The importance of thermoperiod for proper gametogenesis and successful egg and sperm production in meagre (Argyrosomus regius) breeders in aquaculture

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Published: Mar 31, 2021
DOI: https://doi.org/10.12681/mms.25806
Keywords:
Argyrosomus regius GnRHa spawning temperature gametogenesis sperm quality.
PAULO H. DE MELLO
Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, Crete, Greece São Paulo State University – Aquaculture Center, Jaboticabal, São Paulo, Brazil
https://orcid.org/0000-0003-3815-2504
STEFANO LANCEROTTO
Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, Crete, Greece University of Crete, Department of Biology, Heraklion, Crete, Greece
IOANNIS FAKRIADIS
Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, Crete, Greece
PANAGIOTA TSOUKALI
Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, Crete, Greece
MARIA PAPADAKI
Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, Crete, Greece
CONSTANTINOS CHRYSANTHOS MYLONAS
Institute of Marine Biology, Biotechnology and Aquaculture (IMBBC),Hellenic Center for Marine Research (HCMR), Greece
https://orcid.org/0000-0003-1805-4392
Abstract

We examined the effect of constant water temperature throughout the year on gametogenesis, spawning success and egg/sperm/embryo quality in meagre (Argyrosomus regius). Two broodstocks were exposed to simulated natural photoperiod, and either attenuated seasonal water temperature (SeasT, 16.4 to 19.6ºC) or relatively constant water temperature (CoT, 19.4 ± 0.6ºC).In the spawning period (May), 4 couples per group were induced to spawn with gonadotropin releasing hormone agonist (GnRHa). Gonadal stage of development, sperm quality parameters and plasma levels of sex steroids were evaluated prior to the GnRHa treatment. Spawning success and egg/sperm quality were examined over the following 4 weeks. Constant temperature did not prevent gametogenesis, but exposure to attenuated seasonal water temperature with the inclusion of winter low temperature was beneficial to both sexes. The mean (±SD) diameter of the largest vitellogenic oocytes prior to GnRHa administration was significantly higher in the SeasT compared to the CoT group (598 ± 27 vs 520 ± 17 μm). Testosterone plasma levels in the females were significantly higher in the SeasT group, but all other hormones were similar in both sexes. SeasT females spawned more consistently with higher relative fecundity, and 24-h embryo survival of the produced eggs. A more pronounced negative effect of constant water temperature was observed in males, since CoT males exhibited a spermiation index of 0 prior to GnRHa treatment, the latter clearly having a beneficial effect over the following 4 weeks. The study demonstrated that meagre do undergo gametogenesis to a significant extent even under constant water temperatures during the year. However, a seasonal thermal regime -even an attenuated one- was necessary for the proper development of the gametes, allowing for the successful spawning induction using the established GnRHa induction protocol.

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Author Biography
CONSTANTINOS CHRYSANTHOS MYLONAS, Institute of Marine Biology, Biotechnology and Aquaculture (IMBBC),Hellenic Center for Marine Research (HCMR), Greece

Director

Institute of Marine Biology, Biotechnology and Aquaculture (IMBBC)

References
Anderson, K., Swanson, P., Pankhurst, N., King, H., Elizur, A., 2012. Effect of thermal challenge on plasma gonadotropin levels and ovarian steroidogenesis in female maiden and repeat spawning Tasmanian Atlantic salmon (Salmo salar). Aquaculture. 334-337, 205-212.
Anonymous, 1998. Guidelines for the treatment of animals in behavioural research and teaching. Animal Behaviour. 55, 251-257.
Beirão, J., Soares, F., Herráez, M.P., Dinis, M.T., Cabrita, E., 2011. Changes in Solea senegalensis sperm quality throughout the year. Animal Reproduction Science. 126, 122-129.
Bennett, H.S., Wyrick, A.D., Lee, S.W., McNeil, J.H., 1976. Science and art in preparing tissues embedded in plastic for light microscopy, with special reference to glycol methacrylate, glass knives and simple stains. Stain Technology. 51, 71-97.
Bromage, N., Porter, M., Randall, C., 2001. The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture. 197, 63-98.
Bromage, N.R., Roberts, R.J., 1995. Broodstock Management and Egg and Larval Quality. Blackwell Science, Oxford, 424 pp.
Brown, N.P., Shields, R.J., Bromage, N.R., 2006. The influence of water temperature on spawning patterns and egg quality in the Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture. 261, 993-1002.
Cárdenas, S., 2010. Crianza de la Corvina (Argyrosomus regius). Fundación Observatorio Español de Acuicultura, Madrid, Spain, 96 pp.
Carrillo, M., Bromage, N., Zanuy, S., Serrano, R., Prat, F., 1989. The effect of modifications in photoperiod on spawning time, ovarian development and egg quality in the sea bass (Dicentrarchus labrax L.). Aquaculture. 81, 351-365.
Carrillo, M., Zanuy, S., Prat, F., Cerda, J., Ramos, J. et al., 1995. Sea bass (Dicentrarchus labrax). p. 138-168 In: Broodstock Management and Egg and Larval Quality. Bromage, N.R., and Roberts, R.J. (Eds.). Blackwell Science, Oxford.
Cejko, B.I., Judycka, S., Juchno, D., Boroń, A., Leska, A. et al., 2016. Hormonal treatment affects sperm motility in the spined loach (Cobitis taenia, Pisces, Cobitidae). Aquaculture Research, n/a-n/a.
Cerdá, J., Zanuy, S., Carrillo, M., Ramos, J., Serrano, R., 1995. Short- and long-term dietery effects on female sea bass (Dicentrarchus labrax): seasonal changes in plasma profiles of lipids and sex steroids in relation to reproduction. Comparative Biochemistry and Physiology. 111C, 83-91.
Chatzifotis, S., Panagiotidou, M., Papaioannou, N., Pavlidis, M., Nengas, I. et al., 2010. Effect of dietary lipid levels on growth, feed utilization, body composition and serum metabolites of meagre (Argyrosomus regius) juveniles. Aquaculture. 307, 65-70.
Clark, R.W., Henderson-Arzapalo, A., Sullivan, C.V., 2005. Disparate effects of constant and annually-cycling daylength and water temperature on reproductive maturation of striped bass (Morone saxatilis). Aquaculture. 249, 497-513.
Cuisset, B., Pradelles, P., Kime, D.E., Kühn, E.R., Babin, P. et al., 1994. Enzyme immunoassay for 11-ketotestosterone using acetylcholinesterase as label: application to the measurement of 11-ketotestosterone in plasma of Siberian sturgeon. Comparative Biochemistry and Physiology. 108C, 229-241.
Donelson, J.M., Munday, P.L., McCormick, M.I., Pankhurst, N.W., Pankhurst, P.M., 2010. Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish. Marine Ecology Progress Series. 401, 233-243.
Duncan, N.J., Estévez, A., Fernández-Palacios, H., Gairin, I., Hernández-Cruz, C.M. et al., 2013. Aquaculture production of meagre (Argyrosomus regius): hatchery techniques, ongrowing and market. p. 519-541 In: Advances in Aquaculture Hatchery Technology. Allan, G., and Burnell, G. (Eds.). Woodhead Publishing Limited, Cambridge, UK.
Duncan, N.J., Mylonas, C.C., Milton Sullon, E., Karamanlidis, D., França Nogueira, M.C. et al., 2018. Paired spawning with male rotation of meagre Argyrosomus regius using GnRHa injections, as a method for producing multiple families for breeding selection programs. Aquaculture. 495, 506-512.
Duncan, N.J., Estévez, A., Porta, J., Carazo, I., Norambuena, F. et al., 2012. Reproductive development, GnRHa-induced spawning and egg quality of wild meagre (Argyrosomus regius) acclimatised to captivity. Fish Physiology and Biochemistry. 38, 1273-1286.
Durant, J.M., Hjermann, D.Ø., Ottersen, G., Stenseth, N.S., 2007. Climate and the match or mismatch between predator requirements and resource availability. Climate Research. 33, 271-283.
Elisio, M., Chalde, T., Miranda, L.A., 2012. Effects of short periods of warm water fluctuations on reproductive endocrine axis of the pejerrey (Odontesthes bonariensis) spawning. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 163(1), 47-55.
EU, 2010. Directive 2010/63/EU of the European parliament and the council of 22 September 2010 on the protection of animals used for scientific purposes. Official Journal of the European Union. L 276, 33-79.
Fakriadis, I., Zanatta, E.M., Fleck, R., Sena Mateo, D.L., Papadaki, M. et al., 2020. Endocrine regulation of long-term enhancement of spermiation in meagre (Argyrosomus regius) with GnRHa controlled-delivery systems. Gen Comp Endocrinol. 297, 113549.
Falcon, J., Migaud, H., MuÒoz-Cueto, J.A., Carrillo, M., 2010. Current knowledge on the melatonin system in teleost fish. General and Comparative Endocrinology. 165, 469-482.
Fenkes, M., Fitzpatrick, J.L., Ozolina, K., Shiels, H.A., Nudds, R.L., 2017. Sperm in hot water: direct and indirect thermal challenges interact to impact on brown trout sperm quality. Journal of Experimental Biology, 220 (14), 2513-2520.
Fernández-Palacios, H., Schuchardt, D., Roo, J., Izquierdo, M., Hernández-Cruz, C. et al., 2014. Dose dependent effect of a single GnRHa injection on the spawning of meagre (Argyrosomus regius) broodstock reared in captivity. Spanish Journal of Agricultural Research. 12, 1038-1048.
Gordoa, A., Carreras, G., 2014. Determination of Temporal Spawning Patterns and Hatching Time in Response to Temperature of Atlantic Bluefin Tuna (Thunnus thynnus) in the Western Mediterranean. PLoS ONE. 9, e90691.
Grigorakis, K., Fountoulaki, E., Vasilaki, A., Mittakos, I., Nathanailides, C., 2011. Lipid quality and filleting yield of reared meagre (Argyrosomus regius). International Journal of Food Science and Technology. 46, 711-716.
Hani, Y.M.I., Turies, C., Palluel, O., Delahaut, L., Bado-Nilles, A. et al., 2019. Effects of a chronic exposure to different water temperatures and/or to an environmental cadmium concentration on the reproduction of the threespine stickleback (Gasterosteus aculeatus). Ecotoxicology and environmental safety 174, 48-57.
Hermelink, B., Wuertz, S., Trubiroha, A., Rennert, B., Kloas, W. et al., 2011. Influence of temperature on puberty and maturation of pikeperch, Sander lucioperca. General and Comparative Endocrinology, 172 (2), 282-292.
Jobling, M., Johnsen, H., Pettersen, G.W., Henderson, R.J., 1995. Effect of temperature on reproductive development in Arctic charr, Salvelinus alpinus (L.). Journal of Thermal Biology. 20.
Karamanlidis, D., 2017. Evolution of sex ratio and egg production in a population of gilthead seabream (Sparus aurata) over the course of five reproductive seasons, Biology Department. University of Crete, Crete, Greece, pp. 46.
Lahnsteiner, F., Leitner, S., 2013. Effect of temperature on gametogenesis and gamete quality in brown trout , Salmo trutta. Journal of Experimental Zoology. 319, 138-148.
Metcalfe, J.D., Craig, J.F., 2011. Ethical justification for the use and treatment of fishes in research: an update. Journal of Fish Biology. 78, 393-394.
Migaud, H., Davie, A., Taylor, J.F., 2010. Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. Journal of Fish Biology, 76 (1), 27-68.
Migaud, H., Wang, N., Gardeur, J.N., Fontaine, P., 2005. Influence of photoperiod on reproductive performances in Eurasian perch Perca fluviatilis. Aquaculture. 252: 385-393.
Migaud, H., Fontaine, P., Sulistyo, I., Kestemont, P., Gardeur, J.N., 2002. Induction of out-of-season spawning in Eurasian perch Perca fluviatilis: effects of rates of cooling and cooling durations on female gametogenesis and spawning. Aquaculture. 205, 253-267.
Monfort, M.C., 2010. Present market situation and prospects of meagre (Argyrosomus regius), as an emerging species in Mediterranean aquaculture, Studies and Reviews. General Fisheries Commission for the Mediterranean No. 89. Food and Agriculture Organization of the United Nations, Roma, pp. 28.
Mylonas, C.C., Hinshaw, J.M., Sullivan, C.V., 1992. Gn- RHa-induced ovulation of brown trout (Salmo trutta) and tts effects on egg quality. Aquaculture. 106, 379-392.
Mylonas, C.C., Duncan, N.J., Asturiano, J.F., 2017. Hormonal manipulations for the enhancement of sperm production in cultured fish and evaluation of sperm quality. Aquaculture. 472, 21-44.
Mylonas, C.C., Papadaki, M., Pavlidis, M., Divanach, P., 2004. Evaluation of egg production and quality in the Mediterranean red porgy (Pagrus pagrus) during two consecutive spawning seasons. Aquaculture. 232, 637-649.
Mylonas, C.C., Cardinaletti, G., Sigelaki, I., Polzonetti-Magni, A., 2005. Comparative efficacy of clove oil and 2-phenoxyethanol as anesthetics in the aquaculture of European sea bass (Dicentrarchus labrax) and gilthead sea bream (Sparus aurata) at different temperatures. Aquaculture. 246, 467-481.
Mylonas, C.C., Mitrizakis, N., Papadaki, M., Sigelaki, I., 2013a. Reproduction of hatchery-produced meagre Argyrosomus regius in captivity I. Description of the annual reproductive cycle. Aquaculture. 414-415, 309-317.
Mylonas, C.C., Mitrizakis, N., Castaldo, C.A., Cerviño, C.P., Papadaki, M. et al., 2013b. Reproduction of hatchery-produced meagre Argyrosomus regius in captivity II. Hormonal induction of spawning and monitoring of spawning kinetics, egg production and egg quality. Aquaculture. 414-415, 318-327.
Mylonas, C.C., Fatira, E., Karkut, P., Sigelaki, I., Papadaki, M. et al., 2015. Reproduction of hatchery-produced meagre Argyrosomus regius in captivity III. Comparison between Gn- RHa implants and injections on spawning kinetics and egg/ larval performance parameters. Aquaculture. 448, 44-53.
Mylonas, C.C., Salone, S., Biglino, T., de Mello, P.H., Fakriadis, I. et al., 2016. Enhancement of oogenesis/spermatogenesis in meagre Argyrosomus regius using a combination of temperature control and GnRHa treatments. Aquaculture. 464, 323-330.
Nash, J.P., Davail-Cuisset, B., Bhattacharyya, S., Suter, H.C., Le Menn, F. et al., 2000. An enzyme linked immunosorbent assay (ELISA) for testosterone, estradiol, and 17,20b-dihydroxy- 4-pregnen-3-one using acetylcholinesterase as tracer: application to measurement of diel patterns in rainbow trout (Oncorhynchus mykiss). Fish Physiology and Biochemistry. 22, 355-363.
Panini, E., Mylonas, C.C., Zanuy, S., Carrillo, M., Ramos, J. et al., 2001. Incubation of embryos and larvae of marine fish using microtiter plates. Aquaculture International. 9, 189-196.
Pankhurst, N.W., Porter, M.J.R., 2003. Cold and dark or warm and light: variations on the theme of environmental control of reproduction. Fish Physiology and Biochemistry. 28, 385-389.
Pankhurst, N.W., King, H.R., Anderson, K., Elizur, A., Pankhurst, P.M. et al., 2011. Thermal impairment of reproduction is differentially expressed in maiden and repeat spawning Atlantic salmon. Aquaculture. 316, 77-87.
Papadaki, M., Mazzella, D., Santinelli, V., Fakriadis, I., Sigelaki, I. et al., 2018. Hermaphroditism and reproductive function of hatchery-produced sharpsnout seabream (Diplodus puntazzo) under attenuated annual thermal cycles. Aquaculture. 482, 231-240.
Pavlidis, M., Keravec, L., Greenwood, L., Mourot, B., Scott, A.P., 2001. Reproductive performance of common dentex, Dentex dentex, broodstock held under different photoperiod and constant temperature conditions. Fish Physiology and Biochemistry. 25, 171-180.
Poli, B.M., Parisi, G., Zampacavallo, G., Iurzan, F., Mecatti, M. et al., 2003. Preliminary results on quality and quality changes in reared meagre (Argyrosomus regius): body and fillet traits and freshness changes in refrigerated commercial- size fish. Aquaculture International. 11, 301-311.
Povoa, I., Davie, A., Treasurer, J., Migaud, H., 2011. Broodstock spawning and larviculture of whiting (Merlangius merlangus L.) reared in captivity. Aquaculture Research. 42, 386-398.
Quéméner, L., Suquet, M., Mero, D., Gaignon, J.-L., 2002. Selection method of new candidates for finfish aquaculture: the case of the French Atlantic, the Channel and the North Sea coasts. Aquatic Living Resources. 15, 293-302.
Ramos-Júdez, S., González, W., Dutto, G., Mylonas, C.C., Fauvel, C. et al., 2019. Gamete quality and management for in vitro fertilisation in meagre (Argyrosomus regius). Aquaculture. 509, 227-235.
Rodríguez, L., Begtashi, I., Zanuy, S., Carrillo, M., 2000. Development and validation of an enzyme immunoassay for testosterone: effects of photoperiod on plasma testosterone levels and gonadal development in male sea bass (Dicentrarchus labrax, L.) at puberty. Fish Physiology and Biochemistry. 23, 141-150.
Santos, M., Soares, F., Moreira, M., Beirão, J., 2018. Evaluation of different extenders for the cold storage of meagre (Argyrosomus regius) semen. Aquaculture Research. 49, 2723-2731.
Schiavone, R., Zilli, L., Storelli, C., Vilella, S., 2012. Changes in hormonal profile, gonads and sperm quality of Argyrosomus regius (Pisces, Scianidae) during the first sexual differentiation and maturation. Theriogenology. 77, 888-898.
Schulz, R.W., de França, L.R., Lareyre, J.-J., LeGac, F., Chiarini- Garcia, H. et al., 2010. Spermatogenesis in fish. General and Comparative Endocrinology. 165, 390-411.
Shewmon, L.N., Godwin, J.R., Murashige, R.S., Daniels, H.V., 2007. Environmental Manipulation of Growth and Sexual Maturation in Yellow Perch, Perca flavescens. Journal of the World Aquaculture Society. 38, 383-394.
Soares, F., Ribeiro, L., Gamboa, M., Duarte, S., Mendes, A.C. et al., 2015. Comparative analysis on natural spawning of F1 meagre, Argyrosomus regius, with wild broodstock spawns in Portugal. Fish Physiology and Biochemistry. 41, 1509-1514.
Stipa, P., Angelini, M., 2005. Cultured Aquatic Species Information Programme. Argyrosomus regius, FAO Fisheries Division. FAO, Rome.
Tveiten, H., Johnsen, H.K., 1999. Temperature experienced during vitellogenesis influences ovarian maturation and the timing of ovulation in common wolffish. Journal of Fish Biology. 55, 809-819.
van Nes, S., Andersen, O., 2006. Temperature effects on sex determination and ontogenetic gene expression of the aromatases cyp19a and cyp19b, and the estrogen receptors esr1 and esr2 in atlantic halibut (Hippoglossus hippoglossus). Molecular Reproduction and Development, 73 (12), 1481-1490.
Vikingstad, E., Andersson, E., Hansen, T.J., Norberg, B., Mayer, I. et al., 2016. Effects of temperature on the final stages of sexual maturation in Atlantic salmon (Salmo salar L.). Fish physiology and biochemistry, 42 (3), 895-907.
Wang, N., Teletchea, F., Kestemont, P., Milla, S., Fontaine, P., 2010. Photothermal control of the reproductive cycle in temperate fishes. Reviews in Aquaculture. 2, 209-222.
Zakęś, Z., 2007. Out-of-season spawning of cultured pikeperch [Sander lucioperca (L.)]. Aquaculture Research. 38, 1419- 1427. Zohar, Y., Muñoz-Cueto, J.A., Elizur, A., Kah, O., 2010. Neuroendocrinology of reproduction in teleost fish. General and Comparative Endocrinology. 165, 438-455.