译者的话：
炎热季节热应激造成的夏季配种的母猪分娩率降低、夏季配种母猪所产后代的胴体肥度增加、高温条件下育肥猪生长速度和胴体重降低，是造成养猪业重大经济损失的三大影响因素。此外还有增加母猪非生产天数、增加死亡率等其他方面的影响。据估计，在美国热应激导致养猪业每年损失21.86亿元。来自澳大利亚的不完全统计显示，夏季高温对澳大利亚养猪业造成的三大影响带来的经济损失估计为每年1.053亿元。
作者 Authors:
F. Liu a,⇑, W. Zhao b, H.H. Le b, J.J. Cottrell b, M.P. Green c, B.J. Leury b, F.R. Dunshea b,d, A.W. Bell e
澳大利亚瑞瓦里亚澳大利亚有限公司研究与创新部
a Research and Innovation Unit, Rivalea Australia Pty Ltd, Corowa, NSW 2646, Australia
澳大利亚墨尔本大学兽医与农业科学学院
b Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville, VIC 3010, Australia
澳大利亚墨尔本大学理学院
c Faculty of Science, University of Melbourne, Parkville, VIC 3010, Australia
英国利兹大学生物科学学院
d Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom
美国康奈尔大学动物科学系
e Department of Animal Science, Cornell University, Ithaca 14853-4801, USA
文献综述：热应激对养猪生产的影响（一）
Review: What have we learned about the effects of heat stress on the pig industry? - Part 1
摘要 Abstract
养猪生产面临季节性波动。夏季配种的母猪分娩率偏低、其所产后代的胴体脂肪增加、以及夏季育肥猪生长速度减慢是已知的季节对养猪业的三个重要经济影响。本综述的目的是审查过去十年在理解与夏季气候条件(特别是热应激(HS))相关的上述三种影响的机制方面的进展，并提供可能的改善策略。对于第一种影响，夏季配种母猪的分娩率偏低，主要是由于妊娠早期出现的妊娠失败。本文讨论了精细胞DNA损伤、卵母细胞质量差、局部孕酮浓度和胚胎雌激素分泌欠佳等因素，因为这些在受胎期间都可能导致热应激介导效应。尽管如此，我们目前尚不清楚潜在的作用机制是什么，因此目前缺乏可行的商业解决方案。对于第二种影响，行业最近在了解妊娠期热应激对母猪和胎儿的影响方面取得了进展，妊娠期热应激可导致胎儿肌纤维数量减少、出生重较轻的仔猪比例增加以及屠宰时胴体脂肪增加。到目前为止，还没有有效的策略来减轻妊娠期热应激对胎儿的影响。至于第三种影响，夏季生猪生长速度减慢是夏季胴体重降低的原因之一。研究表明，生长速度的降低可能不仅仅是由于采食量的减少，肠道屏障功能受损和炎症反应也是影响因素。此外，一直有报道称，热应激会减弱脂肪动员，当胴体重增加时，脂肪动员可能会加剧胴体脂肪肥度。新型饲料添加剂已显示出可降低热应激对生长猪肠道屏障功能影响的潜力。综上所述，基于这三种影响，可以估算出与热应激相关的经济损失。有必要对这些影响进行审查，以便更好地使未来的研究方向与养猪业的需求保持一致。最终，更好地理解潜在机制并持续投资于开发针对热应激的商业可行的策略从而使养猪业受益。
Pig production faces seasonal fluctuations. The low farrowing rate of sows mated in summer, increased carcass fatness of progeny born to the sows mated in summer, and slower growth rate of finisher pigs in summer are three economically important impacts identified in the pig industry. The purpose of this review is to examine advances over the past decade in understanding the mechanisms underlying the three impacts associated with summer conditions, particularly heat stress (HS), and to provide possible amelioration strategies. For impact 1, summer mating results in low farrowing rates mainly caused by the high frequency of early pregnancy disruptions. The contributions of semen DNA damage, poor oocyte quality, local progesterone concentrations, and suboptimal embryonic oestrogen secretion are discussed, as these all may contribute to HS-mediated effects around conception. Despite this, it is still unclear what the underlying mechanisms might be and thus, there is currently a lack of commercially viable solutions. For impact 2, there have been recent advances in the understanding of gestational HS on both the sow and foetus, with gestational HS implicated in decreased foetal muscle fibre number, a greater proportion of lighter piglets, and increased carcass fatness at slaughter. So far, no effective strategies have been developed to mitigate the impacts associated with gestational HS on foetuses. For impact 3, the slowed growth rate of pigs during summer is one reason for the reduced carcass weights in summer. Studies have shown that the reduction in growth rates may be due to more than reductions in feed intake alone, and the impaired intestinal barrier function and inflammatory response may also play a role. In addition, it is consistently reported that HS attenuates fat mobilisation which can potentially exacerbate carcass fat- ness when carcass weight is increased. Novel feed additives have exhibited the potential to reduce the impacts of HS on intestinal barrier function in grower pigs. Collectively, based on these three impacts, the economic loss associated with HS can be estimated. A review of these impacts is warranted to better align the future research directions with the needs of the pig industry. Ultimately, a better understanding of the underlying mechanisms and continuous investments in developing commercially viable strategies to combat HS will benefit the pig industry.
研究意义Implications
夏季环境条件，特别是热应激，会影响生猪的生产效率。夏季配种的母猪分娩率低、夏季配种母猪的后代胴体脂肪增加、育肥猪夏季生长速度减慢是已知的主要影响。这些影响导致的相关的养猪业年度经济损失是巨大的。
Summer conditions, particularly heat stress, compromise pig production efficiency. The low farrowing rate of sows mated in summer, increased carcass fatness of progeny born to the sows mated in summer, and slower growth rate of finisher pigs in summer are three known major impacts. The annual economic loss associated with these impacts in the pig industry is significant.
研究已经使我们对热应激的生理影响有了进一步的了解，但养猪业仍然需要商业上可行的解决方案：(1)减轻夏季断奶和配种的母猪的早期妊娠损失；(2)改善夏季配种和妊娠的母猪所产后代的胎儿发育情况；(3)提高炎热季节育肥猪的生长速度。
Research has progressed our understanding of the physiological impacts of heat stress, but the pig industry still requires commercially viable solutions on (1) mitigating the early pregnancy disruption of sows weaned and mated in summer; (2) improving foetal development of progeny born to the sows mated and gestated in summer, and; (3) increasing the growth rate of pigs finished in hot seasons.
研究背景Introduction
夏季的热应激(HS)条件会降低生产效率，并使全球猪肉生产的成本增高。种猪群繁殖性能下降和生长/育肥猪生长速度减慢是与热应激相关的两个典型影响。当环境温度超过猪的热中性区上限时，猪就会出现热应激。热应激对猪的生理影响是广泛的。了解和减轻热应激对猪的生理影响已成为近十年来的重要研究课题之一。量化热应激对养猪业的影响也很重要，因为它有助于研究向受热应激限制最大的方向进展。由于气候条件、生产体系和市场需求不同，在全球范围内概括热应激对养猪业的影响具有挑战性。回顾热应激对代表性地区养猪业的影响对于提供更有针对性和更深入的分析是有价值的，并且它创造了利用全球研究产生的知识交叉验证和解释热应激影响的机会。本文以以亚热带气候为主的澳大利亚为例，综述了热应激对养猪业的影响。本综述总结的知识可以应用于全球养猪业由于全球变暖热应激的影响明显或热应激正在出现的地区。
Heat stress (HS) conditions in summer can compromise production efficiency and present a high cost to pork production globally. Reductions of reproductive performance in breeding herds and slowed growth rate in grower/finisher pigs are two typical impacts associated with HS. Heat stress can occur in pigs when the environmental temperature goes beyond their thermoneutral zones’ upper limits. The physiological impacts of HS in pigs are comprehensive. Understanding and mitigating the physiological impacts of HS has been one of the key research topics of the past decade. Quantifying the impacts of HS in the pig industry is also important, because it helps research advances in the direction where the pig production is most limited by HS. Generalising the impacts of HS in global pig industry is challenging due to diverse climatic conditions, production systems, and market requirements. Reviewing the impacts of HS on the pig industry in a representative region is valuable for pro- viding a more focused and in-depth analysis, and it creates opportunities to cross validate and interpret the HS impacts using the knowledge generated from global studies. The impacts of HS in the pig industry are reviewed here using Australia, where its pig industry mainly under sub-tropical climate, as an example. The knowledge summarised in this review can be applied to the global pig industry where HS impacts are evident or emerging due to global warming.
澳大利亚的许多养猪户都位于亚热带地区，那里的季节之间温度变化很大。高环境温度是澳大利亚夏季最关键的特征之一。图1显示了1970年至2020年间集约化生猪生产区(澳大利亚新南威尔士州克洛瓦, 35.99°S, 146.48°E)的最高和最低温度。11月至3月的平均最高气温高于生长猪(Huynh et al.，2005)和哺乳母猪(Quiniou and Noblet, 1999)的热中性区上限。通常预计在这几个月里猪的生产性能会显著下降。与其他受热应激影响的地区一样，在澳大利亚开展了多个研究项目，以了解和减轻热应激对生猪生产的影响，这些研究项目得到了猪肉中心、澳大利亚猪肉有限公司、农业部、大学和其他行业合作伙伴的资助支持。在母猪中进行的研究部分使用了自然条件下的季节性比较设计，由于缺乏气候可控的研究设施和所需的高样本量，因此生理影响与夏季条件有关(包括但不限于高环境温度)。同时，关于热应激对生长猪的影响已经进行了大量的气候控制实验。当前综述的范围将集中在降低养猪业生产效率的三个主要影响上——(1)夏季配种母猪繁殖失败增加，(2)夏季配种母猪的后代胴体脂肪增加，(3)夏季育肥猪生长速度减慢(图2)。本文根据最近的全球证据讨论了每种影响，估计了与这些影响相关的经济损失，并总结了已评估的解决方案。当前的综述旨在就热应激对养猪业的主要影响提供最新的研究总结，并确定未来研究的知识空白，以提高在这些具有挑战性和不断变化的气候条件下猪肉生产的效率。
Many pig producers in Australia are located in sub-tropical regions, where considerable changes of temperature occur between seasons. High environmental temperature is one of the most critical features of summer in Australia. Fig. 1 illustrates the maximum and minimum temperatures in an intensive pig production region (Corowa, NSW, Australia, 35.99°S, 146.48°E) between 1970 and 2020. The average maximum temperature between November and March was above the upper limits of the thermoneutral zone for grower pigs (Huynh et al., 2005) and lactating sows (Quiniou and Noblet, 1999). Significant reductions in pig performance are usually anticipated during those months. Same as other regions that suffer from HS impacts, multiple research projects have been conducted in Australia to understand and mitigate the impacts of HS on pig production with the funding support from the Pork CRC, Australian Pork Limited, Department of Agriculture, universities and other industry partners. The research conducted in sows has partially used a seasonal comparison design under natural conditions, due to the lack of climatically controlled research facilities and high sample sizes required, so the physiological impacts were related to summer conditions (hence include but are not limited to high environmental temperature). At the same time, there has been a considerable amount of climatically con- trolled experiments on the effect of HS on grower pigs. The current review’s scope will focus on three major impacts that are reducing production efficiency in the pig industry – (1) increased reproductive failure of sows mated in summer, (2) increased carcass fatness of progeny of sows mated in summer, and (3) slower growth rate of finisher pigs in summer (Fig. 2). This review discusses each impact based on recent worldwide evidence, estimates the economic loss associated with these impacts, and summarises the solutions that have been evaluated. The current review aims to provide an updated research summary on the major impacts of HS on the pig industry and identify knowledge gaps for future research to improve the efficiency of pork production in these challenging and changing climatic conditions.
图1：澳大利亚主要生猪产区的历史温度记录(1970-2020年)(平均值±标准差)。横轴为月份，纵轴为温度，上面的带箭头虚线为生长/育肥猪的热中性温度上限，下面的带箭头虚线为哺乳母猪的热中性温度上限。数据来自澳大利亚新南威尔士州克洛瓦机场气象站(35.99°S, 146.48°E;ID:074034，澳大利亚气象局)。热中性区的上限（橙色曲线）定义为猪开始减少总产热时的环境温度(生长猪约为23°C (Huynh et al.， 2005)，哺乳母猪约为22°C (Quiniou and Noblet, 1999))。
Fig. 1. Temperature record of a major pig production region in Australia (1970–2020) (mean ± SD). Data were retrieved from Corowa Airport weather station, NSW, Australia (35.99°S, 146.48°E; ID:074034, Bureau of Meteorology). The upper limit of the thermoneutral zone is defined as the environmental temperature when the pig starts to reduce total heat production (approximately 23 °C for growers (Huynh et al., 2005) and 22 °C for lactating sows (Quiniou and Noblet, 1999)).
图2：夏季气候条件对生猪生产的三个主要影响。首先，夏季配种母猪的分娩率低，增加了非生产天数，需要配种更多的母猪来维持育肥猪的市场供应，这提高了猪群的料重比。第二，对于夏季配种后成功分娩的母猪，由于妊娠热应激对胎儿发育的影响，后代出生体重较轻(≤1.1 kg)的比例较大。出生体重轻的仔猪比例的增加会导致仔猪群生长速度下降，成活率降低，胴体脂肪升高。第三，高温条件下生猪生长速度的减慢降低了胴体重，从而限制了养猪生产者的收入。
Fig. 2. Three major impacts associated with summer conditions in pig production. First, the reduced farrowing rate of sows mated in summer increased the non-reproductive days and requires more sows to be mated for maintaining the supply of finisher pigs to the market, which inflates the herd feed conversion ratio. Second, for sows that manage to farrow after summer mating, a greater proportion of progeny is born with light BW (≤1.1 kg) due to the impacts of gestational heat stress on foetal development. The increased proportion of born-light progeny pigs can result in inferior growth rate, reduced survival rate, and higher carcass fatness of the progeny population. Third, the slowed growth rate of pigs during hot conditions reduces carcass weight and consequently limits the revenue of pig producers.
影响1：夏季配种母猪的分娩率偏低Impact 1: Reduced farrowing rate of sows mated in summer 夏季配种母猪分娩率偏低的证据Evidence for reduced farrowing rate of sows mated in summer 夏季配种的母猪分娩率降低仍然是包括澳大利亚在内的全球养猪业面临的一个主要问题。在澳大利亚，用于终端商品猪生产的常见母系品种是大白母猪和长白母猪，父系品种是杜洛克公猪(第一产业部，2016年)。澳大利亚两家主要养猪场的最新生产数据(2010-2018年)显示，分娩率的下降始于12月份。12月至次年3月的平均分娩率比年平均分娩率低5%至10% (Hermesch和Bunz, 2020)。最近公布的澳大利亚夏季配种的商业化养殖的母猪的分娩率在64%至83%之间，低于较冷月份的89% (Liu et al., 2019; 2020; Plush et al., 2019)。高环境温度加上日照长度的变化被认为会影响夏季的繁殖能力。一项2012年至2017年对澳大利亚一家大型猪场的分娩记录的分析发现，如果在配种前35天出现高环境温度(>29°C)，会导致分娩率的最大下降(Bunz et al.，2019)。Reduced farrowing rate of domestic sows that were mated in summer remains a major issue in the global pig industry, including Australia. The common breeds used for terminal pig production in Australia are Large White- and Landrace-based genetics for the maternal line and Duroc-based genetics for the sire line (Department of Primary Industries, 2016). Recent production data (2010–2018) from two major Australian piggeries showed that the decline in the farrowing rate began in December. The average farrowing rate between December and March was 5% to 10% lower than the annual average (Hermesch and Bunz, 2020). Recently published Australian commercial farrowing rates of sows mated in summer range from 64% to 83% which is lower than cooler months (89%) (Liu et al., 2019; 2020; Plush et al., 2019). The high environmental temperature coupled with the daylight length change is postulated to affect fertility in summer. An analysis of the farrowing records from a large Australian piggery between 2012 and 2017 found that if a high environmental temperature (>29 °C) occurred 35 days before mating, it caused the largest reduction in farrowing rate (Bunz et al., 2019). 母猪的分娩成绩取决于一系列因素。卵泡的形成导致发情和随后的排卵。当活性卵母细胞与优质精子受精时，就会发生受孕。母体对怀孕的认知触发了内分泌的变化和子宫的准备，以促进胚胎着床(Spencer and Bazer, 2004)。黄体分泌的黄体酮在维持妊娠中起着重要作用。夏季繁殖障碍主要表现为母猪配种后不规律返情的比例增加，因此需要增加配种次数以确保有效的妊娠。来自澳大利亚的数据显示，窝均总仔数和窝均活产仔数在不同季节保持不变(Lewis和Bunter, 2011年)。在过去的40年里，提高对夏季繁殖障碍背后的生理机制的理解和制定干预策略一直是一个关键的研究重点(King, 2017)。在过去的5年里，夏季繁殖障碍研究的共识是，夏季配种母猪分娩率的降低主要是由于早期妊娠失败，而不是未成功受孕。Farrowing success of sows relies on a series of events. Folliculo genesis results in oestrus and subsequent ovulation. Conception can take place when competent oocytes are fertilised by quality sperm. Maternal recognition of pregnancy triggers endocrine changes and the preparation of the uterus to facilitate embryo implantation (Spencer and Bazer, 2004). The progesterone secreted from functional corpora lutea plays an important role in the maintenance of pregnancy. Summer infertility mainly manifests as an increased proportion of sows that have an irregular return after mating, and thus an increased number of matings are required to establish a viable pregnancy. Data from Australia show the total number of piglets born per litter and the number of piglets born alive both remain constant among seasons (Lewis and Bunter, 2011). In the past 40 years, improved understanding of the physiological mechanisms behind summer infertility and developing intervention strategies have been a critical research focus (King, 2017). In the last 5 years, the consensus of summer infertility studies has been that the reduction in the farrowing rate of sows mated in summer is mainly due to early pregnancy disruption rather than a failure to conceive. 夏季配种时发情至排卵间隔的改变Altered oestrus-to-ovulation interval during summer mating 养猪生产者通常根据行为发情的检测来安排人工授精(AI)，因此了解准确的发情至排卵间隔(OOI)对于安排人工授精时机以实现最佳受孕至关重要。在热应激环境下对发情至排卵间隔有相互矛盾的发现。一项气候控制研究发现，哺乳期热应激(31°C, 8:00-16:00；26°C 16:00-8.00)将卵泡大小从6.7毫米减少到5.8毫米，并将发情至排卵间隔从1天延长到2.5天(Cabezón et al.，2017)。而另一项研究发现了相反的结果，夏季断奶母猪的发情至排卵间隔比冬季断奶母猪短10小时(21.8小时比31.4小时)(van Wettere, 2013)。同样，在夏季哺乳和配种的母猪(2019年12月- 2020年3月；25.4±5.01℃平均值±标准偏差；澳大利亚)其平均发情至排卵间隔为1.1天(Liu et al.， 2021a)。研究结果之间的矛盾可能是由于不同的环境条件或基因型导致的。值得注意的是，即使在夏季发情至排卵间隔的变化很明显，当使用两次人工授精配种时(即：断奶后首次检测到发情行为时进行第一次人工授精，24小时候进行第二次)，受孕的时机和成功也不太可能受到不合时宜的配种或授精的影响。在发情开始时就配种仍然是夏季发情至排卵间隔为1.1天的断奶母猪的最佳配种时机，因为在排卵前0-24小时进行授精可以获得最佳的母猪受胎率(Kemp和Soede, 1996)。有意思是，平均发情至排卵间隔为1.1天的母猪在夏季接受两次人工授精后，它们的分娩率依旧偏低(65%)(Liu et al.， 2021a)。因此，妊娠早期(第35天之前)的因素，包括母体对妊娠的识别、胚胎存活、子宫环境、精子和卵母细胞质量，可能是分娩率较低的原因，我们将在下一节讨论。Pig producers usually schedule artificial insemination (AI) based on the detection of behavioural oestrus, so knowing the accurate oestrus-to-ovulation interval (OOI) is essential for scheduling AI to achieve optimum conception. There are conflicting findings on OOI during HS conditions. A climatic controlled study found that HS during lactation (31 °C, 8:00–16:00; 26 °C 16:00–8.00) reduced follicle size from 6.7 to 5.8 mm and prolonged OOI from 1 to 2.5 days (Cabezón et al., 2017). Conversely, OOI was 10 hours shorter in sows whose litters were weaned in summer than winter (21.8 h vs 31.4 h) (van Wettere, 2013). Similarly, the sows lactated and mated under summer conditions (December 2019–March 2020; 25.4 ± 5.01 °C mean ± SD; Australia) had an average OOI of 1.1 days (Liu et al., 2021a). The conflicting findings between studies may be due to different environmental conditions or genotypes. Notably, even if changes in OOI are evident in summer, the timing and success of conception are unlikely to be affected due to a mistimed mating or insemination, when a double AI programme is used (i.e.: 1st AI at the first detectable behaviour oestrus after weaning and 2nd AI at 24 h after this). Insemination at the onset of oestrus remains the best timing for mating weaned sows with such an OOI (1.1 days) in summer because insemination performed at 0–24 h before ovulation can achieve optimum sow conception rates (Kemp and Soede, 1996). Interestingly, the farrowing rate of the sows with an average OOI of 1.1 days that received two AIs in summer remained low (65%) (Liu et al., 2021a). Hence, factors during early pregnancy (before day 35), including maternal recognition of pregnancy, embryo survival, uterine environment, and sperm as well as oocyte quality, may be responsible for lower farrowing rates and are discussed in the next section.
未完待续……To be continued…
1.本文由猪译官蔚飞，佟彤编辑，猪译馆享有中文版权，如需转载，请联系我们。
2.参考文献：关注“猪译馆”微信公众平台，回复“ 20230906 ”获取。