Skip to main content
SpringerLink
Log in

Retinue attraction and ovary activation: responses of wild type and anarchistic honey bees (Apis mellifera) to queen and brood pheromones

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

In most social insect colonies, workers do not attempt to lay eggs in the presence of a queen. However, in the honey bee (Apis mellifera), a rare phenotype occurs in which workers activate their ovaries and lay large numbers of male eggs despite the presence of a fecund queen. We examined the proximate mechanisms by which this ‘anarchistic’ behaviour is expressed. We tested the effects of brood and queen pheromones on retinue attraction and worker ovary activation using caged worker bees. We found no difference between the anarchistic and wild type queen pheromones in the retinue response elicited in either wild type or anarchistic workers. Further, we found that anarchistic queens produce a pheromone blend that is as effective at inhibiting ovary activation as the wild type queen pheromone. However, anarchistic workers are less inhibited by queen pheromones than their wild type counterparts, in a dose-dependent manner. These results show that the anarchistic phenomenon is not due to changes in the production of queen pheromones, but rather is due in part to a shift in the worker response to these queen-produced signals. In addition, we demonstrate the dose-dependent nature of the effect of queen pheromones on honey bee worker ovary activation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amdam GV, Norberg K, Fondrk MK, Page RE Jr (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behaviour in honey bees. PNAS 101:11350–11355

    Article  PubMed  CAS  Google Scholar 

  • Arnold G, LeConte Y, Trouiller J, Hervet H, Chappe B, Masson C (1994) Inhibition of worker honeybee ovaries development by a mixture of fatty acid esters from larvae. C R Acad des Sci Paris 317:511–515

    CAS  Google Scholar 

  • Barron AB, Oldroyd BP (2001) Social regulation of ovary activation in 'anarchistic' honey-bees (Apis mellifera). Behav Ecol Sociobiol 49:214–219

    Article  Google Scholar 

  • Barron AB, Oldroyd BP, Ratnieks FLW (2001) Worker reproduction in honey- bees and the anarchic syndrome. A review. Behav Ecol Sociobiol 50:199–208

    Article  Google Scholar 

  • Châline N, Ratnieks FLW, Bourke T (2002) Anarchy in the UK: Detailed genetic analysis of worker reproduction in a naturally-occuring British anarchistic honeybee, Apis mellifera, colony using DNA microsatellites. Mol Ecol 11:1795–1803

    Article  PubMed  Google Scholar 

  • Dampney JR, Barron AB, Oldroyd BP (2002) Policing of adult honey bees with activated ovaries is error prone. Insectes Sociaux 49:270–274

    Article  Google Scholar 

  • Dampney JR, Barron AB, Oldroyd BP (2004) Measuring the cost of worker reproduction in honey bees: work tempo in an ‘anarchic’ line. Apidologie 35:83–88

    Article  Google Scholar 

  • Hamilton WD (1972) Altruism and related phenomenon, mainly in social insects. Ann Rev Ecol Syst 3:193–232

    Article  Google Scholar 

  • Hoover SER, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480

    Article  PubMed  CAS  Google Scholar 

  • Hoover SER, Oldroyd BP, Wossler TC Winston ML (In press) Anarchistic queen honey bees have normal queen mandibular pheromones. Insectes Soc 52(1):6–10

  • Kaminski L-A, Slessor KN, Winston ML, Hay NW, Borden JH (1990) Honeybee response to queen mandibular pheromone in laboratory bioassays. J Chem Ecol 16:841–850

    Article  CAS  Google Scholar 

  • Keeling CI, Slessor KN, Higo HA, Winston ML (2003) New components of the honey bee (Apis mellifera L.) queen retinue pheromone. Proc Nat Acad Sci 100:4486–4491

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • LeConte Y, Arnold G, Trouiller J, Masson C (1990) Identification of a brood pheromone in honey bees. Naturwissenschaften 77:334–336

    Article  CAS  Google Scholar 

  • Mohammedi A, Paris A, Crauser D, LeConte Y (1998) Effect of aliphatic esters on ovary development of queenless bees (Apis mellifera L.). Naturwissenschaften 85:455–458

    Article  CAS  Google Scholar 

  • Montague CE, Oldroyd BP (1998) The evolution of worker sterility in honey bees: an investigation into a behavioral mutant causing a failure of worker policing. Evolution 52:1408–1415

    Article  Google Scholar 

  • Neumann P, Radloff SE, Pirk CWW, Hepburn R (2003) The behaviour of drifted Cape honeybee workers (Apis mellifera capensis): predisposition for social parasitism? Apidologie 34:585–590

    Article  Google Scholar 

  • Oldroyd BP, Smolenski AJ, Cornuet J-M, Crozier RH (1994) Anarchy in the beehive. Nature 371:749

    Article  CAS  Google Scholar 

  • Oldroyd BP, Halling L, Rinderer TE (1999) Development and behaviour of anarchistic honey bees. Proc R Soc Lond B 266:1875–1878

    Article  Google Scholar 

  • Oldroyd BP, Ratnieks FLW (2000) Anarchistic honey bee workers evade worker policing by laying eggs that have low removal rates. Behav Ecol Sociobiol 47:268–273

    Article  Google Scholar 

  • Oldroyd BP, Wossler T, Ratnieks FLW (2001) Regulation of ovary activation in worker bees: larval signal production and adult response thresholds differ between anarchistic and wild-type bees. Behav Ecol Sociobiol 50: 366–370

    Article  Google Scholar 

  • Pankiw T, Winston M, Slessor KN (1994) Variation in worker response to honey bee (Apis mellifera L.) queen mandibular pheromone (Hymenoptera: Apidae). J Insect Behav 7:1–15

    Article  Google Scholar 

  • Pankiw T, Winston ML, Slessor KN (1995) Queen attendance behaviour of worker honey bees (Apis mellifera L.) that are high and low responding to queen mandibular pheromone. Ins Soc 42:371–378

    Article  Google Scholar 

  • Pernal SF, Currie RW (2000) Pollen quality of fresh and 1-year-old single pollen diets for worker honey bees (Apis mellifera L.). Apidologie 31:387–409

    Article  Google Scholar 

  • Seeley TD (1985) Honey Bee Ecology. Princeton University Press, Princeton, NJ

    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 

  • Visscher PK (1989) A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247–254

    Article  Google Scholar 

  • Visscher PK, Dukas R (1995) Honey bees recognize development of nestmates’ ovaries. Anim Behav 49:542–544

    Article  Google Scholar 

  • Zar JH (1984) Biostatistical Analysis, 2nd edn. Prentice-Hall inc. Englewood Cliffs, New Jersey

    Google Scholar 

Download references

Acknowledgements

This research was supported by grants from the Australian Research Council to BPO, and the Canadian Natural Science and Engineering Research Council to MLW. Fellowship support was provided SERH from NSERC. We appreciate the technical assistance of C. Keeling, E. Plettner, M. Duncan, and J. Lim. B. Crespi, L. Dill, J. Woyke, and two anonymous reviewers gave us comments that greatly improved the manuscript. This study complies with the current laws of Canada and Australia.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, Canada

    Shelley E. R. Hoover & Mark L. Winston

  2. School of Biological Sciences A12, University of Sydney 2006, Sydney, New South Wales, Australia

    Benjamin P. Oldroyd

Authors
  1. Shelley E. R. Hoover
    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. Benjamin P. Oldroyd
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shelley E. R. Hoover.

Additional information

Communicated by R. Page

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hoover, S.E.R., Winston, M.L. & Oldroyd, B.P. Retinue attraction and ovary activation: responses of wild type and anarchistic honey bees (Apis mellifera) to queen and brood pheromones. Behav Ecol Sociobiol 59, 278–284 (2005). https://doi.org/10.1007/s00265-005-0039-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-005-0039-2

Keywords

Search

Navigation