Skip to main content

Pheromone Communication in the Honeybee (Apis mellifera L.)

Journal of Chemical Ecology volume 31, pages 2731–2745 (2005)Cite this article

Abstract

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.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

References

  • G. Arnold Y. Conte ParticleLe J. Trouiller H. Hervet B. Chappe C. Masson (1994) ArticleTitleInhibition of worker honeybee ovaries development by a mixture of fatty acid esters from larvae C. R. Acad. Sci., Ser. 3 Sci. vie 317 511–515

    Google Scholar 

  • A. R. Avitabile R. E. Morse R. Boch (1975) ArticleTitleSwarming honeybees guided by pheromones Ann. Entomol. Soc. Am. 68 1079–1082

    Google Scholar 

  • J. Barbier E. Lederer (1960) ArticleTitleStructure chimique de la substance royale de la reine d'abeille (Apis mellifera L.) C. R. Acad. Sci., Ser. 3 Sci. vie 251 1131–1135

    Google Scholar 

  • W. J. Bell R. T. Cardé (1984) NoChapterTitle W. J. Bell R. T. Cardé (Eds) Chemical Ecology of Insects Chapman and Hall London

    Google Scholar 

  • M. D. Breed T. M. Stiller M. S. Blum R. E. Page (1992) ArticleTitleHoneybee nestmate recognition—effects of queen fecal pheromones J. Chem. Ecol. 18 IssueID9 1633–1640 Occurrence Handle10.1007/BF00993235

    Article  Google Scholar 

  • M. D. Breed M. F. Garry A. N. Pearce B. E. Hibbard L. B. Bjostad R. E. Page (1995) ArticleTitleThe role of wax comb in honey bee nestmate recognition Anim. Behav. 50 489–496 Occurrence Handle10.1006/anbe.1995.0263

    Article  Google Scholar 

  • M. D. Breed E. A. Leger A. N. Pearce Y. J. Wang (1998) ArticleTitleComb wax effects on the ontogeny of honey bee nestmate recognition Anim. Behav. 55 13–20 Occurrence Handle10.1006/anbe.1997.0581 Occurrence Handle9480667

    Article  PubMed  Google Scholar 

  • M. D. Breed E. Guzman-Novoa G. J. Hunt (2004) ArticleTitleDefensive behavior of honey bees: organization, genetics, and comparisons with other bees Annu. Rev. Entomol. 49 271–298 Occurrence Handle10.1146/annurev.ento.49.061802.123155 Occurrence Handle14651465

    Article  PubMed  Google Scholar 

  • C. Brillet G. E. Robinson R. Bues Y. Conte ParticleLe (2002) ArticleTitleRacial differences in division of labor in colonies of the honey bee (Apis mellifera) Ethology 108 115–126 Occurrence Handle10.1046/j.1439-0310.2002.00760.x

    Article  Google Scholar 

  • C. G. Butler E. M. Fairey (1963) ArticleTitleThe role of the queen in preventing oogenesis in worker honey bees J. Apic. Res. 2 IssueID1 14–18

    Google Scholar 

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

    Google Scholar 

  • A. P. Groot Particlede A. Voogd (1954) ArticleTitleOn the ovary development in queenless worker bees (Apis mellifera L.) Experientia 10 384–385 Occurrence Handle10.1007/BF02160554 Occurrence Handle13210347

    Article  PubMed  Google Scholar 

  • J. B. Free (1987) Pheromones of Social Bees Chapman and Hall London

    Google Scholar 

  • N. E. Gary (1962) ArticleTitleChemical mating attractants in the queen honey bee Science 136 773–774

    Google Scholar 

  • C. M. Grozinger N. M. Sharabash C. W. Whitfield G. E. Robinson (2003) ArticleTitlePheromone-mediated gene expression in the honey bee brain Proc. Natl. Acad. Sci. USA 100 14519–14525 Occurrence Handle10.1073/pnas.2335884100 Occurrence Handle14573707

    Article  PubMed  Google Scholar 

  • H. A. Higo M. L. Winston K. N. Slessor (1992) ArticleTitleMechanisms by which honey bee (Hymenoptera: Apidae) queen pheromone sprays enhance pollination Ann. Entomol. Soc. Am. 88 366–373

    Google Scholar 

  • S. E. R. Hoover C. I. Keeling M. L. Winston K. N. Slessor (2003) ArticleTitleThe effect of queen pheromones on worker honey bee ovary development Naturwissenschaften 90 477–480 Occurrence Handle10.1007/s00114-003-0462-z Occurrence Handle14564409

    Article  PubMed  Google Scholar 

  • Z. Y. Huang G. E. Robinson (1996) ArticleTitleRegulation of honey bee division of labor by colony age demography Behav. Ecol. Sociobiol. 39 147–158 Occurrence Handle10.1007/s002650050276

    Article  Google Scholar 

  • G. J. Hunt K. V. Wood E. Guzman-Novoa H. D. Lee A. P. Rothwell C. C. Bonham (2003) ArticleTitleDiscovery of 3-methyl-2-buten-1-yl acetate, a new alarm component in the sting apparatus of Africanized honeybees J. Chem. Ecol. 29 453–463 Occurrence Handle10.1023/A:1022694330868 Occurrence Handle12737269

    Article  PubMed  Google Scholar 

  • S. C. Jay (1968) ArticleTitleFactors influencing ovary development of worker honeybees under natural conditions Can. J. Zool. 46 345–347

    Google Scholar 

  • S. C. Jay (1972) ArticleTitleOvary development of worker honeybees when separated from worker brood by various methods Can. J. Zool. 50 661–664

    Google Scholar 

  • H. H. Kaatz H. Hildebrandt W. Engels (1992) ArticleTitlePrimer effect of queen pheromone on juvenile hormone biosynthesis in adult worker honey bees J. Comp. Physiol., B 162 588–592

    Google Scholar 

  • T. Katzav-Gozansky V. Soroker A. Hefetz M. Cojocaru D. H. Erdmann W. Francke (1997) ArticleTitlePlasticity of caste-specific Dufour's gland secretion in the honey bee (Apis mellifera L.) Naturwissenschaften 84 238–241 Occurrence Handle10.1007/s001140050386

    Article  Google Scholar 

  • T. Katzav-Gozansky V. Soroker A. Ionescu G. E. Robinson A. Hefetz (2001a) ArticleTitleTask-related chemical analysis of labial gland volatile secretion in worker honeybees (Apis mellifera ligustica) J. Chem. Ecol. 27 919–926 Occurrence Handle10.1023/A:1010330902388

    Article  Google Scholar 

  • T. Katzav-Gozansky V. Soroker F. Ibarra W. Francke A. Hefetz (2001b) ArticleTitleDufour's gland secretion of the queen honeybee (Apis mellifera): an egg discriminator pheromone or a queen signal? Behav. Ecol. Sociobiol. 51 76–86 Occurrence Handle10.1007/s002650100406

    Article  Google Scholar 

  • 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.

  • C. I. Keeling K. N. Slessor H. A. Higo M. L. Winston (2003) ArticleTitleNew components of the honey bee (Apis mellifera L.) queen retinue pheromone Proc. Natl. Acad. Sci. USA 100 4486–4491 Occurrence Handle10.1073/pnas.0836984100 Occurrence Handle12676987

    Article  PubMed  Google Scholar 

  • Y. Conte ParticleLe G. Arnold J. Trouiller C. Masson B. Chappe G. Ourisson (1989) ArticleTitleAttraction of the parasitic mite Varroa to the drone larvae of honey bees by simple aliphatic esters Science 245 638–639

    Google Scholar 

  • Y. Conte ParticleLe G. Arnold J. Trouiller C. Masson B. Chappe (1990) ArticleTitleIdentification of a brood pheromone in honeybees Naturwissenschaften 77 334–336 Occurrence Handle10.1007/BF01138390

    Article  Google Scholar 

  • Y. Conte ParticleLe L. Sreng J. Trouiller (1994) ArticleTitleThe recognition of larvae by worker honeybees Naturwissenschaften 81 462–465 Occurrence Handle10.1007/BF01136651

    Article  Google Scholar 

  • Y. Conte ParticleLe L. Sreng N. Sacher J. Trouiller G. Dusticier S. H. Poitout (1994/1995) ArticleTitleChemical recognition of queen cells by honey bee workers Apis mellifera (Hymenoptera: Apidae) Chemoecology 5/6 6–12 Occurrence Handle10.1007/BF01259967

    Article  Google Scholar 

  • Y. Conte ParticleLe L. Sreng S. H. Poitout (1995) ArticleTitleBrood pheromone can modulate the feeding behavior of Apis mellifera workers (Hymenoptera: Apidae) J. Econ. Entomol. 88 798–804

    Google Scholar 

  • Y. Conte ParticleLe A. Mohammedi G. E. Robinson (2001) ArticleTitlePrimer effects of a brood pheromone on honeybee behavioural development Proc. R. Soc. Lond., B Biol. Sci. 268 163–168

    Google Scholar 

  • M. N. Ledoux M. L. Winston H. Higo C. I. Keeling K. N. Slessor Y. Conte ParticleLe (2001) ArticleTitleQueen pheromonal factors influencing comb construction by simulated honey bee (Apis mellifera L.) swarms Insectes Soc. 48 14–20

    Google Scholar 

  • 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.

  • I. Leoncini Y. Conte ParticleLe G. Costagliola E. Plettner A. L. Toth M. Wang Z. Huang J. Bécard D. Crauser K. N. Slessor G. E. Robinson (2004) ArticleTitleRegulation of behavioral maturation by a primer pheromone produced by adult worker honey bees Proc. Natl. Acad. Sci. USA 101 17559–17564 Occurrence Handle10.1073/pnas.0407652101 Occurrence Handle15572455

    Article  PubMed  Google Scholar 

  • M. Lindauer (1953) ArticleTitleDivision of labour in the honeybee colony Bee World 34 63–73

    Google Scholar 

  • S. J. Martin G. R. Jones (2004) ArticleTitleConservation of biosynthetic pheromone pathways in honeybees Apis Naturwissenschaften 91 232–236 Occurrence Handle10.1007/s00114-004-0517-9 Occurrence Handle15146271

    Article  PubMed  Google Scholar 

  • A. Mohammedi D. Crauser A. Paris Y. Conte ParticleLe (1996) ArticleTitleEffect of a brood pheromone on honeybee hypopharyngeal glands C. R. Acad. Sci. Paris, Sci. Vie/Life Sci. 319 769–772

    Google Scholar 

  • A. Mohammedi A. Paris D. Crauser Y. Conte ParticleLe (1998) ArticleTitleEffect of aliphatic esters on ovary development of queenless bees (Apis mellifera L.) Naturwissenschaften 85 455–458 Occurrence Handle10.1007/s001140050531

    Article  Google Scholar 

  • K. Naumann M. L. Winston K. N. Slessor G. D. Prestwich F. X. Webster (1991) ArticleTitleProduction and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone Behav. Ecol. Sociobiol. 29 321–332 Occurrence Handle10.1007/BF00165956

    Article  Google Scholar 

  • K. Naumann M. L. Winston K. N. Slessor (1993) ArticleTitleMovement of honey bee (Apis mellifera L.) queen mandibular gland pheromone in populous and unpopulous colonies J. Insect Behav. 6 211–223 Occurrence Handle10.1007/BF01051505

    Article  Google Scholar 

  • J. Pain (1961) ArticleTitleSur la phéromone des reines d'abeilles et ses effets physiologiques Ann. Abeille 4 73–152

    Google Scholar 

  • T. Pankiw (2004) ArticleTitleCued in: honey bee pheromones as information flow and collective decision-making Apidologie 35 217–226 Occurrence Handle10.1051/apido:2004009

    Article  Google Scholar 

  • T. Pankiw R. E. Page (2001) ArticleTitleBrood pheromone modulates honeybee (Apis mellifera L.) sucrose response thresholds Behav. Ecol. Sociobiol. 49 206–213 Occurrence Handle10.1007/s002650000282

    Article  Google Scholar 

  • T. Pankiw Z. Y. Huang M. L. Winston G. E. Robinson (1998) ArticleTitleQueen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) foraging ontogeny and juvenile hormone titers J. Insect Physiol. 44 685–692 Occurrence Handle10.1016/S0022-1910(98)00040-7 Occurrence Handle12769952

    Article  PubMed  Google Scholar 

  • T. Pankiw M. L. Winston M. K. Fondrk K. N. Slessor (2000) ArticleTitleSelection on worker honeybee responses to queen pheromone (Apis mellifera L.) Naturwissenschaften 87 487–490 Occurrence Handle10.1007/s001140050764 Occurrence Handle11151667

    Article  PubMed  Google Scholar 

  • T. Pankiw R. Roman R. Sagili K. Zhu-Salzman (2004) ArticleTitlePheromone-modulated behavioral suites influence colony growth in the honey bee (Apis mellifera) Naturwissenschaften 91 575–578 Occurrence Handle10.1007/s00114-004-0568-y Occurrence Handle15452700

    Article  PubMed  Google Scholar 

  • J. A. Pickett I. H. Williams M. C. Smith A. P. Martin (1980) ArticleTitleNasonov pheromone of honey bee, Apis mellifica L. (Hymenoptera Apidae). Part I. Chemical characterization J. Chem. Ecol. 6 425–434 Occurrence Handle10.1007/BF01402919

    Article  Google Scholar 

  • E. Plettner K. N. Slessor M. L. Winston J. E. Oliver (1996) ArticleTitleCaste-selective pheromone biosynthesis in honeybees Science 271 1851–1853

    Google Scholar 

  • F. L. W. Ratnieks (1995) ArticleTitleEvidence for a queen-produced egg-marking pheromone and its use in worker policing in the honey bee J. Apic. Res. 34 31–37

    Google Scholar 

  • F. L. W. Ratnieks P. K. Visscher (1989) ArticleTitleWorkers policing in the honeybee Nature 342 796–797 Occurrence Handle10.1038/342796a0

    Article  Google Scholar 

  • G. E. Robinson (1992) ArticleTitleRegulation of division of labor in insect societies Annu. Rev. Entomol. 37 637–665 Occurrence Handle10.1146/annurev.en.37.010192.003225 Occurrence Handle1539941

    Article  PubMed  Google Scholar 

  • G. E. Robinson R. E. Page SuffixJr. C. Strambi A. Strambi (1989) ArticleTitleHormonal and genetic control of behavioral integration in honey bee colonies Science 246 109–112

    Google Scholar 

  • T. D. Seeley (1979) ArticleTitleQueen substance dispersal by messenger workers in honeybee colonies Behav. Ecol. Sociobiol. 5 391–415 Occurrence Handle10.1007/BF00292527

    Article  Google Scholar 

  • K. N. Slessor (2003) Sociochemicals: more complicated than expected T. Kikuchi N. Azuma S. Higashi (Eds) Genes, Behaviors and Evolution of Social Insects Hokkaido University Press Sapporo 55–77

    Google Scholar 

  • K. N. Slessor L. A. Kaminski G. G. S. King J. H. Borden M. L. Winston (1988) ArticleTitleSemiochemical basis of the retinue response to queen honey bees Nature 332 354–356 Occurrence Handle10.1038/332354a0

    Article  Google Scholar 

  • K. Frisch Particlevon (1967) The Dance Language and Orientation of Bees The Belnap Press of Harvard University Press Cambridge, MA 578

    Google Scholar 

  • C. W. Whitfield M. R. Band M. F. Bonaldo C. G. Kumar L. Liu J. R. Pardinas H. M. Robertson M. B. Soares G. E. Robinson (2002) ArticleTitleAnnotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee Genome Res. 12 555–566 Occurrence Handle10.1101/gr.5302 Occurrence Handle11932240

    Article  PubMed  Google Scholar 

  • E. O. Wilson W. H. Bossert (1963) ArticleTitleChemical communication among animals Recent Prog. Horm. Res. 19 673–716 Occurrence Handle14284035

    PubMed  Google Scholar 

  • M. L. Winston (1987) The Biology of the Honey Bee Harvard Univ. Press Cambridge, MA

    Google Scholar 

  • M. L. Winston H. A. Higo S. J. Colley T. Pankiw K. N. Slessor (1991) ArticleTitleThe role of queen mandibular pheromone and colony congestion in honey bee (Apis mellifera L.) reproductive swarming (Hymenoptera: Apidae) J. Insect Behav. 4 649–660 Occurrence Handle10.1007/BF01048076

    Article  Google Scholar 

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

    Google Scholar 

  • T. C. Wossler R. M. Crewe (1999b) ArticleTitleThe releaser effects of the tergal gland secretion of queen honeybees (Apis mellifera) J. Insect Behav. 12 343–351 Occurrence Handle10.1023/A:1020839505622

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Department of Chemistry, Simon Fraser University, Burnaby, BC, Canada, V5A 1S6

    Keith N. Slessor

  2. Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada, V5A 1S6

    Mark L. Winston

  3. Laboratoire de Biologie de l'Abeille, Institut National de la Recherche Agronomique, UMR 406 INRA/UAPV, Site Agroparc, Domaine Saint-Paul, 84914, Avignon Cedex 9, France

    Yves Le Conte

Authors
  1. Keith N. Slessor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mark L. Winston
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yves Le Conte
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yves Le Conte.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Slessor, K.N., Winston, M.L. & Le Conte, Y. Pheromone Communication in the Honeybee (Apis mellifera L.). J Chem Ecol 31, 2731–2745 (2005). https://doi.org/10.1007/s10886-005-7623-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-005-7623-9

Key Words

  • Apis mellifera
  • honeybee
  • social insect
  • chemical communication
  • pheromone
  • chemoecology