Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Amphidromy and marine larval phase of ancestral gobioids Rhyacichthys guilberti and Protogobius attiti (Teleostei: Rhyacichthyidae)

H. Tabouret A D , M. Tomadin A , L. Taillebois A , M. Iida B , C. Lord A , C. Pécheyran C and P. Keith A
+ Author Affliations
- Author Affliations

A Biologie des Organismes et Ecosystèmes Aquatiques (UMR BOREA 7208 MNHN–CNRS–IRD–UPMC), Muséum National d’Histoire Naturelle, Département Milieux et Peuplements Aquatiques, CP-026, 43 Rue Cuvier, 75231, Paris, France.

B Faculty of Science, University of the Ryukyus, Senbaru, Nishihara, Okinawa Prefecture 903-0213, Japan.

C Laboratoire de Chimie Analytique Bio-Inorganique et Environnement, Institut des Sciences Analytiques et de Physico-Chimie pour l’Environnement et les Matériaux, UMR 5254 CNRS – Université de Pau et des Pays de l’Adour, Pau, France.

D Corresponding author. Email: tabouret@mnhn.fr

Marine and Freshwater Research 65(9) 776-783 https://doi.org/10.1071/MF13146
Submitted: 11 June 2013  Accepted: 21 November 2013   Published: 16 June 2014

Abstract

Even if amphidromous fish species contribute most to the diversity of fish communities in the tropical insular rivers, their biological cycle remain poorly known. For the first time, the otolith elemental composition and microstructure of two ancestral gobioids, Rhyacichthys guilberti and Protogobius attiti, were investigated to describe their biological cycle and pelagic larval duration (PLD). The otolith analysis using a femtosecond laser ablation coupled to an inductively coupled plasma–mass spectrometer (fs-LA-ICP-MS) revealed an amphidromous life history for R. guilberti and it suggested a progressive habitat shift from a marine habitat to a freshwater environment for P. attiti. For the first time, an endemic species, P. attiti, showed longer and more variable PLD (55.2 ± 13.5 days) than did a widespread one (R. guilberti: ~30 days). These results need to be confirmed by analysing more samples but suggest that factors other than the PLD control endemism and dispersal processes. In association with this first description of the biological cycle for both species, such an approach is a prerequisite for the management and conservation of both patrimonial species.

Additional keywords: diadromy, freshwater gobies, otolith microchemistry, tropical islands.


References

Arai, T., and Hirata, T. (2006). Differences in the trace element deposition in otoliths between marine and freshwater-resident Japanese eels, Anguilla japonica, as determined by laser ablation ICPMS. Environmental Biology of Fishes 75, 173–182.
Differences in the trace element deposition in otoliths between marine and freshwater-resident Japanese eels, Anguilla japonica, as determined by laser ablation ICPMS.CrossRef | open url image1

Bradbury, I. R., and Snelgrove, P. V. R. (2001). Contrasting larval transport in demersal fish and benthic invertebrates: the roles of behavior and advective processes in determining spatial pattern. Canadian Journal of Fisheries and Aquatic Sciences 58, 811–823.
Contrasting larval transport in demersal fish and benthic invertebrates: the roles of behavior and advective processes in determining spatial pattern.CrossRef | open url image1

Brothers, E. B., Williams, D., and Sale, P. F. (1983). Length of larval life in twelve families of fish at ‘One Tree Lagoon’, Great Barrier Reef, Australia. Marine Biology 76, 319–324.
Length of larval life in twelve families of fish at ‘One Tree Lagoon’, Great Barrier Reef, Australia.CrossRef | open url image1

Campana, S. E. (1999). Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Marine Ecology Progress Series 188, 263–297.
Chemistry and composition of fish otoliths: pathways, mechanisms and applications.CrossRef | 1:CAS:528:DC%2BD3cXjtFKmtA%3D%3D&md5=137a3d6e07f27f5ca56fde4d338c588fCAS | open url image1

Daverat, F., and Tomas, J. (2006). Tactics and demographic attributes in the European eel Anguilla anguilla in the Gironde watershed, SW France. Marine Ecology Progress Series 307, 247–257.
Tactics and demographic attributes in the European eel Anguilla anguilla in the Gironde watershed, SW France.CrossRef | open url image1

Elsdon, T. S., and Gillanders, B. M. (2005). Alternative life-history patterns of estuarine fish: barium in otoliths elucidates freshwater residency. Canadian Journal of Fisheries and Aquatic Sciences 62, 1143–1152.
Alternative life-history patterns of estuarine fish: barium in otoliths elucidates freshwater residency.CrossRef | 1:CAS:528:DC%2BD2MXoslGqs7o%3D&md5=e46c0e2d33967998a0ef75fc273db8c9CAS | open url image1

Feutry, P., Keith, P., Pécheyran, C., Claverie, F., and Robinet, T. (2011). Evidence of diadromy in the French Polynesian Kuhlia malo (Teleostei:Pecoidei) inferred from otolith microchemistry analysis. Ecology Freshwater Fish 20, 636–645.
Evidence of diadromy in the French Polynesian Kuhlia malo (Teleostei:Pecoidei) inferred from otolith microchemistry analysis.CrossRef | open url image1

Feutry, P., Tabouret, H., Maeda, K., Pécheyran, C., and Keith, P. (2012). Diadromous life cycle and behavioural plasticity in freshwater and estuarine Kuhliidae species (Teleostei) revealed by otolith microchemistry. Aquatic Biology 15, 195–204.
Diadromous life cycle and behavioural plasticity in freshwater and estuarine Kuhliidae species (Teleostei) revealed by otolith microchemistry.CrossRef | open url image1

Gillanders, B. M. (2005). Otolith chemistry to determine movements of diadromous and freshwater fish. Aquatic Living Resources 18, 291–300.
Otolith chemistry to determine movements of diadromous and freshwater fish.CrossRef | 1:CAS:528:DC%2BD2MXhtlCktb7P&md5=ea71306b6f9a33effcbdeecd4233093fCAS | open url image1

Hamer, P. A., Jenkins, G. P., and Coutin, P. (2006). Barium variation in Pagrus auratus (Sparidae) otoliths: a potential indicator of migration between an embayment and ocean waters in south-eastern Australia. Estuarine, Coastal and Shelf Science 68, 686–702.
Barium variation in Pagrus auratus (Sparidae) otoliths: a potential indicator of migration between an embayment and ocean waters in south-eastern Australia.CrossRef | open url image1

Hoese, D. F., and Gill, A. (1993). Phylogenetic relationships of eleotridid fishes (Perciformes: Gobioidei). Bulletin of Marine Science 52, 415–440. open url image1

Iida, M., Watanabe, S., Shinoda, A., and Tsukamoto, K. (2008). Recruitment of the amphidromous goby Sicyopterus japonicus to the estuary of the Ota River, Wakayama, Japan. Environmental Biology of Fishes 83, 331–341.
Recruitment of the amphidromous goby Sicyopterus japonicus to the estuary of the Ota River, Wakayama, Japan.CrossRef | open url image1

Iida, M., Watanabe, S., Yamada, Y., Lord, C., Keith, P., and Tsukamoto, K. (2010). Survival and behavioral characteristics of amphidromous goby larvae of Sicyopterus japonicus (Tanaka, 1909) during their downstream migration. Journal of Experimental Marine Biology and Ecology 383, 17–22.
Survival and behavioral characteristics of amphidromous goby larvae of Sicyopterus japonicus (Tanaka, 1909) during their downstream migration.CrossRef | open url image1

Kalish, J. M. (1990). Use of otolith microchemistry to distinguish the progeny of sympatric anadromous and non-anadromous salmonids Fishery Bulletin 88, 657–666. open url image1

Keith, P. (2002). Threatened fishes of the World: Rhyacichthys guilberti Dingerkus Séret, 1992 (Rhyacichthyidae). Environmental Biology of Fishes 63, 40.
Threatened fishes of the World: Rhyacichthys guilberti Dingerkus Séret, 1992 (Rhyacichthyidae).CrossRef | open url image1

Keith, P. (2003). Biology and ecology of amphidromous Gobiidae in the Indo-Pacific and the Caribbean regions. Journal of Fish Biology 63, 831–847.
Biology and ecology of amphidromous Gobiidae in the Indo-Pacific and the Caribbean regions.CrossRef | open url image1

Keith, P., and Lord, C. (2011). Tropical freshwater gobies: amphidromy as a life cycle. In ‘The Biology of Gobies’. (Eds. R. Patzner, J. Van Tassell, M. Kovačić and B. G. Kapoor.) pp. 243–277. (Science Publishers: Enfield, NH.)

Keith, P., Galewski, T., Cattaneo-Berrebi, G., Hoareau, T., and Berrebi, P. (2005). Ubiquity of Sicyopterus lagocephalus (Teleostei: Gobioidei) and phylogeography of the genus Sicyopterus in the Indo-Pacific area inferred from mitochondrial cytochrome b gene. Molecular Phylogenetics and Evolution 37, 721–732.
Ubiquity of Sicyopterus lagocephalus (Teleostei: Gobioidei) and phylogeography of the genus Sicyopterus in the Indo-Pacific area inferred from mitochondrial cytochrome b gene.CrossRef | 1:CAS:528:DC%2BD2MXht1SrtbjM&md5=0a04b40e2b15c2fbc293409e2dfee719CAS | 16214374PubMed | open url image1

Keith, P., Hoareau, T., Lord, C., Ah-Yane, O., Gimmoneau, G., Robinet, T., and Valade, P. (2008). Characterisation of post-larval to juvenile stages, metamorphosis and recruitments of an amphidromous goby, Sicyopterus lagocephalus (Pallas) (Teleostei: Gobiidae: Sicydiinae). Marine and Freshwater Research 59, 876–889.
Characterisation of post-larval to juvenile stages, metamorphosis and recruitments of an amphidromous goby, Sicyopterus lagocephalus (Pallas) (Teleostei: Gobiidae: Sicydiinae).CrossRef | open url image1

Keith, P., Marquet, G., Lord, C., Kalfatak, D., and Vigneux, E. (2010). ‘Vanuatu Freshwater Fish and Crustaceans.’ (Société Française d’Ichtyologie: Paris.)

Keith, P., Lord, C., Lorion, J., Watanabe, S., Tsukamoto, K., Couloux, A., and Dettai, A. (2011). Phylogeny and biogeography of Sicydiinae (Teleostei: Gobiidae) inferred from mitochondrial and nuclear genes. Marine Biology 158, 311–326.
Phylogeny and biogeography of Sicydiinae (Teleostei: Gobiidae) inferred from mitochondrial and nuclear genes.CrossRef | open url image1

Larson, H. (2012). Protogobius attiti. In ‘IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2’. Available at www.iucnredlist.org [accessed October 2012].

Lecomte-Finiger, R. (1999). L’otolithe: la ‘boite noire’ des Téléostéens L'Annee Biologique 38, 107–122.
L’otolithe: la ‘boite noire’ des TéléostéensCrossRef | open url image1

Lord, C., and Keith, P. (2006). Threatened fishes of the world: Protogobius attiti Watson and Pöllabauer, 1998 (Rhyacichthyidae) Environmental Biology of Fishes 77, 101–102.
Threatened fishes of the world: Protogobius attiti Watson and Pöllabauer, 1998 (Rhyacichthyidae)CrossRef | open url image1

Lord, C., Brun, C., Hautecœur, M., and Keith, P. (2010). Insights on endemism: comparison of the duration of the marine larval phase estimated by otolith microstructural analysis of three amphidromous Sicyopterus species (Gobiidae: Sicydiinae) from Vanuatu and New Caledonia. Ecology Freshwater Fish 19, 26–38.
Insights on endemism: comparison of the duration of the marine larval phase estimated by otolith microstructural analysis of three amphidromous Sicyopterus species (Gobiidae: Sicydiinae) from Vanuatu and New Caledonia.CrossRef | open url image1

Lord, C., Tabouret, H., Claverie, F., Pécheyran, C., and Keith, P. (2011). Femtosecond laser ablation ICP-MS measurement of otolith Sr : Ca and Ba : Ca composition reveal differential use of freshwater habitats for three amphidromous Sicyopterus (Teleostei: Gobioidei: Sicydiinae) species. Journal of Fish Biology 79, 1304–1321.
Femtosecond laser ablation ICP-MS measurement of otolith Sr : Ca and Ba : Ca composition reveal differential use of freshwater habitats for three amphidromous Sicyopterus (Teleostei: Gobioidei: Sicydiinae) species.CrossRef | 1:CAS:528:DC%2BC3MXhs1Glt7jI&md5=f49dd5f470784b82aa1ae3685c766eb6CAS | 22026607PubMed | open url image1

Maeda, K., Yamasaki, N., and Tachihara, K. (2007). Size and age at recruitment and spawning season of sleeper, genus Eleotris (Teleostei: Eleotridae) on Okinawa Island, southern Japan. The Raffles Bulletin of Zoology 14, 199–207. open url image1

Maeda, K., Mukai, T., and Tachihara, K. (2011). Newly collected specimens of the sleeper Eleotris acanthopoma (Teleostei: Eleotridae) from French Polynesia indicate a wide and panmictic distribution in the West and South Pacific. Pacific Science 65, 257–264.
Newly collected specimens of the sleeper Eleotris acanthopoma (Teleostei: Eleotridae) from French Polynesia indicate a wide and panmictic distribution in the West and South Pacific.CrossRef | open url image1

McDowall, R. M. (2007). On amphidromy, a distinct from of diadromy in aquatic organisms. Fish and Fisheries 8, 1–13.
On amphidromy, a distinct from of diadromy in aquatic organisms.CrossRef | open url image1

Murphy, C. A., and Cowan, J. H. (2007). Production, marine larval retention or dispersal, and recruitment of amphidromous Hawaiian gobioids: issues and implications. Bishop Museum Bulletin in Cultural and Environmental Studies 3, 63–74. open url image1

Panfili, J., de Pontual, H., Troadec, H., and Wright, P. J. (2002). ‘Manuel de Sclérochronologie des Poissons.’ (Ifremer-IRD: Brest, France.)

R Development Core Team (2011). ‘R: a Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna.) Available at http://www.R-project.org [accessed July 2012].

Radtke, R. L., and Kinzie, R. A. (1996). Evidence of a marine larval stage in endemic Hawaiian stream gobies from isolated high-elevation locations. Transactions of the American Fisheries Society 125, 613–621.
Evidence of a marine larval stage in endemic Hawaiian stream gobies from isolated high-elevation locations.CrossRef | open url image1

Radtke, R. L., Kinzie, R. A., and Shafer, D. J. (2001). Temporal and spatial variation in length and size at settlement of the Hawaiian amphidromous goby Lentipes concolor. Journal of Fish Biology 59, 928–938. open url image1

Secor, D. H., and Rooker, J. R. (2000). Is otolith strontium a useful scalar of life cycles in estuarine fishes? Fisheries Research 46, 359–371.
Is otolith strontium a useful scalar of life cycles in estuarine fishes?CrossRef | open url image1

Shafer, D. J. (2000). Evaluation of periodic and aperiodic otolith microchemistry and somatic-otolith scaling for use in retrospective life history analysis of a tropical marine goby, Bathygobius coalitus. Marine Ecology Progress Series 199, 217–229.
Evaluation of periodic and aperiodic otolith microchemistry and somatic-otolith scaling for use in retrospective life history analysis of a tropical marine goby, Bathygobius coalitus.CrossRef | open url image1

Shen, K. N., and Tzeng, W. N. (2002). Formation of a metamorphosis check in otolith of the amphidromous goby Sicyopterus japonicus. Marine Ecology Progress Series 228, 205–211.
Formation of a metamorphosis check in otolith of the amphidromous goby Sicyopterus japonicus.CrossRef | open url image1

Shen, K. N., and Tzeng, W. N. (2008). Reproductive strategy and recruitment dynamics of amphidromous goby Sicyopterus japonicus as revealed by otolith microstructure. Journal of Fish Biology 73, 2497–2512.
Reproductive strategy and recruitment dynamics of amphidromous goby Sicyopterus japonicus as revealed by otolith microstructure.CrossRef | open url image1

Shen, K.N., Lee, Y.C., and Tzeng, W.N. (1998). Use of otolith microchemistry to investigate the life history pattern of gobies in a Taiwanese stream. Zoological Studies 37, 322–329. open url image1

Shiao, J. C., Lozys, L., Iizuka, Y., and Tzeng, W. N. (2006). Migratory patterns and contribution of stocking to the population of European eel in Lithuanian waters as indicated by otolith Sr : Ca ratios. Journal of Fish Biology 69, 749–769.
Migratory patterns and contribution of stocking to the population of European eel in Lithuanian waters as indicated by otolith Sr : Ca ratios.CrossRef | 1:CAS:528:DC%2BD28XhtFamtLrI&md5=81be065c41d4e8f9209e151094ca3cedCAS | open url image1

Sponaugle, S., and Cowen, R. K. (1994). Larval durations and recruitment patterns of two Caribbean gobies (Gobiidae): contrasting early life histories in demersal spawners. Marine Biology 120, 133–143. open url image1

Tabouret, H., Bareille, G., Claverie, F., Pécheyran, C., Prouzet, P., and Donard, O. F. X. (2010). Simultaneous use of strontium : calcium and barium : calcium in otolith as markers of habitat: application to the European eel (Anguilla anguilla) in the Adour basin. Marine Environmental Research 70, 35–45.
Simultaneous use of strontium : calcium and barium : calcium in otolith as markers of habitat: application to the European eel (Anguilla anguilla) in the Adour basin.CrossRef | 1:CAS:528:DC%2BC3cXntVOntbk%3D&md5=ef7a49cead76f907f8c949ddd1f874c1CAS | 20338633PubMed | open url image1

Tabouret, H., Lord, C., Bareille, G., Pécheyran, C., Monti, D., and Keith, P. (2011). Otolith microchemistry in Sicydium punctatum: indices of environmental condition changes after recruitment. Aquatic Living Resources 24, 369–378.
Otolith microchemistry in Sicydium punctatum: indices of environmental condition changes after recruitment.CrossRef | open url image1

Taillebois, L. (2012). Endémisme et dispersion chez les Gobiidae Sicydiinae: traits d’histoire de vie et histoire évolutive. Ph.D. Thesis, Muséum National d’Histoire Naturelle, Paris.

Taillebois, L., Keith, P., Valade, P., Torres, P., Baloche, S., Dufour, S., and Rousseau, K. (2011). Involvement of thyroid hormones in the control of larval metamorphosis in Sicyopterus lagocephalus (Teleostei: Gobioidei) at the time of river recruitment. General and Comparative Endocrinology 173, 281–288.
Involvement of thyroid hormones in the control of larval metamorphosis in Sicyopterus lagocephalus (Teleostei: Gobioidei) at the time of river recruitment.CrossRef | 1:CAS:528:DC%2BC3MXpvFSmsL4%3D&md5=2218d82a4b7894a545f2367ef671d22cCAS | 21703271PubMed | open url image1

Taillebois, L., Maeda, K., Vigne, S., and Keith, P. (2012). Pelagic larval duration of three amphidromous Sicydiinae gobies (Teleostei: Gobioidei) including widespread and endemic species. Ecology Freshwater Fish 21, 552–559.
Pelagic larval duration of three amphidromous Sicydiinae gobies (Teleostei: Gobioidei) including widespread and endemic species.CrossRef | open url image1

Tsunagawa, T., and Arai, T. (2008). Flexible migration of Japanese freshwater gobies Rhinogobius spp. as revealed by otolith Sr : Ca ratios. Journal of Fish Biology 73, 2421–2433. open url image1

Tsunagawa, T., Suzuki, T., and Arai, T. (2010). Migratory history of Rhinogobius sp. OR morphotype ‘Shimahire’ as revealed by otolith Sr : Ca ratios. Ichthyological Research 57, 10–15.
Migratory history of Rhinogobius sp. OR morphotype ‘Shimahire’ as revealed by otolith Sr : Ca ratios.CrossRef | open url image1

Tzeng, W. N. (1996). Effects of salinity and ontogenic movements on strontium: calcium ratios in the otoliths of the Japanese eel, Anguilla japonica Temminck and Schlegel. Journal of Experimental Marine Biology and Ecology 199, 111–122.
Effects of salinity and ontogenic movements on strontium: calcium ratios in the otoliths of the Japanese eel, Anguilla japonica Temminck and Schlegel.CrossRef | 1:CAS:528:DyaK28XlsVWgtbs%3D&md5=fc854b76b7811faf986f9f11f150008aCAS | open url image1

Victor, B. C. (1986a). Delayed metamorphosis with reduced larval growth in a coral reef fish (Thalassoma bifasciatum). Canadian Journal of Fisheries and Aquatic Sciences 43, 1208–1213.
Delayed metamorphosis with reduced larval growth in a coral reef fish (Thalassoma bifasciatum).CrossRef | open url image1

Victor, B. C. (1986b). Duration of the planktonic larval stage of one hundred species of Pacific and Atlantic wrasses (Family Labridae). Marine Biology 90, 317–326.
Duration of the planktonic larval stage of one hundred species of Pacific and Atlantic wrasses (Family Labridae).CrossRef | open url image1

Wellington, G. M., and Victor, B. C. (1989). Planktonic larval duration of one hundred species of Pacific and Atlantic damselfishes (Pomacentridae). Marine Biology 101, 557–567.
Planktonic larval duration of one hundred species of Pacific and Atlantic damselfishes (Pomacentridae).CrossRef | open url image1

Wilson, D. T., and McCormick, M. I. (1999). Microstructure of settlement-marks in the otoliths of tropical reef fishes. Marine Biology 134, 29–41.
Microstructure of settlement-marks in the otoliths of tropical reef fishes.CrossRef | open url image1

Yamasaki, N., Maeda, K., and Tachihara, K. (2007). Pelagic larval duration and morphology at recruitment of Stiphodon percopterygionus (Gobiidae: Sicydiinae). The Raffles Bulletin of Zoology 14, 209–214. open url image1



Rent Article (via Deepdyve) Export Citation Cited By (2)