Skip to main content
SpringerLink
Log in

Cleaning behavior is riskier and less profitable than an alternative strategy for a facultative cleaner fish

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Cleaning symbioses on coral reefs involve small cleaner fish or shrimps picking ectoparasites from the exterior surfaces of larger client organisms. These mutualisms are thought to evolve in part because the cleaner receives a reliable source of profitable prey items and immunity from predation. However, the benefits of cleaning behavior have never been measured relative to those of alternative, non-cleaning strategies. This study examined these costs and benefits in the sharknose goby, Elacatinus evelynae, a facultative cleaner fish, at the Caribbean island of St. Croix. Sharknose gobies are found on coral heads, where they maintain cleaning stations, and on basket sponges, where they spend little time cleaning and feed predominantly on nonparasitic copepods. For immature gobies that are not allocating energy to reproduction, hindcast otolith growth rates (a reliable proxy for somatic growth) were significantly higher for non-cleaning sponge-dwellers than for coral-dwellers. Furthermore, tagging large, competitively dominant gobies on sponges and corals revealed that mortality rates were higher for coral-dwelling gobies. These unexpected results provide further evidence that cleaning mutualisms are context dependent: far from being a uniformly profitable life history strategy, cleaning may be a suboptimal choice at some times and places.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Arnal C, Côté IM (1998) Interactions between cleaning gobies and territorial damselfish on coral reefs. Anim Behav 55:1429–1442

    Article  Google Scholar 

  • Bansemer C, Grutter AS, Poulin R (2002) Geographic variation in the behaviour of the cleaner fish Labroides dimidiatus (Labridae). Ethology 108:353–366

    Article  Google Scholar 

  • Bronstein JL (1994a) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217

    Article  Google Scholar 

  • Bronstein JL (1994b) Our current understanding of mutualism. Q Rev Biol 69:31–51

    Article  Google Scholar 

  • Böhlke JE, Robins CR (1968) Western Atlantic seven-spined gobies, with descriptions of ten new species and a new genus, and comments on Pacific relatives. Proc Acad Nat Sci Phila 120:45–174

    Google Scholar 

  • Carr MH, Hixon MA (1995) Predation effects on early post-settlement survivorship of coral-reef fishes. Mar Ecol Prog Ser 124:31–42

    Google Scholar 

  • Cheney KL, Côté IM (2001) Are Caribbean cleaning symbioses mutualistic? Costs and benefits of visiting cleaning stations to longfin damselfish. Anim Behav 62:927–933

    Article  Google Scholar 

  • Cheney KL, Côté IM (2005) Mutualism or parasitism? The variable outcome of cleaning symbioses. Biol Lett 1:162–165

    Article  Google Scholar 

  • Colin PI (1975) The neon gobies. T.F.H. Publications, Neptune City, New Jersey

  • Cox DR (1972) Regression models and life-tables. J Roy Stat Soc B Stat Meth 34:187–220

    Google Scholar 

  • Côté IM (2000) Evolution and ecology of cleaning symbioses in the sea. Oceanogr Mar Biol Annu Rev 38:311–355

    Google Scholar 

  • Darcy GH, Maisel E, Ogden JC (1974) Cleaning preferences of gobies Gobiosoma evelynae and G. prochilos and the wrasse Thalassoma bifasciatum. Copeia 1974:375–378

    Article  Google Scholar 

  • Francini-Filho RB, Moura RL, Sazima I (2000) Cleaning by the wrasse Thalassoma noronhanum, with two records of predation by its grouper client Cephalopholis fulva. J Fish Biol 56:802–809

    Google Scholar 

  • Freckleton RP, Côté IM (2003) Honesty and cheating in cleaning symbioses: evolutionarily stable strategies defined by variable pay-offs. Proc R Soc Lond B Biol Sci 270:299–305

    Article  Google Scholar 

  • Grutter AS (1997) Spatiotemporal variation and feeding selectivity in the diet of the cleaner fish Labroides dimidiatus. Copeia 1997:346–355

    Article  Google Scholar 

  • Grutter AS, McCallum H, Lester RJG (2002) Optimising cleaning behaviour: minimising the costs and maximising ectoparasite removal. Mar Ecol Prog Ser 234:257–264

    Google Scholar 

  • Grutter AS, Murphy JM, Choat JH (2003) Cleaner fish drives local fish diversity on coral reefs. Curr Biol 13:64–67

    Article  Google Scholar 

  • Hamilton SL, White JW, Caselle JE, Swearer SE, Warner RR (2006) Consistent long-term spatial gradients in replenishment for an island population of a coral reef fish. Mar Ecol Prog Ser 306:247–256

    Google Scholar 

  • Harding JA, Almany GR, Houck LD, Hixon MA (2003) Experimental analysis of monogamy in the Caribbean cleaner goby Gobiosoma evelynae. Anim Behav 65:865–874

    Article  Google Scholar 

  • Hernaman V, Munday PL, Schläppy ML (2000) Validation of otolith growth-increment periodicity in tropical gobies. Mar Biol 137:715–726

    Article  Google Scholar 

  • Johnson WS, Ruben P (1988) Cleaning behavior of Bodianus rufus, Thalassoma bifasciatum, Gobiosoma evelynae, and Periclimenes pedersoni along a depth gradient at Salt River submarine canyon, St. Croix. Env Biol Fish 23:225–232

    Article  Google Scholar 

  • Jones CM, Grutter AS, Cribb TH (2004) Cleaner fish become hosts: a novel form of parasite transmission. Coral Reefs 23:521–529

    Google Scholar 

  • Knowlton N, Jackson JBC (2001) The ecology of coral reefs. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 395–422

  • Lobel PS (1976) Predation on a cleanerfish (Labroides) by a hawkfish (Cirrhites). Copeia 1976:384–385

    Article  Google Scholar 

  • Poulin R, Grutter AS (1996) Cleaning symbioses: proximate and adaptive explanations. BioScience 46:512–517

    Article  Google Scholar 

  • Poulin R, Vickery WL (1995) Cleaning symbiosis as an evolutionary game: to cheat or not to cheat? J Theor Biol 175:63–70

    Article  Google Scholar 

  • Simms EL, Taylor DL (2002) Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integr Comp Biol 42:369–380

    Article  Google Scholar 

  • Stamps JA, Krishnan VV, Reid ML (2005) Search costs and habitat selection by dispersers. Ecology 86:510–518

    Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109

    Article  Google Scholar 

  • Thorrold SR, Hare JA (2002) Otolith applications in reef fish ecology. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic, San Diego, pp 243–264

  • Trivers RL (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57

    Article  Google Scholar 

  • Warner RR (1997) Evolutionary ecology: how to reconcile pelagic dispersal with local adaptation. Coral Reefs 16:S115–S120

    Article  Google Scholar 

  • Whiteman EA, Côté IM (2002a) Cleaning activity of two Caribbean cleaning gobies: intra- and interspecific comparisons. J Fish Biol 60:1443–1458

    Article  Google Scholar 

  • Whiteman EA, Côté IM (2002b) Sex differences in cleaning behaviour and diet of a Caribbean cleaning goby. J Mar Biol Assoc UK 82:655–664

    Article  Google Scholar 

  • Whiteman EA, Côté IM (2004a) Dominance hierarchies in group-living cleaning gobies: causes and foraging consequences. Anim Behav 67:239–247

    Article  Google Scholar 

  • Whiteman EA, Côté IM (2004b) Individual differences in microhabitat use in a Caribbean cleaning goby: a buffer effect in a marine species? J Anim Ecol 73:831–840

    Article  Google Scholar 

  • Wilson J, Osenberg CW (2002) Experimental and observational patterns of density-dependent settlement and survival in the marine fish Gobiosoma. Oecologia 130:205–215

    Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice-Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

We thank S. Hamilton and J. Samhouri for assistance with otolith analysis and expert advice throughout the study. S. Brander, P. Munday, A. Rassweiler, and two anonymous reviewers provided helpful comments on the manuscript. This is contribution 231 from the Partnership for Interdisciplinary Study of Coastal Oceans, funded primarily by the Gordon and Betty Moore Foundation and the David and Lucile Packard Foundation.

Author information

Authors and Affiliations

  1. Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA, 93106, USA

    J. W. White, C. J. Grigsby & R. R. Warner

Authors
  1. J. W. White
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. J. Grigsby
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. R. Warner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. W. White.

Additional information

Communicated by Biology Editor M.I. McCormick.

Rights and permissions

Reprints and permissions

About this article

Cite this article

White, J.W., Grigsby, C.J. & Warner, R.R. Cleaning behavior is riskier and less profitable than an alternative strategy for a facultative cleaner fish. Coral Reefs 26, 87–94 (2007). https://doi.org/10.1007/s00338-006-0161-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-006-0161-2

Keywords

Search

Navigation