譯者的話：
炎熱季節熱應激造成的夏季配種的母豬分娩率降低、夏季配種母豬所産後代的胴體肥度增加、高溫條件下育肥豬生長速度和胴體重降低，是造成養豬業重大經濟損失的三大影響因素。此外還有增加母豬非生産天數、增加死亡率等其他方面的影響。據估計，在美國熱應激導緻養豬業每年損失21.86億元。來自澳洲的不完全統計顯示，夏季高溫對澳洲養豬業造成的三大影響帶來的經濟損失估計為每年1.053億元。
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
澳洲瑞瓦裡亞澳洲有限公司研究與創新部
a Research and Innovation Unit, Rivalea Australia Pty Ltd, Corowa, NSW 2646, Australia
澳洲墨爾本大學獸醫與農業科學學院
b Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville, VIC 3010, Australia
澳洲墨爾本大學理學院
c Faculty of Science, University of Melbourne, Parkville, VIC 3010, Australia
英國利茲大學生物科學學院
d Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom
美國康奈爾大學動物科學系
e Department of Animal Science, Cornell University, Ithaca 14853-4801, USA
文獻綜述：熱應激對養豬生産的影響（一）
Review: What have we learned about the effects of heat stress on the pig industry? - Part 1
摘要 Abstract
養豬生産面臨季節性波動。夏季配種的母豬分娩率偏低、其所産後代的胴體脂肪增加、以及夏季育肥豬生長速度減慢是已知的季節對養豬業的三個重要經濟影響。本綜述的目的是審查過去十年在了解與夏季氣候條件(特别是熱應激(HS))相關的上述三種影響的機制方面的進展，并提供可能的改善政策。對于第一種影響，夏季配種母豬的分娩率偏低，主要是由于妊娠早期出現的妊娠失敗。本文讨論了精細胞DNA損傷、卵母細胞品質差、局部孕酮濃度和胚胎雌激素分泌欠佳等因素，因為這些在受胎期間都可能導緻熱應激介導效應。盡管如此，我們目前尚不清楚潛在的作用機制是什麼，是以目前缺乏可行的商業解決方案。對于第二種影響，行業最近在了解妊娠期熱應激對母豬和胎兒的影響方面取得了進展，妊娠期熱應激可導緻胎兒肌纖維數量減少、出生重較輕的仔豬比例增加以及屠宰時胴體脂肪增加。到目前為止，還沒有有效的政策來減輕妊娠期熱應激對胎兒的影響。至于第三種影響，夏季生豬生長速度減慢是夏季胴體重降低的原因之一。研究表明，生長速度的降低可能不僅僅是由于采食量的減少，腸道屏障功能受損和發炎反應也是影響因素。此外，一直有報道稱，熱應激會減弱脂肪動員，當胴體重增加時，脂肪動員可能會加劇胴體脂肪肥度。新型飼料添加劑已顯示出可降低熱應激對生長豬腸道屏障功能影響的潛力。綜上所述，基于這三種影響，可以估算出與熱應激相關的經濟損失。有必要對這些影響進行審查，以便更好地使未來的研究方向與養豬業的需求保持一緻。最終，更好地了解潛在機制并持續投資于開發針對熱應激的商業可行的政策進而使養豬業受益。
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.
研究意義Implications
夏季環境條件，特别是熱應激，會影響生豬的生産效率。夏季配種的母豬分娩率低、夏季配種母豬的後代胴體脂肪增加、育肥豬夏季生長速度減慢是已知的主要影響。這些影響導緻的相關的養豬業年度經濟損失是巨大的。
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.
研究已經使我們對熱應激的生理影響有了進一步的了解，但養豬業仍然需要商業上可行的解決方案：(1)減輕夏季斷奶和配種的母豬的早期妊娠損失；(2)改善夏季配種和妊娠的母豬所産後代的胎兒發育情況；(3)提高炎熱季節育肥豬的生長速度。
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
夏季的熱應激(HS)條件會降低生産效率，并使全球豬肉生産的成本增高。種豬群繁殖性能下降和生長/育肥豬生長速度減慢是與熱應激相關的兩個典型影響。當環境溫度超過豬的熱中性區上限時，豬就會出現熱應激。熱應激對豬的生理影響是廣泛的。了解和減輕熱應激對豬的生理影響已成為近十年來的重要研究課題之一。量化熱應激對養豬業的影響也很重要，因為它有助于研究向受熱應激限制最大的方向進展。由于氣候條件、生産體系和市場需求不同，在全球範圍内概括熱應激對養豬業的影響具有挑戰性。回顧熱應激對代表性地區養豬業的影響對于提供更有針對性和更深入的分析是有價值的，并且它創造了利用全球研究産生的知識交叉驗證和解釋熱應激影響的機會。本文以以亞熱帶氣候為主的澳洲為例，綜述了熱應激對養豬業的影響。本綜述總結的知識可以應用于全球養豬業由于全球變暖熱應激的影響明顯或熱應激正在出現的地區。
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.
澳洲的許多養豬戶都位于亞熱帶地區，那裡的季節之間溫度變化很大。高環境溫度是澳洲夏季最關鍵的特征之一。圖1顯示了1970年至2020年間集約化生豬生産區(澳洲新南威爾士州克洛瓦, 35.99°S, 146.48°E)的最高和最低溫度。11月至3月的平均最高氣溫高于生長豬(Huynh et al.，2005)和哺乳母豬(Quiniou and Noblet, 1999)的熱中性區上限。通常預計在這幾個月裡豬的生産性能會顯著下降。與其他受熱應激影響的地區一樣，在澳洲開展了多個研究項目，以了解和減輕熱應激對生豬生産的影響，這些研究項目得到了豬肉中心、澳洲豬肉有限公司、農業部、大學和其他行業合作夥伴的資助支援。在母豬中進行的研究部分使用了自然條件下的季節性比較設計，由于缺乏氣候可控的研究設施和所需的高樣本量，是以生理影響與夏季條件有關(包括但不限于高環境溫度)。同時，關于熱應激對生長豬的影響已經進行了大量的氣候控制實驗。目前綜述的範圍将集中在降低養豬業生産效率的三個主要影響上——(1)夏季配種母豬繁殖失敗增加，(2)夏季配種母豬的後代胴體脂肪增加，(3)夏季育肥豬生長速度減慢(圖2)。本文根據最近的全球證據讨論了每種影響，估計了與這些影響相關的經濟損失，并總結了已評估的解決方案。目前的綜述旨在就熱應激對養豬業的主要影響提供最新的研究總結，并确定未來研究的知識空白，以提高在這些具有挑戰性和不斷變化的氣候條件下豬肉生産的效率。
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.
圖1：澳洲主要生豬産區的曆史溫度記錄(1970-2020年)(平均值±标準差)。橫軸為月份，縱軸為溫度，上面的帶箭頭虛線為生長/育肥豬的熱中性溫度上限，下面的帶箭頭虛線為哺乳母豬的熱中性溫度上限。資料來自澳洲新南威爾士州克洛瓦機場氣象站(35.99°S, 146.48°E;ID:074034，澳洲氣象局)。熱中性區的上限（橙色曲線）定義為豬開始減少總産熱時的環境溫度(生長豬約為23°C (Huynh et al.， 2005)，哺乳母豬約為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)).
圖2：夏季氣候條件對生豬生産的三個主要影響。首先，夏季配種母豬的分娩率低，增加了非生産天數，需要配種更多的母豬來維持育肥豬的市場供應，這提高了豬群的料重比。第二，對于夏季配種後成功分娩的母豬，由于妊娠熱應激對胎兒發育的影響，後代出生體重較輕(≤1.1 kg)的比例較大。出生體重輕的仔豬比例的增加會導緻仔豬群生長速度下降，成活率降低，胴體脂肪升高。第三，高溫條件下生豬生長速度的減慢降低了胴體重，進而限制了養豬生産者的收入。
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.
影響1：夏季配種母豬的分娩率偏低Impact 1: Reduced farrowing rate of sows mated in summer 夏季配種母豬分娩率偏低的證據Evidence for reduced farrowing rate of sows mated in summer 夏季配種的母豬分娩率降低仍然是包括澳洲在内的全球養豬業面臨的一個主要問題。在澳洲，用于終端商品豬生産的常見母系品種是大白母豬和長白母豬，父系品種是杜洛克公豬(第一産業部，2016年)。澳洲兩家主要養豬場的最新生産資料(2010-2018年)顯示，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)。最近公布的澳洲夏季配種的商業化養殖的母豬的分娩率在64%至83%之間，低于較冷月份的89% (Liu et al., 2019; 2020; Plush et al., 2019)。高環境溫度加上日照長度的變化被認為會影響夏季的繁殖能力。一項2012年至2017年對澳洲一家大型豬場的分娩記錄的分析發現，如果在配種前35天出現高環境溫度(>29°C)，會導緻分娩率的最大下降(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). 母豬的分娩成績取決于一系列因素。卵泡的形成導緻發情和随後的排卵。當活性卵母細胞與優質精子受精時，就會發生受孕。母體對懷孕的認知觸發了内分泌的變化和子宮的準備，以促進胚胎着床(Spencer and Bazer, 2004)。黃體分泌的黃體酮在維持妊娠中起着重要作用。夏季繁殖障礙主要表現為母豬配種後不規律返情的比例增加，是以需要增加配種次數以確定有效的妊娠。來自澳洲的資料顯示，窩均總仔數和窩均活産仔數在不同季節保持不變(Lewis和Bunter, 2011年)。在過去的40年裡，提高對夏季繁殖障礙背後的生理機制的了解和制定幹預政策一直是一個關鍵的研究重點(King, 2017)。在過去的5年裡，夏季繁殖障礙研究的共識是，夏季配種母豬分娩率的降低主要是由于早期妊娠失敗，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. 夏季配種時發情至排卵間隔的改變Altered oestrus-to-ovulation interval during summer mating 養豬生産者通常根據行為發情的檢測來安排人工授精(AI)，是以了解準确的發情至排卵間隔(OOI)對于安排人工授精時機以實作最佳受孕至關重要。在熱應激環境下對發情至排卵間隔有互相沖突的發現。一項氣候控制研究發現，哺乳期熱應激(31°C, 8:00-16:00；26°C 16:00-8.00)将卵泡大小從6.7毫米減少到5.8毫米，并将發情至排卵間隔從1天延長到2.5天(Cabezón et al.，2017)。而另一項研究發現了相反的結果，夏季斷奶母豬的發情至排卵間隔比冬季斷奶母豬短10小時(21.8小時比31.4小時)(van Wettere, 2013)。同樣，在夏季哺乳和配種的母豬(2019年12月- 2020年3月；25.4±5.01℃平均值±标準偏差；澳洲)其平均發情至排卵間隔為1.1天(Liu et al.， 2021a)。研究結果之間的沖突可能是由于不同的環境條件或基因型導緻的。值得注意的是，即使在夏季發情至排卵間隔的變化很明顯，當使用兩次人工授精配種時(即：斷奶後首次檢測到發情行為時進行第一次人工授精，24小時候進行第二次)，受孕的時機和成功也不太可能受到不合時宜的配種或授精的影響。在發情開始時就配種仍然是夏季發情至排卵間隔為1.1天的斷奶母豬的最佳配種時機，因為在排卵前0-24小時進行授精可以獲得最佳的母豬受胎率(Kemp和Soede, 1996)。有意思是，平均發情至排卵間隔為1.1天的母豬在夏季接受兩次人工授精後，它們的分娩率依舊偏低(65%)(Liu et al.， 2021a)。是以，妊娠早期(第35天之前)的因素，包括母體對妊娠的識别、胚胎存活、子宮環境、精子和卵母細胞品質，可能是分娩率較低的原因，我們将在下一節讨論。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.
未完待續……To be continued…
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