinas, J. R., Robertson, H. M., Soares, M. B., Robinson, G. E. 2002Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey beeGenome Res.12555566CrossRefPubMedGoogle Scholar
  60. Wilson, E. O., Bossert, W. H. 1963Chemical communication among animalsRecent Prog. Horm. Res.19673716PubMedGoogle Scholar
  61. Winston, M. L. 1987The Biology of the Honey BeeHarvard Univ. PressCambridge, MAGoogle Scholar
  62. Winston, M. L., Higo, H. A., Colley, S. J., Pankiw, T., Slessor, K. N. 1991The role of queen mandibular pheromone and colony congestion in honey bee (Apis mellifera L.) reproductive swarming (Hymenoptera: Apidae)J. Insect Behav.4649660CrossRefGoogle Scholar
  63. Wossler, T. C., Crewe, R. M. 1999aMass spectral identification of the tergal gland secretions of female castes of two African honey bee races (Apis mellifera)J. Apic. Res.38137148Google Scholar
  64. Wossler, T. C., Crewe, R. M. 1999bThe releaser effects of the tergal gland secretion of queen honeybees (Apis mellifera)J. Insect Behav.12343351CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Keith N. Slessor
    • 1
  • Mark L. Winston
    • 2
  • Yves Le Conte
    • 3
    Email author
  1. 1.Department of ChemistrySimon Fraser UniversityBurnabyCanada
  2. 2.Department of Biological SciencesSimon Fraser UniversityBurnabyCanada
  3. 3.Laboratoire de Biologie de l'AbeilleInstitut National de la Recherche Agronomique, UMR 406 INRA/UAPVAvignon Cedex 9France

Personalised recommendations