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The reproductive dilemmas of queenless red dwarf honeybee (Apis florea) workers

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Abstract

Honeybee (Apis) workers cannot mate, but retain functional ovaries. When colonies have lost their queen, many young workers begin to activate their ovaries and lay eggs. Some of these eggs are reared, but most are not and are presumably eaten by other workers (worker policing). Here we explore some of the factors affecting the reproductive success of queenless workers of the red dwarf honeybee Apis florea. Over a 2-year period we collected 40 wild colonies and removed their queens. Only two colonies remained at their translocated site long enough to rear males to pupation while all the others absconded. Absconding usually occurred after worker policing had ceased, as evidenced by the appearance of larvae. Dissections of workers from eight colonies showed that in A. florea, 6% of workers have activated ovaries after 4 days of queenlessness, and that 33% of workers have activated ovaries after 3 weeks. Worker-laid eggs may appear in nests within 4 days and larvae soon after, but this is highly variable. As with Apis mellifera, we found evidence of unequal reproductive success among queenless workers of A. florea. In the two colonies that reared males to pupation and which we studied with microsatellites, some subfamilies had much higher proportions of workers with activated ovaries than others. The significance of absconding and internest reproductive parasitism to the alternative reproductive strategies of queenless A. florea workers is discussed.

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References

  • Akratanakul P (1977) The natural history of the dwarf honey bee, Apis florea F. in Thailand. Ph.D. thesis, Cornell University, p 88

  • Bai ARK, Reddy CC (1975) Ovary development and egg laying in Apis cerana indica workers. J Apic Res 14:149–152

    Google Scholar 

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

    Article  Google Scholar 

  • Birmingham AL, Hoover SE, Winston ML, Ydenberg RC (2004) Drifting bumble bee (Hymenoptera: Apidae) workers in commercial greenhouses may be social parasites. Can J Zool 82:1843–1853

    Article  Google Scholar 

  • Blanford EJ (1923) Chinese bees as we find them. Bee World 5:104–106

    Google Scholar 

  • Châline N, Martin SJ, Ratnieks FLW (2004) Worker policing persists in a hopelessly queenless honey bee colony (Apis mellifera). Insectes Soc 51:113–116

    Article  Google Scholar 

  • Dawkins R, Carlisle TR (1976) Parental investment, mate desertion, and a fallacy. Nature 262:131–133

    Article  Google Scholar 

  • Duangphakdee O (2006) Biological active compounds used by worker bees to repel ants. Ph.D. thesis, Chulalongkorn University

  • Dzierzon J (1845) Gutachten über die von Herrn Direktor Stöhr im ersten und zweiten Kapitel des General-Gutachtens aufgestellten Fragen. Eichstädter Bienenzeitung 1:109–113, 119–121

    Google Scholar 

  • Estoup A, Solignac M, Cornuet J-M (1994) Precise assessment of the number of patrilines and of genetic relatedness in honey bee colonies. Proc R Soc Lond B 258:1–7

    CAS  Google Scholar 

  • Estoup A, Largiader CR, Perrot E, Chourrout D (1997) Rapid one tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol Mar Biol Biotechnol 5:205–208

    Google Scholar 

  • Free JB, Williams IH (1979) Communication by pheromones and other means in Apis florea colonies. J Apic Res 18:16–25

    Google Scholar 

  • Halling LA, Oldroyd BP (2003) Do policing honeybee workers target eggs in drone comb? Insectes Soc 50:59–61

    Article  Google Scholar 

  • Halling LA, Oldroyd BP, Wattanachaiyingcharoen W, Barron AB, Nanork P, Wongsiri S (2001) Worker policing in the bee Apis florea. Behav Ecol Sociobiol 49:509–513

    Article  Google Scholar 

  • Hepburn HR, Reece SL, Neumann P, Moritz RFA, Radloff SE (1999) Absconding in honeybees (Apis mellifera) in relation to queen status and mode of worker reproduction. Insectes Soc 46:323–326

    Article  Google Scholar 

  • Lewontin RC, Felsenstein J (1965) The robustness of homogeneity tests in 2 x N tables. Biometrics 21:19–33

    Article  Google Scholar 

  • Lin H, Winston ML, Haunerland NH, Slessor KN (1999) Influence of age and population size on ovarian development, and of trophallaxis on ovarian development and vitellogenin titres of queenless worker honey bee (Hymenoptera: Apidae). Can Entomol 131:695–706

    Article  Google Scholar 

  • Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557–560

    Article  PubMed  CAS  Google Scholar 

  • Martin CJ, Oldroyd BP, Beekman M (2004) Differential reproductive success among subfamilies in queenless honey bee colonies (Apis mellifera L.). Behav Ecol Sociobiol 56:42–49

    Article  Google Scholar 

  • Martin S, Châline N, Drijfhout F, Jones G (2005) Role of esters in egg removal behaviour in honeybee (Apis mellifera) colonies. Behav Ecol Sociobiol 59:24–29

    Article  Google Scholar 

  • Miller DG, Ratnieks FLW (2001) The timing of worker reproduction and breakdown of policing behaviour in queenless honey bee (Apis mellifera L.) societies. Insectes Soc 48:178–184

    Article  Google Scholar 

  • Moritz RFA, Southwick EE (1992) Bees as superorganisms. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Moritz RFA, Simon UE, Crewe RM (2000) Pheromonal contest between honeybee workers (Apis mellifera capensis). Naturwissenschaften 87:395–397

    Article  PubMed  CAS  Google Scholar 

  • Nanork P, Paar J, Chapman NC, Wongsiri S, Oldroyd BP (2005) Asian honey bees parasitize the future dead. Nature 437:829

    Article  PubMed  CAS  Google Scholar 

  • Neumann P, Hepburn HR, Radloff SE (2000) Modes of worker reproduction, reproductive dominance and brood cell construction in queenless honeybee (Apis mellifera L.) colonies. Apidologie 31:479–486

    Article  Google Scholar 

  • Neumann P, Pirk CWW, Hepburn R, Radloff SE (2001a) A scientific note on the natural merger of two honeybee colonies (Apis mellifera capensis). Apidologie 32:113–114

    Article  Google Scholar 

  • Neumann P, Radloff SE, Moritz RFA, Hepburn HR, Reece SL (2001b) Social parasitism by honeybee workers (Apis mellifera capensis Escholtz): host finding and resistance of hybrid host colonies. Behav Ecol 12:419–428

    Article  Google Scholar 

  • Oldroyd BP, Wongsiri S (2006) Asian honey bees. Biology, conservation and human interactions. Harvard University Press, Cambridge

    Google Scholar 

  • Oldroyd BP, Halling LA, Good G, Wattanachaiyingchareon W, Barron AB, Nanork P, Wongsiri S, Ratnieks FLW (2001) Worker policing and worker reproduction in Apis cerana. Behav Ecol Sociobiol 50:371–377

    Article  Google Scholar 

  • Page RE, Erickson EH (1988) Reproduction by worker honey bees (Apis mellifera). Behav Ecol Sociobiol 23:117–126

    Article  Google Scholar 

  • Palmer KA, Oldroyd BP (2001) Mating frequency in Apis florea revisited (Hymenoptera: Apidae). Insectes Soc 48:40–43

    Article  Google Scholar 

  • Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236

    Article  Google Scholar 

  • Ratnieks FLW (1993) Egg-laying, egg-removal, and ovary development by workers in queenright honey bee colonies. Behav Ecol Sociobiol 32:191–198

    Article  Google Scholar 

  • Ratnieks FLW, Visscher PK (1989) Worker policing in honeybees. Nature 342:796–797

    Article  Google Scholar 

  • Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608

    Article  PubMed  CAS  Google Scholar 

  • Robinson GE, Page RE, Fondrk MK (1990) Intracolonial behavioural variation in worker oviposition, oophagy and larval care in queenless honey bee colonies. Behav Ecol Sociobiol 26:315–323

    Article  Google Scholar 

  • Seeley TD (1985) Honeybee ecology. Princeton University Press, Princeton

    Google Scholar 

  • Seeley TD (1989) The honey bee colony as a superorganism. Am Sci 77:546–553

    Google Scholar 

  • Solignac M, Vautrin D, Loiseau A, Mougel F, Baudry E, Estoup A, Garnery L, Haberl M, Cornuet J-M (2003) Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Mol Ecol Notes 3:307–311

    Article  CAS  Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex (R)100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:507

    Google Scholar 

  • Wattanachaiyingcharoen W, Oldroyd BP, Good G, Halling LA, Ratnieks FLW, Wongsiri S (2001) Lack of worker reproduction in Apis dorsata. Insectes Soc 49:80–85

    Article  Google Scholar 

  • Wenseleers T, Hart AG, Ratnieks FLW (2004a) When resistance is useless: policing and the evolution of reproductive acquiescence in insect societies. Am Nat 164:E154–E167

    Article  Google Scholar 

  • Wenseleers T, Helanterä H, Hart A, Ratnieks FLW (2004b) Worker reproduction and policing in insect societies: an ESS analysis. J Evol Biol 17:1035–1047

    Article  PubMed  CAS  Google Scholar 

  • Woyke J (1976) Brood-rearing efficiency and absconding in Indian honeybees. J Apic Res 15:133–143

    Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall, Upper Saddle River

    Google Scholar 

Download references

Acknowledgements

This work was supported by the Thailand Research Fund through the Royal Golden Jubilee Ph.D. Project (No. PHD/0144/2544) and the Australian Research Council. We acknowledge the technical assistance of Julie Lim and Yon Nuanchan. We also thank the members of the Centre of Excellence in Entomology: Bee Biology, Biodiversity of Insects and Mites, Chulalongkorn University, Bangkok, Thailand and the Behavior and Genetics of Social Insects Lab, School of Biological Sciences, University of Sydney, and particularly Madeleine Beekman, who gave helpful comments on this manuscript.

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Correspondence to Benjamin P. Oldroyd.

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Communicated by R.F.A. Moritz

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Nanork, P., Wongsiri, S. & Oldroyd, B.P. The reproductive dilemmas of queenless red dwarf honeybee (Apis florea) workers. Behav Ecol Sociobiol 61, 91–97 (2006). https://doi.org/10.1007/s00265-006-0239-4

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