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International journal of biometeorology2026; 70(3); 89; doi: 10.1007/s00484-025-03123-y

The fertility of a sub-population of stallions is negatively affected by ambient climatic conditions, mediated through DNA damage.

Abstract: Exposure to systemic heat stress in male mammals adversely affects sperm production, fertility, and DNA integrity. To date, few studies have investigated this phenomenon in horses, particularly in industry-relevant environments. Therefore, this study examined the relationship between ambient climatic conditions and fertility within a population of commercially fertile stallions. Post-coital semen samples ( = 804) were collected weekly from 46 Thoroughbred stallions during two successive breeding seasons (NSW, Australia; 22 weeks total). Semen samples were processed via single-layer colloidal centrifugation on-site to remove contaminants, seminal plasma and poor-quality sperm cells. The remaining sperm fraction was resuspended in Biggers, Whitten and Whittingham (BWW) medium for analyses, including sperm concentration, motility, and DNA damage. Fertility data (first cycle and per-cycle pregnancy rates) were collected from farms. Loggers were placed in the stables and paddocks of stallions to record ambient temperature and humidity, on 3-min cycles. Our results indicate that current management regimens, involving the stabling of stallions at night, with paddock access during the day, expose stallions to highest ambient climatic conditions. Polynomial distributed lag modelling identified 18 stallions whose fertility was adversely affected by heat stress, based on correlations between fertility and ambient climatic conditions ( ≤ 0.05). Of these 18 candidate stallions, six (13% of the overall population) exhibited repeated positive relationships between ambient climatic conditions and sperm DNA damage, and repeated negative relationships between fertility and sperm DNA damage ( ≥ 0.50;  ≤ 0.05). These results suggest that heat-induced subfertility was most likely mediated via oxidative damage to the sperm DNA, and that current management strategies should be assessed to prevent exposure of stallions to maximal climatic conditions. The online version contains supplementary material available at 10.1007/s00484-025-03123-y.
Publication Date: 2026-03-09 PubMed ID: 41801466PubMed Central: PMC12971856DOI: 10.1007/s00484-025-03123-yGoogle Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

Overview

  • This study investigated how ambient climate, specifically heat stress, negatively impacts the fertility of a subset of Thoroughbred stallions through damage to sperm DNA in commercial breeding environments.

Study Background and Rationale

  • Heat stress in male mammals is known to reduce sperm production, fertility, and DNA integrity, but this has not been widely studied in horses under realistic industry conditions.
  • The researchers aimed to fill this knowledge gap by assessing how natural climatic variations affect stallion fertility on commercial farms over two breeding seasons.

Methodology

  • Subjects: 46 Thoroughbred stallions on farms located in New South Wales (NSW), Australia.
  • Data collection period: Two breeding seasons totaling 22 weeks.
  • Sample collection: 804 post-coital semen samples collected weekly from the stallions.
  • Semen processing: Samples were cleaned using single-layer colloidal centrifugation to remove contaminants, seminal plasma, and poor-quality sperm.
  • Sample analysis: Processed sperm were resuspended in BWW (Biggers, Whitten and Whittingham) medium to assess:
    • Sperm concentration
    • Motility (movement ability)
    • DNA damage
  • Fertility measures: First cycle pregnancy rate and per-cycle pregnancy rate collected from the breeding farms.
  • Environmental monitoring: Temperature and humidity loggers recorded ambient conditions every 3 minutes in both stables and paddocks where stallions were kept.

Key Findings

  • The common management practice was to stable stallions at night and give them paddock access during the day, exposing them to higher daytime temperatures.
  • Statistical modeling using polynomial distributed lag identified 18 stallions whose fertility showed significant negative correlations with heat stress (p ≤ 0.05).
  • Among these 18 susceptible stallions, 6 exhibited:
    • Repeated positive correlations between heat exposure and sperm DNA damage (correlation coefficient ≥ 0.50, p ≤ 0.05).
    • Repeated negative correlations between sperm DNA damage and fertility rates (correlation coefficient ≥ 0.50, p ≤ 0.05).
  • This subset represents approximately 13% of the overall stallion population that was studied.
  • Results indicate that heat-induced subfertility is likely mediated through oxidative damage to sperm DNA rather than other sperm parameters alone.

Implications

  • The study highlights the sensitivity of some stallions to ambient heat exposure and the associated decline in fertility via DNA damage mechanisms.
  • Current management practices may not adequately protect stallions from heat stress, especially since daytime paddock access coincides with peak temperatures.
  • Recommendations include reassessing stallion housing and management regimes to minimize heat exposure during vulnerable periods.
  • Improved environmental control or timing of paddock access could help maintain sperm DNA integrity and fertility rates.

Additional Resources

  • The paper includes supplementary material available online at the provided DOI link for those interested in detailed data and methods.

Cite This Article

APA
Griffin RA, Miller K, Colyvas K, Sheridan A, De Iuliis G, Aitken RJ, Baker MA, Gibb Z, Swegen A. (2026). The fertility of a sub-population of stallions is negatively affected by ambient climatic conditions, mediated through DNA damage. Int J Biometeorol, 70(3), 89. https://doi.org/10.1007/s00484-025-03123-y

Publication

ISSN: 1432-1254
NlmUniqueID: 0374716
Country: United States
Language: English
Volume: 70
Issue: 3
PII: 89

Researcher Affiliations

Griffin, Róisín A
  • Infertility and Reproduction Research Program, Hunter Medical Research Institute, New Lambton Heights, Australia. roisin.griffin@newcastle.edu.au.
  • School of Environment and Life Sciences, College of Engineering, Science and Environment, University of Newcastle, Callaghan, Australia. roisin.griffin@newcastle.edu.au.
Miller, Kasey
  • School of Environment and Life Sciences, College of Engineering, Science and Environment, University of Newcastle, Callaghan, Australia.
Colyvas, Kim
  • School of Engineering (Statistics), College of Engineering, Science and Environment, University of Newcastle, Callaghan, Australia.
Sheridan, Alecia
  • School of Environment and Life Sciences, College of Engineering, Science and Environment, University of Newcastle, Callaghan, Australia.
De Iuliis, Geoffry
  • Infertility and Reproduction Research Program, Hunter Medical Research Institute, New Lambton Heights, Australia.
  • School of Environment and Life Sciences, College of Engineering, Science and Environment, University of Newcastle, Callaghan, Australia.
Aitken, Robert John
  • Infertility and Reproduction Research Program, Hunter Medical Research Institute, New Lambton Heights, Australia.
  • School of Environment and Life Sciences, College of Engineering, Science and Environment, University of Newcastle, Callaghan, Australia.
Baker, Mark A
  • Infertility and Reproduction Research Program, Hunter Medical Research Institute, New Lambton Heights, Australia.
  • School of Biomedical Sciences and Pharmacy, College of Health, Medicine and Wellbeing, University of Newcastle, Callaghan, Australia.
Gibb, Zamira
  • Infertility and Reproduction Research Program, Hunter Medical Research Institute, New Lambton Heights, Australia.
  • School of Environment and Life Sciences, College of Engineering, Science and Environment, University of Newcastle, Callaghan, Australia.
Swegen, Aleona
  • Infertility and Reproduction Research Program, Hunter Medical Research Institute, New Lambton Heights, Australia.
  • School of Environment and Life Sciences, College of Engineering, Science and Environment, University of Newcastle, Callaghan, Australia.

References

This article includes 80 references
  1. Abdelhamid MHM, Walschaerts M, Ahmad G, Mieusset R, Bujan L, Hamdi S. Mild experimental increase in testis and epididymis temperature in men: effects on sperm morphology according to spermatogenesis stages.. Transl Androl Urol 8(6):651–665.
    doi: 10.21037/tau.2019.11.18pmc: PMC6987600pubmed: 32038961google scholar: lookup
  2. Aitken RJ. DNA Damage in Human Spermatozoa; Important Contributor to Mutagenesis in the Offspring.. Transl Androl Urol 6(Suppl 4):S761-s764.
    doi: 10.21037/tau.2017.09.13pmc: PMC5643656pubmed: 29082208google scholar: lookup
  3. Aitken RJ, Bakos HW. Should we be measuring DNA damage in human spermatozoa? New light on an old question.. Hum Reprod .
    doi: 10.1093/humrep/deab004pubmed: 33532854google scholar: lookup
  4. Aitken RJ, Baker MA, De Iuliis GN, Nixon B. New insights into sperm physiology and pathology.. Handb Exp Pharmacol 198:99–115.
    doi: 10.1007/978-3-642-02062-9_7pubmed: 20839089google scholar: lookup
  5. Aitken RJ, De Iuliis GN, Nixon B. The sins of our forefathers: paternal impacts on de novo mutation rate and development.. Annu Rev Genet 54:1–24.
  6. Allen WR. Luteal deficiency and embryo mortality in the mare.. Reprod Domest Anim 36(3–4):121–131.
  7. Allen WR, Brown L, Wright M, Wilsher S. Reproductive efficiency of flatrace and National Hunt thoroughbred mares and stallions in England.. Equine Vet J 39(5):438–445.
    doi: 10.2746/042516407X1737581pubmed: 17910269google scholar: lookup
  8. Argov-Argaman N, Mahgrefthe K, Zeron Y, Roth Z. Season-induced variation in lipid composition is associated with semen quality in Holstein bulls.. Reproduction 145(5):479–489.
    doi: 10.1530/rep-12-0498pubmed: 23630332google scholar: lookup
  9. Atkins IK, Cook NB, Mondaca MR, Choi CY. Continuous respiration rate measurement of heat-stressed dairy cows and relation to environment, body temperature, and lying time.. Trans ASABE 61(5):1475–1485.
    doi: 10.13031/trans.12451google scholar: lookup
  10. Balić IM, Milinković-Tur S, Samardžija M, Vince S. Effect of age and environmental factors on semen quality, glutathione peroxidase activity and oxidative parameters in simmental bulls.. Theriogenology 78(2):423–431.
  11. Biggers J, Whitten W, Whittingham D. The culture of mouse embryos in vitro.. .
  12. Blanchard T, Jorgensen J, Varner D, Forrest D, Evans J. Clinical observations on changes in concentrations of hormones in plasma of two stallions with thermally-induced testicular degeneration.. J Equine Vet Sci 16(5):195–201.
  13. Brouk MJ, Smith, Harner JP, J. F.. Effect of Sprinkling Frequency and Airflow on Respiration Rate, Body Surface Temperature and Body Temperature of Heat Stressed Dairy Cattle. ASABE .
    doi: 10.13031/2013.11630google scholar: lookup
  14. Bromfield EG, Aitken RJ, Anderson AL, McLaughlin EA, Nixon B. The impact of oxidative stress on chaperone-mediated human sperm–egg interaction.. Hum Reprod 30(11):2597–2613.
    doi: 10.1093/humrep/dev214pubmed: 26345691google scholar: lookup
  15. Carabaño MJ, Ramón M, Menéndez-Buxadera A, Molina A, Díaz C. Selecting for heat tolerance.. Anim Front 9(1):62–68.
    doi: 10.1093/af/vfy033pmc: PMC6951854pubmed: 32002241google scholar: lookup
  16. Casanovas A, Ribas-Maynou J, Lara-Cerrillo S, Jimenez-Macedo AR, Hortal O, Benet J, Carrera J, García-Peiró A. Double-Stranded sperm DNA damage is a cause of delay in embryo development and can impair implantation rates.. Fertil Steril 2019 111(4):699–707 e691.
  17. Champroux A, Torres-Carreira J, Gharagozloo P, Drevet J, Kocer A. Mammalian sperm nuclear organization: resiliencies and vulnerabilities.. Basic Clin Androl 2016 26(1):1–22.
    doi: 10.1186/s12610-016-0044-5pmc: PMC5175393pubmed: 28031843google scholar: lookup
  18. Christian SL, Fantes JA, Mewborn SK, Huang B, Ledbetter DH. Large genomic duplicons map to sites of instability in the Prader-Willi/Angelman syndrome chromosome region (15q11–Q13).. Hum Mol Genet 1999 8(6):1025–1037.
    doi: 10.1093/hmg/8.6.1025pubmed: 10332034google scholar: lookup
  19. Cook R, Coulter G, Kastelic J. The testicular vascular cone, scrotal thermoregulation, and their relationship to sperm production and seminal quality in beef bulls.. Theriogenology 1994 41(3):653–671.
    doi: 10.1016/0093-691X(94)90175-Ipubmed: 16727420google scholar: lookup
  20. Crowe MW, Swerczek TW. Equine congenital defects.. Am J Vet Res 1985 46(2):353–358.
    doi: 10.2460/ajvr.1985.46.02.353pubmed: 3994101google scholar: lookup
  21. Cruz Júnior CA, Lucci CM, Peripolli V, Silva AF, Menezes AM, Morais SRL, Araújo MS, Ribeiro LMCS, Mattos RC, McManus C. Effects of testicle insulation on seminal traits in rams: preliminary study.. Small Ruminant Res 2015 130:157–165.
  22. Dada R, Kumar M, Jesudasan R, Fernández JL, Gosálvez J, Agarwal A. Epigenetics and its role in male infertility.. J Assist Reprod Genet 2012 29(3):213–223.
    doi: 10.1007/s10815-012-9715-0pmc: PMC3288140pubmed: 22290605google scholar: lookup
  23. Dahl EV, Herrick JF. A vascular mechanism for maintaining testicular temperature by counter-current exchange.. Surg Gynecol Obstet 1959 108(6):697–705.
    pubmed: 13659355
  24. De Iuliis GN, Thomson LK, Mitchell LA, Finnie JM, Koppers AJ, Hedges A, Nixon B, Aitken RJ. DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-2′-deoxyguanosine, a marker of oxidative stress1.. Biol Reprod 2009 81(3):517–524.
    doi: 10.1095/biolreprod.109.076836pubmed: 19494251google scholar: lookup
  25. de Souza-Pinto NC, Eide L, Hogue BA, Thybo T, Stevnsner T, Seeberg E, Klungland A, Bohr VA. Repair of 8-oxodeoxyguanosine lesions in mitochondrial Dna depends on the oxoguanine Dna glycosylase (Ogg1) gene and 8-oxoguanine accumulates in the mitochondrial Dna of Ogg1-defective mice.. Cancer Res 2001 61(14):5378.
    pubmed: 11454679
  26. Dierlamm J, Schilling G, Michaux L, Hinz K, Penas EMM, Seeger D, Hagemeijer A, Hossfeld DK. Deletion of chromosome 15 represents a rare but recurrent chromosomal abnormality in myelocytic malignancies.. Cancer Genet Cytogenet 2003 144(1):1–5.
    doi: 10.1016/S0165-4608(02)00863-4pubmed: 12810248google scholar: lookup
  27. Feng Z, Hu W, Amin S, Tang MS. Mutational spectrum and genotoxicity of the major lipid peroxidation product, trans-4-hydroxy-2-nonenal, induced DNA adducts in nucleotide excision repair-proficient and -deficient human cells.. Biochemistry 2003 42(25):7848–7854.
    doi: 10.1021/bi034431gpubmed: 12820894google scholar: lookup
  28. Galvin N, Corley K. Causes of disease and death from birth to 12 months of age in the thoroughbred horse in Ireland.. Ir Vet J 2010 63(1):37–43.
    doi: 10.1186/2046-0481-63-1-37pmc: PMC3113843pubmed: 21851741google scholar: lookup
  29. Gaughan JB, Mader TL, Holt SM, Josey MJ, Rowan KJ. Heat tolerance of Boran and Tuli crossbred steers.. J Anim Sci 1999 77(9):2398–2405.
    doi: 10.2527/1999.7792398xpubmed: 10492446google scholar: lookup
  30. Gaughan JB, Sharman K, McGowan MR. The effect of day-only versus day-plus-night cooling of dairy cows.. J Dairy Sci 2023 106(7):5002–5017.
    doi: 10.3168/jds.2022-22819pubmed: 37268568google scholar: lookup
  31. Gibb Z, Lambourne SR, Aitken RJ. The paradoxical relationship between stallion fertility and oxidative stress.. Biol Reprod 2014 91(3):77.
    doi: 10.1095/biolreprod.114.118539pubmed: 25078685google scholar: lookup
  32. Giles RC, Donahue JM, Hong CB, Tuttle PA, Petrites-Murphy MB, Poonacha KB, Roberts AW, Tramontin RR, Smith B, Swerczek TW. Causes of abortion, stillbirth, and perinatal death in horses: 3,527 cases (1986–1991).. J Am Vet Med Assoc 1993 203(8):1170–1175.
    doi: 10.2460/javma.1993.203.08.1170pubmed: 8244867google scholar: lookup
  33. Gong Y, Guo H, Zhang Z, Zhou H, Zhao R, He B. Heat stress reduces sperm motility via activation of glycogen synthase kinase-3α and inhibition of mitochondrial protein import.. Front Physiol 2017 8:718.
    doi: 10.3389/fphys.2017.00718pmc: PMC5615227pubmed: 29018353google scholar: lookup
  34. Gourdine JL, Mandonnet N, Giorgi M, Renaudeau D. Genetic parameters for thermoregulation and production traits in lactating sows reared in tropical climate.. Anim 2017 11(3):365–374.
    doi: 10.1017/s175173111600135xpubmed: 27378416google scholar: lookup
  35. Griffin RA, Swegen A, Baker M, Aitken RJ, Skerrett-Byrne DA, Silva Rodriguez A, Martín-Cano FE, Nixon B, Peña FJ, Delehedde M, Sergeant N, Gibb Z. Mass spectrometry reveals distinct proteomic profiles in High- and Low-Quality stallion spermatozoa.. Reproduction 2020 160(5):695–707.
    doi: 10.1530/rep-20-0284pubmed: 32805711google scholar: lookup
  36. Guérin JF, Mathieu C, Lornage J, Pinatel MC, Boulieu D. Improvement of survival and fertilizing capacity of human spermatozoa in an IVF programme by selection on discontinuous Percoll gradients.. Hum Reprod 1989 4(7):798–804.
  37. Hahn GL. Dynamic responses of cattle to thermal heat loads.. J Anim Sci 1999 77(suppl2):10–20.
    pubmed: 15526777
  38. Hamilton TR, de Castro LS, Jde D, de Assis C, Siqueira PM, Mendes AF, Goissis CM, Muiño-Blanco MD, Cebrián-Pérez T, Nichi J, Visintin M, J. A. and, D’Ávila Assumpção ME. Induced lipid peroxidation in Ram sperm: semen Profile, DNA fragmentation and antioxidant status.. Reproduction 2016 151(4):379–390.
    doi: 10.1530/rep-15-0403pubmed: 26811546google scholar: lookup
  39. Heerema NA, Sather HN, Sensel MG, La MKL, Hutchinson RJ, Nachman JB, Reaman GH, Lange BJ, Steinherz PG, Bostrom BC, Gaynon PS, Uckun FM. Abnormalities of chromosome bands 15q13-15 in childhood acute lymphoblastic leukemia.. Cancer 2002 94(4):1102–1110.
    doi: 10.1002/cncr.10325pubmed: 11920481google scholar: lookup
  40. Houston BJ, Nixon B, Martin JH, De Iuliis GN, Trigg NA, Bromfield EG, McEwan KE, Aitken RJ. Heat exposure induces oxidative stress and DNA damage in the male germ line.. Biol Reprod 2018 98(4):593–606.
    doi: 10.1093/biolre/ioy009pubmed: 29351587google scholar: lookup
  41. Houston BJ, Nixon B, McEwan KE, Martin JH, King BV, Aitken RJ, De Iuliis GN. Whole-body exposures to radiofrequency-electromagnetic energy can cause DNA damage in mouse spermatozoa via an oxidative mechanism.. Sci Rep 2019 9(1):17478.
    doi: 10.1038/s41598-019-53983-9pmc: PMC6877509pubmed: 31767903google scholar: lookup
  42. Jain K, Suryakumar G, Ganju L, Singh SB. Differential hypoxic tolerance is mediated by activation of heat shock response and nitric oxide pathway.. Cell Stress Chaperones 2014 19(6):801–812.
    doi: 10.1007/s12192-014-0504-9pmc: PMC4389840pubmed: 24590457google scholar: lookup
  43. Janecka M, Hansen SN, Modabbernia A, Browne HA, Buxbaum JD, Schendel DE, Reichenberg A, Parner ET, Grice DE. Parental age and differential estimates of risk for neuropsychiatric disorders: findings from the Danish birth cohort.. J Am Acad Child Adolesc Psychiatry 2019 58(6):618–627.
    doi: 10.1016/j.jaac.2018.09.447pmc: PMC10790681pubmed: 30825496google scholar: lookup
  44. Johnson L, Blanchard TL, Varner DD, Scrutchfield WL. Factors affecting spermatogenesis in the stallion.. Theriogenology 1997 48(7):1199–1216.
    doi: 10.1016/s0093-691x(97)00353-1pubmed: 16728209google scholar: lookup
  45. Jones RC, Stewart DL. The effects of cooling to 5 degrees C and freezing and thawing on the ultrastructure of bull spermatozoa.. J Reprod Fertil 1979 56(1):233–238.
    doi: 10.1530/jrf.0.0560233pubmed: 469847google scholar: lookup
  46. Karamahmutoglu H, Erdem A, Erdem M, Mutlu MF, Bozkurt N, Oktem M, Ercan DD, Gumuslu S. The gradient technique improves success rates in intrauterine insemination cycles of unexplained subfertile couples when compared to swim up technique; a prospective randomized study.. J Assist Reprod Genet 2014 31(9):1139–1145.
    doi: 10.1007/s10815-014-0274-4pmc: PMC4156944pubmed: 25026953google scholar: lookup
  47. Kasai H. Analysis of a form of oxidative DNA damage, 8-hydroxy-2’-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis.. Mutat Res 1997 387(3):147–163.
    doi: 10.1016/S1383-5742(97)00035-5pubmed: 9439711google scholar: lookup
  48. Kim KS, Seibert JT, Edea Z, Graves KL, Kim ES, Keating AF, Baumgard LH, Ross JW, Rothschild MF. Characterization of the acute heat stress response in gilts: Iii. genome-wide association studies of thermotolerance traits in pigs.. J Anim Sci 2018 96(6):2074–2085.
    doi: 10.1093/jas/sky131pmc: PMC6095244pubmed: 29669012google scholar: lookup
  49. Liu Y, Li D, Li H, Zhou X, Wang G. A novel Snp of the Atp1a1 gene is associated with heat tolerance traits in dairy cows.. Mol Biol Rep 2011 38(1):83–88.
    doi: 10.1007/s11033-010-0080-8pubmed: 20336380google scholar: lookup
  50. Liu S, Ye T, Li Z, Li J, Jamil AM, Zhou Y, Hua G, Liang A, Deng T, Yang L. Identifying hub genes for heat tolerance in water Buffalo (Bubalus Bubalis) using transcriptome data.. Front Genet 2019 10(209).
    pmc: PMC6424900pubmed: 30918514doi: 10.3389/fgene.2019.00209google scholar: lookup
  51. Love CC, Kenney RM. Scrotal heat stress induces altered sperm chromatin structure associated with a decrease in protamine disulfide bonding in the stallion.. Biol Reprod 1999 60(3):615–620.
    doi: 10.1095/biolreprod60.3.615pubmed: 10026107google scholar: lookup
  52. Mader TL. Environmental stress in confined beef cattle.. J Anim Sci 2003 81(14suppl2):E110–E119.
  53. Martin JH, Aitken RJ, Bromfield EG, Nixon B. DNA damage and repair in the female germline: contributions to Art.. Hum Reprod Update 2019 25(2):180–201.
    doi: 10.1093/humupd/dmy040pubmed: 30541031google scholar: lookup
  54. Mathevon M, Buhr MM, Dekkers JC. Environmental, management, and genetic factors affecting semen production in Holstein bulls.. J Dairy Sci 1998 81(12):3321–3330.
  55. Mignon-Ravix C, Depetris D, Luciani JJ, Cuoco C, Krajewska-Walasek M, Missirian C, Collignon P, Delobel B, Croquette MF, Moncla A, Kroisel PM, Mattei MG. Recurrent rearrangements in the proximal 15q11-Q14 region: a new breakpoint cluster specific to unbalanced translocations.. Eur J Hum Genet 2007 15(4):432–440.
    doi: 10.1038/sj.ejhg.5201775pubmed: 17264869google scholar: lookup
  56. Mislei B, Bucci D, Malama E, Bollwein H, Mari G. Seasonal changes in Ros concentrations and sperm quality in unfrozen and frozen-thawed stallion semen.. Theriogenology 2020 144:89–97.
  57. Netherton JK, Hetherington L, Ogle RA, Velkov T, Baker MA. Proteomic analysis of good- and poor-quality human sperm demonstrates that several proteins are routinely aberrantly regulated.. Biol Reprod 2018 99(2):395–408.
    doi: 10.1093/biolre/iox166pubmed: 29228106google scholar: lookup
  58. Netherton JK, Robinson BR, Ogle RA, Gunn A, Villaverde AISB, Colyvas K, Wise C, Russo T, Dowdell A, Baker MA. Seasonal variation in bull semen quality demonstrates there are heat-sensitive and heat-tolerant bulls.. Sci Rep 2022 12(1):15322.
    doi: 10.1038/s41598-022-17708-9pmc: PMC9468146pubmed: 36097009google scholar: lookup
  59. Neto CR, Monteiro GA, Delfiol DJZ, Farras MC, Dell’aqua JA Jr, Papa FO, Alvarenga MA. The relationships between scrotal surface Temperature, age and sperm quality in stallions.. Livest Sci 2013 157(1):358–363.
  60. NSW Office of Environment and Heritage (2014) ‘Hunter Climate Change Snapshot’, https://www.climatechange.environment.nsw.gov.au/sites/default/files/2021-06/Hunter%20climate%20change%20snapshot.pdf. Accessed 23/10/2023
  61. Ohno M, Sakumi K, Fukumura R, Furuichi M, Iwasaki Y, Hokama M, Ikemura T, Tsuzuki T, Gondo Y, Nakabeppu Y. 8-oxoguanine causes spontaneous de novo germline mutations in mice.. Sci Rep 2014 4(1):4689.
    doi: 10.1038/srep04689pmc: PMC3986730pubmed: 24732879google scholar: lookup
  62. Osei-Amponsah R, Dunshea FR, Leury BJ, Cheng L, Cullen B, Joy A, Abhijith A, Zhang MH, Chauhan SS. Heat stress impacts on lactating cows grazing Australian summer pastures on an automatic robotic dairy.. Animals 2020 10(5):869.
    doi: 10.3390/ani10050869pmc: PMC7278445pubmed: 32429603google scholar: lookup
  63. Paul C, Teng S, Saunders PT. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death.. Biol Reprod 2009 80(5):913–919.
  64. Pérez-Crespo M, Pintado B, Gutiérrez-Adán A. Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice.. Mol Reprod Dev 2008 75(1):40–47.
    doi: 10.1002/mrd.20759pubmed: 17474098google scholar: lookup
  65. Rahman MB, Vandaele L, Rijsselaere T, Maes D, Hoogewijs M, Frijters A, Noordman J, Granados A, Dernelle E, Shamsuddin M. Scrotal insulation and its relationship to abnormal morphology, chromatin protamination and nuclear shape of spermatozoa in Holstein-Friesian and Belgian blue bulls.. Theriogenology 2011 76(7):1246–1257.
  66. Rao M, Xia W, Yang J, Hu LX, Hu SF, Lei H, Wu YQ, Zhu CH. Transient scrotal hyperthermia affects human sperm DNA integrity, sperm apoptosis, and sperm protein expression.. Andrology 4(6):1054–1063.
    doi: 10.1111/andr.12228pubmed: 27410176google scholar: lookup
  67. Sakkas D, Urner F, Bizzaro D, Manicardi G, Bianchi PG, Shoukir Y, Campana A. Sperm nuclear DNA damage and altered chromatin structure: effect on fertilization and embryo development.. Hum Reprod 13(Supplement 4):11–19.
    doi: 10.1093/humrep/13.suppl_4.11pubmed: 10091054google scholar: lookup
  68. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B. Fiji: an open-source platform for biological-image analysis.. Nat Methods 9(7):676–682.
    doi: 10.1038/nmeth.2019pmc: PMC3855844pubmed: 22743772google scholar: lookup
  69. Shiva M, Gautam AK, Verma Y, Shivgotra V, Doshi H, Kumar S. Association between sperm quality, oxidative stress, and seminal antioxidant activity.. Clin Biochem 44(4):319–324.
  70. Stefansson H, Rujescu D, Cichon S, Pietiläinen OP, Ingason A, Steinberg S, Fossdal R, Sigurdsson E, Sigmundsson T, Buizer-Voskamp JE. Large recurrent microdeletions associated with schizophrenia.. Nature 455(7210):232–236.
    doi: 10.1038/nature07229pmc: PMC2687075pubmed: 18668039google scholar: lookup
  71. Thom EC. The discomfort index.. Weatherwise 12(2):57–61.
  72. Vazza G, Bertolin C, Scudellaro E, Vettori A, Boaretto F, Rampinelli S, De Sanctis G, Perini G, Peruzzi P, Mostacciuolo ML. Genome-wide scan supports the existence of a susceptibility locus for schizophrenia and bipolar disorder on chromosome 15q26.. Mol Psychiatry 12(1):87–93.
    doi: 10.1038/sj.mp.4001895pubmed: 16969366google scholar: lookup
  73. Vogler CJ, Saacke RG, Bame JH, Dejarnette JM, McGilliard ML. Effects of scrotal insulation on viability characteristics of cryopreserved bovine semen.. J Dairy Sci 74(11):3827–3835.
  74. Vogler C, Bame J, DeJarnette J, McGilliard M, Saacke R. Effects of elevated testicular temperature on morphology characteristics of ejaculated spermatozoa in the bovine.. Theriogenology 40(6):1207–1219.
  75. Wach-Gygax L, Burger D, Malama E, Bollwein H, Fleisch A, Jeannerat E, Thomas S, Schuler G, Janett F. Seasonal changes of DNA fragmentation and quality of raw and cold-stored stallion spermatozoa.. Theriogenology 99:98–104.
  76. Waites GM. Thermoregulation of the scrotum and testis: studies in animals and significance for man.. .
    pubmed: 2042522
  77. Waites GM, Setchell BP. Effect of local heating on blood flow and metabolism in the testis of the conscious ram.. Reproduction 8(3):339–349.
    doi: 10.1530/jrf.0.0080339pubmed: 14248594google scholar: lookup
  78. Waites GM. Chapter 4 -Temperature Regulation and the Testis.. 1970, Academic Press, 241–279.
  79. Walters A, Saacke R, Pearson R, Gwazdauskas F. The incidence of apoptosis after IVF with morphologically abnormal bovine spermatozoa.. Theriogenology 64(6):1404–1421.
  80. Xavier MJ, Nixon B, Roman SD, Scott RJ, Drevet JR, Aitken RJ. Paternal impacts on development: identification of genomic regions vulnerable to oxidative DNA damage in human spermatozoa.. Hum Reprod 34(10):1876–1890.
    doi: 10.1093/humrep/dez153pubmed: 31593593google scholar: lookup

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