Looking for environmental and endocrine factors inducing the transformation of Sicyopterus lagocephalus (Pallas 1770) (Teleostei: Gobiidae: Sicydiinae) freshwater prolarvae into marine larvae
During their ontogenetic development, many species of fishes undergo drastic changes which may be defined as true metamorphosis when they are induced by thyroid hormones. Sicyopterus lagocephalus is an amphidromous goby that has to change biome twice during its life cycle. The first biome shift occurs few hours after hatching in the river. The aim of the present study is to determine what external/environmental and internal/endocrine factors induce the transformation of freshwater prolarvae into marine larvae. First, we experimentally determined that the minimum salinity threshold inducing the transformation of all the prolarvae into marine larvae is 1.5, whereas a salinity of 0.2 induces the transformation of a few prolarvae. Similarly, an 18-h immersion in seawater before the return to freshwater is enough to induce the transformation of all the prolarvae into marine larvae, even though an immersion for 3 h can induce the transformation of a few prolarvae. Furthermore, we demonstrated that a simulated increase in the osmotic pressure of freshwater does not trigger the transformation of the prolarvae into marine larvae. Our study also reveals that among the various constituent salts of seawater, it is primarily NaCl and K+ that induce the transformation of the prolarvae, leading to the assumption that the membrane protein Na+/K+-ATPase is activated simultaneously with the prolarval transformation. Finally, we showed that thyroid hormones and cortisol are not involved in the prolarval transformation, leading to the conclusion that this first transformation in the life cycle of S. lagocephalus cannot be considered as a true metamorphosis.
KeywordsAmphidromy Metamorphosis Salinity Osmotic pressure Thyroid hormones Cortisol
This work was supported by the French National Museum of Natural History (MNHN) through the Action Thématique du Museum “Cycles Biologiques” funding programme. The authors thank Prof. Philippe Keith for proofing the draft and for his advices during our work. The authors thank David Lord, accredited advanced translator, for the time he spent on proofing our manuscript and for his invaluable help in improving the quality of the text. We also thank the two reviewers for their useful comments that helped us improving the quality of the manuscript.
All authors contributed to the study conception and design. Data collection was performed by CE, UW, RC and NT. The experiments were carried out by CE, UW and RC. The first draft of the manuscript was written by CE, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
- Aboussouan A (1969) Note sur les “bichiques” de l’île de la Réunion. Rec Trav Sta Mar Endoume, Fasc hors serie 9:25–31Google Scholar
- Cuvier G, Valenciennes A (1837) Histoire naturelle des poissons. Tome XII. Levrault (ed) Paris, FranceGoogle Scholar
- Delacroix P (1987) Etude des « bichiques » , juvéniles de Sicyopterus lagocephalus (Pallas), poisson Gobiidae migrateur des rivières de la Réunion (océan Indien): exploitation, répartition, biologie de la reproduction et de la croissance. Université de la Réunion, Saint Denis, La Réunion, Thesis, p 144Google Scholar
- Ellien C, Valade P, Bosmans J, Taillebois L, Teichert N, Keith P (2011) Influence of salinity on larval development of Sicyopterus lagocephalus (Pallas, 1770) (Gobioidei). Cybium 35(4):381–390Google Scholar
- Keith P, Marquet G, Valade P, Bosc P, Vigneux E (2006) Atlas des poissons et des crustacés d’eau douce des Comores, Mascareignes et Seychelles. MNHN, Paris, p 250Google Scholar
- Keith P, Hoareau T, Lord C, Ah-Yane O, Gimmoneau G, Robinet T, Valade P (2008) Characterisation of post-larval to juvenile stages, metamorphosis, and recruitment of an amphidromous goby, Sicyopterus lagocephalus (Pallas, 1767) (Teleostei: Gobiidae: Sicydiinae). Mar Fresh Res 59(10):876–889CrossRefGoogle Scholar
- Lord C, Lorion J, Dettai A, Watanabe S, Tsukamoto K, Cruaud C, Keith P (2012) Phylogeography of three amphidromous Sicyopterus species (Teleostei: Gobioidei: Sicydiinae): extensive genetic connectivity with breaks identified at biogeographical barriers. Mar Ecol Prog Ser 455:269–285CrossRefGoogle Scholar
- McDowall RM (1988) Diadromy in fishes: migrations between freshwater and marine environments. In: McDowall RM (ed) (London) Croom HelmGoogle Scholar
- Rousseau K, Dufour S (2012) Introduction to fish first and secondary metamorphoses. In: Dufour S, Rousseau K, Kapoor BG (eds) Metamorphosis in fish. CRC Press, Science Publishers, Edenbridge Ltd., Enfield, pp 1–11Google Scholar
- Sakai H, Arai T, Imai C, Sugiyama H, Sato H, Jeon SR (2004) Landlocked populations of an amphidromous goby, Rhino-gobius sp.CO. Japan. Rhino-gobius spCO Japan. J Ichthyol 51(2):175–180Google Scholar
- Sanchez-Garces GC (2017) A review of amphidromous freshwater fishes of the Choco biogeographical region (Colombia and Ecuador): diversity, ecology, fisheries and conservation. Cybium 41(2):157–169Google Scholar
- Teichert N, Valade P, Grondin H, Trichet E, Sardenne F, Gaudin P (2016) Pelagic larval traits of the amphidromous goby Sicyopterus lagocephalus display seasonal variations related to temperature in La Reunion Island. Ecol Fresh Fish 25(2):234–247. https://doi.org/10.1111/eff.12205 CrossRefGoogle Scholar
- Vaillant L (1890) Remarques sur la pêche de la Bichique à l’île de la Réunion. Compte Rendu de l’Académie des Sciences de Paris 110:93–95Google Scholar
- Valade P, Lord C, Grondin H, Bosc P, Taillebois L, Iida M, Tsukamoto K, Keith P (2009) Early life history and description of larval stages of an amphidromous goby, Sicyopterus lagocephalus (Pallas, 1767) (Teleostei: Gobiidae: Sicydiinae). Cybium 33(4):309–319Google Scholar