Abstract
Predation risk is amongst the most pervasive selective pressures influencing behaviour and animals have been repeatedly shown to trade-off foraging success for safety. We examined the nature of this trade-off in cleaning symbioses amongst Caribbean coral reef fishes. We predicted that cleaning gobies (Elacatinus evelynae and Elacatinus prochilos) should prefer fish clients that pose a low risk of predation (e.g. herbivores) over clients that may have more ectoparasites but pose a higher risk (e.g. piscivores). Our field observations revealed that cleaners did clean preferentially client species with more parasites but predatory and non-predatory clients had similar ectoparasite loads. Despite the lack of a foraging advantage for inspecting predators, cleaners did not avoid risky clients. On the contrary, a larger proportion of visiting predators than non-predators was inspected, gobies initiated more interactions with predatory clients, and predators were attended to immediately upon arrival at cleaning stations. This preferential treatment of dangerous clients may allow the rapid identification of cleaners as non-prey item or may be due to the effect of predators on the rest of the cleaners’ clientele, which avoided cleaning stations whilst predators were present. Dealing with potentially risky clients may allow gobies to regain access to their main food source: non-predatory clients.
Similar content being viewed by others
References
Arnal C, Côté IM (1998) Interactions between cleaning gobies and territorial damselfish on coral reefs. Anim Behav 55:1429–1442
Arnal C, Côté IM (2000) Diet of the broadstripe cleaning gobies on a Barbadian reef. J Fish Biol 57:1075–1082
Arnal C, Morand S (2001) Importance of ectoparasites and mucus in cleaning interactions in the Mediterranean cleaner wrasse Symphodus melanocercus. Mar Biol 138:771–784
Arnal C, Côté IM, Morand S (2001) Why clean and be cleaned? The importance of client ectoparasites and mucus in a marine cleaning symbioses. Behav Ecol Sociobiol 51:1–7
Arnal C, Verneau O, Desdevises Y (2006) Phylogenetic relationships and evolution of cleaning behaviour in the family Labridae: importance of body colour pattern. J Evol Biol 19:755–763
Bateson M (2002) Recent advances in our understanding of risk-sensitive foraging preferences. Proc Nutr Soc 61:1–8
Bshary R (2001) The cleaner-fish market. In: Noë R, van Hoof J, Hammerstein P (eds) Economics in nature. Cambridge University Press, Cambridge, pp 146-172
Bshary R, Grutter AS (2002) Asymmetric cheating opportunities and partner control in a cleaner fish mutualism. Anim Behav 63:547–555
Bshary R, Noë R (2003) Biological markets. The ubiquitous influence of partner choice on the dynamcis of cleaner fish — client reef fish interactions. In: Hammerstein P (ed) Genetic and cultural evolution of cooperation. Dahlem Workshop Reports, pp 167–184
Bshary R, Würth M (2001) Cleaner fish Labroides dimidiatus manipulate client reef fish by providing tactile stimulation. Proc R Soc Lond B 268:1495–1501
Cheney KL, Côté IM (2005) Mutualism or parasitism? The variable outcome of cleaning symbioses. Biol Lett 2:162–165
Colin P (1975) The neon gobies: the comparative biology of the gobies of the genus Gobiosoma, subgenus Elacatinus, (Pisces: Gobiidae) in the tropical western North Atlantic Ocean. TFH, London
Côté IM (2000) Evolution and ecology of cleaning symbioses in the sea. Oceanogr Mar Biol 38:311–355
Côté IM, Cheney KL (2004) Distance-dependent costs and benefits of aggressive mimicry in a cleaning symbiosis. Proc R Soc Lond B 271:2627–2630
Côté IM, Arnal C, Reynolds JD (1998) Variation in posing behaviour among fish species visiting cleaning stations. J Fish Biol 53:256–266
Dill LM, Fraser AHG (1984) Risk of predation and the feeding behaviour of juvenile coho salmon (Oncorhynchus kisutch). Behav Ecol Sociobiol 16:65–71
Feder HM (1966) Cleaning symbioses in the marine environment. In: Henry SM (ed) Symbioses. Academic, New York, pp 317–380
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
Gorlick DL (1984) Preference for ectoparasite-infected host fishes by the Hawaiian cleaning wrasse, Labroides phthirophagus (Labridae). Copeia 1984:758–762
Grutter AS (1995) Relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:8–51
Grutter AS (2004) Cleaner fish use tactile dancing behavior as a preconflict management strategy. Curr Biol 14:1080–1083
Hobson ES (1965) Diurnal-nocturnal activity of some inshore fishes in the Gulf of California. Copeia 1965:291–302
Hobson ES (1971) Cleaning symbioses among California inshore fishes. Fish B–NOAA 69:491–523
Johnson WS, Ruben P (1988) Cleaning behaviour of Bodianus rufus, Thalassoma bifasciatum, Gobiosoma evelinae, and Periclimenes pedersoni along a depth gradient at Salt River Submarine Canyon, St Croix. Environ Biol Fisches 23:225–232
Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Potts GW (1973a) The ethology of Labroides dimidiatus (Cuv. And Val.)(Labridae; Pisces) on Aldabra. Anim Behav 21:250–291
Potts GW (1973b) Cleaning symbioses among British fish with special reference to Crenilabrus melops (Labridae). J Mar Biol Assoc UK 53:1–10
Randall JE (1967) Food habits of reef fishes of the West Indies. Stud Trop Oceanogr 5:665–847
Rohde K (1980) Comparative studies on microhabitat utilization by ectoparasites of some marine fishes from the North Sea and Papua New Guinea. Zool Anz 204:27–63
Sazima I, Moura RL, Gasparini JL (1998) The wrasse Halichoeres cyanocephalus (Labridae) as a specialized cleaner fish. Bull Mar Sci 63:605–610
Sikkel PC, Cheney KL, Côté IM (2004) In situ evidence for ectoparasites as a proximate cause of cleaning interactions in reef fish. Anim Behav 68:241–247
Stummer LE, Weller JA, Johnson ML, Côté IM (2004) Size and stripes: how fish clients recognize cleaners. Anim Behav 68:145–150
Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100
Whiteman EA, Côté IM (2002) Cleaning activity of two Caribbean cleaning gobies: intra- and interspecific comparisons. J Fish Biol 60:1443–1458
Acknowledgements
We thank Karen Cheney for valuable comments and help. We also thank the staff of the Bellairs Research Institute for logistical support. M.C.S. was supported by Fundação para a Ciência e a Tecnologia studentship from the Portuguese Ministry of Science and Technology. The data collection complied with the laws of Barbados.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Gabor
Rights and permissions
About this article
Cite this article
Soares, M.C., Cardoso, S.C. & Côté, I.M. Client preferences by Caribbean cleaning gobies: food, safety or something else?. Behav Ecol Sociobiol 61, 1015–1022 (2007). https://doi.org/10.1007/s00265-006-0334-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-006-0334-6