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Strategic exploitation in a socially parasitic bee: a benefit in waiting?

Abstract

Social parasitism has evolved at least ten times in the allodapine bees but studies that explore the parasite’s integration and exploitation of host colonies are lacking. Using colony content and dissection data, we examine how Inquilina schwarzi affects the social organisation of its host Exoneura robusta. Our samples include three critical periods in the host life cycle: initial formation of dominance hierarchies in late autumn, commencement of oviposition by host queens in late winter, and development of secondary reproductives in late spring. I. schwarzi preferentially parasitises larger host colonies in autumn, but during autumn and winter, the parasite appears to be socially invisible, living in the nest without disrupting the normal functioning of these colonies. Inquilines begin egg laying much later than their hosts, and by late spring, they have disrupted host reproductive hierarchies, leading to lower skew in ovarian sizes of their host nestmates. Living invisibly within the host nest for the first 6 months and waiting until well after host reproduction has begun before disrupting their social organisation appear to be unique among social insects. Such a change in strategy may be facilitated by the different social systems found in allodapine bees, with the social parasites possibly disrupting the reproductive hierarchies during spring to prevent or reduce the normal dispersal of some host females from their natal nests.

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References

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton

    Google Scholar 

  • Bull NJ, Mibus AC, Norimatsu Y, Jarmyn BI, Schwarz MP (1998) Giving your daughters the edge: bequeathing reproductive dominance in a primitively social bee. Proc R Soc Lond B Biol Sci 265:1–5

    Article  Google Scholar 

  • Cervo R, Turillazzi S (1996) Host nest preference and nest choice in the cuckoo paper wasp Polistes sulcifer (Hymenoptera: Vespidae). J Insect Behav 9:297–306

    Article  Google Scholar 

  • Cervo R, Stemmer C, Castle W, Queller D, Strassmann JE (2004) Social parasitism of Polistes dominulus by Polistes nimphus (Hymenoptera, Vespidae). Insectes Soc 51:101–108

    Article  Google Scholar 

  • Dapporto L, Cervo R, Sledge MF, Turillazzi S (2004) Rank integration in dominance hierarchies of host colonies by the paper wasp social parasite Polistes sulcifer. J Insect Physiol 50:217–223

    PubMed  Article  CAS  Google Scholar 

  • D’Ettorre P, Mondy N, Lenoir A, Errard C (2002) Blending in with the crowd: social parasites integrate into their host colonies using a flexible chemical signature. Proc R Soc Lond B Biol Sci 269:1911–1918

    Article  CAS  Google Scholar 

  • Fisher RM (1984) Dominance by a bumble bee social parasite (Psithyrus citrinus) over workers of its host (Bombus impatiens). Anim Behav 32:303–304

    Google Scholar 

  • Foitzik S, Fischer B, Heinze J (2003) Arms race between social parasites and their hosts: geographic patterns of manipulation and resistance. Behav Ecol 14:80–88

    Article  Google Scholar 

  • Hogendoorn K, Schwarz MP (1998) Guarding specialisation in pre-reproductive colonies in the allodapine bee Exoneura bicolor. Ethol Ecol Evol 10:67–77

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Hurst PS, Gray S, Schwarz MP, Tilly JA, Foran AC, Adams M (1997) Increased nest cofounding and high intra-colony relatedness in the bee Exoneura bicolor (Hymenoptera: Apidae): results from an experimental situation. Aust J Ecol 22:419–424

    Article  Google Scholar 

  • Johnson CA, Topoff H, Vander RK, Lavine B (2005) Do these eggs smell funny to you?: an experimental study of egg discrimination by hosts of the social parasite Polyergus breviceps (Hymenoptera: Formicidae). Behav Ecol Sociobiol 57:245–255

    Article  Google Scholar 

  • Lenoir A, D’Ettorre P, Errard C (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599

    PubMed  Article  CAS  Google Scholar 

  • Lorenzi MC, Filippone F (2000) Opportunistic discrimination of alien eggs by social wasps (Polistes biglumis, Hymenoptera Vespidae): a defense against social parasitism? Behav Ecol Sociobiol 48:402–406

    Article  Google Scholar 

  • Michener CD (1970) Social parasites among African allodapine bees (Hymenoptera, Anthophoridae, Ceratinini). Zool J Linn Soc 49:199–215

    Google Scholar 

  • Michener CD (2000) The bees of the world. The John Hopkins University Press, Baltimore

    Google Scholar 

  • Neumann P, Moritz RFA (2002) The cape honeybee phenomenon: the sympatric evolution of a social parasite in real time? Behav Ecol Sociobiol 52:271–281

    Article  Google Scholar 

  • Nonacs P, Tobin JE (1992) Selfish larvae: development and the evolution of parasitic behaviour in the hymenoptera. Evolution 46:1605–1621

    Article  Google Scholar 

  • Passera L, Gilbert M, Aron S (2001) Social parasitism in ants: effects of the inquiline parasite Plagiolepis xexe St. on queen distribution and worker production of its host Plagiolepis pygmaea Latr. Insectes Soc 48:74–79

    Article  Google Scholar 

  • Queller DC, Zacchi F, Cervo R, Turillazzi S, Henshaw MT, Santorelli LA, Strassmann JE (2000) Unrelated helpers in a social insect. Nature 405:784–787

    Article  Google Scholar 

  • Reyes SG, Michener CD (1990) Observations on a parasitic allodapine bee and its hosts in Java and Malaysia. Trop Zool 3:139–149

    Google Scholar 

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

    Google Scholar 

  • Schwarz MP (1986) Persistent multi-female nests in an Australian allodapine bee, Exoneura bicolor. Insectes Soc 33:258–277

    Article  Google Scholar 

  • Schwarz MP (1987) Intra-colony relatedness and sociality in the Allodapine bee, Exoneura bicolor. Behav Ecol Sociobiol 21:387–392

    Article  Google Scholar 

  • Schwarz MP (1988) Local resource enhancement and sex ratios in a primitively social bee. Nature 331:346–348

    Article  Google Scholar 

  • Schwarz MP (1994) Female biased sex ratios in a facultatively social bee and their implication for social evolution. Evolution 48:1648–1697

    Article  Google Scholar 

  • Schwarz MP, Scholz O, Jensen G (1987) Ovarian inhibition among nestmates of the allodapine bee Exoneura bicolor. J Aust Entomol Soc 26:355–359

    Article  Google Scholar 

  • Schwarz MP, Silberbauer LX, Hurst PS (1997) Intrinsic and extrinsic factors associated with social evolution in allodapine bees. In: Choe JC, Crespi BJ (eds) The evolution of social behaviour in insects and arachnids. Princeton University Press, Princeton, pp 333–346

    Google Scholar 

  • Schwarz MP, Bull NJ, Hogendoorn K (1998) Evolution of sociality in the allodapine bees: a review of sex allocation, ecology and evolution. Insectes Soc 45:349–368

    Article  Google Scholar 

  • Sudd JH, Franks NR (1987) The behavioural ecology of ants. Chapman and Hall, New York

    Google Scholar 

  • Sumner S, Hughes WOH, Boomsma JJ (2003) Evidence for differential selection and potential evolution in the worker caste of an inquiline social parasite. Behav Ecol Sociobiol 54:258–277

    Article  Google Scholar 

  • Tierney SM, Schwarz MP, Adams M (1997) Social behaviour in an Australian allodapine bee Exoneura (Brevineura) xanthoclypeata (Hymenoptera: Apidae). Aust J Zool 45:385–398

    Article  Google Scholar 

  • Visscher PK (1996) Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing. Behav Ecol Sociobiol 39:137–244

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

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Acknowledgements

We thank Narelle Joyce, Meg Schwarz and Nathan Smith for help with fieldwork. We also thank Tom Chapman and Jocelyn Smith for comments on previous versions of this paper. This work was supported by an ARC Discovery Grant to M. Schwarz, S. Cooper, B. Crespi and T. Chapman (DPO346322) and complied with the current laws of Australia.

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Correspondence to Jaclyn A. Smith.

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Communicated by R.F.A. Moritz

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Smith, J.A., Schwarz, M.P. Strategic exploitation in a socially parasitic bee: a benefit in waiting?. Behav Ecol Sociobiol 60, 108–115 (2006). https://doi.org/10.1007/s00265-005-0147-z

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  • DOI: https://doi.org/10.1007/s00265-005-0147-z

Keywords

  • Inquiline
  • Social parasitism
  • Allodapine bee