Symbiotic relationship between the carapid fish Onuxodon fowleri (Ophidiiformes: Carapidae) and the pearl oyster Pinctada margaritifera (Mollusca: Bivalvia: Pteriidae)

Authors

DOI:

https://doi.org/10.3989/scimar.04627.04A

Keywords:

symbiosis, stable isotopes, diet, pearl oyster, Carapidae

Abstract


At Makemo Atoll (French Polynesia), the carapid fish Onuxodon fowleri lives in symbiosis with the black-lip pearl oyster Pinctada margaritifera. Although the symbiont seems to live inside its host bivalve by using it as a shelter, additional data are still needed to better understand the exact nature of this association. For this purpose, we implemented an approach using stable isotope ratios of carbon (13C/12C) and nitrogen (15N/14N). The δ13C and δ15N values were measured in tissues of the pearl oyster (gonads, gills, mantle and muscles), white muscle tissue from the fish and other food sources. This stable isotope approach was also complemented by the analysis of stomach contents in the carapid fish. Overall, the isotopic compositions measured in the present study support a commensal relationship between O. fowleri and P. margaritifera. In addition, our isotopic data bring new information about another guest living inside P. margaritifera, namely the palaemonid shrimp Conchodytes meleagrinae. Based on the δ13C and δ15N values, it appears that the shrimp might feed on the bivalve gonads.

Downloads

Download data is not yet available.

References

Bierbaum R.M., Ferson S. 1986. Do symbiotic pea crabs decrease growth rate in mussels? Biol. Bull. 170: 51-61. https://doi.org/10.2307/1541380

Bruce A.J. 1976. Shrimps and prawns of coral reefs, with special reference to commensalism. In: Jones O.A., Dean R.M. (eds), Biology and geology of coral reefs. Academic Press, New York, pp. 37-94. https://doi.org/10.1016/B978-0-12-395527-2.50009-3

Cabanellas-Reboredo M., Blanco A., Deudero S., et al. 2010. Effects of the invasive macroalga Lophocladia lallemandii on the diet and trophism of Pinna nobilis (Mollusca: Bivalvia) and its guests Potonia pinnophylax and Nepinnotheres pinnotheres (Crustacea: Decapoda). Sci. Mar. 74: 101-110. https://doi.org/10.3989/scimar.2010.74n1101

Colleye O., Brié C., Malpot E., et al. 2008. Temporal variability of settlement in Carapidae larvae at Rangiroa atoll. Env. Biol. Fish. 81: 277-285. https://doi.org/10.1007/s10641-007-9199-4

de Bary A. 1879. Die erscheinung der symbiose. Verlag von Karl J. Trubner, Strassburg.

DeNiro M.J., Epstein S. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42: 495-506. https://doi.org/10.1016/0016-7037(78)90199-0

DeNiro M.J., Epstein S. 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 45: 341-351. https://doi.org/10.1016/0016-7037(81)90244-1

Fowler H.W. 1927. Fishes of the tropical central Pacific. B. P. Bishop. Mus. Bull. 38: 1-32.

Frédérich B., Fabry G., Lepoint G., et al. 2009. Trophic niches of thirteen damselfishes (Pomacentridae) at the Grand Récif of Toliara, Madagascar. Ichthyol. Res. 56: 10-17. https://doi.org/10.1007/s10228-008-0053-2

Frédérich B., Colleye O., Lepoint G., et al. 2012. Mismatch between shape changes and ecological shifts during the post-settlement growth of the surgeonfish, Acanthurus triostegus. Front. Zool. 9: 8. https://doi.org/10.1186/1742-9994-9-8

Gervis M.H., Sims N.A. 1992. The Biology and Culture of Pearl Oysters (Bivalvia: Pteriidae). ICLARM Stud. Rev. 21: 1-56.

Guo W., Yang Y., Wu L., et al. 2002. Carbon isotope study on trophic relationships of Zhubi reef ecosystem in Nansha Islands. J. Oceanogr. Taiwan 21: 94-101.

Haines C.M.C., Edmunds M., Pewsey A.R. 1994. The pea crab, Pinnotheres pisum (Linnaeus, 1767), and its association with the common mussel, Mytilus edulis (Linnaeus, 1758), in the solent (UK). J. Shellfish. Res. 13: 5-10.

Kéver L., Colleye O., Lugli M., et al. 2014. Sound production in Onuxodon fowleri (Carapidae) and its amplification by the host shell. J. Exp. Biol. 217: 4283-4294. https://doi.org/10.1242/jeb.109363 PMid:25520383

Leis J.M. 1991. The pelagic stage of reef fishes: the larval biology of coral reef fishes. In: Sale P.F. (ed.), The ecology of fishes on coral reefs. Academic Press, San Diego, pp. 183-230. https://doi.org/10.1016/B978-0-08-092551-6.50013-1

Leis J.M., McCormick M.I. 2002. The Biology, Behavior, and Ecology of the Pelagic, Larval Stage of Coral Reef Fishes. In: Sale P.F. (ed.), Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem. Academic Press, San Diego, pp. 171-200. https://doi.org/10.1016/B978-012615185-5/50011-6

Markle D.F., Olney J.E. 1990. Systematics of the pearlfishes (Pisces: Carapidae). Bull. Mar. Sci. 47: 269-410.

Parmentier E. 2016. Further insights into the metamorphosis process of a carapid fish. J. Zool. 298: 249-256. https://doi.org/10.1111/jzo.12314

Parmentier E., Das K. 2004. Commensal vs. parasitic relationship between Carapini fish and their hosts: Some further insight through ?13C and ?15N measurements. J. Exp. Mar. Biol. Ecol. 310: 47-58. https://doi.org/10.1016/j.jembe.2004.03.019

Parmentier E., Michel L. 2013. Boundary lines in symbiosis forms. Symbiosis 60: 1-5. https://doi.org/10.1007/s13199-013-0236-0

Parmentier E., Chardon M., Poulicek M., et al. 1998. Morphology of the buccal apparatus and related structures in four species of Carapidae. Aust. J. Zool. 46: 391-404. https://doi.org/10.1071/ZO97035

Parmentier E., Chardon M., Poulicek M., et al. 1999. Morphological particularities of the head in four Carapidae (Ophidiiformes). In: Séret B., Sire J.Y. (eds), Proc. 5th Indo-Pacific Conf, Nouméa, 1997. Soc. Fr. Ichthyol., pp. 135-146.

Parmentier E., Castro-Aguirre J.L., Vandewalle P. 2000. Morphological comparison of the buccal apparatus in two bivalve commensal Teleostei, Encheliophis dubius and Onuxodon fowleri (Ophidiiformes, Carapidae). Zoomorphology 120: 29-37. https://doi.org/10.1007/s004359900020

Parmentier E., Lagardère F., Vandewalle P. 2002. Relationships between inner ear and sagitta growth during ontogenesis of three Carapini species and consequences of life-history events on the otolith microstructure. Mar. Biol. 141: 491-501. https://doi.org/10.1007/s00227-002-0853-2

Parmentier E., Lecchini D., Vandewalle P. 2004a. Remodelling of the vertebral axis during metamorphic shrinkage in the pearlfish. J. Fish. Biol. 64: 159-169. https://doi.org/10.1111/j.1095-8649.2004.00294.x

Parmentier E., Lecchini D., Lagardère F., et al. 2004b. Ontogenic and ecological control of metamorphosis onset in a carapid fish, Carapus homei: experimental evidence from vertebra and otolith comparisons. J. Exp. Zool. Part A 301: 617-628. https://doi.org/10.1002/jez.a.50 PMid:15286941

Peterson B.J., Fry B. 1987. Stable isotopes in ecosystem studies. Ann. Rev. Ecolog. Syst. 18: 293-320. https://doi.org/10.1146/annurev.es.18.110187.001453

Pinnegar J.K., Polunin N.V.C. 1999. Differential of ?13C and ?15N among fish tissues: implications for the study of trophic interactions. Funct. Ecol. 13: 225-231. https://doi.org/10.1046/j.1365-2435.1999.00301.x

Poupin J. 1998. Crustacea Decapoda and Stromatopoda of French Polynesia. Atoll Res. Bull. 451: 1-62. https://doi.org/10.5479/si.00775630.451.1

Ruppert E.E., Fox R.S., Barnes R.D. 2004. Invertebrate Zoology, A functional Evolutionary Approach. Brooks/Cole – Thomson Learning Inc., Belmont, CA, USA, 963 pp.

Salvat B. 2009. Dominant benthic mollusks in closed atolls, French Polynesia. J. Coral Reef Stud. 11: 197-206. https://doi.org/10.3755/galaxea.11.197

Smith C.L. 1964. Some Pearlfishes from Guam, with Notes on Their Ecology. Pac. Sci. 18: 34-40.

Smith C.L., Tyler J.C., Feinberg M.N. 1981. Population ecology and biology of the pearlfish (Carapus bermudensis) in the lagoon at Bimini, Bahamas. Bull. Mar. Sci. 31: 876-902.

Southgate P.C., Lucas J.S. 2008. The Pearl Oyster. Elsevier, Amsterdam, The Netherlands.

Stauber L.A. 1945. Pinnotheres ostreum, parasitic on the American oyster, Ostrea (Gryphaea) virginica. Biol. Bull. 88: 269-291. https://doi.org/10.2307/1538315

Trott L.B. 1970. Contribution of the biology of carapid fishes (Paracanthopterygian: Gadiformes). Univ. Calif. Publ. Zool. 89: 1-41.

Trott L.B. 1981. A general review of the pearlfishes (Pisces, Carapidae). Bull. Mar. Sci. 31: 623-629.

Trott L.B., Trott E.B. 1972. Pearlfishes (Carapidae: Gadiformes) collected from Puerto Galera, Minobra, Philippines. Copeia 1972: 839-843. https://doi.org/10.2307/1442743

Tyler J.C. 1970. A redescription of the inquiline carapid fish Onuxodon parvibrachium, with a discussion of the skull structure and the host. Bull. Mar. Sci. 29: 148-164.

Vahirua-Lechat I., Laure F., LeCoz J.R., et al. 2008. Changes in fatty acid and sterol composition during oogenesis in the pearl oyster Pinctada margaritifera. Aquacult. Res. 39: 1739-1746. https://doi.org/10.1111/j.1365-2109.2008.02050.x

Vanden Spiegel D., Jangoux M. 1989. La symbiose entre poissons Carapidae et holothuries autour de l'île de Laing (Mer de Bismarck, Papouasie Nouvelle-Guinée). Indo-Malayan Zool. 6: 223-228.

Vander Zanden M.J., Hulshof M. 1998. Application of stable isotope techniques to trophic studies of age-0 smallmouth bass. Trans. Am. Fish. Soc. 127: 729-739. https://doi.org/10.1577/1548-8659(1998)127<0729:AOSITT>2.0.CO;2

Wyatt A.S.J., Waite A.M., Humphries S. 2010. Variability in Isotope Discrimination Factor in Coral Reef Fishes: Implications for Diet and Food Web Reconstruction. PLoS ONE 5: e13682. https://doi.org/10.1371/journal.pone.0013682 PMid:21060681 PMCid:PMC2965116

Published

2018-03-30

How to Cite

1.
Colleye O, Kéver L, Lepoint G, Lecchini D, Parmentier E. Symbiotic relationship between the carapid fish Onuxodon fowleri (Ophidiiformes: Carapidae) and the pearl oyster Pinctada margaritifera (Mollusca: Bivalvia: Pteriidae). Sci. mar. [Internet]. 2018Mar.30 [cited 2024Mar.29];82(1):35-41. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1746

Issue

Section

Articles