Comparative Study of Semen Parameters and Hormone Profile in Small-Spotted Catshark (Scyliorhinus canicula): Aquarium-Housed vs. Wild-Captured
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
34679905
PubMed Central
PMC8532847
DOI
10.3390/ani11102884
PII: ani11102884
Knihovny.cz E-zdroje
- Klíčová slova
- Elasmobranchii, Scyliorhinidae, conservation biology, sperm, spotted dogfish,
- Publikační typ
- časopisecké články MeSH
Several chondrichthyan species are threatened, and we must increase our knowledge of their reproductive biology in order to establish assisted reproductive protocols for ex situ or in situ endangered species. The small-spotted catshark (Scyliorhinus canicula) is one of the most abundant shark species of the Mediterranean coast and is easy to maintain in aquaria; therefore, it is considered an ideal reproductive model. This study aimed to compare S. canicula male reproductive function in aquarium-housed (n = 7) and wild-captured animals, recently dead (n = 17). Aquarium-housed animals had lower semen volume (p = 0.005) and total sperm number (p = 0.006) than wild-captured animals, but similar sperm concentrations. In terms of sperm parameters, aquarium-housed sharks showed higher total sperm motility (p = 0.004), but no differences were observed regarding sperm viability, mitochondrial membrane potential, or membrane integrity. A morphometric study pointed to a significantly longer head (p = 0.005) and acrosome (p = 0.001) in wild-captured animals. The results of the spermatozoa morphological study of S. canicula were consistent with previous results obtained in other chondrichthyan species. With regard to sex hormones, testosterone levels were significantly lower in aquarium-housed animals (p ≤ 0.001), while similar levels of 17β-estradiol and progesterone were found. In short, the present study provides evidence of good in vitro semen quality in S. canicula housed in an aquarium, underlining their excellent potential for application in reproductive technologies for this and other chondrichthyan species.
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Gascon C., Brooks T.M., Contreras-MacBeath T., Heard N., Konstant W., Lamoreux J., Launay F., Maunder M., Mittermeier R.A., Molur S., et al. The importance and benefits of species. Curr. Biol. 2015;25:431–438. doi: 10.1016/j.cub.2015.03.041. PubMed DOI
McClenachan L., Cooper A.B., Carpenter K.E., Dulvy N.K. Extinction risk and bottlenecks in the conservation of charismatic marine species. Conserv. Lett. 2012;5:73–80. doi: 10.1111/j.1755-263X.2011.00206.x. DOI
Frölicher T.L., Laufkötter C. Emerging risks from marine heat waves. Nat. Commun. 2018;9:650. doi: 10.1038/s41467-018-03163-6. PubMed DOI PMC
Johnson J.E., Allain V., Basel B., Bell J.D., Chin A., Dutra L.X.C., Hooper E., Loubser D., Lough J., Moore B.R., et al. Impacts of climate change on marine resources in the Pacific Island region. In: Kumar L., editor. Climate Change and Impacts in the Pacific. Springer; Cham, Switzerland: 2020. pp. 359–402.
Schéré C.M., Dawson T.P., Schreckenberg K. Multiple conservation designations: What impact on the effectiveness of marine protected areas in the Irish Sea? Int. J. Sustain. Dev. World Ecol. 2020;27:596–610. doi: 10.1080/13504509.2019.1706058. DOI
Walls R.H.L., Dulvy N.K. Eliminating the dark matter of data deficiency by predicting the conservation status of Northeast Atlantic and Mediterranean Sea sharks and rays. Biol. Conserv. 2020;246:108459. doi: 10.1016/j.biocon.2020.108459. DOI
Oegelund-Nielsen R., da Silva R., Juergens J., Staerk J., Lindholm Sørensen L., Jackson J., Smeele S.Q., Conde D.A. Standardized data to support conservation prioritization for sharks and batoids (Elasmobranchii) Data Br. 2020;33:106337. doi: 10.1016/j.dib.2020.106337. PubMed DOI PMC
Finucci B., Cheok J., Ebert D.A., Herman K., Kyne P.M., Dulvy N.K. Ghosts of the deep—Biodiversity, fisheries, and extinction risk of ghost sharks. Fish Fish. 2021;22:391–412. doi: 10.1111/faf.12526. DOI
Giménez J., Cardador L., Mazor T., Kark S., Bellido J.M., Coll M., Navarro J. Marine protected areas for demersal elasmobranchs in highly exploited Mediterranean ecosystems. Mar. Environ. Res. 2020;160:105033. doi: 10.1016/j.marenvres.2020.105033. PubMed DOI
Janse M., Zimmerman B., Geerlings L., Brown C., Nagelkerke L.A.J. Sustainable species management of the elasmobranch populations within European aquariums: A conservation challenge. J. Zoo Aquar. Res. 2017;5:172–181.
Leonetti F.L., Sperone E., Travaglini A., Mojetta A.R., Signore M., Psomadakis P.N., Dinkel T.M., Bottaro M. Filling the gap and improving conservation: How IUCN red lists and historical scientific data can shed more light on threatened sharks in the Italian seas. Diversity. 2020;12:389. doi: 10.3390/d12100389. DOI
Tiktak G.P., Butcher D., Lawrence P.J., Norrey J., Bradley L., Shaw K., Preziosi R., Megson D. Are concentrations of pollutants in sharks, rays and skates (Elasmobranchii) a cause for concern? A systematic review. Mar. Pollut. Bull. 2020;160:111701. doi: 10.1016/j.marpolbul.2020.111701. PubMed DOI
Porte C., Janer G., Lorusso L.C., Ortiz-Zarragoitia M., Cajaraville M.P., Fossi M.C., Canesi L. Endocrine disruptors in marine organisms: Approaches and perspectives. Comp. Biochem. Physiol. Toxicol. Pharmacol. CBP. 2006;143:303–315. doi: 10.1016/j.cbpc.2006.03.004. PubMed DOI
Simpfendorfer C.A., Dulvy N.K. Bright spots of sustainable shark fishing. Curr. Biol. 2017;27:97–98. doi: 10.1016/j.cub.2016.12.017. PubMed DOI
Dulvy N.K., Simpfendorfer C.A., Davidson L.N.K., Fordham S.V., Bräutigam A., Sant G., Welch D.J. Challenges and priorities in shark and ray conservation. Curr. Biol. 2017;27:565–572. doi: 10.1016/j.cub.2017.04.038. PubMed DOI
Ellis J., Mancusi C., Serena F., Haka F., Guallart J., Ungaro N., Coello R., Schembri T., MacKenzie K. Scyliorhinus canicula. IUCN Red L. Threat. Species Eur. 2009:e.T161399A5415204. doi: 10.2305/IUCN.UK.2009-2.RLTS.T161399A5415204.en. DOI
Jeffree R.A., Warnau M., Teyssié J.-L., Markich S.J. Comparison of the bioaccumulation from seawater and depuration of heavy metals and radionuclides in the spotted dogfish Scyliorhinus Canicula (Chondrichthys) and the Turbot Psetta Maxima (Actinopterygii: Teleostei) Sci. Total Environ. 2006;368:839–852. doi: 10.1016/j.scitotenv.2006.03.026. PubMed DOI
Mancia A., Chenet T., Bono G., Geraci M.L., Vaccaro C., Munari C., Mistri M., Cavazzini A., Pasti L. Adverse effects of plastic ingestion on the Mediterranean small-spotted catshark (Scyliorhinus canicula) Mar. Environ. Res. 2020;155:104876. doi: 10.1016/j.marenvres.2020.104876. PubMed DOI
Musa S.M., Ripley D.M., Moritz T., Shiels H.A. Ocean warming and hypoxia affect embryonic growth, fitness and survival of small-spotted catsharks, Scyliorhinus canicula. J. Fish Biol. 2020;97:257–264. doi: 10.1111/jfb.14370. PubMed DOI
Barongi R., Fisken F., Parker M., Gusset M. Committing to Conservation: The World Zoo and Aquarium Conservation Strategy. WAZA Executive Office; Gland, Switzerland: 2015.
Wyffels J.T., George R., Adams L., Adams C., Clauss T., Newton A., Hyatt M.W., Yach C., Penfold L.M. Testosterone and semen seasonality for the Sand Tiger shark Carcharias Taurus. Biol. Reprod. 2020;102:876–887. doi: 10.1093/biolre/ioz221. PubMed DOI PMC
Penning M., Reid G., Koldewey H., Andrews B., Araj K., Garratt P., Gendron S., Lange J., Tanner K., Tonge S., et al. World Association of Zoos and Aquariums. WAZA; Bern, Switzerland: 2009. Turning the tide: A global aquarium strategy for conservation and sustainability.
Daly J., Jones R. The use of reproductive technologies in breeding programs for elasmobranchs in aquaria. In: Smith M., Warmolts D., Thoney D., Hueter R., Murray M., Ezcurra J., editors. The Elasmobranch Husbandry Manual II: Recent Advances in the Care of Sharks, Rays and their Relatives. Special Publication of the Ohio Biological Survey; Columbus, OH, USA: 2017. pp. 363–374.
Capapé C., Mnasri-Sioudi N., El Kamel-Moutalibi O., Boumaïza M., Amor M.M.B., Reynaud C. Production, maturity, reproductive cycle and fecundity of small-spotted catshark, Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) from the northern coast of Tunisia (central Mediterranean) J. Ichthyol. 2014;54:111–126. doi: 10.1134/S0032945214010020. DOI
Garnier D.H., Sourdaine P., Jégou B. Seasonal variations in sex steroids and male sexual characteristics in Scyliorhinus Canicula. Gen. Comp. Endocrinol. 1999;116:281–290. doi: 10.1006/gcen.1999.7369. PubMed DOI
Kousteni V., Megalofonou P. Reproductive strategy of Scyliorhinus canicula (L., 1758): A holistic approach based on macroscopic measurements and microscopic observations of the reproductive organs. Mar. Freshw. Res. 2020;71:596–616. doi: 10.1071/MF18474. DOI
Dzyuba V., Ninhaus-Silveira A., Veríssimo-Silveira R., Rodina M., Dzyuba B. Sperm antioxidant system in ocellate river stingray Potamotrygon motoro at transition from seminal vesicle to cloaca. Fish Physiol. Biochem. 2020;46:1975–1980. doi: 10.1007/s10695-020-00848-y. PubMed DOI
Minamikawá S., Morisawa M. Acquisition, initiation and maintenance of sperm motility in the shark, Ttiakis Scyllia. Comp. Biochem. Physiol. A Physiol. 1996;113:387–392. doi: 10.1016/0300-9629(95)02080-2. DOI
Morales-Gamba R.D., Caldas J.S., Godoy L., Marcon J.L. Sperm characterization of the Amazonian freshwater cururu stingray Potamotrygon wallacei (Potamotryogonidae): Basic knowledge for reproduction and conservation plans. Zygote. 2019;27:259–261. doi: 10.1017/S096719941900039X. PubMed DOI
Rowley A., Locatello L., Kahrl A., Rego M., Boussard A., Garza-Gisholt E., Kempster R.M., Collin S.P., Giacomello E., Follesa M.C., et al. Sexual selection and the evolution of sperm morphology in sharks. J. Evol. Biol. 2019;32:1027–1035. doi: 10.1111/jeb.13501. PubMed DOI
Fitzpatrick J.L., Kempster R.M., Daly-Engel T.S., Collin S.P., Evans J.P. Assessing the potential for post-copulatory sexual selection in elasmobranchs. J. Fish Biol. 2012;80:1141–1158. doi: 10.1111/j.1095-8649.2012.03256.x. PubMed DOI PMC
Jamieson B.G.M., Hamlett W.C. Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids and Chimaeras. Science Publishers, Inc.; Hauppauge, NY, USA: 2005. Chondrichthyan spermatozoa and phylogeny; pp. 201–236.
Stanley H.P. Fine structure of spermiogenesis in the elasmobranch fish Squalus suckleyi. I. Acrosome formation, nuclear elongation and differentiation of the midpiece axis. J. Ultrastruct. Res. 1971;36:86–102. doi: 10.1016/S0022-5320(71)80090-4. PubMed DOI
Stanley H.P. Fine structure of spermiogenesis in the elasmobranch fish Squalus suckleyi. II. Late stages of differentiation and structure of the mature spermatozoon. J. Ultrastruct. Res. 1971;36:103–118. doi: 10.1016/S0022-5320(71)80091-6. PubMed DOI
Kousteni V., Kontopoulou M., Megalofonou P. Sexual maturity and fecundity of Scyliorhinus canicula (Linnaeus, 1758) in the Aegean Sea. Mar. Biol. Res. 2010;6:390–398. doi: 10.1080/17451000903233771. DOI
Henningsen A.D. Tonic immobility in 12 elasmobranchs: Use as an aid in captive husbandry. Zoo Biol. 1994;13:325–332. doi: 10.1002/zoo.1430130406. DOI
Lawrence M., Raby G., Teffer A., Jeffries K., Danylchuk A., Eliason E., Hasler C., Clark T., Cooke S. Best practices for non-lethal blood sampling of fish via the caudal vasculature. J. Fish Biol. 2020;97:4–15. doi: 10.1111/jfb.14339. PubMed DOI
Mylniczenko N., Clauss T. The Elasmobranch Husbandry Manual II: Recent Advances in the Care of Sharks, Rays and Their Relatives. Ohio Biological Survey Inc.; Columbus, OH, USA: 2017. Pharmacology of elasmobranchs: Updates and techniques; pp. 289–302.
Ros-Santaella J.L., Domínguez-Rebolledo Á.E., Garde J.J. Sperm flagellum volume determines freezability in red deer spermatozoa. PLoS ONE. 2014;9:e112382. doi: 10.1371/journal.pone.0112382. PubMed DOI PMC
Carlson J.K., Heupel M.R., Young C.N., Cramp J.E., Simpfendorfer C.A. Are we ready for elasmobranch conservation success? Environ. Conserv. 2019;46:264–266. doi: 10.1017/S0376892919000225. DOI
Pacoureau N., Rigby C.L., Kyne P.M., Sherley R.B., Winker H., Carlson J.K., Fordham S.V., Barreto R., Fernando D., Francis M.P., et al. Half a century of global decline in oceanic sharks and rays. Nature. 2021;589:567–571. doi: 10.1038/s41586-020-03173-9. PubMed DOI
O’Brien J.K., Robeck T.R. The relationship of maternal characteristics and circulating progesterone concentrations with reproductive outcome in the bottlenose dolphin (Tursiops truncatus) after artificial insemination, with and without ovulation induction, and natural breeding. Theriogenology. 2012;78:469–482. doi: 10.1016/j.theriogenology.2012.02.011. PubMed DOI
O’Brien J.K., Robeck T.R. The value of ex situ cetacean populations in understanding reproductive physiology and developing assisted reproductive technology for ex situ and in situ species management and conservation efforts. Int. J. Comp. Psychol. 2010;23:227–248.
Penfold L.M., Wyffels J.T. Reproductive science in sharks and rays. In: Comizzoli P., Brown J.L., Holt W.V., editors. Reproductive Sciences in Animal Conservation. Volume 1200. Springer International Publishing; Cham, Switzerland: 2019. pp. 465–488. PubMed
Magnotti C., Cerqueira V., Lee-Estevez M., Farias J.G., Valdebenito I., Figueroa E. Cryopreservation and vitrification of fish semen: A review with special emphasis on marine species. Rev. Aquac. 2018;10:15–25. doi: 10.1111/raq.12145. DOI
Beirao J., Boulais M., Gallego V., O′Brien J.K., Peixoto S., Robeck T.R., Cabrita E. Sperm handling in aquatic animals for artificial reproduction. Theriogenology. 2019;133:161–178. doi: 10.1016/j.theriogenology.2019.05.004. PubMed DOI
Griffiths A., Jacoby D., Casane D., McHugh M., Croft D., Genner M., Sims D. First analysis of multiple paternity in an oviparous shark, the small-spotted catshark (Scyliorhinus canicula, L.) J. Hered. 2011;103:166–173. doi: 10.1093/jhered/esr112. PubMed DOI
Gilroy C.E., Litvak M.K. Swimming kinematics and temperature effects on spermatozoa from wild and captive shortnose sturgeon (Acipenser brevirostrum) Anim. Reprod. Sci. 2019;204:171–182. doi: 10.1016/j.anireprosci.2019.03.022. PubMed DOI
Locatello L., Bertotto D., Cerri R., Parmeggiani A., Govoni N., Trocino A., Xiccato G., Mordenti O. Sperm quality in wild-caught and farmed males of the European eel (Anguilla Anguilla) Anim. Reprod. Sci. 2018;198:167–176. doi: 10.1016/j.anireprosci.2018.09.016. PubMed DOI
Zupa R., Fauvel C., Mylonas C.C., Santamaria N., Valentini L., Pousis C., Papadaki M., Suquet M., Gándara F.l., Bello G., et al. Comparative analysis of male germ cell proliferation and apoptosis in wild and captive Atlantic bluefin tuna (Thunnus Thynnus L.) J. Appl. Ichthyol. 2013;1:71–81. doi: 10.1111/j.1439-0426.2012.02045.x. DOI
Luer C.A., Walsh C.J., Bodine A.B., Wyffels J.T. Normal embryonic development in the clearnose skate, Raja Eglanteria, with experimental observations on artificial insemination. Environ. Biol. Fishes. 2007;80:239–255. doi: 10.1007/s10641-007-9219-4. DOI
Tanaka S., Kurokawa H., Hara M. Advances in Spermatozoal Phylogeny and Taxonomy. Volume 166. Mémoires du Muséum National d′Histoire Naturelle; Paris, France: 1995. Comparative morphology of the sperm in chondrichthyan fishes; pp. 313–320.
Chatchavalvanich K., Thongpan A., Nakai M. Ultrastructure of spermiogenesis in a freshwater stingray. Ichthyol. Res. 2005;52:379–385. doi: 10.1007/s10228-005-0300-8. DOI
Takemura A., Hara M., Mizue K., Malagrino G. Electron microscopic study on the spermatogenesis of Chimaera, Chimaera phantasma. Bull. Fac. Fish. Nagasaki Univ. 1983;54:35–54.
Stanley H.P. The fine structure of spermatozoa of Hydrolagus colliei (Chondrichthyes, Holocephali) J. Ultrastruct. Res. 1983;83:184–194. doi: 10.1016/S0022-5320(83)90076-X. PubMed DOI
Jones R.C., Jones N., Djakiew D. Luminal composition and maturation of spermatozoa in the male genital ducts of the Port Jackson shark, Heterodontus Portusjacksoni. J. Exp. Zool. 1984;230:417–426. doi: 10.1002/jez.1402300311. DOI
Bondarenko V., Cosson J. Structure and beating behavior of the sperm motility apparatus in aquatic animals. Theriogenology. 2019;135:152–163. doi: 10.1016/j.theriogenology.2019.06.005. PubMed DOI
Dobson S., Dodd J. Roles of temperature and photoperiod in response of testis of dogfish, Scyliorhinus-Canicula L to partial hypophysectomy (ventral lobectomy) Gen. Comp. Endocrinol. 1977;32:114–115. doi: 10.1016/0016-6480(77)90088-0. PubMed DOI
Capapé C., Reynaud C., Vergne Y., Quignard J.-P. Biological observations on the smallspotted catshark Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) off the Languedocian coast (southern France, northern Mediterranean) Pan Am. J. Aquat. Sci. 2008;3:282–289.
Pickering A.D., Pottinger T.G., Carragher J., Sumpter J.P. The effects of acute and chronic stress on the levels of reproductive hormones in the plasma of mature male brown trout, Salmo trutta, L. Gen. Comp. Endocrinol. 1987;68:249–259. doi: 10.1016/0016-6480(87)90036-0. PubMed DOI
Becerril-García E.E., Arellano-Martínez M., Bernot-Simon D., Hoyos-Padilla E.M., Galván-Magaña F., Godard-Codding C. Steroid hormones and chondrichthyan reproduction: Physiological functions, scientific research, and implications for conservation. PeerJ. 2020;8:e9686. doi: 10.7717/peerj.9686. DOI