Abstract
A wild-caught stock of greater amberjack Seriola dumerili reared in sea cages in two commercial aquaculture facilities in Greece was administered gonadotropin-releasing hormone agonist (GnRHa), loaded in controlled release implants, and was used in spawning induction experiments throughout the reproductive season. Sperm quality was evaluated using computer-assisted sperm analysis (CASA) before and after GnRHa administration and the extent of the spermiation period was determined. Males were in spermiation throughout the monitoring period from May 30 until July 18, at temperatures between 19 and 24 °C. However, lower sperm motility duration, density, and survival under cold storage were observed from early July onwards. Sperm quality did not recover after the end of spawning induction experiments in tanks and the return of the fish for 14–28 days to the sea cage in mid-July, which could be related to the high temperatures of this period. An improvement trend was observed in the quality of the milt collected on day 7 after a single GnRHa administration, but a significant decrease was observed on day 21 in sperm density, survival under cold storage, and straight line velocity (VSL). On the contrary, a double GnRHa administration spaced 14 days apart maintained the same sperm quality for a longer period of 29 days. Further spermiation enhancement experiments should be conducted in the future to describe in more detail the kinetics of sperm production after GnRHa therapy and its effects on sperm quality.
Similar content being viewed by others
Data availability
The original data of the study are available on request.
References
Abascal FJ, Cosson J, Fauvel C (2007) Characterization of sperm motility in sea bass: the effect of heavy metals and physicochemical variables on sperm motility. J Fish Biol 70:509–522. https://doi.org/10.1111/j.1095-8649.2007.01322.x
Alavi HSM, Cosson J (2005) Sperm motility in fishes. I. Effects of temperature and pH: a review. Cell Biol Int 29:101–110
Anonymous (1998) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 55:251–257
Bobe J, Labbé C (2010) Egg and sperm quality in fish. Gen Comp Endocrinol 165:535–548
Clearwater SJ, Crim LW (1998) Gonadotropin releasing hormone-analogue treatment increases sperm motility, seminal plasma pH and sperm production in yellowtail flounder Pleuronectes ferrugineus. Fish Physiol Biochem 19:349–357
Corriero A, Medina A, Mylonas CC, Bridges CR, Santamaria N, Deflorio M, Losurdo M, Zupa R, Gordin H, de la Gandara F, Belmonte Rìos A, Pousis C, de Metrio G (2009) Proliferation and apoptosis of male germ cells in captive Atlantic bluefin tuna (Thunnus thynnus L.) treated with gonadotroping releasing hormone agonist (GnRHa). Anim Reprod Sci 116:346–357
Cosson J, Groison AL, Suquet M, Fauvel C, Dreanno C, Billard R (2008) Studying sperm motility in marine fish: an overview on the state of the art. J Appl Ichthyol 24:460–486. https://doi.org/10.1111/j.1439-0426.2008.01151.x
Dadras H, Dzyuba B, Cosson J, Golpour A, Siddique MAM, Linhart O (2017) Effect of water temperature on the physiology of fish spermatozoon function: a brief review. Aquac Res 48:729–740. https://doi.org/10.1111/are.13049
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. Off J Eur Union L 276:33–79
Fakriadis I, Lisi F, Sigelaki I, Papadaki M, Mylonas CC (2019) Spawning kinetics and egg/larval quality of greater amberjack (Seriola dumerili) in response to multiple GnRHa injections or implants. Gen Comp Endocrinol 279:78–87. https://doi.org/10.1016/j.ygcen.2018.12.007
Fakriadis I, Miccoli A, Karapanagiotis S, Tsele N, Mylonas CC (2020a) Optimization of a GnRHa treatment for spawning commercially reared greater amberjack Seriola dumerili: Dose response and extent of the reproductive season. Aquaculture 521:735011. https://doi.org/10.1016/j.aquaculture.2020.735011
Fakriadis I, Sigelaki I, Papadaki M, Papandroulakis N, Raftopoulos A, Tsakoniti K, Mylonas CC (2020b) Control of reproduction of greater amberjack Seriola dumerili reared in aquaculture facilities. Aquaculture 519:734880. https://doi.org/10.1016/j.aquaculture.2019.734880
Fakriadis I, Zanatta EM, Fleck R, Sena Mateo DL, Papadaki M, Mylonas CC (2020c) Endocrine regulation of long-term enhancement of spermiation in meagre (Argyrosomus regius) with GnRHa controlled-delivery systems. Gen Comp Endocrinol 297:113549. https://doi.org/10.1016/j.ygcen.2020.113549
Fauvel C, Suquet M, Cosson J (2010) Evaluation of fish sperm quality. J Appl Ichthyol 26:636–643. https://doi.org/10.1111/j.1439-0426.2010.01529.x
Forner-Piquer I, Fakriadis I, Mylonas CC, Piscitelli F, di Marzo V, Maradonna F, Calduch-Giner J, Pérez-Sánchez J, Carnevali O (2019a) Effects of dietary bisphenol A on the reproductive function of gilthead sea bream (Sparus aurata) testes. Int J Mol Sci 20:5003
Forner-Piquer I et al (2019b) Effects of diisononyl phthalate (DiNP) on the endocannabinoid and reproductive systems of male gilthead sea bream (Sparus aurata) during the spawning season. Arch Toxicol:1–15. https://doi.org/10.1007/s00204-018-2378-6
Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14:44–47
Gallego V, Asturiano JF (2018) Sperm motility in fish: technical applications and perspectives through CASA-Mot systems. Reprod Fertil Dev 30:820–832. https://doi.org/10.1071/RD17460
Jerez S, Fakriadis I, Papadaki M, Martín M, Cejas J, Mylonas CC (2018) Spawning induction of first-generation (F1) greater amberjack Seriola dumerili in the Canary Islands, Spain using GnRHa delivery systems. Fishes 3:1–22. https://doi.org/10.3390/fishes3030035
Kowalski RK, Cejko BI (2019) Sperm quality in fish: Determinants and affecting factors. Theriogenology 135:94–108. https://doi.org/10.1016/j.theriogenology.2019.06.009
Kozul V, Skaramuca B, Glamuzina B, Glavic N, Tutman P (2001) Comparative gonadogenesis and hormonal induction of spawning of cultured and wild Mediterranean amberjack (Seriola dumerili, Risso 1810). Sci Mar 65:215–220
Metcalfe JD, Craig JF (2011) Ethical justification for the use and treatment of fishes in research: an update. J Fish Biol 78:393–394. https://doi.org/10.1111/j.1095-8649.2010.02900.x
Mylonas CC, Zohar Y (2001) Use of GnRHa-delivery systems for the control of reproduction in fish. Rev Fish Biol Fish 10:463–491
Mylonas CC, Gissis A, Magnus Y, Zohar Y (1997a) Hormonal changes in male white bass (Morone chrysops) and evaluation of milt quality after treatment with a sustained-release GnRHa delivery system. Aquaculture 153:301–313. https://doi.org/10.1016/S0044-8486(97)00021-5
Mylonas CC, Scott AP, Vermeirssen EL, Zohar Y (1997b) Changes in plasma gonadotropin II and sex steroid hormones, and sperm production of striped bass after treatment with controlled-release gonadotropin-releasing hormone agonist-delivery systems. Biol Reprod 57:669–675
Mylonas CC, Papandroulakis N, Smboukis A, Papadaki M, Divanach P (2004) Induction of spawning of cultured greater amberjack (Seriola dumerili) using GnRHa implants. Aquaculture 237:141–154. https://doi.org/10.1016/J.Aquaculture.2004.04.015
Mylonas CC, 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. https://doi.org/10.1016/J.Aquaculture.2005.02.046
Mylonas CC et al (2007) Preparation and administration of gonadotropin-releasing hormone agonist (GnRHa) implants for the artificial control of reproductive maturation in captive-reared Atlantic bluefin tuna (Thunnus thynnus thynnus). Rev Fish Sci 15:183–210. https://doi.org/10.1080/10641260701484572
Mylonas CC, Fostier A, Zanuy S (2010) Broodstock management and hormonal manipulations of fish reproduction. Gen Comp Endocrinol 165:516–534. https://doi.org/10.1016/j.ygcen.2009.03.007
Mylonas CC, Duncan NJ, Asturiano JF (2017) Hormonal manipulations for the enhancement of sperm production in cultured fish and evaluation of sperm quality. Aquaculture 472:21–44
Rainis S, Mylonas CC, Kyriakou Y, Divanach P (2003) Enhancement of spermiation in European sea bass (Dicentrarchus labrax) at the end of the reproductive season using GnRHa implants. Aquaculture 219:873–890
Rosenfeld H, Mylonas CC, Bridges CR, Heinisch G, Corriero A, Vassallo-Aguis R, Medina A, Belmonte A, Garcia A, de la Gándara F, Fauvel C, de Metrio G, Meiri-Ashkenazi I, Gordin H, Zohar Y (2012) GnRHa-mediated stimulation of the reproductive endocrine axis in captive Atlantic bluefin tuna, Thunnus thynnus. Gen Comp Endocrinol 175:55–64
Rurangwa E, Kime DE, Ollevier F, Nash JP (2004) The measurement of sperm motility and factors affecting sperm quality in cultured fish. Aquaculture 234:1–28
Sarih S, Djellata A, La Barbera A, Fernández-Palacios Vallejo H, Roo J, Izquierdo M, Fernández-Palacios H (2018) High-quality spontaneous spawning in greater amberjack (Seriola dumerili, Risso 1810) and its comparison with GnRHa implants or injections. Aquac Res 49:3442–3450. https://doi.org/10.1111/are.13808
Sarih S, Djellata A, Roo J, Hernández-Cruz CM, Fontanillas R, Rosenlund G, Izquierdo M, Fernández-Palacios H (2019) Effects of increased protein, histidine and taurine dietary levels on egg quality of greater amberjack (Seriola dumerili, Risso, 1810). Aquaculture 499:72–79. https://doi.org/10.1016/j.aquaculture.2018.09.011
Sarih S, Djellata A, Fernández-Palacios H, Ginés R, Fontanillas R, Rosenlund G, Izquierdo M, Roo J (2020) Adequate n-3 LC-PUFA levels in broodstock diets optimize reproductive performance in GnRH injected greater amberjack (Seriola dumerili) equaling to spontaneously spawning broodstock. Aquaculture 520:735007. https://doi.org/10.1016/j.aquaculture.2020.735007
Schulz RW, de França LR, Lareyre J-J, LeGac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411
Smith-Vaniz WF, Pina Amargos F, Brown J, Curtis M, Williams JT (2015) Seriola dumerili. The IUCN Red List of Threatened Species 2015
Sorbera LA, Mylonas CC, Zanuy S, Carillo M, Zohar Y (1996) Sustained administration of GnRHa increases milt volume without altering sperm counts in the sea bass. J Exp Zool 276:361–368
Suquet M, Cosson J, de la Gándara F, Mylonas CC, Papadaki M, Lallemant S, Fauvel C (2010) Sperm features of captive Atlantic bluefin tuna (Thunnus thynnus). J Appl Ichthyol 26:775–778
Tuset VM, Trippel EA, De Monserrat J (2008) Sperm morphology and its influence on swimming speed in Atlantic cod. J Appl Ichthyol 24:398–405
Vermeirssen ELM, Shields RJ, Mazorra de Quero C, Scott AP (2000) Gonadotrophin-releasing hormone agonist raises plasma concentrations of progestogens and enhances milt fluidity in male Atlantic halibut (Hippoglossus hippoglossus). Fish Physiol Biochem 22:77–87
Zupa P et al (2017a) Rearing in captivity affects spermatogenesis and sperm quality in greater amberjack, Seriola dumerili (Risso, 1810). J Anim Sci 95:4085–4100. https://doi.org/10.2527/jas2017.1708
Zupa R, Rodríguez C, Mylonas CC, Rosenfeld H, Fakriadis I, Papadaki M, Pérez JA, Pousis C, Basilone G, Corriero A (2017b) Comparative study of reproductive development in wild and captive-reared greater amberjack Seriola dumerili (Risso, 1810). PLoS One 12:e0169645. https://doi.org/10.1371/journal.pone.0169645
Acknowledgements
The authors are grateful to the staff of Argosaronikos Fishfarms SA and Galaxidi Marine Farms SA.
Funding
This study has been undertaken within the framework of the EU 7th FP project DIVERSIFY (7FP-KBBE-GA-603121) titled “Exploring the biological and socio-economic potential of new/emerging fish species for the expansion of the European aquaculture industry” awarded to Constantinos C. Mylonas.
Author information
Authors and Affiliations
Contributions
Constantinos C. Mylonas designed the experiment. Material preparation and data collection were performed by Constantinos C. Mylonas and Ioannis Fakriadis. Data analysis was performed by Ioannis Fakriadis and the first draft was written by the same author. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
Ethical approval for the experiment was obtained by the relevant Greek authorities (National Veterinary Services) under the license No 255356 (ΑΔΑ: 6ΛΙ17ΛΚ-ΠΛΩ). All procedures involving animals were conducted in accordance to the “Guidelines for the treatment of animals in behavioral research and teaching” (Anonymous 1998), the Ethical justification for the use and treatment of fishes in research: an update (Metcalfe and Craig 2011), and the “Directive 2010/63/EU of the European parliament and the council of 22 September 2010 on the protection of animals used for scientific purposes” (EU 2010). The greater amberjack is classified as “Least Concern” in the IUCN Red List of Threatened Species (Smith-Vaniz et al. 2015).
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Fakriadis, I., Mylonas, C.C. Sperm quality of greater amberjack Seriola dumerili throughout the reproductive season and in response to GnRHa treatment with controlled release implants. Fish Physiol Biochem 47, 281–292 (2021). https://doi.org/10.1007/s10695-020-00910-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-020-00910-9