Fish Physiology and Biochemistry

, Volume 45, Issue 6, pp 1791–1800 | Cite as

In vitro antioxidant enzyme activity and sperm motility at different temperatures in sterlet Acipenser ruthenus and rainbow trout Oncorhynchus mykiss

  • Hadiseh DadrasEmail author
  • Viktoriya Dzyuba
  • Amin Golpour
  • Miaomiao Xin
  • Borys Dzyuba


Influence of in vitro temperature on sperm antioxidant enzyme activity, thiobarbituric acid-reactive substance (TBARS) content and motility parameters was evaluated in sterlet Acipenser ruthenus and rainbow trout Oncorhynchus mykiss. Sperm activation was conducted at 4, 14 and 24 °C in both species. Duration of motility was significantly longer at 4 °C than at 14 and 24 °C in both species. At 60 s post-activation, the velocity of sterlet spermatozoa was highest at 24 °C. This trend continued to 420 s post-activation. In rainbow trout, at 10 s post-activation, the highest velocity was observed at 14 °C. Significantly higher catalase activity was seen at 4 °C in both species. No significant difference in spermatozoon superoxide dismutase activity among temperatures was observed. In sterlet, TBARS content was significantly higher at 24 °C compared to other temperatures, but, in rainbow trout, it was highest at 4 °C. The results presume species-specific level of antioxidant enzyme activity and TBARS content at studied temperatures.


Antioxidant enzyme Fish Sperm function Temperature 



The study was financially supported by the Ministry of Education, Youth and Sports of the Czech Republic, projects: CENAKVA (LM2018099), Biodiversity (CZ.02.1.01./0.0/0.0/16_025/0007370) and GAJU (122/2019/Z) and by the Ministry of Agriculture of the Czech Republic, project NAZV QK1710310.


  1. Aas GH, Refstie T, Gjerde B (1991) Evaluation of milt quality of Atlantic salmon. Aquaculture 95:125–132Google Scholar
  2. Alavi SMH, Cosson J (2005) Sperm motility in fishes: I. Effects of temperature and pH. Cell Biol Int 29:101–110PubMedGoogle Scholar
  3. Alvarez JG, Storey BT (1985) Spontaneous lipid peroxidation in rabbit and mouse spermatozoa: dependence of rate on temperature and oxygen concentration. Biol Reprod 32:342–351PubMedGoogle Scholar
  4. Alvarez JG, Touchstone JC, Blasco L, Storey BT (1987) Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa: superoxide dismutase as major enzyme protectant against oxygen toxicity. Andrology 8:338–348Google Scholar
  5. Asakawa T, Matsushita S (1980) Coloring conditions of thiobarbituric acid test for detecting lipid hydroperoxides. Lipids 15:137–140Google Scholar
  6. Beirão J, Soares F, MP H’e, Dinis MT, Cabrita E (2011) Changes in Solea senegalensis sperm quality throughout the year. Anim Reprod Sci 126:122–129PubMedGoogle Scholar
  7. Beirão J, Purchase CF, Wringe B, Fleming IA (2014) Sperm plasticity to seawater temperatures in Atlantic cod Gadus morhua is affected more by population origin than individual environmental exposure. Mar Ecol Prog Ser 495:263–274Google Scholar
  8. Billard R, Cosson J, Crim LW, Suquet M (1995) Sperm physiology and quality. In: Bromage NR, Roberts RJ (eds) Brood stock management and egg and larval quality. Blackwell Science, London, Chap.2, pp 25–52Google Scholar
  9. Boryshpolets S, Dzyuba B, Drokin S (2009) Pre-spawning water temperature affects sperm respiration and reactivation parameters in male carps. Fish Physiol Biochem 35:661–668PubMedGoogle Scholar
  10. Bradford MM (1976) Rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle dye binding. Anal Biochem 72:248–254PubMedPubMedCentralGoogle Scholar
  11. Cabrita E, Martínez-Páramo S, Gavaia PJ, Riesco MF, Valcarce DG, Sarasquete C, Herráez MP, Robles V (2014) Factors enhancing fish sperm quality and emerging tools for sperm analysis. Aquaculture 432:389–401Google Scholar
  12. Christen R, Gatti JL, Billard R (1987) Trout sperm motility. The transient movement of trout sperm is related to changes in the concentration of ATP following the activation of the flagellar movement. Eur J Biochem 166:667–671PubMedGoogle Scholar
  13. Ciereszko A, Dabrowski K, Lin F, Liu L (1999) Protective role of ascorbic acid against damage to male germ cells in rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 56:178–183Google Scholar
  14. Dadras H, Dzyuba V, Cosson J, Golpour A, Dzyuba B (2016) The in vitro effect of temperature on motility and antioxidant response of common carp Cyprinus carpio spermatozoa. J Therm Biol 59:64–68PubMedGoogle Scholar
  15. Dadras H, Dzyuba B, Cosson J, Golpour A, Siddique MAM, Linhart O (2017) Effect of water temperature on the physiology of fish spermatozoa function: a brief review. Aquac Res 48:729–740Google Scholar
  16. Dzyuba V, Cosson J, Dzyuba B, Rodina M (2015) Oxidative stress and motility in tench Tinca tinca spermatozoa. Czech J Anim Sci 60(6):250–255Google Scholar
  17. Fedorov P, Dzyuba B, Fedorova G, Grabic R, Cosson J, Rodina M (2015) Quantification of adenosine triphosphate, adenosine diphosphate, and creatine phosphate in sterlet Acipenser ruthenus spermatozoa during maturation. J Anim Sci 93:5214–5221PubMedGoogle Scholar
  18. Foldesy RG, Bedford JM (1982) Biology of the scrotum. I. Temperature and androgen as determinants of the sperm storage capacity of the rat cauda epididymidis. Biol Reprod 26:673–682PubMedGoogle Scholar
  19. Ingermann RL (2008) Energy metabolism and respiration in fish spermatozoa. In: Alavi SMH, Cosson J, Coward K, Rafiee G (eds) Fish spermatology. Alpha Science, Oxford, pp 241–279Google Scholar
  20. Khosrowbeygi A, Zarghami N, Deldar Y (2004) Correlation between sperm quality parameters and seminal plasma antioxidants status. Iran J Reprod Med 2:58–64Google Scholar
  21. Kim KS, Lee D, Song CG, Kang PM (2015) Reactive oxygen species-activated nanomaterials as theranostic agents. Nanomedicine 10(17):2709–2723PubMedPubMedCentralGoogle Scholar
  22. Lahnsteiner F (2012) Thermotolerance of brown trout, Salmo trutta, gametes and embryos to increased water temperatures. J Appl Ichthyol 28:745–751Google Scholar
  23. Lahnsteiner F, Caberlotto S (2012) Motility of gilthead seabream Sparus aurata spermatozoa and its relation to temperature, energy metabolism and oxidative stress. Aquaculture 370:76–83Google Scholar
  24. Lahnsteiner F, Mansour N (2010) A comparative study on antioxidant systems in semen of species of the Percidae, Salmonidae, Cyprinidae, and Lotidae for improving semen storage techniques. Aquaculture 307:130–140Google Scholar
  25. Lahnsteiner F, Mansour N (2012) The effect of temperature on sperm motility and enzymatic activity in brown trout, Salmo trutta, burbot, Lota lota and grayling, Thymallus thymallus. J Fish Biol 81(1):197–209PubMedGoogle Scholar
  26. Lahnsteiner F, Berger B, Weismann T (1999) Sperm metabolism of the teleost fishes Oncorhynchus mykiss and Chalcalburnus chalcoides and its relation to motility and viability. J Exp Zool 284:454–465PubMedGoogle Scholar
  27. Lahnsteiner F, Mansour N, Plaetzer K (2010) Antioxidant systems of brown trout (Salmo trutta f. fario) semen. Anim Reprod Sci 119(3–4):314–321PubMedGoogle Scholar
  28. Liu QH, Wang XY, Wang WQ, Zhang XL, Xu SH, Ma DY, Xiao ZY, Xiao YS, Li J (2014) Effect of the addition of six antioxidants on sperm motility, membrane integrity and mitochondrial function in red seabream (Pagrus major) sperm cryopreservation. Fish Physiol Biochem 41(2):413–422PubMedGoogle Scholar
  29. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30PubMedGoogle Scholar
  30. Lushchak VI, Bagnyukova TV (2006) Temperature increase results in oxidative stress in goldfish tissues. Antioxidant and associated enzymes. Comp Biochem Physiol 143:36–41Google Scholar
  31. Madeira D, Narciso L, Cabral HN, Vinagre C, Diniz MS (2013) Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comp Biochem Physiol A 166:237–243Google Scholar
  32. Mansour N, McNiven MA, Richardson GF (2006) The effect of dietary supplement with blueberry, alpha-tocopherol or astaxanthin on oxidative stability of Arctic char (Salvelinus alpines) semen. Theriogenology 66:373–382PubMedGoogle Scholar
  33. Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474Google Scholar
  34. Marklund S, Nordensson I, Back O (1981) Normal CuZn superoxide dismutase, Mn superoxide dismutase, catalase and glutathione peroxidase in Werner's syndrome. J Gerontol 36:405–409PubMedGoogle Scholar
  35. Mehlis M, Bakker TCM (2014) The influence of ambient water temperature on sperm performance and fertilization success in three-spined sticklebacks (Gasterosteus aculeatus). Evol Ecol 28:655–667Google Scholar
  36. Morgulis S, Beber M, Rabkin I (1926) Studies on the effect of temperature on the catalase reaction: I. Effect of different hydrogen peroxide concentrations. J Biol Chem 68:521–533Google Scholar
  37. Nichi M, Bols PEJ, Zuge RM, Barnabe VH, Goovaerts IGF, Barnabe RC, Cortada CNM (2006a) Seasonal variation in semen quality in Bos indicus and Bos taurus bulls raised under tropical conditions. Theriogenology 66:822–828PubMedGoogle Scholar
  38. Nichi M, De Clercq JBP, Goovaerts IGF, Barnabe VH, Bols PEJ (2006b) Effect of bull epididymis storage conditions on sperm resistance against lipid peroxidation and subsequent in vitro embryo production. Rep Fert Dev 18:261Google Scholar
  39. Perchec G, Jeulin C, Cosson J, Andr’e F, Billard R (1995) Relationship between sperm ATP content and motility of carp spermatozoa. J Cell Sci 108:747–753PubMedGoogle Scholar
  40. Purchase CF, Butts IAE, Alonso-Fernandez A, Trippel EA (2010) Thermal reaction norms in sperm performance of Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 67:498–510Google Scholar
  41. Rurangwa E, Volckaert F, Huyskens G, Kime D, Ollevier F (2001) Quality control of refrigerated and cryopreserved semen using computer-assisted sperm analysis (CASA), viable staining and standardized fertilization in African catfish (Clarias gariepinus). Theriogenology 55:751–769PubMedGoogle Scholar
  42. Rurangwa E, Kimeb DE, Ollevier F, Nash JP (2004) The measurement of sperm motility and factors affecting sperm quality in cultured fish. Aquaculture 234:1–28Google Scholar
  43. Saleh RA, Agarwal A (2002) Oxidative stress and male infertility: from research bench to clinical practice. J Androl 23:737–752PubMedGoogle Scholar
  44. Shaliutina-Kolešová A, Gazo I, Cosson J, Linhart O (2013) Comparison of oxidant and antioxidant status of seminal plasma and spermatozoa of several fish species. Czech J Anim Sci 58(7):313–320Google Scholar
  45. Shaliutina-Kolešová A, Rui N, Ashtiani S, Rodina M, Cosson J, Linhart O (2018) Oxidative stress and antioxidant enzyme defence system in seminal plasma of common carp (Cyprinus carpio) and rainbow trout (Oncorhynchus mykiss) during spawning season. Czech J Anim Sci 63(2):78–84Google Scholar
  46. Sharma RK, Agarwal A (1996) Role of reactive oxygen species in male infertility. Urology 48:835–850PubMedGoogle Scholar
  47. Shiva M, Gautam AK, Verma Y, Shivgotra V, Doshi H, Kumar S (2011) Association between sperm quality, oxidative stress, and seminal antioxidant activity. Clin Biochem 44:319–324PubMedGoogle Scholar
  48. Sikka SC (2004) Role of oxidative stress and antioxidants in andrology and assisted reproductive technology. Andrology 25:5–18Google Scholar
  49. Sikka SC, Rajasekaran M, Hellstrom WJ (1995) Role of oxidative stress and antioxidants in male infertility. Andrology 16:464–468Google Scholar
  50. Stoss J (1983) Fish gamete preservation and spermatozoan physiology. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology, vol 1X B. Academic Press, New York, USA, pp 305–350Google Scholar
  51. Tsvetkova LI, Cosson J, Linhart O, Billard R (1996) Motility and fertilizing capacity of native and frozen-thawed spermatozoa in sturgeon baeri (Acipenser baeri) and sterlet (Acipenser ruthenus). J Appl Ichthyol 12:107–112Google Scholar
  52. Williot P, Kopeika EF, Goncharov BF (2000) Influence of testis state, temperature and delay in semen collection on spermatozoa motility in the cultured Siberian sturgeon (Acipenser baerii Brand). Aquaculture 189:53–61Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Faculty of Fisheries and Protection of Waters, South Bohemia in Research Center of Aquaculture and Biodiversity of Hydrocenoses, Research Institute of Fish Culture and HydrobiologyUniversity of South Bohemia in Ceske BudejoviceVodňanyCzech Republic
  2. 2.State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology Chinese Academy of Sciences, Innovation Academy for Seed DesignWuhanChina

Personalised recommendations