[en] Advancement and diversification of the aquaculture industry is reliant on the development of captive breeding and rearing protocols for novel fish species. Orbicular batfish (Platax orbicularis), a major emerging species in Polynesian aquaculture, live in brackish and marine waters around coral reefs, and are highly prized by Pacific Island communities for their high-quality meat. The present study describes the larval growth of P. orbicularis from hatching until 16 days after hatching (DAH) using meristics and thyroid hormone (T3) quantification. Our study highlighted that metamorphosis of P. orbicularis is critical to their production in aquaculture, as found for other species. Levels of the thyroid hormone T3 in P. orbicularis reached a peak at 12 DAH (i.e. hormonal metamorphosis). This peak occurred in concert with important morphological changes and increased mortality and growth between 9 and 12 DAH, clearly illustrating the sensitivity of this fish during metamorphosis. Overall, our study sheds light on the metamorphosis and larval development of a novel aquaculture species, and the interplay between hormonal and morphological changes throughout a critical period of its rearing. These findings may promote the development of protocols for mass-scale production of orbicular batfish in captivity, which may be particularly beneficial to the aquaculture industries of many Pacific Island countries.
Disciplines :
Aquatic sciences & oceanology Animal production & animal husbandry
Author, co-author :
Waqalevu, Viliame; Kagoshima University, Japan > Laboratory of Larval Rearing Management, United Graduate School of Agricultural Sciences
Besson, Marc; International Atomic Energy Agency > Environment Laboratories
Gache, Camille; PSL Research University
Roux, Natacha; PSL Research University
Fogg, Lily; University of Queensland > Queensland Brain Institute
Bertucci, Frédéric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Metian, Marc; International Atomic Energy Agency > Environment Laboratories
Lafille, Marc-André; Direction des Ressources Marines
Maamaatuaiahutapu, Moana; Direction des Ressources Marines
Gasset, Eric; Université Montpellier > MARBEC
Saulnier, Denis; IFREMER
Laudet, Vincent; Sorbonne Université > Observatoire Oc´eanologique de Banyuls-sur-Mer
Barros, B., Sakai, Y., Hashimoto, H., Gushima, K., Feeding behavior of leaf-like juveniles of the round batfish Platax orbicularis (Ephippidae) on reefs of Kuchierabu-jima Island, southern Japan. J. Ethology 26 (2008), 287–293.
Barros, B., Sakai, Y., Pereira, P.H.C., Gasset, E., Buchet, V., Maamaatuaiahutapu, M., Ready, J.S., Oliviera, Y., Giarrizzo, T., Vallinoto, M., Comparative allometric growth of the mimetic ephippid reef fishes Chaetodipterus faber and Platax orbicularis. PLoS One, 10, 2015, e0143838.
Benetti, D.D., Matera, J.A., Stevens, O.M., Alarcn, J.F., Feeley, M.W., Rotman, F.J., Minemoto, Y., Stevens, G.B., Fanke, J., Zimmerman, S., Eldridge, L., Growth, survival, and feed conversion rates of hatchery-reared mutton snapper Lutjanus analis cultured in floating cages. J. World Aquaculture Soc. 33 (2007), 349–357.
Besson, M., Salis, P., Laudet, V., Lecchini, D., Complete and rapid reversal of the body color pattern in juveniles of the convict surgeonfish Acanthurus triostegus at Moorea island (French Polynesia). Coral Reefs 37 (2018), 31–35.
Besson, M., Feeney, W., Moniz, I., François, L., Brooker, R., Holzer, G., Metian, M., Roux, N., Laudet, V., Lecchini, D., Anthropogenic stressors impact fish sensory development and survival via thyroid disruption. Nat. Comm., 11, 2020, 3614.
Björnsson, B.T., Einarsdottir, I.E., Power, D., Is salmon smoltification an example of vertebrate metamorphosis? Lessons learnt from work on flatfish larval development. Aquaculture 28 (2012), 264–272.
Blaxter, J.H.S., Hempel, G., The influence of egg size on herring larvae (Clupea harengus L.). J. Cons. Perm. Int. Explor. Mer 28 (1963), 211–240.
Blaxter, J.H.S., Staines, M.E., Food searching potential in marine fish larvae. Crisp, D.J., (eds.) Fourth European Marine Biology Symposium, 1971, University Press, Cambridge, 467–485.
Bolasina, S., Pérez, A., Yamashita, Y., Digestive enzymes activity during ontogenetic development and effect of starvation in Japanese flounder, Paralichthys olivaceus. Aquaculture 252 (2006), 503–515.
Bruno, E., Aquaculture and Feeding Ecology: Feeding Behaviour in Turbot Larvae. Phd, 2016, Technical University of Denmark, Kemitorvet, 2800, Kgs. Lyngby, Denmark.
Burbano, M.F., Torres, G.A., Prieto, M.J., Gamboa, J.H., Chapman, F.A., Increased survival of larval spotted rose snapper Lutjanus guttatus (Steindachner, 1869) when fed with the copepod Cylopina sp. And Artemia nauplii. Aquaculture 519 (2020), 1–11.
Cavalluzzi, M.R., Leis, J.M., Trnski, T., Ephippidae (Batfishes, Spadefishes). Leis, J.M., Carson-Ewart, B.M., (eds.) The Larvae of Indo-Pacific Coastal Fishes: An Identification Guide to Marine Fish Larvae, second ed., 2004, Brill, Leiden, 660–665.
Chou, R., Lee, H.B., Commercial marine fish farming in Singapore. Aqua. Res. 28 (2008), 767–776.
Dabrowski, K., The feeding of fish larvae: present “state of the art” and perspectives. Reprod. Nutr. Devel. 24 (1984), 807–833.
Datta, S.N., Kaur, V.I., Dhawan, A., Jassal, G., Estimation of length-weight relationship and condition factor of spotted snakehead Channa punctate (Bloch) under different feeding regimes. Springer Plus, 2013.
Ditty, J.G., Shaw, R.F., Cope, J.S., A re-description of Atlantic spadefish larvae, Chaetodipterus faber (family: ephippidae), and their distribution, abundance, and seasonal occurrence in the northern Gulf of Mexico. Fish. Bull. 92 (1994), 262–274.
Doherty, P.J., Dufour, V., Galzin, R., Hixon, M., Planes, S., High mortality during settlement is a population bottleneck for a tropical surgeonfish. Ecology 85 (2004), 2422–2428.
Gasset, E., Remoissenet, G., Le Paraha Peue (Platax Orbicularis), Biologie, Peche, Aquaculture Et Marché. 2011, 63 Editions Quae.
Godin, J.G.J., Behavioral Ecology of Teleost Fishes. 1997, Oxford University Press, New York.
Holt, G.J., Leu, M.Y., Callan, C.K., Erisma, B., Large angelfish and other pelagic spawners. Calado, R.O., livotto, I., Planas, M., Holt, G.J., (eds.) Marine Ornamental Species Aquaculture, 2017, John Wiley & Sons, Ltd, West Sussex, UK, 251.
Holzer, G., Laudet, V., Thyroid hormones and postembryonic development in Amniotes. Curr. Top. Develop. Biol. 103 (2013), 397–425.
Holzer, G., Laudet, V., Thyroid hormones: a triple-edged sword for life history transitions. Curr. Biol. 25 (2015), 328–347.
Holzer, G., Besson, M., Lambert, A., Francois, L., Barth, P., Gillet, B., Hughes, S., Piganeau, G., Leulier, F., Viriot, L., Laudet, V., Lecchini, D., Fish larval recruitment to reefs is a thyroid hormone-mediated metamorphosis sensitive to the pesticide chlorpyrifos. eLife, 6, 2017, e27595.
Hothorn, T., Bretz, F., Westfall, P., Simultaneous inference in general parametric models. Biom. J. 50 (2008), 346–363.
Johnson, G.D., Percoidei: development and relationship. Moser, H.G., Richards, W.J., Cohen, D.M., Fahay, M.P., Kendall, A.W. Jr., Richardson, S.L., (eds.) Ontogeny and Systematics of Fishes, 1984, American Society of Ichthyologists and Herpetologists, Allen Press, Lawrence, KS, 464–498 Special Publication No.1.
Kinoshita, I., Ephippidae. Okiyama, M., (eds.) An Atlas of Early Fishes in Japan Second Edition–II, second ed., 2014, Tokai University Press, Hadano-shi, Kanagawa, 1340–1341.
Kishimoto, H., Hayashi, M., Kohno, H., Moriyama, 0, Revision of Japanese batfishes, genus platax. Scientif. Rep. Yokosuka City Museum 36 (1988), 19–40.
Kitano, J., Lema, S.C., Luckenbach, A.J., Mori, S., Kawagishi, Y., Kusakabe, M., Swanson, P., Peichel, C.L., Adaptive divergence in the thyroid hormone signaling pathway in the stickleback radiation. Curr. Biol. 20 (2010), 2124–2130.
Kuiter, R.H., Debelius, H., Surgeonfishes, Rabbitfishes and Their Relatives: a Comprehensive Guide to Acanthuroidei. 2001, TMC publishing, Chorleywood.
Laudet, V., The origins and evolution of vertebrate metamorphosis. Curr. Biol. 21 (2011), 26–37.
Laurence, G.C., Growth and survival of haddock Melanogrammus aeglefinus larvae in relation to planktonic prey concentration. J. Fish. Res. Bd Can. 31 (1974), 1415–1419.
Le Maréchal, B., Optimisation Des Techniques De Production De Moi (Tarpon Des Sables, Polydactylus sexfilis) Réalisation De Premiers Essais d’élevage Larvaire De Paraha Peue (Poisson Lune, Platax Orbicularis). Rapport Final Convention N°3.0050 De Prestation Pour Le Service De La Pêche. 2004.
Lecchini, D., Galzin, R., Influence of pelagic and benthic, biotic and abiotic, stochastic and deterministic processes on the dynamics of auto-recruitment of coral reef fish. Cybium 27 (2003), 167–184.
Lecchini, D., Planes, S., Galzin, R., The influence of habitat characteristics and conspecifics on attraction and survival of coral reef fish juveniles. J. Exp. Mar. Biol. Ecol. 341 (2007), 85–90.
Leis, J.M., Trnski, T., The Larvae of Indo-pacific Shorefishes. 1989, Univ. Hawaii Press, Honolulu, 371.
Leu, M.Y., Tai, K.Y., Meng, P.J., Tang, C.H., Wang, P.H., Tew, K.S., Embryonic, larval and juvenile development of the longfin batfish, Platax teira (Forsskål, 1775) under controlled conditions with special regard to mitigate cannibalism for larviculture. Aquaculture 493 (2018), 204–213.
Liem, K.F., Comparative functional anatomy of the Nandidae (pisces, Teleostei). Fieldiana Zool. 56 (1970), 1–166.
Little, A.G., Kunisue, T., Kannan, K., Seebacher, F., Thyroid hormone actions are temperature-specific and regulate thermal acclimation in zebrafish (Danio rerio). BMC Biol. 11 (2013), 26–35.
Liu, O.R., Molina, R., Wilson, M., Halpern, B.S., Global opportunities for mariculture development to promote human nutrition. PeerJ, 6, 2018, e4733.
Loper, C., Pomeroy, R., Hoon, V., McConney, P., Pena, M., Sanders, A., Socioeconomic Conditions Along the World׳s Tropical Coasts: 2008 Global Coral Reef Monitoring Network/Conservation International, Townsville, Australia. 2008.
Lowe-McConnell, R.H., Ecological Studies in Tropical Fish Communities. 1987, Cambridge University Press, New York.
Masanet, P., Reproduction en aquarium de Platax orbicularis. Revue fr. Aquariol. 21 (1995), 97–105.
McCormick, S.D., Saunders, R.L., Preparatory physiological adaptations for marine life of salmonids: osmoregulation, growth, and metabolism. Am. Fish. Soc. Symp. 1 (1987), 211–229.
Moritz, C., Vii, J., Lee Long, W., Tamelander, J., Thomassin, A., Planes, S., Status and trends of coral reefs of the Pacific. GCRMN, 2018, 114.
Moteki, M., Ishikawa, T., Teraoka, N., Fushimi, H., Transition from endogenous to exogenous nutritional sources in larval red sea bream, Pagrus major. Suisanzoshoku 49 (2001), 323–328.
Pomeroy, R.S., Parks, J.E., Balboa, C.M., Farming the reef: is aquaculture a solution for reducing fishing pressure on coral reefs? Mar. Polic. 30 (2006), 111–130.
Randall, J.E., Reef and Shore Fishes of the South Pacific: New Caledonia to Tahiti and the Pitcairn Islands. 2005, University of Hawaii Press, Hawaii.
Randall, J.E., Randall, H.A., Examples of mimicry and protective resemblance in tropical marine fishes. Bull. Mar. Sci. 10 (1960), 444–480.
Reverter, M., Saulnier, D., David, R., Bardon-Albaret, A., Belliard, C., Bontemps, N., Lecchini, D., Sasal, P., Effects of local Polynesian plants and algae on growth and expression of two immune-related genes in orbicular batfish (Platax orbicularis). Fish Shellfish Immun. 58 (2016), 82–88.
Rosenthal, H., Hempel, G., Experimental studies in feeding and food requirements of herring larvae (clupea harengus L.). Steele, H., (eds.) Marine Food Chains, 1970, Oliver & Boyd, Edinburgh, 344–364.
Singh, B.K., Sinha, R.A., Yen, P.M., Novel transcriptional mechanisms for regulating metabolism by thyroid hormone. Int. J. Mol. Sci., 19, 2018, 3284.
Teruya, K., Yoseda, K., Successful mass production of early-stage larvae of kelp grouper Epinephelus bruneus in improved rearing condition. Suisan Zoshouku 54 (2006), 187–194.
Wang, C., Tzeng, W., The timing of metamorphosis and growth rates of American and European eel leptocephali: a mechanism of larval segregative migration. Fish. Res. 46 (2000), 191–205.
Waqalevu, V., Honda, A., Dossou, S., Khoa, T.N.D., Matsui, H., Mzengereza, K., Liu, H., Ishikawa, M., Shiozaki, K., Kotani, T., Effect of oil enrichment on Brachionus plicatilis rotifer and first feeding red sea bream (Pagrus major) and Japanese flounder (Paralichthys olivaceus). Aquaculture 510 (2019), 73–83.
Westernhagen, H., Rosenthal, H., On condition factor measurements in Pacific herring larvae. Helgoländer Meeresunters 34 (1981), 257–262.
Yoseda, K., Asami, K., Fukumoto, M., Takaira, S., Kurokawa, Y., Kawai, S., Effects of two types of rotifers on first-feeding success and early survival in coral trout Plectropomus leopardus larvae. Suisan Zoshouku 51 (2003), 101–108.
Yoseda, L., Yamamoto, K., Asami, K., Chimura, M., Hashimoto, K., Kosaka, S., Influence of light intensity on feeding, growth, and early survival of leopard coral grouper (Plectropomus leopardus) larvae under mass-scale rearing conditions. Aquaculture 279 (2008), 55–62.
Yu, N.H., New Challenges: Breeding Species in Taiwan. 2002, VIII. Fish Breeding Association of the Republic of China, Kaohsiung, Taiwan.
