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Global warming : consequences for sperm quality and fertility of dairy and beef bulls

(2019)
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(UGent) , Erik Mullaart and Patrick Lonergan
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Abstract
Genital heat stress is a substantial risk factor for male infertility. At present, it is known that bulls exposed to natural heat stress experience a decrease in sperm quality, even in regions with temperate climates. Slight increases in scrotal temperature can disrupt spermatogenesis, resulting in a complex stress response. Negative effects of heat exposure were observed in semen collected between 14 and 42 days after artificial scrotal insulation, indicating that heat stress is more prejudicial for developing germ cells than for mature sperm cells. Bulls exposed to heat stress are more likely to suffer reduction of testicular weight, alteration of testosterone levels and increase of respiratory rate, rectal temperature, and water consumption. Moreover, hyperthermia has been found to disrupt spermatogenesis, reduce the fertilizing ability, sperm motility, normal morphology, viability, and to alter both the concentration and composition of lipids in bovine sperm. Furthermore, ROS production significantly increases in sperm, leading to lipid peroxidation (LPO), DNA fragmentation, and major sperm defects. Rising temperatures as a consequence of climate change not only have adverse effects on male reproduction, but also on animal physiology, welfare, and health. For decades, the continuing rise in global temperatures has been a concern worldwide and it is expected that temperatures will continue to increase. Global temperature has risen 0.9ºC in the last century. This temperature increase has accelerated for the past 35 years; the warmest five years on record have taken place since 2010, where 2016 was the warmest year and July 2019 the hottest month on record since modern recordkeeping began in 1880. Moreover, the number of days with a temperature humidity index (THI) above 68, which is considered the comfort threshold for cows, has increased by 4.1% from 1973 to 2008 in certain parts of Central Europe with 80 to 86 hot heat stress-causing days per year. Therefore, the main objective of this thesis was to elucidate the effects of rising temperatures on bovine sperm cells and the subsequent generations. Although the detrimental effects of heat stress on bovine reproduction have been studied before, the impact of heat stress on in vivo bull fertility and the molecular mechanisms of sperm damage on bulls exposed to heat stress have not been entirely characterized. First, we aimed to evaluate the sperm quality of the heat-stressed sperm cells, the effect on their fertilizing ability, viability, and quality of the subsequent embryos (Chapter 3). For this purpose, semen samples were collected from six Holstein bulls after a low temperature-humidity index (THI) period (in March) and after a high THI period (in August). The objective was to evaluate whether sperm were affected by high temperatures. Therefore, sperm quality parameters from Percoll®-purified sperm samples were examined in order to achieve a closer representative of live sperm cells that were capable of fertilization. The effect of heat stress on sperm quality was assessed by sperm morphology, motility, reactive oxygen species production, lipid peroxidation, viability, and DNA fragmentation. Moreover, we evaluated the development of embryos generated in vitro by low and high THI semen, and determined inner cell mass/trophectoderm ratio, apoptotic cell ratio, and embryonic gene expression in day-8 blastocysts. Results showed an increase in sperm cell death and a tendency towards higher ROS production when the semen was collected at high THI compared to low THI. However, no differences were observed in other sperm quality parameters. Although no differences were observed in the embryo quality parameters and relative abundance of candidate transcripts examined, a decrease was observed in the total blastocyst rates at day 7 post-insemination and day 8 in the high THI compared to the low THI group. Despite selecting the best quality sperm from each sample, the effects of heat stress were still visible after Percoll® and sperm cells affected by heat stress had the potential to fertilize the oocyte, causing deleterious effect on subsequent embryo production. It is acknowledged that Belgian Blue bulls generally have lower sperm quality and appear to be more vulnerable to heat stress than other breeds, like Holstein bulls. We speculate that with the continuing rise in global temperatures this detrimental effect on Belgian Blue sperm will aggravate. Therefore, we aimed to investigate the effect of high ambient temperature on the sperm quality of Belgian Blue bulls (Chapter 4). For this purpose, semen samples were collected from six Belgian Blue bulls after a low THI period (in March) and after a high THI period (in August). The effect of heat stress on semen quality was assessed by volume, sperm concentration and subjective motility of fresh semen, and motion parameters, morphological abnormalities, acrosome integrity, chromatin condensation, viability, and reactive oxygen species (ROS) production from frozen-thawed semen samples without Percoll® gradient separation. A decrease in sperm concentration of fresh semen and a lowered sperm motility were observed, which might be related to the lower viability and normal morphology, and the increase of aberrant chromatin condensation and H2O2 production of frozen sperm of Belgian Blue bulls. These findings suggest that elevated ambient temperature during summer can lead to decreased quality of semen from different bull breeds. However, several studies on seasonal effects on bovine semen quality report contradictory outcomes that may be due to the great variation among climatic zones. Therefore, we aimed to analyze the effect of climatic conditions on sperm quality and fertility in a large-scale study (Chapter 5). For this purpose, we investigated the differences in sperm motion and morphological parameters, as well as non-return rates (NRR), to determine the effect of age, THI, and season at spermatogenesis and semen collection. Semen data based on 29,170 ejaculates from 933 Holstein bulls collected between 2015 and 2018 were evaluated. Our study shows that climatic conditions compromise not only sperm quality but also dairy bull fertility, as NRR of older bulls decrease at higher THI. We observed that climatic conditions affect the cryotolerance of meiotic sperm cells. Moreover, older bulls exhibited increased sensitivity to THI, showing 0.5 to three times bigger negative effect on sperm quality at the time of spermatogenesis, compared to semen collection. However, fresh sperm quality improved with age and was not affected by THI. These results demonstrate also that THI is an important metric and we encourage the use, together with season, when assessing the effect of heat stress.
Keywords
sperm quality, global warming, embryo development, temperate climate

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MLA
Llamas Luceno, Núria. Global Warming : Consequences for Sperm Quality and Fertility of Dairy and Beef Bulls. Universiteit Gent. Faculteit Diergeneeskunde, 2019.
APA
Llamas Luceno, N. (2019). Global warming : consequences for sperm quality and fertility of dairy and beef bulls. Universiteit Gent. Faculteit Diergeneeskunde.
Chicago author-date
Llamas Luceno, Núria. 2019. “Global Warming : Consequences for Sperm Quality and Fertility of Dairy and Beef Bulls.” Universiteit Gent. Faculteit Diergeneeskunde.
Chicago author-date (all authors)
Llamas Luceno, Núria. 2019. “Global Warming : Consequences for Sperm Quality and Fertility of Dairy and Beef Bulls.” Universiteit Gent. Faculteit Diergeneeskunde.
Vancouver
1.
Llamas Luceno N. Global warming : consequences for sperm quality and fertility of dairy and beef bulls. Universiteit Gent. Faculteit Diergeneeskunde; 2019.
IEEE
[1]
N. Llamas Luceno, “Global warming : consequences for sperm quality and fertility of dairy and beef bulls,” Universiteit Gent. Faculteit Diergeneeskunde, 2019.
@phdthesis{8656779,
  abstract     = {Genital heat stress is a substantial risk factor for male infertility. At present, it is known that bulls exposed to natural heat stress experience a decrease in sperm quality, even in regions with temperate climates. Slight increases in scrotal temperature can disrupt spermatogenesis, resulting in a complex stress response. Negative effects of heat exposure were observed in semen collected between 14 and 42 days after artificial scrotal insulation, indicating that heat stress is more prejudicial for developing germ cells than for mature sperm cells. Bulls exposed to heat stress are more likely to suffer reduction of testicular weight, alteration of testosterone levels and increase of respiratory rate, rectal temperature, and water consumption. Moreover, hyperthermia has been found to disrupt spermatogenesis, reduce the fertilizing ability, sperm motility, normal morphology, viability, and to alter both the concentration and composition of lipids in bovine sperm. Furthermore, ROS production significantly increases in sperm, leading to lipid peroxidation (LPO), DNA fragmentation, and major sperm defects. 
Rising temperatures as a consequence of climate change not only have adverse effects on male reproduction, but also on animal physiology, welfare, and health. For decades, the continuing rise in global temperatures has been a concern worldwide and it is expected that temperatures will continue to increase. Global temperature has risen 0.9ºC in the last century. This temperature increase has accelerated for the past 35 years; the warmest five years on record have taken place since 2010, where 2016 was the warmest year and July 2019 the hottest month on record since modern recordkeeping began in 1880. Moreover, the number of days with a temperature humidity index (THI) above 68, which is considered the comfort threshold for cows, has increased by 4.1% from 1973 to 2008 in certain parts of Central Europe with 80 to 86 hot heat stress-causing days per year. Therefore, the main objective of this thesis was to elucidate the effects of rising temperatures on bovine sperm cells and the subsequent generations. Although the detrimental effects of heat stress on bovine reproduction have been studied before, the impact of heat stress on in vivo bull fertility and the molecular mechanisms of sperm damage on bulls exposed to heat stress have not been entirely characterized.
First, we aimed to evaluate the sperm quality of the heat-stressed sperm cells, the effect on their fertilizing ability, viability, and quality of the subsequent embryos (Chapter 3). For this purpose, semen samples were collected from six Holstein bulls after a low temperature-humidity index (THI) period (in March) and after a high THI period (in August). The objective was to evaluate whether sperm were affected by high temperatures. Therefore, sperm quality parameters from Percoll®-purified sperm samples were examined in order to achieve a closer representative of live sperm cells that were capable of fertilization. The effect of heat stress on sperm quality was assessed by sperm morphology, motility, reactive oxygen species production, lipid peroxidation, viability, and DNA fragmentation. Moreover, we evaluated the development of embryos generated in vitro by low and high THI semen, and determined inner cell mass/trophectoderm ratio, apoptotic cell ratio, and embryonic gene expression in day-8 blastocysts. Results showed an increase in sperm cell death and a tendency towards higher ROS production when the semen was collected at high THI compared to low THI. However, no differences were observed in other sperm quality parameters. Although no differences were observed in the embryo quality parameters and relative abundance of candidate transcripts examined, a decrease was observed in the total blastocyst rates at day 7 post-insemination and day 8 in the high THI compared to the low THI group. Despite selecting the best quality sperm from each sample, the effects of heat stress were still visible after Percoll® and sperm cells affected by heat stress had the potential to fertilize the oocyte, causing deleterious effect on subsequent embryo production.
It is acknowledged that Belgian Blue bulls generally have lower sperm quality and appear to be more vulnerable to heat stress than other breeds, like Holstein bulls. We speculate that with the continuing rise in global temperatures this detrimental effect on Belgian Blue sperm will aggravate. Therefore, we aimed to investigate the effect of high ambient temperature on the sperm quality of Belgian Blue bulls (Chapter 4). For this purpose, semen samples were collected from six Belgian Blue bulls after a low THI period (in March) and after a high THI period (in August). The effect of heat stress on semen quality was assessed by volume, sperm concentration and subjective motility of fresh semen, and motion parameters, morphological abnormalities, acrosome integrity, chromatin condensation, viability, and reactive oxygen species (ROS) production from frozen-thawed semen samples without Percoll® gradient separation. A decrease in sperm concentration of fresh semen and a lowered sperm motility were observed, which might be related to the lower viability and normal morphology, and the increase of aberrant chromatin condensation and H2O2 production of frozen sperm of Belgian Blue bulls. 
These findings suggest that elevated ambient temperature during summer can lead to decreased quality of semen from different bull breeds. However, several studies on seasonal effects on bovine semen quality report contradictory outcomes that may be due to the great variation among climatic zones. Therefore, we aimed to analyze the effect of climatic conditions on sperm quality and fertility in a large-scale study (Chapter 5). For this purpose, we investigated the differences in sperm motion and morphological parameters, as well as non-return rates (NRR), to determine the effect of age, THI, and season at spermatogenesis and semen collection. Semen data based on 29,170 ejaculates from 933 Holstein bulls collected between 2015 and 2018 were evaluated. Our study shows that climatic conditions compromise not only sperm quality but also dairy bull fertility, as NRR of older bulls decrease at higher THI. We observed that climatic conditions affect the cryotolerance of meiotic sperm cells. Moreover, older bulls exhibited increased sensitivity to THI, showing 0.5 to three times bigger negative effect on sperm quality at the time of spermatogenesis, compared to semen collection. However, fresh sperm quality improved with age and was not affected by THI. These results demonstrate also that THI is an important metric and we encourage the use, together with season, when assessing the effect of heat stress.},
  author       = {Llamas Luceño, Núria},
  keywords     = {sperm quality,global warming,embryo development,temperate climate},
  language     = {eng},
  pages        = {215},
  publisher    = {Universiteit Gent. Faculteit Diergeneeskunde},
  school       = {Ghent University},
  title        = {Global warming : consequences for sperm quality and fertility of dairy and beef bulls},
  year         = {2019},
}