Insectes Sociaux

, Volume 60, Issue 2, pp 265–271 | Cite as

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

  • M. J. HolmesEmail author
  • K. Tan
  • Z. Wang
  • B. P. Oldroyd
  • M. Beekman
Research Article


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.


Apis cerana Guards Non-natal parasitism Ovary activation 



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).


  1. 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: 25-35Google Scholar
  2. 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: 56-61Google Scholar
  3. Beekman M. and Oldroyd B.P. 2008. When workers disunite: intraspecific parasitism by eusocial bees. Annu. Rev. Entomol 53: 19-37Google Scholar
  4. 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: 216-220Google Scholar
  5. 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: 1843-1853Google Scholar
  6. Bourke A.F.G. 1994. Worker matricide in social bees and wasps. J. Theor. Biol. 167: 283-292Google Scholar
  7. Buschinger A. 2009. Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol. News 12: 219-235Google Scholar
  8. Butler C.G. and Free J.B. 1952. The behaviour of worker honey bees at the hive entrance. Behaviour 4: 262-292Google Scholar
  9. 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: 419-427Google Scholar
  10. 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: 1205-1211Google Scholar
  11. 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: 817-820Google Scholar
  12. 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: 382-386Google Scholar
  13. Clarke F.M. and Faulkes C.C. 2001. Intracolony aggression in the eusocial naked mole-rat, Heterocephalus glaber. Anim. Behav. 61: 311-324Google Scholar
  14. 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: 270-274Google Scholar
  15. 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: 643-648Google Scholar
  16. 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: 326-333Google Scholar
  17. Engel M.S. and Schultz T.R. 1997. Phylogeny and behavior in honey bees (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 90: 43-53Google Scholar
  18. 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: 371-377Google Scholar
  19. 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: 559-568Google Scholar
  20. Fowler J., Cohen L. and Jarvis P. 1998. Practical Statistics for Field Biology. John Wiley and Sons, New YorkGoogle Scholar
  21. Free J.B. 1977. The Social Organization of the Honey Bees. Edward Arnold, LondonGoogle Scholar
  22. Hölldobler B. and Wilson E.O. 1978. The Ants. Harvard University Press, CambridgeGoogle Scholar
  23. 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: 2792-2799Google Scholar
  24. Jarvis J.U.M. 1981. Eusociality in a mammal - cooperative breeding in naked mole-rat colonies. Science 212: 571-573Google Scholar
  25. 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: 345-351Google Scholar
  26. Kupper G. and Schwammberger K.H. 1995. Parasitism in bumble bees (Hymenoptera, Apidae) - observations of Psithyrus sylvestris in Bombus pratorum nests. Apidologie 26: 245-254Google Scholar
  27. 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: 226-233Google Scholar
  28. 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: 557-560Google Scholar
  29. 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: 178-184Google Scholar
  30. 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: 61-65Google Scholar
  31. 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: 1107-1114Google Scholar
  32. Nanork P., Paar J., Chapman N.C., Wongsiri S. and Oldroyd B.P. 2005. Asian honeybees parasitize the future dead. Nature 437: 829Google Scholar
  33. 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: 371-377Google Scholar
  34. Oldroyd B.P. and Wongsiri S. 2006. Asian Honey Bees: Biology, Conservation and Human Interactions. Harvard University Press, CambridgeGoogle Scholar
  35. Ratnieks F.L.W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132: 217-236Google Scholar
  36. 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: 33-65Google Scholar
  37. Ratnieks F.L.W. and Visscher P.K. 1989. Worker policing in the honeybee. Nature 342: 796-797Google Scholar
  38. Sakagami S.F. 1954. Occurrence of an aggressive behaviour in queenless hives, with considerations on the social organisation of honeybee. Insect. Soc. 1: 331-343Google Scholar
  39. 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: 1106-1110Google Scholar
  40. Visscher P.K. and Dukas R. 1995. Honey bees recognize development of nestmates’ ovaries. Anim. Behav. 49: 542-544Google Scholar
  41. 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: 173-176Google Scholar
  42. Wilson E.O. 1971. The Insect Societies. Harvard University Press, CambridgeGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2013

Authors and Affiliations

  • M. J. Holmes
    • 1
    Email author
  • K. Tan
    • 2
    • 3
  • Z. Wang
    • 3
  • B. P. Oldroyd
    • 1
  • M. Beekman
    • 1
  1. 1.Behaviour and Genetics of Social Insects Laboratory, School of Biological SciencesUniversity of SydneySydneyAustralia
  2. 2.Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical GardenChinese Academy of ScienceKunmingPeople’s Republic of China
  3. 3.Eastern Bee Research Institute of Yunnan Agricultural UniversityHeilongtanPeople’s Republic of China

Personalised recommendations