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Pairs of cooperating cleaner fish provide better service quality than singletons

Nature volume 455, pages 964–966 (2008)Cite this article

Abstract

Service providers may vary service quality depending on whether they work alone or provide the service simultaneously with a partner. The latter case resembles a prisoner’s dilemma1,2,3,4, in which one provider may try to reap the benefits of the interaction without providing the service. Here we present a game-theory model based on the marginal value theorem5, which predicts that as long as the client determines the duration, and the providers cooperate towards mutual gain, service quality will increase in the pair situation. This prediction is consistent with field observations and with an experiment on cleaning mutualism, in which stable male–female pairs of the cleaner wrasse Labroides dimidiatus repeatedly inspect client fish jointly. Cleaners cooperate by eating ectoparasites6 off clients but actually prefer to cheat and eat client mucus7. Because clients often leave in response to such cheating, the benefits of cheating can be gained by only one cleaner during a pair inspection. In both data sets, the increased service quality during pair inspection was mainly due to the smaller females behaving significantly more cooperatively than their larger male partners. In contrast, during solitary inspections, cleaning behaviour was very similar between the sexes. Our study highlights the importance of incorporating interactions between service providers to make more quantitative predictions about cooperation between species.

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Figure 1: The marginal value theorem for service providers.
Figure 2: Client jolt rates in response to singleton and pair inspections.
Figure 3: Cleaner fish feed more against their preference when in pairs than when alone.

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References

  1. Axelrod, R. & Hamilton, W. D. On the evolution of co-operation. Science 211, 1390–1396 (1981)

    Article  ADS  MathSciNet  CAS  Google Scholar 

  2. Nowak, M. A. & Sigmund, K. Tit for tat in heterogeneous populations. Nature 355, 250–253 (1992)

    Article  ADS  Google Scholar 

  3. Nowak, M. & Sigmund, K. A strategy of win-stay, lose-shift that outperforms tit-for-tat in the prisoner’s dilemma game. Nature 364, 56–58 (1993)

    Article  ADS  CAS  Google Scholar 

  4. Dugatkin, L. A. Cooperation Among Animals: An Evolutionary Perspective (Oxford Univ. Press, 1997)

    Google Scholar 

  5. Charnov, E. L. Optimal foraging, the marginal value theorem. Theor. Popul. Biol. 9, 129–136 (1976)

    Article  CAS  Google Scholar 

  6. Grutter, A. S. Parasite removal rates by the cleaner wrasse Labroides dimidiatus . Mar. Ecol. Prog. Ser. 130, 61–70 (1996)

    Article  ADS  Google Scholar 

  7. Grutter, A. S. & Bshary, R. Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions. Proc. R. Soc. Lond. B 270 (Suppl.). S242–S244 (2003)

    Article  Google Scholar 

  8. Noë, R., Van Schaik, C. P. & Van Hooff, J. A. R. A. M. The market effect: an explanation for pay-off asymmetries among collaborating animals. Ethology 87, 97–118 (1991)

    Article  Google Scholar 

  9. Noë, R. & Hammerstein, P. Biological markets. Trends Ecol. Evol. 10, 336–339 (1995)

    Article  Google Scholar 

  10. Bowles, S. & Hammerstein, P. in Genetic and Cultural Evolution of Cooperation (ed. Hammerstein, P.) 153–165 (MIT Press, 2003)

    Google Scholar 

  11. Pierce, N. E. et al. The ecology and evolution of ant associations in the Lycaenidae (Lepidoptera). Annu. Rev. Entomol. 47, 733–771 (2002)

    Article  CAS  Google Scholar 

  12. Kiers, E. T., Rousseau, R. A., West, S. A. & Denison, R. F. Host sanctions and the legume–rhizobium mutualism. Nature 425, 78–81 (2003)

    Article  ADS  CAS  Google Scholar 

  13. Côté, I. M. Evolution and ecology of cleaning symbioses in the sea. Oceanogr. Mar. Biol. Ann. Rev. 38, 311–355 (2000)

    Google Scholar 

  14. Grutter, A. S. Relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar. Ecol. Prog. Ser. 118, 51–58 (1995)

    Article  ADS  Google Scholar 

  15. Bshary, R. & Grutter, A. S. Punishment and partner switching cause cooperative behaviour in a cleaning mutualism. Biol. Lett. 1, 396–399 (2005)

    Article  Google Scholar 

  16. Bshary, R. & Grutter, A. S. Image scoring and cooperation in a cleaner fish mutualism. Nature 441, 975–978 (2006)

    Article  ADS  CAS  Google Scholar 

  17. Johnstone, R. A. & Bshary, R. From parasitism to mutualism: partner control in asymmetric interactions. Ecol. Lett. 5, 634–639 (2002)

    Article  Google Scholar 

  18. Robertson, D. R. Social control of sex reversal in a coral-reef fish. Science 177, 1007–1009 (1972)

    Article  ADS  CAS  Google Scholar 

  19. Bshary, R. & Grutter, A. S. Asymmetric cheating opportunities and partner control in a cleaner fish mutualism. Anim. Behav. 63, 547–555 (2002)

    Article  Google Scholar 

  20. Heinsohn, R. & Packer, C. Complex cooperative strategies in group-territorial African lions. Science 269, 1260–1262 (1995)

    Article  ADS  CAS  Google Scholar 

  21. Milinski, M. TIT FOR TAT in sticklebacks and the evolution of cooperation. Nature 325, 433–435 (1987)

    Article  ADS  CAS  Google Scholar 

  22. Dugatkin, L. A. Do guppies play TIT FOR TAT during predator inspection visits? Behav. Ecol. Sociobiol. 23, 395–399 (1988)

    Article  Google Scholar 

  23. Bshary, R. & Schäffer, D. Choosy reef fish select cleaner fish that provide high-quality service. Anim. Behav. 63, 557–564 (2002)

    Article  Google Scholar 

  24. Hammerstein, P. Why is Reciprocity so Rare in Social Animals? A Protestant Appeal in Genetic and Cultural Evolution of Cooperation (ed. Hammerstein, P.) 83–93 (MIT Press, 2003)

    Google Scholar 

  25. Clutton-Brock, T. H. & Parker, G. A. Punishment in animal societies. Nature 373, 209–215 (1995)

    Article  ADS  CAS  Google Scholar 

  26. Clutton-Brock, T. H. & Parker, G. A. Sexual coercion in animal societies. Anim. Behav. 49, 1345–1365 (1995)

    Article  Google Scholar 

  27. Dreber, A., Rand, D. G., Fudenberg, D. & Nowak, M. A. Winners don’t punish. Nature 452, 348–351 (2008)

    Article  ADS  CAS  Google Scholar 

  28. Bshary, R. & Würth, M. Cleaner fish Labroides dimidiatus manipulate client reef fish by providing tactile stimulation. Proc. R. Soc. Lond. B 268, 1495–1501 (2001)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the Egyptian Environmental Affairs Agency for permission to work at Ras Mohammed National Park, the Park Rangers and I. Riepl for local support, and M. Würth and A. Hubl for field assistance. We further thank the Lizard Island Research Station for their support concerning the experiments. R.B. was funded by the Natural Environment Research Council and by the Swiss Science Foundation. A.S.T.W. was funded by the Swiss Science Foundation. A.S.G. was funded by the Australian Research Council. O.L. was funded by the Swedish Research Council.

Author Contributions R.B. and A.S.G. were responsible for the experimental data; A.S.T.W. was responsible for the field data; O.L. was responsible for the model; and R.B., A.S.G. and O.L. contributed to the writing.

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Authors and Affiliations

  1. Department of Zoology, University of Neuchâtel, Rue Emile-Argand 11 Case postale 158, 2009 Neuchâtel, Switzerland,

    Redouan Bshary & Astrid S. T. Willener

  2. University of Queensland, School of Integrative Biology, St Lucia, Queensland 4072, Australia ,

    Alexandra S. Grutter

  3. Department of Zoology, Stockholm University, SE-10691 Stockholm, Sweden

    Olof Leimar

Authors
  1. Redouan Bshary
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  2. Alexandra S. Grutter
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  3. Astrid S. T. Willener
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  4. Olof Leimar
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Corresponding author

Correspondence to Redouan Bshary.

Supplementary information

Supplementary Information

The file contains Supplementary Notes on the model of cleaner-client interactions. Equations (1) and (2) in the main text are derived and an important qualitative prediction of the model is demonstrated: cooperative pairs of cleaner fish provide higher service quality than singletons. (PDF 86 kb)

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Bshary, R., Grutter, A., Willener, A. et al. Pairs of cooperating cleaner fish provide better service quality than singletons. Nature 455, 964–966 (2008). https://doi.org/10.1038/nature07184

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