Environmental Biology of Fishes

, Volume 101, Issue 7, pp 1195–1204 | Cite as

Cleaning interactions at the southern limit of tropical reef fishes in the Western Atlantic

  • J. P. Quimbayo
  • O. R. C. Schlickmann
  • S. R. Floeter
  • I. Sazima


Cleaning associations are one of the most dynamic and complex mutualistic interactions of reef environments and are often influenced by local conditions. In the Western Atlantic (WE) most studies concentrate in tropical areas, with little attention to subtropical areas. We examined an assemblage of cleaner fish and their clients on the rocky reefs of the coast of Santa Catarina state, South Brazil, the southern limit of tropical reef fishes in the WE. We recorded 150 cleaning interactions, in which four fish species and one shrimp species acted as facultative cleaners. The grunt Anisotremus virginicus and the angelfish Pomacanthus paru serviced most clients. Fifteen fish species acted as clients, among which the most frequent was the planktivorous grunt Haemulon aurolineatum (31%). Cleaning interactions occurred mostly (87%) with non-carnivorous clients and the number of interactions was not related to the abundance of the species involved. The absence of dedicated cleaner fishes at the study sites and the replacement of their roles by facultative cleaners may be related to local conditions, including cold currents and reduction of rock cover. Under these circumstances, clients take advantage of the services offered by facultative cleaners, a characteristic of temperate areas.


Mutualism Cleaning behavior Facultative cleaners South Atlantic Brazil 



This study was carried out under “Projeto Ilhas do Sul” (PI: Sergio R. Floeter, Conselho Nacional de Desenvolvimento Científico e Tecnológico 475367/2006-8), “Projeto MAArE – Monitoramento Ambiental do Arvoredo e Entorno” (PI: Barbara Segal, a condition set by the ICMBio in the context of IBAMA’s environmental licensing process), “Projeto Biodiversidade Marinha do Estado de Santa Catarina” (PI: Alberto Lindner, FAPESC 4302/2010-8), and SISBIOTA-Mar (PI: Sergio R. Floeter, CNPq 563276/2010-0; Fundação de Amparo à Pesquisa do Estado de Santa Catarina 6308/2011-8). We also acknowledge LBMM staff for field assistance and comments during the development of this study. R.A. Morais., L.T. Nunes, and J.P. Krajewski for pictures used in Fig. 3. JPQ and ORCS thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior and Conselho Nacional de Desenvolvimento Científico e Tecnológico for financial support. IS thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico and Fundação de Amparo à Pesquisa do Estado de São Paulo for previous financial support to study cleaning symbiosis in the southwestern Atlantic.


  1. Anderson AB, Carvalho-Filho A, Morais RA, Nunes LT, Quimbayo JP, Floeter SR (2015) Brazilian tropical fishes in their southern limit of distribution: checklist of Santa Catarina’s rocky reef ichthyofauna, remarks and new records. Check List 11:1–25. CrossRefGoogle Scholar
  2. Ayling AM, Grace RV (1971) Cleaning symbiosis among New Zealand fishes. New Zeal J Mar Freshw Res 5:205–218. CrossRefGoogle Scholar
  3. Bertoncini AA, Machado LF, Barreiros JP, Hostim-Silva M, Verani JR (2009) Cleaning activity among Labridae in the Azores: the rainbow wrasse Coris julis and the Azorean blue wrasse Centrolabrus caeruleus. J Mar Biol Assoc UK 89:859–861. CrossRefGoogle Scholar
  4. Bonaldo RM, Grutter AS, Sazima I, Krajewski JP (2015) 24/7 service: nocturnal cleaning in a tropical Indo-Pacific reef. Mar Biodivers 45:611–612. CrossRefGoogle Scholar
  5. Campos CEC, Sá-Oliveira JC (2011) Atividade de limpeza e clientes de Elacatinus figaro (Pisces: Gobiidae) nos recifes de coral dos parrachos de Muriú, Nordeste do Brasil. Biota Neotrop 11:47–51. CrossRefGoogle Scholar
  6. Capel KCC, Segal B, Bertuol P, Lindner A (2012) Corallith beds at the edge of the tropical South Atlantic. Coral Reefs 31:75. CrossRefGoogle Scholar
  7. Cheney KL, Bshary R, Grutter AS (2008) Cleaner fish cause predators to reduce aggression toward bystanders at cleaning stations. Behav Ecol 19:1063–1067. CrossRefGoogle Scholar
  8. Cheney KL, Grutter AS, Blomberg SP, Marshall NJ (2009) Blue and yellow signal cleaning behavior in coral reef fishes. Curr Biol 19:1283–1287. CrossRefPubMedGoogle Scholar
  9. Côté IM (2000) Evolution and ecology of cleaning symbiosis in the sea. Oceanogr Mar Biol 38:311–355Google Scholar
  10. Côté IM, Soares MC (2011) Gobies as cleaners. In: Patzner RA, Van Tassel JL, Kovacic M, Kapoor BG (eds) The biology of gobies. Science Publishers, JerseyGoogle Scholar
  11. Darcy GH, Maisel E, Ogden JC (1974) Cleaning preferences of the gobies Gobiosoma evelynae and G. prochilos and the juvenile wrasse Thalassoma bifasciatum. Copeia 1974:375–379CrossRefGoogle Scholar
  12. Dormann CF, Fruend J, Bluethgen N, Gruber B (2008) Introducing the bipartite package: Analysing ecological networks. R news 8(2):8–11Google Scholar
  13. Feitoza BM, Dias TLP, Rocha LA, Gasparini JL (2002) First record of cleaning activity in the slippery dick, Halichoeres bivittatus (Perciformes : Labridae), off northeastern Brazil. Aquat J Ichthyol Biol 5:73–76Google Scholar
  14. Ferreira CEL, Floeter SR, Gasparini JL, Ferreira BP, Joyeux JC (2004) Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J Biogeogr 31:1093–1106. CrossRefGoogle Scholar
  15. Floeter SR, Guimarães RZP, Rocha LA et al (2001) Geographic variation in reef-fish assemblages along the Brazilian coast. Glob Ecol Biogeogr 10:423–431. CrossRefGoogle Scholar
  16. Floeter SR, Ferreira CEL, Dominici-Arosemena A, Zalmon IR (2004) Latitudinal gradients in Atlantic reef fish communities: trophic structure and spatial use patterns. J Fish Biol 64:1680–1699. CrossRefGoogle Scholar
  17. Floeter SR, Krohling W, Gasparini JL, Ferreira CEL, Zalmon IR (2007a) Reef fish community structure on coastal islands of the southeastern Brazil: the influence of exposure and benthic cover. Environ Biol Fish 78:147–160. CrossRefGoogle Scholar
  18. Floeter SR, Vázquez DP, Grutter AS (2007b) The macroecology of marine cleaning mutualisms. J Anim Ecol 76:105–111. CrossRefPubMedGoogle Scholar
  19. Floeter SR, Rocha LA, Robertson DR, Joyeux JC, Smith-Vaniz WF, Wirtz P, Edwards AJ, Barreiros JP, Ferreira CEL, Gasparini JL, Brito A, Falcón JM, Bowen BW, Bernardi G (2008) Atlantic reef fish biogeography and evolution. J Biogeogr 35:22–47. CrossRefGoogle Scholar
  20. 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. CrossRefGoogle Scholar
  21. Francini-Filho RB, Sazima I (2008) A comparative study of cleaning activity of two reef fishes at Fernando de Noronha Archipelago, tropical West Atlantic. Environ Biol Fish 83(2):213–220Google Scholar
  22. Gasparini JL, Floeter SR (2001) The shore fishes of Trindade Island, western South Atlantic. J Nat Hist 35:1639–1656CrossRefGoogle Scholar
  23. Giraldes BW, Freire AS (2015) Extending the southern range of four shrimps (Crustacea: Decapoda: Stenopodidae, Hippolytidae and Alpheidae) in southwestern Atlantic (27° S) and confirming the presence of Mediterranean Stenopus spinosus Risso, 1827 in Brazil. Zootaxa 3972:419–431. CrossRefPubMedGoogle Scholar
  24. Grutter AS (2002) Cleaning symbioses from the parasites’ perspective. Parasitology 124:s61–s81. CrossRefGoogle Scholar
  25. Grutter AS (2004) Cleaner fish use tactile dancing behavior as a preconflict management strategy. Curr Biol 14:1080–1083. CrossRefPubMedGoogle Scholar
  26. Grutter AS, Poulin R (1998) Cleaning of coral reef fishes by the wrasse Labroides dimidiatus: influence of client body size and phylogeny. Copeia 1998:120–127CrossRefGoogle Scholar
  27. Grutter AS, Murphy JM, Choat JH (2003) Cleaner fish drives local fish diversity on coral reefs. Curr Biol 13:64–67. CrossRefPubMedGoogle Scholar
  28. Guimarães PR, Sazima C, dos Reis SF, Sazima I (2007) The nested structure of marine cleaning symbiosis: is it like flowers and bees? Biol Lett 3:51–54. CrossRefPubMedGoogle Scholar
  29. 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. Environ Biol Fish 23:225–232CrossRefGoogle Scholar
  30. Krajewski JP (2007) Cleaning by the occasional cleaner Diplodus argenteus (Perciformes: Sparidae) in South Brazil: why so few client species? J Mar Biol Assoc UK 87:1013–1016. CrossRefGoogle Scholar
  31. Kuwamura T (1976) Different responses of inshore fishes the the cleaning wrasse, Labroides dimidiatus, as observed in Shirahama. Publ Seto Mar Biol Lab 23:119–144CrossRefGoogle Scholar
  32. Losey GS (1972) The ecological importance of cleaning symbiosis. Copeia (4):960–970Google Scholar
  33. Luckhurst E, Luckhurst K (1978) Analysis of the influence of substrate variables on coral reef fish communities. Mar Biol 323:317–323. CrossRefGoogle Scholar
  34. Luiz OJ, Carvalho-Filho A, Ferreira CEL et al (2008) The reef fish assemblage of the Laje de Santos marine State Park, southwestern Atlantic: annotated checklist with comments on abundance, distribution, trophic structure, symbiotic associations, and conservation. Zootaxa 1807:1–25Google Scholar
  35. Moosleitner VH (1980) Putzerfische und –garnelen im Mittelmeer. Zool Anzeiger 205:219–240Google Scholar
  36. Morais RA, Brown J, Ferreira CEL et al (2017) Mob rulers and part-time cleaners: two reef fish associations at the isolated Ascension Island. J Mar Biol Assoc UK 94(4):799–811. CrossRefGoogle Scholar
  37. Narvaez P, Furtado M, Neto A, Moniz I, Azevedo JMN, Soares MC (2015) Temperate facultative cleaner wrasses selectively remove ectoparasites from their client-fish in the Azores. Mar Ecol Prog Ser 540:217–226. CrossRefGoogle Scholar
  38. Potts GW (1973) The ethology of Labroides dimidiatus (Cuv. & Val.) (Labridae) on Aldabra. Anim Behav 21:250–291CrossRefGoogle Scholar
  39. Poulin R, Grutter AS (1996) Cleaning symbioses: proximate and adaptive explanations. BioScience 46(7):512–517Google Scholar
  40. Quimbayo JP, Zapata FA, Floeter SR, Bessudo S, Sazima I (2010) First record of cleaning by a triplefin blenny in the tropical Pacific. Coral Reefs 29:909–909. CrossRefGoogle Scholar
  41. Quimbayo JP, Floeter SR, Noguchi R, Rangel CA, Gasparini JL, Sampaio CLS, Ferreira CEL, Rocha LA (2012) Cleaning mutualism in Santa Luzia (Cape Verde archipelago) and São Tomé Islands, tropical eastern Atlantic. Mar Biodivers Rec e118:5. CrossRefGoogle Scholar
  42. Quimbayo JP, Dias MS, Schlickmann OC, Mendes TC (2017a) Fish cleaning interactions on a remote island from the tropical eastern Pacific. Mar Biodivers 43:603–608. CrossRefGoogle Scholar
  43. Quimbayo JP, Nunes LT, Ozekoski R, et al. (2017b) Cleaning interactions at the only atoll in the South Atlantic. Environ Biol Fishes.
  44. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  45. Sampaio CLS, Loiola M, Colman LP, Medeiros DV, Quimbayo JP, Miranda RJ, Reis-Filho JA, Nunes JACC (2017) Cryptobenthic fish as clients of french angelfish Pomacanthus paru (Pomacanthidae) during cleaning behaviour. Mar Biodivers Rec 10:8. CrossRefGoogle Scholar
  46. Sazima I (1988) Similarities in feeding behaviour between some marine and freshwater fishes in two tropical communities. J Fish Biol 29:53–65CrossRefGoogle Scholar
  47. Sazima I, Moura RL, Rosa RS (1997) Elacatinus figaro sp. n. (Perciformes: Gobiidae), a new cleaner goby from the coast of Brazil. aqua J. Ichthyol. Aquat Biol 2:33–38Google Scholar
  48. Sazima I, Moura RL, Sazima C (1999) Cleaning activity of juvenile angelfish, Pomacanthus paru, on the reefs of the Abrolhos archipelago, western South Atlantic. Environ Biol Fish 56:399–407. CrossRefGoogle Scholar
  49. Sazima I, Sazima C, Francini-Filho RB, Moura RL (2000) Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil. Environ Biol Fish 59:69–77. CrossRefGoogle Scholar
  50. Sazima I, Carvalho-Filho A, Sazima C (2008) A new cleaner species of Elacatinus (Actinopterygii: Gobiidae) from the southwestern Atlantic. Zootaxa 1932:27–32Google Scholar
  51. Sazima C, Grossman A, Sazima I (2010a) Turtle cleaners: reef fishes foraging on epibionts of sea turtles in the tropical southwestern Atlantic, with a summary of this association type. Neotrop Ichthyol 8:187–192. CrossRefGoogle Scholar
  52. Sazima C, Guimarães PRJ, Reis SF, Sazima I (2010b) What makes a species central in a cleaning mutualism network? Oikos 119:1319–1325. CrossRefGoogle Scholar
  53. Sazima I, Krajewski JP, Bonaldo RM, Sazima C (2013) A vida dos peixes em Fernando de Noronha. Terra da Gente, Campinas, BrazilGoogle Scholar
  54. Shepherd SA, Teale J, Muirhead D (2005) Cleaning symbiosis among inshore fishas at Althorpe Island, South Australia and elsewhere. Trans Royal Soc S Aust 129:193–201Google Scholar
  55. Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246.[0235:MFATSO]2.0.CO;2Google Scholar
  56. Vaughan DB, Grutter AS, Costello MJ, Hutson KS (2017) Cleaner fishes and shrimp diversity and a re-evaluation of cleaning symbioses. Fish Fish 18(4):698–716. CrossRefGoogle Scholar
  57. Waldie PA, Blomberg SP, Cheney KL, Goldizen AW, Grutter AS (2011) Long-term effects of the cleaner fish Labroides dimidiatus on coral reef fish communities. PLoS One 6(6):e21201. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Walsh CAJ, Pinheiro HT, Rocha LA, Goodbody-Gringley G (2017) Cleaning service gaps in Bermuda, North Atlantic. Ecology 98:1973–1974. CrossRefPubMedGoogle Scholar
  59. Wicksten MK (1995) Associations of fishes and their cleaners on coral reefs of Bonaire, Netherlands Antilles. Copeia 1995:477–481CrossRefGoogle Scholar
  60. Williams AB (1984) Shrimps, lobsters, and crbs of the Altantic coast of the eastern United States, Maine to Florida. Smithson Inst Press., 8, 77
  61. Zander CD, Sötje I (2002) Seasonal and geographical differences in cleaner fish activity in the Mediterranean Sea. Helgol Mar Reser 55:232–241. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratório de Biogeografia e Macroecologia Marinha, Departamento de Ecologia e Zoologia, Centro de Ciências BiológicasUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  2. 2.Grupo de Investigación en Ecología de Arrecifes CoralinosUniversidade del ValleCaliColombia
  3. 3.Museu de ZoologiaUniversidade Estadual de CampinasCampinasBrazil

Personalised recommendations