Abstract
In a temperature-increasing scenario, due to global warming, the individual thermic resilience of the male assumes a crucial role in the reproductive efficiency of a male since the thermic stress, such as the inability of the male to reduce body or regional temperature on a physiological level, impairs testicular function. In this study, the effect of the environmental conditions on the fresh semen quality, in terms of volume, concentration, total sperm in the ejaculate, total motility, normal morphology, membrane integrity, and discarding rate, were compared longitudinally in Belgian Blue (BB) and Brown Swiss (BS) bulls. The environmental conditions, summarized in the mean temperature-humidity index (THI), were calculated on the day of collection, as well as 7 days (epididymal maturation), 35 days (late spermatogenesis), and 70 days (early spermatogenesis) before the collection, to reflect spermatogenesis time. Our findings showed that limited seasonal effects were present in the semen quality of BS bulls. On the other hand, in BB bulls lower semen quality was found between July and November, with a different timing depending on the seminal parameter. This effect of the season on BB semen parameters appears to be related to the THI. The data presented in this study shows that the temperature and humidity, summarized in THI, could affect the semen quality of the bull on breed basis, given that volume, concentration, total sperm in the ejaculate, total motility, membrane integrity, and sperm normal morphology were significantly reduced by an increasing THI in the Belgian Blue bulls, but not in Brown Swiss bulls.
Similar content being viewed by others
Change history
07 October 2021
A Correction to this paper has been published: https://doi.org/10.1007/s00484-021-02200-2
References
Al-Kanaan A, König S, Brügemann K (2015) Effects of heat stress on semen characteristics of Holstein bulls estimated on a continuous phenotypic and genetic scale. Livest Sci 177:15–24. https://doi.org/10.1016/j.livsci.2015.04.003
Arteaga AA, Barth AD, Brito LFC (2005) Relationship between semen quality and pixel–intensity of testicular ultrasonograms after scrotal insulation in beef bulls. Theriogenology 64:408–415. https://doi.org/10.1016/j.theriogenology.2004.12.008
Barth AD, Oko RJ (1989) Abnormal morphology of bovine spermatozoa. Iowa State University Press, Ames, IA, USA
Blackshaw JK, Blackshaw AW (1994) Heat stress in cattle and the effect of shade on production and behaviour: a review. Aust J Exp Agric 34:285–295. https://doi.org/10.1071/EA9940285
Brito LFC, Silva AEDF, Barbosa RT et al (2003) Effects of scrotal insulation on sperm production, semen quality, and testicular echotexture in Bos indicus and Bos indicus × Bos taurus bulls. Anim Reprod Sci 79:1–15. https://doi.org/10.1016/S0378-4320(03)00082-4
Brito LFC, Silva AEDF, Rodrigues LH et al (2002) Effects of environmental factors, age and genotype on sperm production and semen quality in Bos indicus and Bos taurus AI bulls in Brazil. Anim Reprod Sci 70:181–190. https://doi.org/10.1016/S0378-4320(02)00009-X
Casady RB, Myers RM, Legates JE (1953) The effect of exposure to high ambient temperature on Spermatogenesis in the dairy bull. J Dairy Sci 36:14–23. https://doi.org/10.3168/jds.S0022-0302(53)91449-0
Christidis N, Jones GS, Stott PA (2015) Dramatically increasing chance of extremely hot summers since the 2003 European heatwave. Nat Clim Chang 5:46–50. https://doi.org/10.1038/nclimate2468
Collier RJ, Renquist BJ, Xiao Y (2017) A 100-year review: stress physiology including heat stress. J Dairy Sci 100:10367–10380. https://doi.org/10.3168/jds.2017-13676
Contri A, Gloria A, Robbe D et al (2013) Kinematic study on the effect of pH on bull sperm function. Anim Reprod Sci 136:252–259. https://doi.org/10.1016/j.anireprosci.2012.11.008
Cook RB, Coulter GH, Kastelic JP (1994) The testicular vascular cone, scrotal thermoregulation, and their relationship to sperm production and seminal quality in beef bulls. Theriogenology 41:653–671. https://doi.org/10.1016/0093-691X(94)90175-I
Coopman F, Krafft A, Dewulf J et al (2007) Estimation of phenotypic and genetic parameters for weight gain and weight at fixed ages in the double-muscled Belgian Blue Beef breed using field records. J Anim Breed Genet 124:20–25. https://doi.org/10.1111/j.1439-0388.2007.00632.x
Everett RW, Bean B (1982) Environmental influences on semen output. J Dairy Sci 65:1303–1310. https://doi.org/10.3168/jds.S0022-0302(82)82344-8
García-Ispierto I, López-Gatius F, Santolaria P et al (2006) Relationship between heat stress during the peri-implantation period and early fetal loss in dairy cattle. Theriogenology 65:799–807. https://doi.org/10.1016/j.theriogenology.2005.06.011
Garner DL, Johnson LA (1995) Viability assessment of mammalian sperm using SYBR-14 and propidium iodide1. Biol Reprod 53:276–284. https://doi.org/10.1095/biolreprod53.2.276
Gilad E, Meidan R, Berman A et al (1993) Effect of heat stress on tonic and GnRH-induced gonadotrophin secretion in relation to concentration of oestradiol in plasma of cyclic cows. J Reprod Fertil 99:315–321. https://doi.org/10.1530/jrf.0.0990315
Gloria A, Carluccio A, Contri A et al (2013) The effect of the chamber on kinetic results in cryopreserved bull spermatozoa. Andrology 1:879–885. https://doi.org/10.1111/j.2047-2927.2013.00121.x
Hancock JL (1957) The morphology of boar spermatozoa. J R Microsc Soc (great Britain) 76:84–97
Hansen PJ (2004) Physiological and cellular adaptations of zebu cattle to thermal stress. Anim Reprod Sci 82–83:349–360. https://doi.org/10.1016/j.anireprosci.2004.04.011
Hansen PJ (2009) Effects of heat stress on mammalian reproduction. Philos Trans R Soc B Biol Sci 364:3341–3350. https://doi.org/10.1098/rstb.2009.0131
Hoflack G, Opsomer G, Van Soom A et al (2006) Comparison of sperm quality of Belgian Blue and Holstein Friesian bulls. Theriogenology 66:1834–1846. https://doi.org/10.1016/j.theriogenology.2006.05.007
Hoflack G, Van den BroeckMaes WD et al (2008) Testicular dysfunction is responsible for low sperm quality in Belgian Blue bulls. Theriogenology 69:323–332. https://doi.org/10.1016/j.theriogenology.2007.09.034
Johnston JE, Naelapaa H, Frye JB (1963) Physiological responses of Holstein, Brown Swiss and Red Sindhi crossbred bulls exposed to high temperatures and humidities. J Anim Sci 22:432–436. https://doi.org/10.2527/jas1963.222432x
Kastelic JP, Cook RB, Coulter GH (1997) Contribution of the scrotum, testes, and testicular artery to scrotal/testicular thermoregulation in bulls at two ambient temperatures. Anim Reprod Sci 45:255–261. https://doi.org/10.1016/S0378-4320(96)01587-4
Kastelic JP, Cook RB, Coulter GH, Saacke RG (1996) Insulating the scrotal neck affects semen quality and scrotal/testicular temperatures in the bull. Theriogenology 45:935–942. https://doi.org/10.1016/0093-691X(96)00023-4
Kastelic JP, Coulter GH, Cook RB (1995) Scrotal surface, subcutaneous, intratesticular, and intraepididymal temperatures in bulls. Theriogenology 44:147–152. https://doi.org/10.1016/0093-691X(95)00155-2
Llamas-Luceño N, Hostens M, Mullaart E et al (2020) High temperature-humidity index compromises sperm quality and fertility of Holstein bulls in temperate climates. J Dairy Sci 103:9502–9514. https://doi.org/10.3168/jds.2019-18089
Majić Balić I, Milinković-Tur S, Samardžija M, Vince S (2012) Effect of age and environmental factors on semen quality, glutathione peroxidase activity and oxidative parameters in simmental bulls. Theriogenology 78:423–431. https://doi.org/10.1016/j.theriogenology.2012.02.022
Malama E, Zeron Y, Janett F et al (2017) Use of computer-assisted sperm analysis and flow cytometry to detect seasonal variations of bovine semen quality. Theriogenology 87:79–90. https://doi.org/10.1016/j.theriogenology.2016.08.002
Mathevon M, Buhr MM, Dekkers JCM (1998) Environmental, management, and genetic factors affecting semen production in Holstein bulls. J Dairy Sci 81:3321–3330. https://doi.org/10.3168/jds.S0022-0302(98)75898-9
Meyerhoeffer DC, Wettemann RP, Coleman SW, Wells ME (1985) Reproductive criteria of beef bulls during and after exposure to increased ambient temperature. J Anim Sci 60:352–357. https://doi.org/10.2527/jas1985.602352x
Moazamian R, Polhemus A, Connaughton H et al (2015) Oxidative stress and human spermatozoa: diagnostic and functional significance of aldehydes generated as a result of lipid peroxidation. Mol Hum Reprod 21:502–515. https://doi.org/10.1093/molehr/gav014
Morrell JM (2020) Heat stress and bull fertility. Theriogenology 153:62–67. https://doi.org/10.1016/j.theriogenology.2020.05.014
Murphy EM, Kelly AK, O’Meara C et al (2018) Influence of bull age, ejaculate number, and season of collection on semen production and sperm motility parameters in Holstein Friesian bulls in a commercial artificial insemination centre. J Anim Sci 96:2408–2418. https://doi.org/10.1093/jas/sky130
R-Core-Team (2020) R: a language and environment for statistical computing. In: R Found. Stat. Comput. Wien, Austria. https://www.r-project.org/. Accessed 10 Sept 2020
Rahman MB, Vandaele L, Rijsselaere T et al (2011) Scrotal insulation and its relationship to abnormal morphology, chromatin protamination and nuclear shape of spermatozoa in Holstein-Friesian and Belgian Blue bulls. Theriogenology 76:1246–1257. https://doi.org/10.1016/j.theriogenology.2011.05.031
Rahman MB, Schellander K, Luceño NL, Van Soom A (2018) Heat stress responses in spermatozoa: mechanisms and consequences for cattle fertility. Theriogenology 113:102–112. https://doi.org/10.1016/j.theriogenology.2018.02.012
Roth Z (2020) Reproductive physiology and endocrinology responses of cows exposed to environmental heat stress - experiences from the past and lessons for the present. Theriogenology 155:150–156. https://doi.org/10.1016/j.theriogenology.2020.05.040
Sabés-Alsina M, Lundeheim N, Johannisson A et al (2019) Relationships between climate and sperm quality in dairy bull semen: a retrospective analysis. J Dairy Sci 102:5623–5633. https://doi.org/10.3168/jds.2018-15837
Seifi-Jamadi A, Zhandi M, Kohram H et al (2020) Influence of seasonal differences on semen quality and subsequent embryo development of Belgian Blue bulls. Theriogenology 158:8–17. https://doi.org/10.1016/j.theriogenology.2020.08.037
Senger PL (2005) The organization and function of the male reproductive system. In: Senger PL (ed) Pathways to pregnancy and parturition, 2nd Revise. Current Conceptions Inc, Pullman, WA, USA, pp 44–79
Setchell BP (1978) The mammalian testis. Cornell University Press, Ithaca
Shahat AM, Rizzoto G, Kastelic JP (2020) Amelioration of heat stress-induced damage to testes and sperm quality. Theriogenology 158:84–96. https://doi.org/10.1016/j.theriogenology.2020.08.034
Skinner JD, Louw GN (1966) Heat stress and spermatogenesis in Bos indicus and Bos taurus cattle. J Appl Physiol 21:1784–1790. https://doi.org/10.1152/jappl.1966.21.6.1784
Snoj T, Kobal S, Majdic G (2013) Effects of season, age, and breed on semen characteristics in different Bos taurus breeds in a 31-year retrospective study. Theriogenology 79:847–852. https://doi.org/10.1016/j.theriogenology.2012.12.014
Valeanu S, Johannisson A, Lundeheim N, Morrell JM (2015) Seasonal variation in sperm quality parameters in Swedish red dairy bulls used for artificial insemination. Livest Sci 173:111–118. https://doi.org/10.1016/j.livsci.2014.12.005
Verratti V, Di Giulio C, D’Angeli A et al (2016) Sperm forward motility is negatively affected by short-term exposure to altitude hypoxia. Andrologia 48:800–806. https://doi.org/10.1111/and.12515
Vogler CJ, Bame JH, DeJarnette JM et al (1993) Effects of elevated testicular temperature on morphology characteristics of ejaculated spermatozoa in the bovine. Theriogenology 40:1207–1219. https://doi.org/10.1016/0093-691X(93)90291-C
Wickham H (2016) ggplot2: elegant graphics for data analysis, 2nd edn. Springer Verlag, New York
Acknowledgements
The authors are grateful to the Provincial Breeders Federation of Trento for their support. The authors are also grateful to the Superbrown Consortium Bz/Tn and the “Alpenseme” AI Center (Ton, Trento, Italy) staff for their cooperation.
The authors would like to thank Prof Michael Keane for the kind language revision of the manuscript.
Funding
This project was funded by the project FARDIB 2019, University of Teramo (funded researcher: Dr. Alessia Gloria). The present study was conducted in the framework of the Project “Demetra” (Dipartimenti di Eccellenza 2018 – 2022, CUP_C46C18000530001), funded by the Italian Ministry for Education, University and Research.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Rights and permissions
About this article
Cite this article
Gloria, A., Candeloro, L., Wegher, L. et al. Environmental temperature and relative humidity differently affect the sperm characteristics in Brown Swiss and Belgian Blue bulls. Int J Biometeorol 65, 2189–2199 (2021). https://doi.org/10.1007/s00484-021-02184-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-021-02184-z