Hawksbill turtles visit moustached barbers: cleaning symbiosis between eretmochelys imbricata and the shrimp stenopus hispidus

Sazima, Ivan; Grossman, Alice; Sazima, Cristina

doi:10.1590/S1676-06032004000100011

Abstracts

This seems to be the first record of cleaning symbiosis between marine turtles and shrimps. During their foraging on the reef flat, the turtles regularly visited and posed at the stations. The same stations were visited by a few species of reef fishes, which posed and were cleaned by the shrimps. We suggest that cleaning symbiosis between turtles and shrimps is widespread and went unrecognised due to the superficial resemblance between a resting turtle and a posing and cleaned one. Additionally, we submit a putative origin for the cleaning symbiosis between marine turtles and cleaner shrimps following a few simple behavioural steps.

Marine turtle-cleaner shrimp association; cleaning symbiosis; origin of turtle-shrimp association; reef environment; Equatorial West Atlantic

Nas ilhas oceânicas de Fernando de Noronha, ao largo da costa Nordeste do Brasil, registramos tartarugas-de-pente (Eretmochelys imbricata) visitando estações de limpeza mantidas pelo camarão-palhaço (Stenopus hispidus). Este parece ser o primeiro registro de simbiose de limpeza entre tartarugas marinhas e camarões. Durante o seu forrageamento na planície recifal, as tartarugas visitavam e posavam nas estações regularmente. As mesmas estações eram visitadas por algumas espécies de peixes recifais, que aí posavam e eram limpas pelos camarões. Sugerimos aqui que a simbiose de limpeza entre tartarugas marinhas e camarões seja comum e difundida, porém passa despercebida devido à semelhança superficial entre uma tartaruga que esteja descansando e aquela posando e sendo limpa. Além disso, apresentamos uma origem putativa para a simbiose de limpeza entre tartarugas marinhas e camarões-limpadores, que segue etapas comportamentais relativamente simples.

Associação entre tartarugas marinhas e camarões-limpadores; Simbiose de limpeza; origem da associação tartaruga-camarão; ambiente recifal; Atlântico Equatorial Ocidental

SHORT COMMUNICATIONS

Hawksbill turtles visit moustached barbers: cleaning symbiosis between eretmochelys imbricata and the shrimp stenopus hispidus

Nas ilhas oceânicas de Fernando de Noronha, ao largo da costa Nordeste do Brasil, registramos tartarugas-de-pente (Eretmochelys imbricata) visitando estações de limpeza mantidas pelo camarão-palhaço (Stenopus hispidus)

Ivan Sazima^I,^* * Corresponding author. Tel: + 55-19-3788 7292; fax: +55-19-3289 3124; e-mail: isazima@unicamp.br ; Alice Grossman^II; Cristina Sazima^I,III

^IDepartamento de Zoologia e Museu de História Natural, Caixa Postal 6109, Universidade Estadual de Campinas, 13083-970 Campinas, São Paulo, Brazil (http://www.unicamp.br)

^IIProjeto Tamar/Ibama, Alameda Boldró s/no, 53990-000 Fernando de Noronha, Pernambuco, Brazil

^IIIDepartamento de Zoologia, Caixa Postal 199, Universidade Estadual Paulista, 13506-900 Rio Claro, São Paulo, Brazil

ABSTRACT

This seems to be the first record of cleaning symbiosis between marine turtles and shrimps. During their foraging on the reef flat, the turtles regularly visited and posed at the stations. The same stations were visited by a few species of reef fishes, which posed and were cleaned by the shrimps. We suggest that cleaning symbiosis between turtles and shrimps is widespread and went unrecognised due to the superficial resemblance between a resting turtle and a posing and cleaned one. Additionally, we submit a putative origin for the cleaning symbiosis between marine turtles and cleaner shrimps following a few simple behavioural steps.

Key words: Marine turtle-cleaner shrimp association, cleaning symbiosis, origin of turtle-shrimp association, reef environment, Equatorial West Atlantic

RESUMO

Nas ilhas oceânicas de Fernando de Noronha, ao largo da costa Nordeste do Brasil, registramos tartarugas-de-pente (Eretmochelys imbricata) visitando estações de limpeza mantidas pelo camarão-palhaço (Stenopus hispidus). Este parece ser o primeiro registro de simbiose de limpeza entre tartarugas marinhas e camarões. Durante o seu forrageamento na planície recifal, as tartarugas visitavam e posavam nas estações regularmente. As mesmas estações eram visitadas por algumas espécies de peixes recifais, que aí posavam e eram limpas pelos camarões. Sugerimos aqui que a simbiose de limpeza entre tartarugas marinhas e camarões seja comum e difundida, porém passa despercebida devido à semelhança superficial entre uma tartaruga que esteja descansando e aquela posando e sendo limpa. Além disso, apresentamos uma origem putativa para a simbiose de limpeza entre tartarugas marinhas e camarões-limpadores, que segue etapas comportamentais relativamente simples.

Palavras-chave: Associação entre tartarugas marinhas e camarões-limpadores, Simbiose de limpeza, origem da associação tartaruga-camarão, ambiente recifal, Atlântico Equatorial Ocidental

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6. References

Date Received 01/21/2004

Revised 02/22/2004

Accepted 03/12/2004

ALTMANN, J. 1974. Observational study of behavior: sampling methods. Behavior 49:227-265.
BOOTH, J. & PETERS, J. A. 1972. Behavioural studies on the green turtle (Chelonia mydas) in the sea. Anim. Behav. 20:808-812.
CÔTÉ, I. M. 2000. Evolution and ecology of cleaning symbioses in the sea. In: Oceanography and Marine Biology: an Annual Review 38 (R. N. Gibson & M. Barnes, eds.). Taylor and Francis, London, p. 311-355.
CRIALES, M. M. & CORREDOR, L. 1977. Aspectos etologicos y ecologicos de camarones limpiadores de peces (Natantia: Palaemonidae, Hyppolytidae, Stenopodidae). An. Inst. Inv. Mar. - Punta Betín 9:141-156.
FRANCINI-FILHO, R. B. MOURA, R. L. & SAZIMA, I. 1999. Simbiose de limpeza envolvendo peixes e camarões no Arquipélago de Fernando de Noronha, Pernambuco. Resumos XIII Encontro Brasileiro de Ictiologia, São Carlos: 137
FRANCINI-FILHO, R. B. MOURA, R. L. & 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.
HUMANN, P. 1996. Reef creature identification: Florida, Caribbean, Bahamas. New World Publications, Jacksonville.
LEHNER, P.N. 1979. Handbook of ethological methods. Garland STPM Press, New York.
LIMBAUGH, C., PEDERSON, H., CHACE-Jr., F. A. 1961. Shrimps that clean fishes. Bull. Mar. Sci. Gulf & Carib. 11:237-257.
LOSEY, G. S. 1979. Fish cleaning symbiosis: proximate causes of host behaviour. Anim. Behav. 27:669-685.
LOSEY, G. S. 1993. Knowledge of proximate causes aids our understanding of function and evolutionary history. Mar. Behav. Physiol. 23:175-186.
LOSEY, G. S., BALAZS, G. H. & PRIVITERA, L. A. 1994. Cleaning symbiosis between the wrasse Thalassoma duperrey, and the green turtle Chelonia mydas Copeia 1994:684-690.
MAIDA, M. & FERREIRA, B.P. 1997. Coral reefs of Brazil: an overview. Proc. Int. Coral Reef Symp. 8:263-274.
MAIDA, M., FERREIRA, B.P. & BELLINI, C. 1995. Avaliação preliminar do recife da Baía do Sueste, Fernando de Noronha, com ênfase nos corais escleractíneos. Bol. Téc. Cient. CEPENE 3:37-47.
MEYLAN, A. B. & DONNELLY, M. 1999. Status justification for listing the hawksbill turtle (Eretmochelys imbricata) as critically endangered on the 1996 IUCN Red List of Threatened Animals. Chelon. Conserv. Biol. 3:200-224.
SANCHES, T. M. & BELLINI, C. 1999. Juvenile Eretmochelys imbricata and Chelonia mydas in the Archipelago of Fernando de Noronha, Brazil. Chelon. Conserv. Biol. 3:308-311.
SAZIMA, C. , GROSSMAN, A., BELLINI, C. & SAZIMA, I. 2004. The moving gardens: reef fishes grazing, cleaning, and following green turtles. Cybium 28(1):47-53.
SAZIMA, I. & MOURA, R. L. 2000. Shark (Carcharhinus perezi), cleaned by the goby (Elacatinus randalli), at Fernando de Noronha Archipelago, western South Atlantic. Copeia 2000:297-299.
SAZIMA, I., MOURA, R. L., SAZIMA, C. 1999. Cleaning activity of juvenile angelfish, Pomacanthus paru, on the reefs of the Abrolhos Archipelago, Western South Atlantic. Env. Biol. Fish. 56:399-407.
SMITH, S. H. 1988. Cleaning of the hawksbill turtle (Eretmochelys imbricata) by adult french angelfish (Pomacanthus paru). Herp. Review 19:55.
VAN TASSEL, J. L., BRITO, A. & BORTONE, S. A. 1994. Cleaning behavior among marine fishes and invertebrates in the Canary Islands. Cybium 18:117-127.
WITZELL, W. N. 1983. Synopsis of the biological data on the hawksbill turtle Eretmochelys imbricata (Linnaeus, 1766). FAO Fish. Syn. 137:1-78.

*

Corresponding author. Tel: + 55-19-3788 7292; fax: +55-19-3289 3124; e-mail:

isazima@unicamp.br

Publication Dates

Publication in this collection
10 June 2013
Date of issue
2004

History

Accepted
03 Dec 2004
Reviewed
22 Feb 2004
Received
21 Jan 2004

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] ALTMANN, J. 1974. Observational study of behavior: sampling methods. Behavior 49:227-265.

[2] BOOTH, J. & PETERS, J. A. 1972. Behavioural studies on the green turtle (Chelonia mydas) in the sea. Anim. Behav. 20:808-812.

[3] CÔTÉ, I. M. 2000. Evolution and ecology of cleaning symbioses in the sea. In: Oceanography and Marine Biology: an Annual Review 38 (R. N. Gibson & M. Barnes, eds.). Taylor and Francis, London, p. 311-355.

[4] CRIALES, M. M. & CORREDOR, L. 1977. Aspectos etologicos y ecologicos de camarones limpiadores de peces (Natantia: Palaemonidae, Hyppolytidae, Stenopodidae). An. Inst. Inv. Mar. - Punta Betín 9:141-156.

[5] FRANCINI-FILHO, R. B. MOURA, R. L. & SAZIMA, I. 1999. Simbiose de limpeza envolvendo peixes e camarões no Arquipélago de Fernando de Noronha, Pernambuco. Resumos XIII Encontro Brasileiro de Ictiologia, São Carlos: 137

[6] FRANCINI-FILHO, R. B. MOURA, R. L. & 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.

[7] HUMANN, P. 1996. Reef creature identification: Florida, Caribbean, Bahamas. New World Publications, Jacksonville.

[8] LEHNER, P.N. 1979. Handbook of ethological methods. Garland STPM Press, New York.

[9] LIMBAUGH, C., PEDERSON, H., CHACE-Jr., F. A. 1961. Shrimps that clean fishes. Bull. Mar. Sci. Gulf & Carib. 11:237-257.

[10] LOSEY, G. S. 1979. Fish cleaning symbiosis: proximate causes of host behaviour. Anim. Behav. 27:669-685.

[11] LOSEY, G. S. 1993. Knowledge of proximate causes aids our understanding of function and evolutionary history. Mar. Behav. Physiol. 23:175-186.

[12] LOSEY, G. S., BALAZS, G. H. & PRIVITERA, L. A. 1994. Cleaning symbiosis between the wrasse Thalassoma duperrey, and the green turtle Chelonia mydas Copeia 1994:684-690.

[13] MAIDA, M. & FERREIRA, B.P. 1997. Coral reefs of Brazil: an overview. Proc. Int. Coral Reef Symp. 8:263-274.

[14] MAIDA, M., FERREIRA, B.P. & BELLINI, C. 1995. Avaliação preliminar do recife da Baía do Sueste, Fernando de Noronha, com ênfase nos corais escleractíneos. Bol. Téc. Cient. CEPENE 3:37-47.

[15] MEYLAN, A. B. & DONNELLY, M. 1999. Status justification for listing the hawksbill turtle (Eretmochelys imbricata) as critically endangered on the 1996 IUCN Red List of Threatened Animals. Chelon. Conserv. Biol. 3:200-224.

[16] SANCHES, T. M. & BELLINI, C. 1999. Juvenile Eretmochelys imbricata and Chelonia mydas in the Archipelago of Fernando de Noronha, Brazil. Chelon. Conserv. Biol. 3:308-311.

[17] SAZIMA, C. , GROSSMAN, A., BELLINI, C. & SAZIMA, I. 2004. The moving gardens: reef fishes grazing, cleaning, and following green turtles. Cybium 28(1):47-53.

[18] SAZIMA, I. & MOURA, R. L. 2000. Shark (Carcharhinus perezi), cleaned by the goby (Elacatinus randalli), at Fernando de Noronha Archipelago, western South Atlantic. Copeia 2000:297-299.

[19] SAZIMA, I., MOURA, R. L., SAZIMA, C. 1999. Cleaning activity of juvenile angelfish, Pomacanthus paru, on the reefs of the Abrolhos Archipelago, Western South Atlantic. Env. Biol. Fish. 56:399-407.

[20] SMITH, S. H. 1988. Cleaning of the hawksbill turtle (Eretmochelys imbricata) by adult french angelfish (Pomacanthus paru). Herp. Review 19:55.

[21] VAN TASSEL, J. L., BRITO, A. & BORTONE, S. A. 1994. Cleaning behavior among marine fishes and invertebrates in the Canary Islands. Cybium 18:117-127.

[22] WITZELL, W. N. 1983. Synopsis of the biological data on the hawksbill turtle Eretmochelys imbricata (Linnaeus, 1766). FAO Fish. Syn. 137:1-78.