Skip to main content

The alternative Pharaoh approach: stingless bees mummify beetle parasites alive

Abstract

Workers from social insect colonies use different defence strategies to combat invaders. Nevertheless, some parasitic species are able to bypass colony defences. In particular, some beetle nest invaders cannot be killed or removed by workers of social bees, thus creating the need for alternative social defence strategies to ensure colony survival. Here we show, using diagnostic radioentomology, that stingless bee workers (Trigona carbonaria) immediately mummify invading adult small hive beetles (Aethina tumida) alive by coating them with a mixture of resin, wax and mud, thereby preventing severe damage to the colony. In sharp contrast to the responses of honeybee and bumblebee colonies, the rapid live mummification strategy of T. carbonaria effectively prevents beetle advancements and removes their ability to reproduce. The convergent evolution of mummification in stingless bees and encapsulation in honeybees is another striking example of co-evolution between insect societies and their parasites.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Betz O, Koelsch G (2004) The role of adhesion in prey capture and predator defence in arthropods. Arthropod Structure & Development 33:3–30

    Article  Google Scholar 

  • Breed MD (2003) Nestmate recognition assays as a tool for population and ecological studies in eusocial insects: a review. J Kans Entomol Soc 76:539–550

    Google Scholar 

  • Breed MD, Guzman-Novoa E, Hunt GJ (2004) Defensive behaviour of honey bees: organization, genetics, and comparisons with other bees. Annu Rev Entomol 49:271–298

    Article  CAS  PubMed  Google Scholar 

  • Breed MD, Deng XB, Buchwald R (2007) Comparative nestmate recognition in Asian honey bees, Apis florea, Apis andreniformis, Apis dorsata, and Apis cerana. Apidologie 38(5):411–418

    Article  Google Scholar 

  • Ellis JD, Hepburn HR, Ellis AM, Elzen PJ (2003) Social encapsulation of the small hive beetle (Aethina tumida Murray) by European honeybees (Apis mellifera L.). Insect Soc 50:286–291

    Article  Google Scholar 

  • El-Niweiri MAA, El-Sarrage MS, Neumann P (2008) Filling the Sudan gap: the northern most natural distribution limit of small hive beetles. Journal of Apicultural Research and Bee World 47(3):183–184

    Google Scholar 

  • Elzen PJ, Baxter JR, Neumann P, Solbrig A, Pirk CWW, Hepburn HR, Westervelt D, Randall C (2001) Behaviour of African and European subspecies of Apis mellifera toward the small hive beetle, Aethina tumida. J Apic Res 40:40–41

    Google Scholar 

  • Greco MK, Spooner-Hart R, Holford P (2005) A new technique for monitoring Trigona carbonaria nest contents, brood and activity using X-ray computerised tomography. J Apic Res 44:97–100

    Google Scholar 

  • Greco MK, Bell M, Spooner-Hart R, Holford P (2006) X-ray computerized tomography as a new method for monitoring Amegilla holmesi nest structure, nesting behaviour and adult female activity. Entomol Exp Appl 120:71–76

    Article  Google Scholar 

  • Hoffmann D, Pettis JS, Neumann P (2008) Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens). Insectes Soc 55:153–162

    Article  Google Scholar 

  • Kerr WE, Lello E (1962) Sting glands in stingless bees. J N Y Entomol Soc 70:190–214

    Google Scholar 

  • Lea AM (1910) Australian and Tasmanian Coleoptera inhabiting or resorting to the nests of ants, bees and termites. Proc R Soc Victoria [NS] 23:116–230

    Google Scholar 

  • Lea AM (1912) Australian and Tasmanian Coleoptera inhabiting or resorting to the nests of ants, bees and termites. Proc R Soc Victoria [NS] 25(Suppl):31–78

    Google Scholar 

  • Lehmberg L, Dworschak K, Bluethgen N (2008) Defensive behaviour and chemical deterrence against ants in the stingless bee genus Trigona (Apidae, Meliponini). J Apic Res 47:17–21

    Google Scholar 

  • Lundie AE (1940) The small hive beetle Aethina tumida, Science Bulletin 220. Department of Agriculture and Forestry, Government Printer, Pretoria

    Google Scholar 

  • Michener CD (1961) Observations on the nests and behaviour of Trigona in Australia and New Guinea (Hymenoptera: Apidae). Am Mus Novit 2026:1–45

    Google Scholar 

  • Michener CD (1974) The social behaviour of the bees; A comparative study. Harvard University Press, Harvard, p 404

    Google Scholar 

  • Muerrle TM, Neumann P (2004) Mass production of small hive beetles (Aethina tumida Murray, Coleoptera: Nitidulidae). J Apic Res 43:144–145

    Google Scholar 

  • Nates G, Cepeda O (1983) Comportamiento defensivo en algunas especies de meliponínos. Boletín del Departamento de la Biologia de la Universidad Nacional de Colombia, Bogotá 1:65–81

    Google Scholar 

  • Neumann P, Ellis JD (2008) The small hive beetle (Aethina tumida Murray, Coleoptera: Nitidulidae): distribution, biology and control of an invasive species. J Apic Res 47:181–183

    Article  Google Scholar 

  • Neumann P, Elzen PJ (2004) The biology of the small hive beetle (Aethina tumida Murray, Coleoptera: Nitidulidae): gaps in our knowledge of an invasive species. Apidologie 35:229–247

    Article  Google Scholar 

  • Neumann P, Ritter W (2004) A scientific note on the association of Cychramus luteus (Coleoptera: Nitidulidae) with honeybee (Apis mellifera) colonies. Apidologie 35:665–666

    Article  Google Scholar 

  • Neumann P, Pirk CWW, Hepburn HR, Solbrig AJ, Ratnieks FLW, Elzen PJ, Baxter JR (2001) Social encapsulation of beetle parasites by Cape honeybee colonies (Apis mellifera capensis Esch.). Naturwissenschaften 88:214–216

    Article  CAS  PubMed  Google Scholar 

  • Rayment T (1935) A cluster of bees. The Endeavour, Sydney

    Google Scholar 

  • Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, Cambridge

    Google Scholar 

  • Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton

    Google Scholar 

  • Schmolke MD (1974) A study of Aethina tumida: the small hive beetle, Project Report, University of Rhodesia

  • Spiewok S, Neumann P (2006a) Cryptic low-level reproduction of small hive beetles in honeybee colonies. J Apic Res 45:47–48

    Google Scholar 

  • Spiewok S, Neumann P (2006b) Infestation of commercial bumblebee (Bombus impatiens) field colonies by small hive beetles (Aethina tumida). Ecol Entomol 31:623–628

    Article  Google Scholar 

  • Spiewok S, Pettis JS, Duncan M, Spooner-Hart R, Westervelt D, Neumann P (2007) Small hive beetle, Aethina tumida, populations I: infestation levels of honeybee colonies, apiaries and regions. Apidologie 38:595–605

    Article  Google Scholar 

Download references

Acknowledgements

We thank Macarthur Diagnostic Imaging for donating time on the CT scanner and for use of their Campbelltown facility.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark K. Greco.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Greco, M.K., Hoffmann, D., Dollin, A. et al. The alternative Pharaoh approach: stingless bees mummify beetle parasites alive. Naturwissenschaften 97, 319–323 (2010). https://doi.org/10.1007/s00114-009-0631-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-009-0631-9

Keywords

  • Stingless bee
  • Diagnostic radioentomology
  • Beetles
  • Parasites