Abstract
The present study was designed to evaluate sperm phenotypic variables during in vivo and in vitro storage following multiple sperm stripping in common carp (Cyprinus carpio L.). Each male was injected 3 times with carp pituitary 3 days apart. Sperm was stored in vivo in the body cavity for 0.5 days (Fresh sperm) and 3 days (Old sperm) after hormonal stimulation. Then sperm was collected and diluted with a carp extender at a ratio of 1:1, and stored in vitro on ice for 0, 3, and 6 days. The phenotypic parameters, including the number of total motile spermatozoa, number of fast motile spermatozoa, number of motile spermatozoa, percentage of fast motile spermatozoa, and percentage of spermatozoa motility were the major components of principal component analysis (PCA). In general, Fresh sperm from the first stripping showed slightly better quality than Old sperm from the second and third stripping, especially in the phenotypic parameters of a number of total spermatozoa and a number of total motile spermatozoa (P < 0.05). The highest kinetic and quantitative spermatozoa variables were obtained in Fresh and Old sperm just after sperm collection (0-day storage in vitro), and then they were decreased during the period of in vitro storage up to 6 days (P < 0.05). However, the fertilization, hatching, and malformation rates from Fresh sperm were similar compared with the Old sperm. Sperm could be stripped 0.5 days post hormonal treatment and stored in vitro up to 6 days with good fertilization performance (fertility, hatching, and malformation rates were 92.5%, 91.5%, and 1.3%, respectively). Therefore, our results suggested that multiple hormonal treatments with multiple stripping could be used in artificial reproduction in common carp.
Similar content being viewed by others
Data availability
Data of the present article are available under request.
Code availability
Not applicable.
References
Alavi SMH, Cosson J, Kazemi R (2006) Semen characteristics in Acipenser persicus in relation to sequential stripping. J Appl Ichthyol 22:400–405. https://doi.org/10.1111/j.1439-0426.2007.00994.x
Alavi SMH, Linhart O, Coward K, Rodina M (2008) Fish spermatology: implication for aquaculture management. In: Alavi SMH, Cosson JJ, Coward K, Rafiee R (eds) Fish Spermatology. Alpha Science Ltd, Oxford, pp 397–460
Alavi SMH, Cosson J, Bondarenko O, Linhart O (2019) Sperm motility in fishes: (III) diversity of regulatory signals from membrane to the axoneme. Theriogenology 136:143–165. https://doi.org/10.1016/j.theriogenology.2019.06.038
Aramli MS, Kalbassi MR, Nazari RM, Aramli S (2013) Effects of short-term storage on the motility, oxidative stress, and ATP content of Persian sturgeon (Acipenser persicus) sperm. Anim Reprod Sci 143:112–117. https://doi.org/10.1016/j.anireprosci.2013.10.010
Aramli MS, Kalbassi MR, Gharibi MR (2015) Retracted: Effects of multiple collections on spermatozoa quality of Persian sturgeon, Acipenser persicus: motility, density and seminal plasma composition. J Anim Physiol Anim Nutr 99:66–72. https://doi.org/10.1111/jpn.12212
Babiak I, Ottesen O, Rudolfsen G, Johnsen S (2006) Quantitative characteristics of Atlantic halibut, Hippoglossus hippoglossus L, semen throughout the reproductive season. Theriogenology 65:1587–1604. https://doi.org/10.1016/j.theriogenology.2005.09.004
Beirão J, Soares F, Pousão-Ferreira P, Diogo P, Dias J, Dinis MT, Herráez MP, Cabrita E (2015) The effect of enriched diets on Solea senegalensis sperm quality. Aquaculture 435:187–194. https://doi.org/10.1016/j.aquaculture.2014.09.025
Billard R, Weil C, Bienarz K, Mikolajczyk T, Breton B, Epler P, Bougoussa M (1992) Testicular and some hormonal changes during the first four years of life in the mirror carp, Cyprinus curpio L. J Fish Biol 41:473–487. https://doi.org/10.1111/j.1095-8649.1992.tb02675.x
Billard R, Cosson J, Perchec G, Linhart O (1995) Biology of sperm and artificial reproduction in carp. Aquaculture 129:95–112. https://doi.org/10.1016/0044-8486(94)00231-C
Bokor Z, Żarski D, Palińska-Żarska K, Krejszeff S, Król J, Radóczi JI, Horváth Á, Várkonyi L, Urbányi B, Bernáth G (2021) Standardization of sperm management for laboratory assessment of sperm quality and in vitro fertilization in Eurasian perch (Perca fluviatilis). Aquacult Int 29:2021–2033. https://doi.org/10.1007/s10499-021-00731-4
Boryshpolets S, Kowalski RK, Dietrich GJ, Dzyuba B, Ciereszko A (2013) Different computer-assisted sperm analysis (CASA) systems highly influence sperm motility parameters. Theriogenology 80:758–765. https://doi.org/10.1016/j.theriogenology.2013.06.019
Butts IAE, Litvak MK, Trippel EA (2010) Seasonal variations in seminal plasma and sperm characteristics of wild-caught and cultivated Atlantic cod, Gadus morhua. Theriogenology 73:873–885. https://doi.org/10.1016/j.theriogenology.2009.11.011
Büyükhatipoglu S, Holtz W (1984) Sperm output in rainbow trout (Salmo gairdneri) effect of age, timing and frequency of stripping and presence of females. Aquaculture 37:63–71. https://doi.org/10.1016/0044-8486(84)90044-9
Cabrita E, Martínez-Páramo S, Gavaia PJ, Riesco MF, Valcarce DG, Sarasquete C, Herráez MP, Roblesbc V (2014) Factors enhancing fish sperm quality and emerging tools for sperm analysis. Aquaculture 432:389–401. https://doi.org/10.1016/j.aquaculture.2014.04.034
Caille N, Rodina M, Kocour M, Gela D, Flajšhans M, Linhart O (2006) Quantity, motility and fertility of tench Tinca tinca (L.) sperm in relation to LHRH analogue and carp pituitary treatments. Aquacult Int 14:75–87. https://doi.org/10.1007/s10499-005-9015-0
Cejko BI, Kowalski RK, Kucharczyk D, Zarski D, Targonska K, Glogowski J (2011) Effect of time after hormonal stimulation on semen quality indicators of common carp, Cyprinus carpio (Actinopterygii: Cypriniformes: Cyprinidae). Acta Ichthyol Piscatoria 41:75–80. https://doi.org/10.3750/AIP2011.41.2.01
Cejko BI, Horváth Á, Kollár T, Kása E, Lujić J, Marinović Z, Urbányi B, Kowalski RK (2018a) Optimisation of sodium and potassium concentrations and pH in the artificial seminal plasma of common carp Cyprinus carpio L. Fish Physiol Biochem 44:1435–1442. https://doi.org/10.1007/s10695-018-0491-3
Cejko BI, Sarosiek B, Krejszeff S, Kowalski RK (2018b) Multiple collections of common carp Cyprinus carpio L. semen during the reproductive period and its effects on sperm quality. Anim Reprod Sci 188:178–188. https://doi.org/10.1016/j.anireprosci.2017.12.002
Cheng Y, Franěk R, Rodina M, Xin MM, Cosson J, Zhang SP, Linhart O (2021a) Optimization of sperm management and fertilization in Zebrafish (Danio rerio (Hamilton)). Animals 11:1558. https://doi.org/10.3390/ani11061558
Cheng Y, Vechtova P, Fussy Z, Sterba J, Linhartová Z, Rodina M, Tučková V, Gela D, Samarin AM, Lebeda I, Xin MM, Zhang SP, Rahi D, Linhart O (2021b) Changes in phenotypes and DNA methylation of in vitro aging sperm in common carp Cyprinus carpio. Int J Mol Sci 22:5925. https://doi.org/10.3390/ijms22115925
Cheng Y, Zhang SP, Linhartová Z, Shazada NE, Linhart O (2022) Common carp (Cyprinus carpio) sperm reduction during short-term in vitro storage at 4 °C. Anim Reprod Sci 243:107017
Contreras P, Ulloa P, Merino O, Valdebenito I, Figueroa E, Farıas J, Risopatrón J (2017) Effect of short-term storage on sperm function in Patagonian blenny (Eleginops maclovinus) sperm. Aquaculture 481:58–63. https://doi.org/10.1016/j.aquaculture.2017.08.022
Contreras P, Dumorne K, Ulloa-Rodríguez P, Merino O, Figueroa E, Farias JG, Valdebenito I, Risopatrón J (2020) Effects of short-term storage on sperm function in fish semen: a review. Rev Aquac 12:1373–1389. https://doi.org/10.1111/raq.12387
Core R Team (2019) A language and environment for statistical computing; R Foundation for Statistical Computing: Vienna, Austria, Available online: https://www.R-project.org.
Courtois F, Takashima F, Billard R (1986) Stimulation of spermiation following repeated injection of carp pituitary homogenates in the carp. B Jpn Soc Sci Fish 52:995–997. https://doi.org/10.2331/suisan.52.995
Cruea DD (1969) Some chemical and physical characteristics of fish sperm. Trans Am Fish Sot 98:785–788. https://doi.org/10.1577/1548-8659(1969)98[785:SCAPCO]2.0.CO;2
Dietrich MA, Judycka S, Słowińska M, Kodzik N, Ciereszko A (2021) Short-term storage-induced changes in the proteome of carp (Cyprinus carpio L.) spermatozoa. Aquaculture 530:735784. https://doi.org/10.1016/j.aquaculture.2020.735784.
Dreanno C, Suquet M, Fauvel C, Le Coz JR, Dorange G, Quemener L, Billard R (1999) Effect of the aging process on the quality of sea bass (Dicentrarchus labrax) semen. J Appl Ichthyol 15:176–180
Gage MJG, Macfarlance 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. https://doi.org/10.1016/j.cub.2003.12.028
Gallego V, Pérez L, Asturiano JF, Yoshida M (2013) Relationship between spermatozoa motility parameters, sperm/egg ratio, and fertilization and hatching rates in pufferfish (Takifugu niphobles). Aquaculture 416:238–243. https://doi.org/10.1016/j.aquaculture.2013.08.035
Gallego V, Cavalcante SS, Fujimoto RY, Carneiro PCF, Azevedo HC, Maria AN (2017) Fish sperm subpopulations: changes after cryopreservation process and relationship with fertilization success in tambaqui (Colossoma macropomum). Theriogenology 87:16–24. https://doi.org/10.1016/j.theriogenology.2016.08.001
Gu NH, Zhao WL, Wang GS, Sun F (2019) Comparative analysis of mammalian sperm ultrastructure reveals relationships between sperm morphology, mitochondrial functions and motility. Reprod Biol Endocrinol 17:1–12. https://doi.org/10.1186/s12958-019-0510-y
Hassan MM, Nahiduzzaman M, Al Mamun SN, Taher MA, Hossain MAR (2013) Fertilization by refrigerator stored sperm of the Indian major carp, Labeo calbasu (Hamilton, 1822). Aquac Res 45:150–158. https://doi.org/10.1111/j.1365-2109.2012.03214.x
Horokhovatskyi Y, Dietrich MA, Lebeda I, Fedorov P, Rodina M, Dzyuba B (2018) Cryopreservation effects on a viable sperm sterlet (Acipenser ruthenus) subpopulation obtained by a Percoll density gradient method. PLoS ONE 13:e0202514. https://doi.org/10.1371/journal.pone.0202514
Hulata G, Rothbard S (1979) Cold storage of carp semen for short periods. Aquaculture 16:267–269. https://doi.org/10.1016/0044-8486(79)90116-9
Kołdras M, Bieniarz K, Kime DE (1990) Sperm production and steroidogenesis in testes of the common carp, Cyprinus carpio L, at different stages of maturation. J Fish Biol 37:635–645. https://doi.org/10.1111/j.1095-8649.1990.tb05897.x
Kowalski RK, Cejko BI (2019) Sperm quality in fish: determinants and affecting factors. Theriogenology 135:94–108
Lahnsteiner F, Mansour N, Plaetzer K (2010) Antioxidant systems of brown trout (Salmo trutta f. fario) semen. Anim Reprod Sci 119:314–321. https://doi.org/10.1016/j.anireprosci.2010.01.010
Lemaître JF, Gaillard JM, Ramm SA (2020) The hidden ageing costs of sperm competition. Ecol Lett 23:1573–1588. https://doi.org/10.1111/ele.13593
Linhart O, Mims SD, Gomelsky B, Hiott AE, Shelton WL, Cosson J, Rodina M, Gela D (2000) Spermiation of paddlefish (Polyodon spathula, Acipenseriformes) stimulated with injection of LHRH analogue and carp pituitary powder. Aquat Living Resour 13:455–460. https://doi.org/10.1016/S0990-7440(00)01068-8
Linhart O, Gela D, Rodina M, Kocour M (2004) Optimization of artificial propagation in European catfish, Silurus glanis L. Aquaculture 235:619–632. https://doi.org/10.1016/j.aquaculture.2003.11.031
Linhart O, Rodina M, Gela D, Kocour M, Vandeputte M (2005) Spermatozoal competition in common carp (Cyprinus carpio): what is the primary determinant of competition success? Reproduction 130:705–711. https://doi.org/10.1530/rep.1.00541
Linhart O, Cheng Y, Xin MM, Rodina M, Tučková V, Shelton WL, Kašpar V (2020b) Standardization of egg activation and fertilization in sterlet (Acipenser ruthenus). Aquac Rep 17:100381. https://doi.org/10.1016/j.aqrep.2020.100381
Linhart O, Cheng Y, Rodina M, Tučková V, Shelton WL, Tinkir M, Memiş D, Xin MM (2020a) Sperm management of European catfish (Silurus glanis L.) for effective reproduction and genetic conservation. Aquaculture 529, 735620. https://doi.org/10.1016/j.aquaculture.2020a.735620
Maklakov AA, Chapman T (2019) Evolution of ageing as a tangle of trade-offs: energy versus function. Proc R Soc B 286:20191604. https://doi.org/10.1098/rspb.2019.1604
Malinovskyi O, Policar T, Rahimnejad S, Křišťan J, Dzyuba B, Blecha M, Boryshpolets S (2021) Multiple sperm collection as an effective solution for gamete management in pikeperch (Sander lucioperca). Aquaculture 530:735870. https://doi.org/10.1016/j.aquaculture.2020.735870
Mylonas CC, Duncan NJ, Asturiano JF (2016) Hormonal manipulations for the enhancement of sperm production in cultured fish and evaluation of sperm quality. Aquaculture 472:21–44. https://doi.org/10.1016/j.aquaculture.2016.04.021
Park C, Chapman FA (2005) An extender solution for the short-term storage of sturgeon semen. N Am J Aqualcult 67:52–57. https://doi.org/10.1577/FA03-068.1
Perchec G, Jeulin C, Cosson J, André F, Billard R (1995) Relationship between sperm ATP content and motility of carp spermatozoa. J Cell Sci 108:747–753. https://doi.org/10.1242/jcs.108.2.747
Perchec G, Cosson MP, Cosson J, Jeulin C, Billard R (1996) Morphological and kinetic changes of carp (Cyprinus carpio) spermatozoa after initiation of motility in distilled water. Cell Motil Cytoskeleton 35:113–120. https://doi.org/10.1002/(SICI)1097-0169(1996)35:2%3c113::AID-CM4%3e3.0.CO;2-B
Reinhardt K, Siva-Jothy MT (2005) An advantage for young sperm in the house cricket Acheta domesticus. Am Nat 165:718–723. https://doi.org/10.1086/430010
Risopatrón J, Merino O, Cheuquemán C, Figueroa E, Sánchez R, Farías JG, Valdebenito I (2018) Effect of the age of brood-stock males on sperm function during cold storage in the trout (Oncorhynchus mykiss). Andrologia 50:e12857. https://doi.org/10.1111/and.12857
Rodina M, Cosson J, Gela D, Linhart O (2004) Kurokura solution as immobilizing medium for spermatozoa of tench (Tinca tinca L.). Aquac Int 12:119–131. https://doi.org/10.1023/B:AQUI.0000017192.75993.e3
Rurangwa E, Volckaert FAM, Huyskens G, Kime DE, Ollevier F (2001) A concerted strategy for the quality control of refrigerated and cryopreserved semen using computer-assisted sperm analysis (CASA), viable staining and standardized fertilization: application to preservation of sperm of African catfish (Clarias gariepinus). Theriogenology 55:751–769. https://doi.org/10.1016/S0093-691X(01)00441-1
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. https://doi.org/10.1016/j.aquaculture.2003.12.006
Saad A, Billard R (1987) Spermatozoa production and volume of semen collected after hormonal stimulation in the carp, Cyprinus carpio. Aquaculture 65:67–77. https://doi.org/10.1016/0044-8486(87)90271-7
Saad A, Billard R, Theron MC (1988) Hollebecq MG. Short-term preservation of carp (Cyprinbs carpio) semen. Aquaculture 71:133–150. https://doi.org/10.1016/0044-8486(88)90280-3
Sanocka D, Kurpisz M (2004) Reactive oxygen species and sperm cells. Reprod Biol Endocrinol 2:1–7. https://doi.org/10.1186/1477-7827-2-12
Sarosiek B, Dryl K, Kucharczyk D, Żarski D, Kowalski RK (2014) Motility parameters of perch spermatozoa (Perca fluviatilis L.) during short-term storage with antioxidants addition. Aquacult Int 22:159–165. https://doi.org/10.1007/s10499-013-9679-9
Shaliutina A, Dzyuba B, Hulak M, Boryshpolets S, Li P, Linhart O (2012) Evaluation of spermiation indices with multiple sperm collections in endangered sterlet (Acipenser ruthenus). Reprod Domest Anim 47:479–484. https://doi.org/10.1111/j.1439-0531.2011.01907.x
Shaliutina A, Hulak M, Gazo I, Linhartova P, Linhart O (2013) Effect of short-term storage on quality parameters, DNA integrity, and oxidative stress in Russian (Acipenser gueldenstaedtii) and Siberian (Acipenser baerii) sturgeon sperm. Anim Reprod Sci 139:127–135. https://doi.org/10.1016/j.anireprosci.2013.03.006
Stoss J, Refstie T (1983) Short-term storage and cryopreservation of milt from Atlantic salmon and sea trout. Aquaculture 30:229–236. https://doi.org/10.1016/0044-8486(83)90165-5
Trigo P, Merino O, Figueroa E, Valdebenito I, Sánchez R, Risopatrón J (2015) Effect of short-term semen storage in salmon (Oncorhynchus mykiss) on sperm functional parameters evaluated by flow cytometry. Andrologia 47:407–411. https://doi.org/10.1111/and.12276
Ulloa-Rodríguez P, Contreras P, Dumorné K, Lee-Estevez M, Díaz R, Figueroa E, Valdebenito I, Risopatrón J, Farías JG (2018) Patagonian blenny (Eleginops maclovinus) spermatozoa quality after storage at 4 ºC in Cortland medium. Anim Reprod Sci 197:117–125. https://doi.org/10.1016/j.anireprosci.2018.08.019
Vandeputte M, Launey S (2004) The genetic management of fish domestication. Prod Anim 17:237–242
Zi JM, Pan XF, MacIsaac HJ, Yang JX, Xu RB, Chen SY, Chang XX (2018) Cyanobacteria blooms induce embryonic heart failure in an endangered fish species. Aquat Toxicol 194:78–85. https://doi.org/10.1016/j.aquatox.2017.11.007
Acknowledgements
Thanks to the University of South Bohemia in Ceske Budejovice, the Faculty of Fisheries and Protection of Waters, the Genetic Fisheries Centre (GFC) provided fish for this study.
Funding
This study was funded by the Ministry of Education, Youth and Sports of the Czech Republic (LRI CENAKVA, LM2018099), by the Grant Agency of the University of South Bohemia in Ceske Budejovice (097/2019/Z, 037/2020/Z), by the Czech Science Foundation (20-01251S) and by the National Agency for Agriculture Research, Czech Republic (QK21010141). Songpei Zhang and Yu Cheng were supported by the Chinese Scholarship Council.
Author information
Authors and Affiliations
Contributions
Songpei Zhang conceived, designed, carried out experiments, performed statistical analysis, and wrote and revised the manuscript. Yu Cheng conceived, designed, carried out experiments, performed statistical analysis, and revised the manuscript. Zuzana Linhartová carried out experiments and revised the manuscript. Vladimíra Rodinová carried out experiments. Nururshopa Eskander Shazada revised manuscript. Qing Wu performed statistical analysis. Otomar Linhart conceived, designed, carried out experiments, and wrote and revised the manuscript.
Corresponding author
Ethics declarations
Ethics approval
The facility has the competence to perform experiments on animals (Act no. 246/1992 Coll., ref. number 16OZ19179/2016–17214). The expert committee approved the methodological protocol of the current study of the Institutional Animal Care and Use Committee of the FFPW according to the law on the protection of animals against cruelty (reference number: MSMT-6406/119/2). This research did not involve endangered or protected species. The authors of this study (ZL, and OL) own a certificate of professional competence for designing experiments and experimental projects under Sect. 15d (3) of Act no. 246/1992 Coll. on the Protection of Animals against Cruelty.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, S., Cheng, Y., Linhartová, Z. et al. In vivo and in vitro aging of common carp Cyprinus carpio sperm after multiple hormonal application and stripping of males. Fish Physiol Biochem 48, 1235–1250 (2022). https://doi.org/10.1007/s10695-022-01114-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-022-01114-z