Behavioral Ecology and Sociobiology

, Volume 64, Issue 7, pp 1165–1170 | Cite as

Lack of interspecific parasitism between the dwarf honeybees Apis andreniformis and Apis florea

  • Sitthipong Wongvilas
  • Jessica S. Higgs
  • Madeleine Beekman
  • Wandee Wattanachaiyingcharoen
  • Sureerat Deowanish
  • Benjamin P. Oldroyd
Original Paper


The dwarf honeybees Apis florea and Apis andreniformis are sympatric in Southeast Asia. We examined undisturbed nests of both species finding that heterospecific workers are present in some nests at low frequency. This suggested that workers may enter heterospecific nests as a prelude to reproductive parasitism. To test this hypothesis, we created mixed-species colonies and determined the reproductive response of workers within them based on molecular markers. In queenless colonies, workers of both species activated their ovaries at equal frequency. However, the majority species, A. florea, had complete reproductive dominance over A. andreniformis, most likely because the A. florea workers recognised and removed heterospecific larvae. In queenright mixed-species colonies, workers responded to heterospecific signals of the presence of the queen and did not activate their ovaries. Thus, despite predictions from kin selection theory that workers would benefit from parasitising heterospecific nests, we find no evidence that selection has established a parasitic strategy in these sibling species.


Brood parasitism Worker reproduction Policing Apis florea Apis andreniformis 



We thank Siriwat Wongsiri for advice and Det and Teddy Wattanachaiyingcharoen for help in the field. Funding was provided by an Australian Research Council grant to M. Beekman and B. Oldroyd, and by the Thailand Research Fund TRFC/BIOTECH Special Program for Biodiversity Research and Training, grant BRT R25137.


  1. Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera:Apinae:Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol 37:25–35CrossRefPubMedGoogle Scholar
  2. Beekman M, Oldroyd BP (2008) When workers disunite: intraspecific parasitism in eusocial bees. Annu Rev Entomol 53:19–37CrossRefPubMedGoogle Scholar
  3. Beekman M, Martin CG, Oldroyd BP (2004) Similar policing rates of eggs laid by virgin and mated honey-bee queens. Naturwissenschaften 91:598–601CrossRefPubMedGoogle Scholar
  4. Chapman NC, Beekman M, Oldroyd BP (2009a) Worker reproductive parasitism and drift in the Western honeybee Apis mellifera. Behav Ecol Sociobiol 64:419–427CrossRefGoogle Scholar
  5. Chapman NC, Makinson J, Beekman M, Oldroyd BP (2009b) Honey bee, Apis mellifera, guards use adaptive acceptance thresholds to limit worker reproductive parasitism. Anim Behav 78:1205–1211CrossRefGoogle Scholar
  6. Chapman NC, Nanork P, Gloag RS, Wattanachaiyingcharoen W, Beekman M, Oldroyd BP (2009c) Queenless colonies of the Asian red dwarf honey bee (Apis florea) are infiltrated by workers from other queenless colonies. Behav Ecol 20:817–820CrossRefGoogle Scholar
  7. Chapman NC, Higgs JS, Wattanachaiyingcharoen W, Beekman M, Oldroyd BP (2010) Worker reproductive parasitism in naturally orphaned colonies of the Asian red dwarf honey bee, Apis florea. Insect Soc. doi: 10.1007/s00040-009-0061-x
  8. Free JB (1987) Pheromones of social bees. Chapman and Hall, LondonGoogle Scholar
  9. 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
  10. Higgs JS, Wattanachaiyingcharoen W, Oldroyd BP (2009) A scientific note on a genetically-determined colour morph of the dwarf honey bee, Apis andreniformis (Smith, 1858). Apidologie 40:513–514CrossRefGoogle Scholar
  11. Higgs JS, McHale M, Oldroyd BP (2010) A scientific note on a rapid method for the molecular discrimination of Apis andreniformis and A. florea. Apidologie 41:96–98CrossRefGoogle Scholar
  12. Jay SC (1968) Factors influencing ovary development of worker honey bees under natural conditions. Can J Zool 48:169–173Google Scholar
  13. Ken T, Mingxian Y, Radloff SE, Pirk CWW, Crewe RM, Phiancharoen M, Hepburn R, Oldroyd BP (2009) Worker reproduction in mixed-species colonies of honey bees. Behav Ecol 20:1106–1110CrossRefGoogle Scholar
  14. Koeniger G, Koeniger N, Mardan M, Otis G, Wongsiri S (1991) Comparative anatomy of male genital organs in the genus Apis. Apidologie 22:539–552CrossRefGoogle Scholar
  15. Miller DG, Ratnieks FLW (2001) The timing of worker reproduction and breakdown of policing behaviour in queenless honey bee (Apis mellifera L.) societies. Insect Soc 48:178–184CrossRefGoogle Scholar
  16. Nanork P, Paar J, Chapman NC, Wongsiri S, Oldroyd BP (2005) Asian honey bees parasitize the future dead. Nature 437:829CrossRefPubMedGoogle Scholar
  17. Nanork P, Chapman NC, Wongsiri S, Lim J, Gloag S, Oldroyd BP (2007a) Social parasitism by workers in queenless and queenright Apis cerana colonies. Mol Ecol 16:1107–1114CrossRefPubMedGoogle Scholar
  18. Nanork P, Wongsiri S, Oldroyd BP (2007b) Preservation and loss of the honey bee (Apis) egg-marking signal across evolutionary time. Behav Ecol Sociobiol 61:1509–1514CrossRefGoogle Scholar
  19. Oldroyd BP, Wongsiri S (2006) Asian honey bees. Biology, conservation and human interactions. Harvard University Press, Cambridge, MAGoogle Scholar
  20. 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
  21. Oldroyd BP, Ratnieks FLW, Wossler TC (2002) Egg marking pheromones in honey bees Apis mellifera. Behav Ecol Sociobiol 51:590–591CrossRefGoogle Scholar
  22. Plettner E, Otis GW, Wimalaratne DC, Winston ML, Slessor KN, Pankiw T, Punchihewa PWK (1997) Species- and caste-determined mandibular gland signals in honeybees (Apis). J Chem Ecol 23:363–377CrossRefGoogle Scholar
  23. Raffiudin R, Crozier RH (2007) Phylogenetic analysis of honey bee behavioral evolution. Mol Phylogenet Evol 43:543–552CrossRefPubMedGoogle Scholar
  24. Ratnieks FLW (1993) Egg-laying, egg-removal, and ovary development by workers in queenright honey bee colonies. Behav Ecol Sociobiol 32:191–198CrossRefGoogle Scholar
  25. Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608CrossRefPubMedGoogle Scholar
  26. Rinderer TE, Oldroyd BP, Wongsiri S, Potichot S, Sheppard WS, Buchmann S (1993) Time of drone flight in four bee species in south-eastern Thailand. J Apic Res 32:27–33Google Scholar
  27. Visscher PK (1989) A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247–254CrossRefGoogle Scholar
  28. Visscher PK (1996) Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing. Behav Ecol Sociobiol 39:237–234CrossRefGoogle Scholar
  29. Wenseleers T, Hart AG, Ratnieks FLW (2004) When resistance is useless: policing and the evolution of reproductive acquiescence in insect societies. Am Nat 164:E154–E167CrossRefGoogle Scholar
  30. Winston ML, Slessor KN (1998) Honey bee primer pheromones and colony organization: gaps in our knowledge. Apidologie 29:81–95CrossRefGoogle Scholar
  31. Wongsiri S, Limbipichai P, Tangkanasing P, Mardan M, Rinderer TE, Sylvester HA, Koeniger G, Otis G (1990) Evidence of reproductive isolation confirms that Apis andreniformis (Smith, 1858) is a separate species from sympatric Apis florea (Fabricius, 1787). Apidologie 21:47–52CrossRefGoogle Scholar
  32. Wu Y, Kuang B (1987) Two species of small honeybee—a study of the genus Micrapis. Bee World 68:153–155Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Sitthipong Wongvilas
    • 1
  • Jessica S. Higgs
    • 2
  • Madeleine Beekman
    • 2
  • Wandee Wattanachaiyingcharoen
    • 3
  • Sureerat Deowanish
    • 1
  • Benjamin P. Oldroyd
    • 2
  1. 1.Center of Excellence in Entomology: Bee Biology, Biodiversity of Insects and MitesDepartment of Biology, Chulalongkorn UniversityBangkokThailand
  2. 2.Behaviour and Genetics of Social Insects Lab, School of Biological Sciences A12University of SydneySydneyAustralia
  3. 3.Department of BiologyNaresuan UniversityPhitsanulokThailand

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