Role of trace minerals in bull reproductive physiology and semen quality
Keywords:
Cattle, sperm, zinc, selenium, copper, manganese
Abstract
Testicular dysfunction is often associated with an imbalance in antioxidant/oxidant homeostasis, leading to negative effects of oxidative stress on germ cell proliferation, steroidogenesis, and sperm function. Trace minerals (TM) are involved in basic homeostatic and enzymatic processes like free radical detoxification, cellular respiration, carbohydrates, lipids, nucleic acids, synthesis and metabolism of proteins, and stabilization of membranes and DNA. Dietary source of TM is necessary to support these processes. Supplementing cattle with TM is nowadays a common practice to help support growth, reproduction, and immunity. This review provides information on roles of TM in bulls testicular and sperm functions, and effects of TM mineral supplementation on bull reproductive parameters.
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References
1. USDA report – National Animal Health Monitoring System, Beef 2007-08 Part II: reference of beef cow-calf management practices in the United States, 2007-08, February 2009.
2. Kanter M, Aktas C, Erboga M: Heat stress decreases testicular germ cell proliferation and increases apoptosis in short term: an immunohistochemical and ultrastructural study. Toxicol Ind Health 2013;29:99–113. doi: 10.1177/0748233711425082
3. Paul C, Teng S, Saunders PTK: A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod 2009;80:913–919. doi: 10.1095/biolreprod.108.071779
4. Duramayanthi D, Agarwal A, Ong C: Causes, effects and molecular mechanisms of testicular heat stress. Reprod Biomed Online 2015;30:14–27. doi: 10.1016/j.rbmo.2014.09.018
5. Nenkova G, Petrov L, Alexandrova A: Role of trace elements for oxidative status and quality of human sperm. Balkan Med J 2017;34:343–348. doi: 10.4274/balkanmedj.2016.0147
6. Kumar N, Verma RP, Singh LP, et al: Effect of different levels and sources of zinc supplementation on quantitative and qualitative semen attributes and serum testosterone level in crossbred cattle (Bos indicus × Bos taurus) bulls. Reprod Nutr Dev 2006;46: 663–675. doi: 10.1051/rnd:2006041
7. Juárez-Rojas L, Casillas F, López A, et al: Physiological role of reactive oxygen species in testis and epididymal spermatozoa. Androl 2022;54:e14367. doi: 10.1111/and.14367
8. Mancini A, Oliva A, Vergani E, et al: The dual role of oxidants in male (in)fertility: every rose has a thorn. Int J Mol Sci 2023;24:4994. doi: 10.3390/ijms24054994
9. Upadhyay VR, Ramesh V, Dewry RK, et al: Bimodal interplay of reactive oxygen and nitrogen species in physiology and pathophysiology of bovine sperm function. Theriogenology 2022;187:82–94. doi: 10.1016/j.theriogenology.2022.04.024
10. Bahr GF, Engler WF: Considerations of volume, mass, DNA, and arrangement of mitochondria in the midpiece of bull spermatozoa. Experimental Cell Res 1970;60:338–340. doi: 10.1016/0014-4827(70)90526-4
11. Barati E, Nikzad H, Karimian M: Oxidative stress and male infertility: current knowledge of pathophysiology and role of antioxidant therapy in disease management. Cell Mol Life Sci 2020;77:93–113. doi: 10.1007/s00018-019-03253-8
12. Gibb Z, Blanco-Prieto O, Bucci D: The role of endogenous antioxidants in male animal fertility. Res Vet Sci 2021;136:495–502. doi: 10.1016/j.rvsc.2021.03.024
13. Kowalczyk A: The role of the natural antioxidant mechanism in sperm cells. Reprod Sci 2022;29:1387–1394. doi: 10.1007/s43032-021-00795-w
14. O’Flaherty C, Scarlata E: The protection of mammalian spermatozoa against oxidative stress. Reproduction 2022;164:F67–F78. doi: 10.1530/REP-22-0200
15. Tvrda E, Peer R, Sikka SC, et al: Iron and copper in male reproduction: a double-edged sword. J Assist Reprod Genet 2015;32:3–16. doi: 10.1007/s10815-014-0344-7
16. Arangasamy A, Krishnaiah MV, Manohar N, et al: Cryoprotective role of organic Zn and Cu supplementation in goats (Capra hircus) diet. Cryobiology 2018;81:117–124. doi: 10.1016/j.cryobiol.2018.02.001
17. Arangasamy A, Sharma RB, Hemalatha K, et al: Relationship of organic mineral supplementation and spermatozoa/white blood cells mRNA in goats. Anim Reprod Sci 2018;197:296–304. doi: 10.1016/j.anireprosci.2018.08.044
18. Arangasamy A, Venkata Krishnaiah M, Manohar N, et al: Advancement of puberty and enhancement of seminal characteristics by supplementation of trace minerals to bucks. Theriogenology 2018;110: 182–191. doi: 10.1016/j.theriogenology.2018.01.008
19. Narasimhaiah M, Arunachalam A, Sellappan S, et al: Organic zinc and copper supplementation on antioxidant protective mechanism and their correlation with sperm functional characteristics in goats. Reprod Domest Anim 2018;53:644–654. doi: 10.1111/rda.13154
20. Venkata Krishnaiah M, Arangasamy A, Selvaraju S, et al: Organic Zn and Cu interaction impact on sexual behaviour, semen characteristics, hormones and spermatozoal gene expression in bucks (Capra hircus). Theriogenology 2019;130:130–139. doi: 10.1016/j.theriogenology.2019.02.026
21. Gupta A, Kumar A, Naqvi S, et al: Chronic exposure to multi-metals on testicular toxicity in rats. Toxicol Mech Methods 2021;31: 53–66. doi: 10.1080/15376516.2020.1828522
22. Li Y, Chen H, Liao J, et al: Long-term copper exposure promotes apoptosis and autophagy by inducing oxidative stress in pig testis. Environ Sci Poll Res 2021;28:55140–55153. doi: 10.1007/s11356-021-14853-y
23. Liu JY, Yang X, Sun XD, et al: Suppressive effects of copper sulfate accumulation on the spermatogenesis of rats. Biol Trace Elem Res 2016;174:356–361. doi: 10.1007/s12011-016-0710-7
24. Mayasula VK, Arunachalam A, Babatunde SA, et al: Trace minerals for improved performance: a review of Zn and Cu supplementation effects on male reproduction in goats. Trop Anim Health Prod 2021;53:491. doi: 10.1007/s11250-021-02943-5
25. Harchegani AB, Dahan H, Tahmasbpour E, et al: Effects of zinc deficiency on impaired spermatogenesis and male infertility: the role of oxidative stress, inflammation and apoptosis, Human Fertil 2020;23:5–16. doi: 10.1080/14647273.2018.1494390
26. Wroblewski N, Schill WB, Henkel R: Metal chelators change the human sperm motility pattern. Fertil Steril 2003;79:1584–1589. doi: 10.1016/S0015-0282(03)00255-3
27. Björndahl L, Kvist U: Human sperm chromatin stabilization: a proposed model including zinc bridges. Mol Human Reprod 2010;16:23–29. doi: 10.1093/molehr/gap099
28. Kumari D, Nair N, Bedwal RS: Testicular apoptosis after dietary zinc deficiency: ultrastructural and TUNEL studies. Systems Biol Reprod Med 2011;57:233–243. doi: 10.3109/19396368.2011.584500
29. Mayasula VK, Arunachalam A, Sellappan S, et al: Organic Zn and Cu supplementation imprints on seminal plasma mineral, biochemical/ antioxidant activities and its relationship to spermatozoal characteristics in bucks. Reprod Biol 2020;20:220–228. doi: 10.1016/j.repbio.2020.02.007
30. Rahman HU, Qureshi MS, Khan RU: Influence of dietary zinc on semen traits and seminal plasma antioxidant enzymes and trace minerals of Beetal bucks. Reprod Dom Anim 2014;49:1004–1007. doi: 10.1111/rda.12422
31. Tajaddini S, Ebrahimi S, Behnam B, et al: Antioxidant effect of manganese on the testis structure and sperm parameters of formalin-treated mice. Androl 2014;46:246–253. doi: 10.1111/and.12069
32. Lee B, Pine M, Johnson L, et al: Manganese acts centrally to activate reproductive hormone secretion and pubertal development in male rats. Reprod Toxicol 2006;22:580–585. doi: 10.1016/j.reprotox.2006.03.011
33. Tarun A, Mani V, Bhakat M, et al: Effect of dietary supplementation of manganese, chromium and cobalt on semen qualities in Sahiwal bulls. Indian J Anim Res 2020;54:1109–1114. doi: 10.18805/ijar.B-3870
34. Souza TL, Batschauer AR, Brito PM, et al: Evaluation of Mn exposure in the male reproductive system and its relationship with reproductive dysfunction in mice. Toxicol 2020;441:152504. doi: 10.1016/j.tox.2020.152504
35. Reis LSLS, Ramos AA, Camargos AS, et al: Effect of manganese supplementation on the membrane integrity and the mitochondrial potential of the sperm of grazing Nelore bulls. Anim Reprod Sci 2014;150:1–6. doi: 10.1016/j.anireprosci.2014.06.033
36. El-Sharawy M, Eid E, Darwish S, et al: Effect of organic and inorganic selenium supplementation on semen quality and blood enzymes in buffalo bulls. Anim Sci J 2017;88:999–1005. doi: 10.1111/asj.12736
37. Ahsan U, Kamran Z, Raza I, et al: Role of selenium in male reproduction-A review. Anim Reprod Sci 2014;146:55–62. doi: 10.1016/j.anireprosci.2014.01.009
38. Smith DG, Senger PL, McCutchan JF, et al: Selenium and glutathione peroxidase distribution in bovine semen and selenium-75 retention by the tissues of the reproductive tract in the bull. Biol Reprod 1979;20:377–383. doi: 10.1095/biolreprod20.2.377
39. Vanha-Perttula T, Remes E: Incorporation of Selenium-75 into seminal plasma and spermatozoa of the bull. Andrologia 1989;22:34–41. doi: 10.1111/j.1439-0272.1990.tb01937.x
40. Bartle JL, Senger PL, Hillers JK: Influence of injected selenium in dairy bulls on blood and semen selenium, glutathione peroxidase and seminal quality. Biol Reprod 1980;23: 1007–1013. doi: 10.1095/biolreprod23.5.1007
41. Marin-Guzman J, Mahan DC, Chung YK, et al: Effects of dietary selenium and vitamin e on boar performance and tissue responses, semen quality, and subsequent fertilization rates in mature gilts. J Anim Sci 1997;75:2994–3003. doi: 10.2527/1997.75112994x
42. Piagentini M, Silva DC, Dell’Aqua CFP, et al: Effect of selenium supplementation on semen characteristics of Brazil’s ram. Reprod Dom Anim 2017;52:355–358. doi: 10.1111/rda.12903
43. Kaur P, Bansal MP: Effect of selenium-induced oxidative stress on the cell kinetics in testis and reproductive ability of male mice. Nutrition 2005;21:351–357. doi: 10.1016/j.nut.2004.05.028
44. Yang X, Chen Y, Song W, et al: Review of the role of ferroptosis in testicular function. Nutrients 2022;14:5268. doi: 10.3390/nu14245268
45. Tsao C-W, Liao Y-R, Chang T-C, et al: Effects of iron supplementation on testicular function and spermatogenesis of iron-deficient rats. Nutrients 2022;14:2063. doi: 10.3390/nu14102063
46. Zakošek Pipan M, Zrimšek P, Strajn BJ, et al. Macro- and microelements in serum and seminal plasma as biomarkers for bull sperm cryotolerance. Acta Vet Scand 2021;63:25. doi: 10.1186/s13028-021-00590-2
47. Tvrdá E, Lukáč N, Lukáčová J, et al: Dose- and time-dependent in vitro effects of divalent and trivalent iron on the activity of bovine spermatozoa. Biol Trace Elem Res 2015;167:36–47. doi: 10.1007/s12011-015-0288-5
48. Narud B, Klinkenberg G, Khezri A, et al: Differences in sperm functionality and intracellular metabolites in Norwegian Red bulls of contrasting fertility. Theriogenology 2020;157:24–32. doi: 10.1016/j.theriogenology.2020.07.005
49. Aguiar GFM, Batista BL, Rodrigues JL, et al: Determination of trace elements in bovine semen samples by inductively coupled plasma mass spectrometry and data mining techniques for identification of bovine class. J Dairy Sci 2012;95:7066–7073. doi: 10.3168/jds.2012-5515
50. Khaki A, Araghi A, Lotfi M, et al: Differences between some biochemical components in seminal plasma of first and second ejaculations in dual-purpose Simmental (Fleckvieh) bulls and their relationships with semen quality parameters. Vet Res Forum 2021;12:39–46.
51. Tvrda E, Lukac N, Schneridgenova M, et al: Impact of seminal chemical elements on the oxidative balance in bovine seminal plasma and spermatozoa. J Vet Med 2013;125096. doi: 10.1155/2013/125096
52. Geary TW, Kelly WL, Spickard DS, et al: Effect of supplemental trace mineral level and form on peripubertal bulls. Anim Reprod Sci 2016;168:1–9. doi: 10.1016/j.anireprosci.2016.02.018
53. Geary TW, Waterman RC, Van Emon ML, et al: Effect of supplemental trace minerals on standard and novel measures of bull fertility. Theriogenology 2021;172:307–314. doi: 10.1016/j.theriogenology.2021.07.006
54. Kirchhoff AA, Fike KE, Breiner R: An injectable trace mineral supplement in yearling bulls causes a short-term increase in circulating trace mineral levels but does not improve sperm quality. Kansas Agric Exp Station Res Rep 2015;1:1. doi: 10.4148/2378-5977.1024
55. Preedy GW, Hill SL, Stevenson JS, et al: Injectable trace-mineral supplementation improves sperm motility and morphology of young beef bulls. Anim Sci 2018;34:1–9. doi: 10.15232/pas.2017-01667
56. Rowe MP, Powell JG, Kegley EB, et al: Influence of supplemental trace-mineral source on bull semen quality. Anim Sci 2014;30: 68–73. doi: 10.15232/S1080-7446(15)30085-1
2. Kanter M, Aktas C, Erboga M: Heat stress decreases testicular germ cell proliferation and increases apoptosis in short term: an immunohistochemical and ultrastructural study. Toxicol Ind Health 2013;29:99–113. doi: 10.1177/0748233711425082
3. Paul C, Teng S, Saunders PTK: A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod 2009;80:913–919. doi: 10.1095/biolreprod.108.071779
4. Duramayanthi D, Agarwal A, Ong C: Causes, effects and molecular mechanisms of testicular heat stress. Reprod Biomed Online 2015;30:14–27. doi: 10.1016/j.rbmo.2014.09.018
5. Nenkova G, Petrov L, Alexandrova A: Role of trace elements for oxidative status and quality of human sperm. Balkan Med J 2017;34:343–348. doi: 10.4274/balkanmedj.2016.0147
6. Kumar N, Verma RP, Singh LP, et al: Effect of different levels and sources of zinc supplementation on quantitative and qualitative semen attributes and serum testosterone level in crossbred cattle (Bos indicus × Bos taurus) bulls. Reprod Nutr Dev 2006;46: 663–675. doi: 10.1051/rnd:2006041
7. Juárez-Rojas L, Casillas F, López A, et al: Physiological role of reactive oxygen species in testis and epididymal spermatozoa. Androl 2022;54:e14367. doi: 10.1111/and.14367
8. Mancini A, Oliva A, Vergani E, et al: The dual role of oxidants in male (in)fertility: every rose has a thorn. Int J Mol Sci 2023;24:4994. doi: 10.3390/ijms24054994
9. Upadhyay VR, Ramesh V, Dewry RK, et al: Bimodal interplay of reactive oxygen and nitrogen species in physiology and pathophysiology of bovine sperm function. Theriogenology 2022;187:82–94. doi: 10.1016/j.theriogenology.2022.04.024
10. Bahr GF, Engler WF: Considerations of volume, mass, DNA, and arrangement of mitochondria in the midpiece of bull spermatozoa. Experimental Cell Res 1970;60:338–340. doi: 10.1016/0014-4827(70)90526-4
11. Barati E, Nikzad H, Karimian M: Oxidative stress and male infertility: current knowledge of pathophysiology and role of antioxidant therapy in disease management. Cell Mol Life Sci 2020;77:93–113. doi: 10.1007/s00018-019-03253-8
12. Gibb Z, Blanco-Prieto O, Bucci D: The role of endogenous antioxidants in male animal fertility. Res Vet Sci 2021;136:495–502. doi: 10.1016/j.rvsc.2021.03.024
13. Kowalczyk A: The role of the natural antioxidant mechanism in sperm cells. Reprod Sci 2022;29:1387–1394. doi: 10.1007/s43032-021-00795-w
14. O’Flaherty C, Scarlata E: The protection of mammalian spermatozoa against oxidative stress. Reproduction 2022;164:F67–F78. doi: 10.1530/REP-22-0200
15. Tvrda E, Peer R, Sikka SC, et al: Iron and copper in male reproduction: a double-edged sword. J Assist Reprod Genet 2015;32:3–16. doi: 10.1007/s10815-014-0344-7
16. Arangasamy A, Krishnaiah MV, Manohar N, et al: Cryoprotective role of organic Zn and Cu supplementation in goats (Capra hircus) diet. Cryobiology 2018;81:117–124. doi: 10.1016/j.cryobiol.2018.02.001
17. Arangasamy A, Sharma RB, Hemalatha K, et al: Relationship of organic mineral supplementation and spermatozoa/white blood cells mRNA in goats. Anim Reprod Sci 2018;197:296–304. doi: 10.1016/j.anireprosci.2018.08.044
18. Arangasamy A, Venkata Krishnaiah M, Manohar N, et al: Advancement of puberty and enhancement of seminal characteristics by supplementation of trace minerals to bucks. Theriogenology 2018;110: 182–191. doi: 10.1016/j.theriogenology.2018.01.008
19. Narasimhaiah M, Arunachalam A, Sellappan S, et al: Organic zinc and copper supplementation on antioxidant protective mechanism and their correlation with sperm functional characteristics in goats. Reprod Domest Anim 2018;53:644–654. doi: 10.1111/rda.13154
20. Venkata Krishnaiah M, Arangasamy A, Selvaraju S, et al: Organic Zn and Cu interaction impact on sexual behaviour, semen characteristics, hormones and spermatozoal gene expression in bucks (Capra hircus). Theriogenology 2019;130:130–139. doi: 10.1016/j.theriogenology.2019.02.026
21. Gupta A, Kumar A, Naqvi S, et al: Chronic exposure to multi-metals on testicular toxicity in rats. Toxicol Mech Methods 2021;31: 53–66. doi: 10.1080/15376516.2020.1828522
22. Li Y, Chen H, Liao J, et al: Long-term copper exposure promotes apoptosis and autophagy by inducing oxidative stress in pig testis. Environ Sci Poll Res 2021;28:55140–55153. doi: 10.1007/s11356-021-14853-y
23. Liu JY, Yang X, Sun XD, et al: Suppressive effects of copper sulfate accumulation on the spermatogenesis of rats. Biol Trace Elem Res 2016;174:356–361. doi: 10.1007/s12011-016-0710-7
24. Mayasula VK, Arunachalam A, Babatunde SA, et al: Trace minerals for improved performance: a review of Zn and Cu supplementation effects on male reproduction in goats. Trop Anim Health Prod 2021;53:491. doi: 10.1007/s11250-021-02943-5
25. Harchegani AB, Dahan H, Tahmasbpour E, et al: Effects of zinc deficiency on impaired spermatogenesis and male infertility: the role of oxidative stress, inflammation and apoptosis, Human Fertil 2020;23:5–16. doi: 10.1080/14647273.2018.1494390
26. Wroblewski N, Schill WB, Henkel R: Metal chelators change the human sperm motility pattern. Fertil Steril 2003;79:1584–1589. doi: 10.1016/S0015-0282(03)00255-3
27. Björndahl L, Kvist U: Human sperm chromatin stabilization: a proposed model including zinc bridges. Mol Human Reprod 2010;16:23–29. doi: 10.1093/molehr/gap099
28. Kumari D, Nair N, Bedwal RS: Testicular apoptosis after dietary zinc deficiency: ultrastructural and TUNEL studies. Systems Biol Reprod Med 2011;57:233–243. doi: 10.3109/19396368.2011.584500
29. Mayasula VK, Arunachalam A, Sellappan S, et al: Organic Zn and Cu supplementation imprints on seminal plasma mineral, biochemical/ antioxidant activities and its relationship to spermatozoal characteristics in bucks. Reprod Biol 2020;20:220–228. doi: 10.1016/j.repbio.2020.02.007
30. Rahman HU, Qureshi MS, Khan RU: Influence of dietary zinc on semen traits and seminal plasma antioxidant enzymes and trace minerals of Beetal bucks. Reprod Dom Anim 2014;49:1004–1007. doi: 10.1111/rda.12422
31. Tajaddini S, Ebrahimi S, Behnam B, et al: Antioxidant effect of manganese on the testis structure and sperm parameters of formalin-treated mice. Androl 2014;46:246–253. doi: 10.1111/and.12069
32. Lee B, Pine M, Johnson L, et al: Manganese acts centrally to activate reproductive hormone secretion and pubertal development in male rats. Reprod Toxicol 2006;22:580–585. doi: 10.1016/j.reprotox.2006.03.011
33. Tarun A, Mani V, Bhakat M, et al: Effect of dietary supplementation of manganese, chromium and cobalt on semen qualities in Sahiwal bulls. Indian J Anim Res 2020;54:1109–1114. doi: 10.18805/ijar.B-3870
34. Souza TL, Batschauer AR, Brito PM, et al: Evaluation of Mn exposure in the male reproductive system and its relationship with reproductive dysfunction in mice. Toxicol 2020;441:152504. doi: 10.1016/j.tox.2020.152504
35. Reis LSLS, Ramos AA, Camargos AS, et al: Effect of manganese supplementation on the membrane integrity and the mitochondrial potential of the sperm of grazing Nelore bulls. Anim Reprod Sci 2014;150:1–6. doi: 10.1016/j.anireprosci.2014.06.033
36. El-Sharawy M, Eid E, Darwish S, et al: Effect of organic and inorganic selenium supplementation on semen quality and blood enzymes in buffalo bulls. Anim Sci J 2017;88:999–1005. doi: 10.1111/asj.12736
37. Ahsan U, Kamran Z, Raza I, et al: Role of selenium in male reproduction-A review. Anim Reprod Sci 2014;146:55–62. doi: 10.1016/j.anireprosci.2014.01.009
38. Smith DG, Senger PL, McCutchan JF, et al: Selenium and glutathione peroxidase distribution in bovine semen and selenium-75 retention by the tissues of the reproductive tract in the bull. Biol Reprod 1979;20:377–383. doi: 10.1095/biolreprod20.2.377
39. Vanha-Perttula T, Remes E: Incorporation of Selenium-75 into seminal plasma and spermatozoa of the bull. Andrologia 1989;22:34–41. doi: 10.1111/j.1439-0272.1990.tb01937.x
40. Bartle JL, Senger PL, Hillers JK: Influence of injected selenium in dairy bulls on blood and semen selenium, glutathione peroxidase and seminal quality. Biol Reprod 1980;23: 1007–1013. doi: 10.1095/biolreprod23.5.1007
41. Marin-Guzman J, Mahan DC, Chung YK, et al: Effects of dietary selenium and vitamin e on boar performance and tissue responses, semen quality, and subsequent fertilization rates in mature gilts. J Anim Sci 1997;75:2994–3003. doi: 10.2527/1997.75112994x
42. Piagentini M, Silva DC, Dell’Aqua CFP, et al: Effect of selenium supplementation on semen characteristics of Brazil’s ram. Reprod Dom Anim 2017;52:355–358. doi: 10.1111/rda.12903
43. Kaur P, Bansal MP: Effect of selenium-induced oxidative stress on the cell kinetics in testis and reproductive ability of male mice. Nutrition 2005;21:351–357. doi: 10.1016/j.nut.2004.05.028
44. Yang X, Chen Y, Song W, et al: Review of the role of ferroptosis in testicular function. Nutrients 2022;14:5268. doi: 10.3390/nu14245268
45. Tsao C-W, Liao Y-R, Chang T-C, et al: Effects of iron supplementation on testicular function and spermatogenesis of iron-deficient rats. Nutrients 2022;14:2063. doi: 10.3390/nu14102063
46. Zakošek Pipan M, Zrimšek P, Strajn BJ, et al. Macro- and microelements in serum and seminal plasma as biomarkers for bull sperm cryotolerance. Acta Vet Scand 2021;63:25. doi: 10.1186/s13028-021-00590-2
47. Tvrdá E, Lukáč N, Lukáčová J, et al: Dose- and time-dependent in vitro effects of divalent and trivalent iron on the activity of bovine spermatozoa. Biol Trace Elem Res 2015;167:36–47. doi: 10.1007/s12011-015-0288-5
48. Narud B, Klinkenberg G, Khezri A, et al: Differences in sperm functionality and intracellular metabolites in Norwegian Red bulls of contrasting fertility. Theriogenology 2020;157:24–32. doi: 10.1016/j.theriogenology.2020.07.005
49. Aguiar GFM, Batista BL, Rodrigues JL, et al: Determination of trace elements in bovine semen samples by inductively coupled plasma mass spectrometry and data mining techniques for identification of bovine class. J Dairy Sci 2012;95:7066–7073. doi: 10.3168/jds.2012-5515
50. Khaki A, Araghi A, Lotfi M, et al: Differences between some biochemical components in seminal plasma of first and second ejaculations in dual-purpose Simmental (Fleckvieh) bulls and their relationships with semen quality parameters. Vet Res Forum 2021;12:39–46.
51. Tvrda E, Lukac N, Schneridgenova M, et al: Impact of seminal chemical elements on the oxidative balance in bovine seminal plasma and spermatozoa. J Vet Med 2013;125096. doi: 10.1155/2013/125096
52. Geary TW, Kelly WL, Spickard DS, et al: Effect of supplemental trace mineral level and form on peripubertal bulls. Anim Reprod Sci 2016;168:1–9. doi: 10.1016/j.anireprosci.2016.02.018
53. Geary TW, Waterman RC, Van Emon ML, et al: Effect of supplemental trace minerals on standard and novel measures of bull fertility. Theriogenology 2021;172:307–314. doi: 10.1016/j.theriogenology.2021.07.006
54. Kirchhoff AA, Fike KE, Breiner R: An injectable trace mineral supplement in yearling bulls causes a short-term increase in circulating trace mineral levels but does not improve sperm quality. Kansas Agric Exp Station Res Rep 2015;1:1. doi: 10.4148/2378-5977.1024
55. Preedy GW, Hill SL, Stevenson JS, et al: Injectable trace-mineral supplementation improves sperm motility and morphology of young beef bulls. Anim Sci 2018;34:1–9. doi: 10.15232/pas.2017-01667
56. Rowe MP, Powell JG, Kegley EB, et al: Influence of supplemental trace-mineral source on bull semen quality. Anim Sci 2014;30: 68–73. doi: 10.15232/S1080-7446(15)30085-1
Published
2024-05-20
How to Cite
Ferrer M., Palomares R., & Maldonadox-Estrada J. (2024). Role of trace minerals in bull reproductive physiology and semen quality. Clinical Theriogenology, 16. https://doi.org/10.58292/CT.v16.10351
Section
Review Reports
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