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

  • Piyamas Nanork
  • Siriwat Wongsiri
  • Benjamin P. Oldroyd
Original Article

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.

Keywords

Reproductive competition Apis florea Red dwarf honeybee Social parasitism 

References

  1. Akratanakul P (1977) The natural history of the dwarf honey bee, Apis florea F. in Thailand. Ph.D. thesis, Cornell University, p 88Google Scholar
  2. Bai ARK, Reddy CC (1975) Ovary development and egg laying in Apis cerana indica workers. J Apic Res 14:149–152Google Scholar
  3. Barron AB, Oldroyd BP, Ratnieks FLW (2001) Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review. Behav Ecol Sociobiol 50:199–208CrossRefGoogle Scholar
  4. 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 82:1843–1853CrossRefGoogle Scholar
  5. Blanford EJ (1923) Chinese bees as we find them. Bee World 5:104–106Google Scholar
  6. Châline N, Martin SJ, Ratnieks FLW (2004) Worker policing persists in a hopelessly queenless honey bee colony (Apis mellifera). Insectes Soc 51:113–116CrossRefGoogle Scholar
  7. Dawkins R, Carlisle TR (1976) Parental investment, mate desertion, and a fallacy. Nature 262:131–133CrossRefGoogle Scholar
  8. Duangphakdee O (2006) Biological active compounds used by worker bees to repel ants. Ph.D. thesis, Chulalongkorn UniversityGoogle Scholar
  9. 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, 119–121Google Scholar
  10. 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 258:1–7Google Scholar
  11. 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 5:205–208Google Scholar
  12. Free JB, Williams IH (1979) Communication by pheromones and other means in Apis florea colonies. J Apic Res 18:16–25Google Scholar
  13. Halling LA, Oldroyd BP (2003) Do policing honeybee workers target eggs in drone comb? Insectes Soc 50:59–61CrossRefGoogle Scholar
  14. Halling LA, Oldroyd BP, Wattanachaiyingcharoen W, Barron AB, Nanork P, Wongsiri S (2001) Worker policing in the bee Apis florea. Behav Ecol Sociobiol 49:509–513CrossRefGoogle Scholar
  15. 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 46:323–326CrossRefGoogle Scholar
  16. Lewontin RC, Felsenstein J (1965) The robustness of homogeneity tests in 2 x N tables. Biometrics 21:19–33CrossRefGoogle Scholar
  17. 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 131:695–706CrossRefGoogle Scholar
  18. Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557–560PubMedCrossRefGoogle Scholar
  19. Martin CJ, Oldroyd BP, Beekman M (2004) Differential reproductive success among subfamilies in queenless honey bee colonies (Apis mellifera L.). Behav Ecol Sociobiol 56:42–49CrossRefGoogle Scholar
  20. Martin S, Châline N, Drijfhout F, Jones G (2005) Role of esters in egg removal behaviour in honeybee (Apis mellifera) colonies. Behav Ecol Sociobiol 59:24–29CrossRefGoogle Scholar
  21. 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 48:178–184CrossRefGoogle Scholar
  22. Moritz RFA, Southwick EE (1992) Bees as superorganisms. Springer, Berlin Heidelberg New YorkGoogle Scholar
  23. Moritz RFA, Simon UE, Crewe RM (2000) Pheromonal contest between honeybee workers (Apis mellifera capensis). Naturwissenschaften 87:395–397PubMedCrossRefGoogle Scholar
  24. Nanork P, Paar J, Chapman NC, Wongsiri S, Oldroyd BP (2005) Asian honey bees parasitize the future dead. Nature 437:829PubMedCrossRefGoogle Scholar
  25. 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 31:479–486CrossRefGoogle Scholar
  26. Neumann P, Pirk CWW, Hepburn R, Radloff SE (2001a) A scientific note on the natural merger of two honeybee colonies (Apis mellifera capensis). Apidologie 32:113–114CrossRefGoogle Scholar
  27. 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 12:419–428CrossRefGoogle Scholar
  28. Oldroyd BP, Wongsiri S (2006) Asian honey bees. Biology, conservation and human interactions. Harvard University Press, CambridgeGoogle Scholar
  29. 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 50:371–377CrossRefGoogle Scholar
  30. Page RE, Erickson EH (1988) Reproduction by worker honey bees (Apis mellifera). Behav Ecol Sociobiol 23:117–126CrossRefGoogle Scholar
  31. Palmer KA, Oldroyd BP (2001) Mating frequency in Apis florea revisited (Hymenoptera: Apidae). Insectes Soc 48:40–43CrossRefGoogle Scholar
  32. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236CrossRefGoogle Scholar
  33. Ratnieks FLW (1993) Egg-laying, egg-removal, and ovary development by workers in queenright honey bee colonies. Behav Ecol Sociobiol 32:191–198CrossRefGoogle Scholar
  34. Ratnieks FLW, Visscher PK (1989) Worker policing in honeybees. Nature 342:796–797CrossRefGoogle Scholar
  35. Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608PubMedCrossRefGoogle Scholar
  36. 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 26:315–323CrossRefGoogle Scholar
  37. Seeley TD (1985) Honeybee ecology. Princeton University Press, PrincetonGoogle Scholar
  38. Seeley TD (1989) The honey bee colony as a superorganism. Am Sci 77:546–553Google Scholar
  39. 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 3:307–311CrossRefGoogle Scholar
  40. 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 10:507Google Scholar
  41. Wattanachaiyingcharoen W, Oldroyd BP, Good G, Halling LA, Ratnieks FLW, Wongsiri S (2001) Lack of worker reproduction in Apis dorsata. Insectes Soc 49:80–85CrossRefGoogle Scholar
  42. 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–E167CrossRefGoogle Scholar
  43. Wenseleers T, Helanterä H, Hart A, Ratnieks FLW (2004b) Worker reproduction and policing in insect societies: an ESS analysis. J Evol Biol 17:1035–1047PubMedCrossRefGoogle Scholar
  44. Woyke J (1976) Brood-rearing efficiency and absconding in Indian honeybees. J Apic Res 15:133–143Google Scholar
  45. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Piyamas Nanork
    • 1
    • 2
  • Siriwat Wongsiri
    • 1
    • 3
  • Benjamin P. Oldroyd
    • 4
  1. 1.Department of Biology, Faculty of ScienceChulalongkorn UniversityBangkokThailand
  2. 2.Department of Biology, Faculty of ScienceMahasarakham UniversityMahasarakhamThailand
  3. 3.Faculty of TechnologyMahasarakham UniversityMahasarakhamThailand
  4. 4.Behavior and Genetics of Social Insects Laboratory, School of Biological Sciences A12University of SydneySydneyAustralia

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