Skip to main content
SpringerLink
Log in

Honeybee (Apis cerana) guards do not discriminate between robbers and reproductive parasites

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

A hopelessly queenless honeybee colony has only one reproductive option: some workers must produce sons before the colony dies. This requires the workers to curtail egg policing (removal of worker-produced eggs), rendering the colony vulnerable to non-natal reproductive parasitism. In the Western honeybee, Apis mellifera, guarding (prevention of foreign workers from entering a colony) increases in queenless colonies, providing a defence against non-natal parasitism. However, in the closely related Eastern honeybee A. cerana, queenless colonies appear to be more tolerant of bees from other colonies. We presented guards of four A. cerana colonies with three types of workers: nestmate returning foragers, non-nestmate returning foragers and non-nestmates from a laying-worker colony. The latter are likely to have active ovaries, allowing us to test whether guard bees can detect which potential invaders are more likely to be reproductive parasites. After assessing guards’ reactions, we recaptured test bees and dissected them to determine levels of ovary activation. We found that nestmates were accepted significantly more frequently than the other two types of workers. However, there was no difference in the overall acceptance rates of non-nestmate returning foragers and bees from within laying-worker colonies. In addition, ovary-activated workers were no less likely to be accepted than those with inactive ovaries. Interestingly, colonies were more accepting of all three types of test bee after being made queenless. We conclude that, as has been previously suggested, guarding has no specific role in the prevention of non-natal parasitism in A. cerana.

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

Similar content being viewed by others

References

  • Arias M.C. and Sheppard W.S. 2005. Phylogenetic relationships of honey bees (Hymenoptera: Apinae: Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol. Phyl. Evol. 37: 25-35

    Google Scholar 

  • Beekman M., Calis J.N.M., Oldroyd B.P. and Ratnieks F.L.W. 2002a. When do honey bee guards reject their former nestmates after swarming? Insect. Soc. 49: 56-61

  • Beekman M. and Oldroyd B.P. 2008. When workers disunite: intraspecific parasitism by eusocial bees. Annu. Rev. Entomol 53: 19-37

    Google Scholar 

  • Beekman M., Wossler T.C., Martin S.J. and Ratnieks F.L.W. 2002b. Parasitic Cape honey bee workers (Apis mellifera capensis) are not given differential treatment by African guards (A. m. scutellata). Insect. Soc. 49: 216-220

  • Birmingham A.L., Hoover S.E., Winston M.L. and Ydenberg R.C. 2004. Drifting bumble bee (Hymenoptera: Apidae) workers in commercial greenhouses may be social parasites. Can. J. Zool. 82: 1843-1853

    Google Scholar 

  • Bourke A.F.G. 1994. Worker matricide in social bees and wasps. J. Theor. Biol. 167: 283-292

    Google Scholar 

  • Buschinger A. 2009. Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol. News 12: 219-235

    Google Scholar 

  • Butler C.G. and Free J.B. 1952. The behaviour of worker honey bees at the hive entrance. Behaviour 4: 262-292

    Google Scholar 

  • Chapman N.C., Beekman M. and Oldroyd B.P. 2010. Worker reproductive parasitism and drift in the western honeybee Apis mellifera. Behav. Ecol. Sociobiol. 64: 419-427

    Google Scholar 

  • Chapman N.C., Makinson J., Beekman M. and Oldroyd B.P. 2009a. Honeybee, Apis mellifera, guards use adaptive acceptance thresholds to limit worker reproductive parasitism. Anim. Behav. 78: 1205-1211

  • Chapman N.C., Nanork P., Gloag R.S., Wattanachaiyingcharoen W., Beekman M. and Oldroyd B.P. 2009b. Queenless colonies of the Asian red dwarf honey bee (Apis florea) are infiltrated by workers from other queenless colonies. Behav. Ecol. 20: 817-820

  • Chapman N.C., Nanork P., Reddy M.S., Bhat N.S., Beekman M. and Oldroyd B.P. 2008. Nestmate recognition by guards of the Asian hive bee Apis cerana. Insect. Soc. 55: 382-386

    Google Scholar 

  • Clarke F.M. and Faulkes C.C. 2001. Intracolony aggression in the eusocial naked mole-rat, Heterocephalus glaber. Anim. Behav. 61: 311-324

    Google Scholar 

  • Dampney J.R., Barron A.B. and Oldroyd B.P. 2002. Policing of adult honey bees with activated ovaries is error prone. Insect. Soc. 49: 270-274

    Google Scholar 

  • Downs S.G. and Ratnieks F.L.W. 1999. Recognition of conspecifics by honeybee guards uses nonheritable cues acquired in the adult stage. Anim. Behav. 58: 643-648

    Google Scholar 

  • Downs S.G. and Ratnieks F.L.W. 2000. Adaptive shifts in honey bee (Apis mellifera L.) guarding behavior support predictions of the acceptance threshold model. Behav. Ecol. 11: 326-333

    Google Scholar 

  • Engel M.S. and Schultz T.R. 1997. Phylogeny and behavior in honey bees (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 90: 43-53

    Google Scholar 

  • Erler S. and Lattorff H.M.G. 2010. The degree of parasitism of the bumblebee (Bombus terrestris) by cuckoo bumblebees (Bombus (Psithyrus) vestalis). Insect. Soc. 57: 371-377

  • Faulkes C.G., Abbott D.H. and Jarvis J.U.M. 1990. Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats, Heterocephalus glaber. J. Reprod. Fert. 88: 559-568

    Google Scholar 

  • Fowler J., Cohen L. and Jarvis P. 1998. Practical Statistics for Field Biology. John Wiley and Sons, New York

  • Free J.B. 1977. The Social Organization of the Honey Bees. Edward Arnold, London

  • Hölldobler B. and Wilson E.O. 1978. The Ants. Harvard University Press, Cambridge

  • Holmes M.J., Oldroyd B.P., Allsopp M.H., Lim J., Wossler T.C. and Beekman M. 2010. Maternity of emergency queens in the Cape honey bee, Apis mellifera capensis. Mol. Ecol. 19: 2792-2799

    Google Scholar 

  • Jarvis J.U.M. 1981. Eusociality in a mammal - cooperative breeding in naked mole-rat colonies. Science 212: 571-573

    Google Scholar 

  • Jordan L.A., Allsopp M.H., Oldroyd B.P., Wossler T.C. and Beekman M. 2008. Cheating honeybee workers produce royal offspring. Proc. R. Soc. Lond. B. 275: 345-351

    Google Scholar 

  • Kupper G. and Schwammberger K.H. 1995. Parasitism in bumble bees (Hymenoptera, Apidae) - observations of Psithyrus sylvestris in Bombus pratorum nests. Apidologie 26: 245-254

  • Lo N., Gloag R.S., Anderson D.L. and Oldroyd B.P. 2010. A molecular phylogeny of the genus Apis suggests that the Giant Honey Bee of the Philippines, A. breviligula Maa, and the Plains Honey Bee of southern India, A. indica Fabricius, are valid species. Syst. Entomol. 35: 226-233

  • Lopez-Vaamonde C., Koning J.W., Brown R.M., Jordan W.C. and Bourke A.F.G. 2004. Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430: 557-560

    Google Scholar 

  • Miller D.G. and Ratnieks F.L.W. 2001. The timing of worker reproduction and breakdown of policing behaviour in queenless honey bee (Apis mellifera L.) societies. Insect. Soc. 48: 178-184

    Google Scholar 

  • Monnin T., Ratnieks F.L.W., Jones G.R. and Beard R. 2002. Pretender punishment induced by chemical signalling in a queenless ant. Nature 419: 61-65

    Google Scholar 

  • Nanork P., Chapman N.C., Wongsiri S., Lim J., Gloag R.S. and Oldroyd B.P. 2007. Social parasitism by workers in queenless and queenright Apis cerana colonies. Mol. Ecol. 16: 1107-1114

  • Nanork P., Paar J., Chapman N.C., Wongsiri S. and Oldroyd B.P. 2005. Asian honeybees parasitize the future dead. Nature 437: 829

    Google Scholar 

  • Oldroyd B.P., Halling L.A., Good G., Wattanachaiyingcharoen W., Barron A.B., Nanork P., Wongsiri S. and Ratnieks F.L.W. 2001. Worker policing and worker reproduction in Apis cerana. Behav. Ecol. Sociobiol. 50: 371-377

    Google Scholar 

  • Oldroyd B.P. and Wongsiri S. 2006. Asian Honey Bees: Biology, Conservation and Human Interactions. Harvard University Press, Cambridge

  • Ratnieks F.L.W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132: 217-236

    Google Scholar 

  • Ratnieks F.L.W. and Reeve H.K. 1992. Conflict in single-queen Hymenopteran societies - the structure of conflict and processes that reduce conflict in advanced eusocial species. J. Theor. Biol. 158: 33-65

    Google Scholar 

  • Ratnieks F.L.W. and Visscher P.K. 1989. Worker policing in the honeybee. Nature 342: 796-797

    Google Scholar 

  • Sakagami S.F. 1954. Occurrence of an aggressive behaviour in queenless hives, with considerations on the social organisation of honeybee. Insect. Soc. 1: 331-343

    Google Scholar 

  • Tan K., Yang M., Radloff S., Pirk C.W.W., Crewe R.M., Phiancharoen M., Hepburn R. and Oldroyd B.P. 2009. Worker reproduction in mixed-species colonies of honey bees. Behav. Ecol. 20: 1106-1110

    Google Scholar 

  • Visscher P.K. and Dukas R. 1995. Honey bees recognize development of nestmates’ ovaries. Anim. Behav. 49: 542-544

    Google Scholar 

  • Wenseleers T., Alves D.A., Francoy T.M., Billen J. and Imperatriz-Fonseca V.L. 2011. Intraspecific queen parasitism in a highly eusocial bee. Biol. Lett. 7: 173-176

    Google Scholar 

  • Wilson E.O. 1971. The Insect Societies. Harvard University Press, Cambridge

Download references

Acknowledgments

We thank Zhongwen Hu for his assistance in the field. This research was supported by an Endeavour Research Fellowship (MJH) and the Australian Research Council (MB and BPO).

Author information

Authors and Affiliations

  1. Behaviour and Genetics of Social Insects Laboratory, School of Biological Sciences, University of Sydney, Macleay Building A12, Sydney, NSW, 2006, Australia

    M. J. Holmes, B. P. Oldroyd & M. Beekman

  2. Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Science, Kunming, Yunnan Province, People’s Republic of China

    K. Tan

  3. Eastern Bee Research Institute of Yunnan Agricultural University, Heilongtan, Kunming, People’s Republic of China

    K. Tan & Z. Wang

Authors
  1. M. J. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Z. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B. P. Oldroyd
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Beekman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. J. Holmes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Holmes, M.J., Tan, K., Wang, Z. et al. Honeybee (Apis cerana) guards do not discriminate between robbers and reproductive parasites. Insect. Soc. 60, 265–271 (2013). https://doi.org/10.1007/s00040-013-0292-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-013-0292-8

Keywords

Search

Navigation