Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (17): 3450-3460.doi: 10.3864/j.issn.0578-1752.2022.17.015

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles     Next Articles

Effects of Heat Stress on Ileal Microbiota of Broilers

WANG XueJie(),XING Shuang(),ZHAO ShaoMeng,ZHOU Ying,LI XiuMei,LIU QingXiu,MA DanDan,ZHANG MinHong,FENG JingHai()   

  1. Institute of Animal Sciences, Chinese Academy of Agricultural Sciences/State Key Laboratory of Animal Nutrition, Beijing 100193
  • Received:2021-07-25 Accepted:2022-07-13 Online:2022-09-01 Published:2022-09-07
  • Contact: JingHai FENG E-mail:927683542@qq.com;1194325185@qq.com;fengjinghai@caas.cn

Abstract:

【Objective】 To explore how heat stress influences the composition and structure of intestinal microbiota in broilers, and to provide a basis for alleviating the adverse effects of heat stress. 【Method】 144 broilers ((1 771±40) g, 35 d) were randomly divided into three groups with six replicates and raised in three controlled climate chambers from 35 to 42 days in this study. They were allocated to one of a thermoneutral control group (TC, 21℃, ad libitum), a heat stress group (HT, 31℃, ad libitum), or a pair-feeding group(PF, 21℃, pair-feeding as much as the consumption of the HT birds). 【Result】 Compared with broilers in TC, the feed intake and body weight gain were significantly decreased and F/G was increased in broilers of HT (P<0.01), the feed intake and body weight gain were also significantly decreased in broilers of PF (P<0.01). The feed intake of broilers in HT was as same as it in PF, but the body weight gain in HT was lower than it in PF, and the F/G was higher (P<0.05), which indicated that the heat stress still decreased the body weight gain of broilers even at the same level of feed intake. Compared with broilers in TC, the core temperature (P=0.079) and serum corticosterone content (P=0.071) have an increasing tendency in broilers of HT, and have similar levels in PF (P>0.05). The richness of species(sobs and Chao1)and diversity indices(Shannon)of samples in the HT and PF group were higher than those in the TC group (P<0.05). There was no significant difference in terms of the diversity estimators of the ileal microbiota between the HT and the PF groups. The PCoA showed that the HT and PF groups were gathered together but were distinctly separated from the TC group. This tendency was also verified by the similarity analysis. Moreover, the feed consumption was significantly correlated with the principal coordinate 1 in the PCoA (R = 0.786, P<0.001), but the body temperature or the serum corticosterone was not correlated with the principal coordinate 1 (P>0.05). Furthermore, 18 differential genera between the HTG and the TC groups were identified by LEfSe analysis (score ≥ 3). The relative abundance of these genera in the PF and HT groups was similar but had significant differences compared with that in the TC group. In addition, among the 50 most abundant genera in the ileal microbiota, the feed consumption was significantly correlated with 30 genera, but the body temperature and serum corticosterone were significantly correlated with only two and no genera, respectively. 【Conclusion】 The core temperature and serum corticosterone content were different, the feed intake was similar between HT and PF, and the composition and community structure of ileal microbiota were similar between those two groups; the core temperature and serum corticosterone content were similar, but the feed intake was different between TC and PF, and the composition and community structure of ileal microbiota were also different between those two groups, these results indicate that the effects of constant heat stress on composition and community structure of ileal microbiota in broilers are related to reduced feed consumption. This conclusion was also proved by the results of correlation analysis.

Key words: heat stress, broilers, ileum, microbiota, feed consumption

Table 1

Composition and nutrient levels of the basal diet (as-fed basis)"

原料组成Ingredients 含量 Content (%) 营养水平Nutrient levels 2)
玉米Corn 56.51 代谢能ME (MJ/kg) 12.73
豆粕Soybean meal 35.52 粗蛋白CP(%) 20.07
石粉Limestone 1.00 钙Ca(%) 0.90
磷酸氢钙CaHPO4 1.78 有效磷AP(%) 0.40
豆油Soybean oil 4.50 赖氨酸Lys(%) 1.00
蛋氨酸DL-Met 0.11 蛋氨酸Met(%) 0.42
食盐NaCl 0.30 蛋+胱氨酸Met+Cys 0.78
预混料Premix 1) 0.28
合计Total 100.00

Table 2

Effects of heat stress on growth performance of broilers (n=6)"

Group ADFI (g) ADG (g) F/G
TC 208.38±6.02a 110.07±6.11a 1.90±0.06a
HT 132.45±26.08b 38.78±6.68b 3.41±0.24b
PF 143.30±22.91b 69.49±5.95c 2.07±0.35a

Fig. 1

The effects of high temperature on the core temperature (A) and serum corticosterone (B) of broilers * 0.05<P<0.1, ** P<0.05, n=6"

Fig. 2

The effects of heat stress on the alpha diversity of ileal microflora in broilers (A) The species richness index. (B) The evenness index. (C) The diversity estimators. * 0.05<P<0.1, ** P<0.05 by Mann-Whitney test; n=6"

Fig. 3

The effects of heat stress on beta diversity of ileal microflora in broilers A: The principal coordinate analysis (PCoA) of the community membership based on the unweighted UniFrac distance metric matrices. B: The analysis of similarity (ANOSIM) of the community membership based on the unweighted UniFrac distance metric matrices. C-E: The spearman’s coefficient analysis between the core temperature, serum corticosterone, or feed intake with principal coordinate 1 in PCoA. Each spot represented the average values of birds in each replicate, n=18"

Fig. 4

The effects of heat stress on the relative abundance of dominant bacteria in ileum of broilers A: The phylum level; B: The order level; C: The genus level"

Fig. 5

The effects of heat stress on the composition of ileal microbiome in broilers."

[1] LARA L J, ROSTAGNO M H. Impact of heat stress on poultry production. Animals: An Open Access Journal from MDPI, 2013, 3(2): 356-369. doi: 10.3390/ani3020356.
doi: 10.3390/ani3020356
[2] SUGIHARTO S, YUDIARTI T, ISROLI I, WIDIASTUTI E, KUSUMANTI E. Dietary supplementation of probiotics in poultry exposed to heat stress-A review. Annals of Animal Science, 2017, 17(3): 591-604. doi: 10.1515/aoas-2016-0062.
doi: 10.1515/aoas-2016-0062
[3] NAWAB A, IBTISHAM F, LI G H, KIESER B, WU J, LIU W C, ZHAO Y, NAWAB Y, LI K Q, XIAO M, AN L L. Heat stress in poultry production: Mitigation strategies to overcome the future challenges facing the global poultry industry. Journal of Thermal Biology, 2018, 78: 131-139. doi: 10.1016/j.jtherbio.2018.08.010.
doi: 10.1016/j.jtherbio.2018.08.010
[4] FARAG M R, ALAGAWANY M. Physiological alterations of poultry to the high environmental temperature. Journal of Thermal Biology, 2018, 76: 101-106. doi: 10.1016/j.jtherbio.2018.07.012.
doi: 10.1016/j.jtherbio.2018.07.012
[5] WAITE D W, TAYLOR M W. Characterizing the avian gut microbiota: membership, driving influences, and potential function. Frontiers in Microbiology, 2014, 5: 223. doi: 10.3389/fmicb.2014.00223.
doi: 10.3389/fmicb.2014.00223
[6] WAITE D W, TAYLOR M W. Exploring the avian gut microbiota: current trends and future directions. Frontiers in Microbiology, 2015, 6: 673. doi: 10.3389/fmicb.2015.00673.
doi: 10.3389/fmicb.2015.00673
[7] BARKO P C, MCMICHAEL M A, SWANSON K S, WILLIAMS D A. The gastrointestinal microbiome: A review. Journal of Veterinary Internal Medicine, 2018, 32(1): 9-25. doi: 10.1111/jvim.14875.
doi: 10.1111/jvim.14875
[8] STOKES C R. The development and role of microbial-host interactions in gut mucosal immune development. Journal of Animal Science and Biotechnology, 2017, 8: 12. doi: 10.1186/s40104-016-0138-0.
doi: 10.1186/s40104-016-0138-0
[9] YADAV S, JHA R. Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of Animal Science and Biotechnology, 2019, 10: 2. doi: 10.1186/s40104-018-0310-9.
doi: 10.1186/s40104-018-0310-9
[10] SUZUKI K, HARASAWA R, YOSHITAKE Y, MITSUOKA T. Effects of crowding and heat stress on intestinal flora, body weight gain, and feed efficiency of growing rats and chicks. Nihon Juigaku Zasshi the Japanese Journal of Veterinary Science, 1983, 45(3): 331-338. doi: 10.1292/jvms1939.45.331.
doi: 10.1292/jvms1939.45.331
[11] SONG J, XIAO K, KE Y L, JIAO L F, HU C H, DIAO Q Y, SHI B, ZOU X T. Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress. Poultry Science, 2014, 93(3): 581-588. doi: 10.3382/ps.2013-03455.
doi: 10.3382/ps.2013-03455
[12] BURKHOLDER K M, THOMPSON K L, EINSTEIN M E, APPLEGATE T J, PATTERSON J A. Influence of stressors on normal intestinal microbiota, intestinal morphology, and susceptibility to Salmonella enteritidis colonization in broilers. Poultry Science, 2008, 87(9): 1734-1741. doi: 10.3382/ps.2008-00107.
doi: 10.3382/ps.2008-00107
[13] 彭骞骞, 王雪敏, 张敏红, 冯京海, 甄龙, 张少帅. 持续偏热环境对肉鸡盲肠菌群多样性的影响. 中国农业科学, 2016, 49(1): 186-194.
PENG Q Q, WANG X M, ZHANG M H, FENG J H, ZHEN L, ZHANG S S. Effects of constant moderate temperatures on the diversity of the intestinal microbial flora of broilers. Scientia Agricultura Sinica, 2016, 49(1): 186-194. (in Chinese)
[14] 常双双, 李萌, 厉秀梅, 石玉祥, 张敏红, 冯京海. 日循环变化偏热环境对肉鸡血清脑肠肽和盲肠菌群多样性的影响. 中国农业科学, 2018, 51(22): 4364-4372. doi: 10.3864/j.issn.0578-1752.2018.22.014.
doi: 10.3864/j.issn.0578-1752.2018.22.014
CHANG S S, LI M, LI X M, SHI Y X, ZHANG M H, FENG J H. Effects of the daily cycle variation of the moderate ambient temperatures on the serum brain gut peptide and the diversity of caecal microflora in broilers. Scientia Agricultura Sinica, 2018, 51(22): 4364-4372. doi: 10.3864/j.issn.0578-1752.2018.22.014. (in Chinese)
doi: 10.3864/j.issn.0578-1752.2018.22.014
[15] WANG X J, FENG J H, ZHANG M H, LI X M, MA D D, CHANG S S. Effects of high ambient temperature on the community structure and composition of ileal microbiome of broilers. Poultry Science, 2018, 97(6): 2153-2158. doi: 10.3382/ps/pey032.
doi: 10.3382/ps/pey032
[16] SHI D Y, BAI L, QU Q, ZHOU S S, YANG M M, GUO S N, LI Q H, LIU C. Impact of gut microbiota structure in heat-stressed broilers. Poultry Science, 2019, 98(6): 2405-2413. doi: 10.3382/ps/pez026.
doi: 10.3382/ps/pez026
[17] LIU G H, ZHU H B, MA T H, YAN Z Y, ZHANG Y Y, GENG Y Y, ZHU Y, SHI Y X. Effect of chronic cyclic heat stress on the intestinal morphology, oxidative status and cecal bacterial communities in broilers. Journal of Thermal Biology, 2020, 91: 102619. doi: 10.1016/j.jtherbio.2020.102619.
doi: 10.1016/j.jtherbio.2020.102619
[18] WANG G J, LI X M, ZHOU Y, FENG J H, ZHANG M H. Effects of heat stress on gut-microbial metabolites, gastrointestinal peptides, glycolipid metabolism, and performance of broilers. Animals: An Open Access Journal from MDPI, 2021, 11(5): 1286. doi: 10.3390/ani11051286.
doi: 10.3390/ani11051286
[19] ROSTAGNO M H. Effects of heat stress on the gut health of poultry. Journal of Animal Science, 2020, 98(4): skaa090. doi: 10.1093/jas/skaa090.
doi: 10.1093/jas/skaa090
[20] HE J, HE Y X, PAN D D, CAO J X, SUN Y Y, ZENG X Q. Associations of gut microbiota with heat stress-induced changes of growth, fat deposition, intestinal morphology, and antioxidant capacity in ducks. Frontiers in Microbiology, 2019, 10: 903. doi: 10.3389/fmicb.2019.00903.
doi: 10.3389/fmicb.2019.00903
[21] SOHAIL M U, HUME M E, BYRD J A, NISBET D J, IJAZ A, SOHAIL A, SHABBIR M Z, REHMAN H. Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress. Poultry Science, 2012, 91(9): 2235-2240. doi: 10.3382/ps.2012-02182.
doi: 10.3382/ps.2012-02182
[22] SEIFI K, REZAEI M, YANSARI A T, RIAZI G H, ZAMIRI M J, HEIDARI R. Saturated fatty acids may ameliorate environmental heat stress in broiler birds by affecting mitochondrial energetics and related genes. Journal of Thermal Biology, 2018, 78: 1-9. doi: 10.1016/j.jtherbio.2018.08.018.
doi: 10.1016/j.jtherbio.2018.08.018
[23] CHENG Y F, CHEN Y P, CHEN R, SU Y, ZHANG R Q, HE Q F, WANG K, WEN C, ZHOU Y M. Dietary mannan oligosaccharide ameliorates cyclic heat stress-induced damages on intestinal oxidative status and barrier integrity of broilers. Poultry Science, 2019, 98(10): 4767-4776. doi: 10.3382/ps/pez192.
doi: 10.3382/ps/pez192
[24] CHANG Y, WANG X J, FENG J H, ZHANG M H, DIAO H J, ZHANG S S, PENG Q Q, ZHOU Y, LI M, LI X. Real-time variations in body temperature of laying hens with increasing ambient temperature at different relative humidity levels. Poultry Science, 2018, 97(9): 3119-3125. doi: 10.3382/ps/pey184.
doi: 10.3382/ps/pey184
[25] DALE N M, FULLER H L. Effect of diet composition on feed intake and growth of chicks under heat stress: II. constant vs. cycling temperatures. Poultry Science, 1980, 59(7): 1434-1441. doi: 10.3382/ps.0591434.
doi: 10.3382/ps.0591434
[26] ALHENAKY A, ABDELQADER A, ABUAJAMIEH M, AL- FATAFTAH A R. The effect of heat stress on intestinal integrity and Salmonella invasion in broiler birds. Journal of Thermal Biology, 2017, 70: 9-14. doi: 10.1016/j.jtherbio.2017.10.015.
doi: 10.1016/j.jtherbio.2017.10.015
[27] SONG Z H, CHENG K, ZHANG L L, WANG T. Dietary supplementation of enzymatically treated Artemisia annua could alleviate the intestinal inflammatory response in heat-stressed broilers. Journal of Thermal Biology, 2017, 69: 184-190. doi: 10.1016/j.jtherbio.2017.07.015.
doi: 10.1016/j.jtherbio.2017.07.015
[28] UERLINGS J, SONG Z G, HU X Y, WANG S K, LIN H, BUYSE J, EVERAERT N. Heat exposure affects jejunal tight junction remodeling independently of adenosine monophosphate-activated protein kinase in 9-day-old broiler chicks. Poultry Science, 2018, 97(10): 3681-3690. doi: 10.3382/ps/pey229.
doi: 10.3382/ps/pey229
[29] CHOI J H, KIM G B, CHA C J. Spatial heterogeneity and stability of bacterial community in the gastrointestinal tracts of broiler chickens. Poultry Science, 2014, 93(8): 1942-1950. doi: 10.3382/ps.2014-03974.
doi: 10.3382/ps.2014-03974
[30] XIAO Y P, XIANG Y, ZHOU W D, CHEN J G, LI K F, YANG H. Microbial community mapping in intestinal tract of broiler chicken. Poultry Science, 2017, 96(5): 1387-1393. doi: 10.3382/ps/pew372.
doi: 10.3382/ps/pew372
[31] HEENEY D D, GAREAU M G, MARCO M L. Intestinal Lactobacillus in health and disease, a driver or just along for the ride? Current Opinion in Biotechnology, 2018, 49: 140-147. doi: 10.1016/j.copbio.2017.08.004.
doi: 10.1016/j.copbio.2017.08.004
[32] WANG T W, TENG K L, LIU Y Y, SHI W X, ZHANG J, DONG E Q, ZHANG X, TAO Y, ZHONG J. Lactobacillus plantarum PFM 105 promotes intestinal development through modulation of gut microbiota in weaning piglets. Frontiers in Microbiology, 2019, 10: 90. doi: 10.3389/fmicb.2019.00090.
doi: 10.3389/fmicb.2019.00090
[33] ZHANG W, WU Q, ZHU Y H, YANG G Y, YU J, WANG J F, JI H F. Probiotic Lactobacillus rhamnosus GG induces alterations in ileal microbiota with associated CD3 - CD19 - T-bet + IFNγ +/- cell subset homeostasis in pigs challenged with Salmonella enterica serovar 4, [5], 12: i:. Frontiers in Microbiology, 2019, 10: 977. doi: 10.3389/fmicb.2019.00977.
doi: 10.3389/fmicb.2019.00977
[34] SONOYAMA K, FUJIWARA R, TAKEMURA N, OGASAWARA T, WATANABE J, ITO H, MORITA T. Response of gut microbiota to fasting and hibernation in Syrian hamsters. Applied and Environmental Microbiology, 2009, 75(20): 6451-6456. doi: 10.1128/AEM.00692-09.
doi: 10.1128/AEM.00692-09
[35] COSTELLO E K, GORDON J I, SECOR S M, KNIGHT R. Postprandial remodeling of the gut microbiota in Burmese pythons. The ISME Journal, 2010, 4(11): 1375-1385. doi: 10.1038/ismej.2010.71.
doi: 10.1038/ismej.2010.71
[36] SANDHU K V, SHERWIN E, SCHELLEKENS H, STANTON C, DINAN T G, CRYAN J F. Feeding the microbiota-gut-brain axis: diet, microbiome, and neuropsychiatry. Translational Research, 2017, 179: 223-244. doi: 10.1016/j.trsl.2016.10.002.
doi: 10.1016/j.trsl.2016.10.002
[37] GUEVARRA R B, LEE J H, LEE S H, SEOK M J, KIM D W, KANG B N, JOHNSON T J, ISAACSON R E, KIM H B. Piglet gut microbial shifts early in life: Causes and effects. Journal of Animal Science and Biotechnology, 2019, 10: 1. doi: 10.1186/s40104-018-0308-3.
doi: 10.1186/s40104-018-0308-3
[38] OSMAN A M, TANIOS N I. The effect of heat on the intestinal and pancreatic levels of amylase and maltase of laying hens and broilers. Comparative Biochemistry and Physiology Part A: Physiology, 1983, 75(4): 563-567. doi: 10.1016/0300-9629(83)90421-8.
doi: 10.1016/0300-9629(83)90421-8
[39] ROUTMAN K S, YOSHIDA L, FRIZZAS DE LIMA A C, MACARI M, PIZAURO J M Jr. Intestinal and pancreas enzyme activity of broilers exposed to thermal stress. Revista Brasileira De Ciência Avícola, 2003, 5(1): 23-27. doi: 10.1590/s1516-635x2003000100003.
doi: 10.1590/s1516-635x2003000100003
[40] PETROSUS E, SILVA E B, LAY D, EICHER S D. Effects of orally administered cortisol and norepinephrine on weanling piglet gut microbial populations and Salmonella passage1. Journal of Animal Science, 2018, 96(11): 4543-4551. doi: 10.1093/jas/sky312.
doi: 10.1093/jas/sky312
[41] AATSINKI A K, KESKITALO A, LAITINEN V, MUNUKKA E, UUSITUPA H M, LAHTI L, KORTESLUOMA S, MUSTONEN P, RODRIGUES A J, COIMBRA B, HUOVINEN P, KARLSSON H, KARLSSON L. Maternal prenatal psychological distress and hair cortisol levels associate with infant fecal microbiota composition at 2.5 months of age. Psychoneuroendocrinology, 2020, 119: 104754. doi: 10.1016/j.psyneuen.2020.104754.
doi: 10.1016/j.psyneuen.2020.104754
[42] AMINI-KHOEI H, HAGHANI-SAMANI E, BEIGI M, SOLTANI A, MOBINI G R, BALALI-DEHKORDI S, HAJ-MIRZAIAN A, RAFIEIAN-KOPAEI M, ALIZADEH A, HOJJATI M R, VALIDI M. On the role of corticosterone in behavioral disorders, microbiota composition alteration and neuroimmune response in adult male mice subjected to maternal separation stress. International Immunopharmacology, 2019, 66: 242-250. doi: 10.1016/j.intimp.2018.11.037.
doi: 10.1016/j.intimp.2018.11.037
[1] SUI XinYi,ZHAO XiaoGang,CHEN PengYu,LI YaLing,WEN XiangZhen. Cloning of Alternative Splice Variants of LsPHYB in Lettuce and Its Expression Patterns Under Heat Stress [J]. Scientia Agricultura Sinica, 2022, 55(9): 1822-1830.
[2] KONG FanLin,LI Yuan,FU Tong,DIAO QiYu,TU Yan. Effects of 2-Hydroxy-4-(Methylthio)-Butanoic Acid on Rumen Fermentation and Microbiota in Holstein Female Calves [J]. Scientia Agricultura Sinica, 2022, 55(4): 796-806.
[3] REN Yifang,YANG ZhangPing,LING Fenghua,XIAO LiangWen. Risk Zoning of Heat Stress Risk Zoning of Dairy Cows in Jiangsu Province and Its Characteristics Affected by Climate Change [J]. Scientia Agricultura Sinica, 2022, 55(22): 4513-4525.
[4] LIU RuiYao,HUANG GuoHong,LI HaiYan,LIANG MinMin,LU MingHui. Screening and Functional Analysis in Heat-Tolerance of the Upstream Transcription Factors of Pepper CaHsfA2 [J]. Scientia Agricultura Sinica, 2022, 55(16): 3200-3209.
[5] YuYan YANG,YaoWen LI,Shuang XING,MinHong ZHANG,JingHai FENG. The Temperature-Humidity Index Estimated by the Changes of Surface Temperature of Broilers at Different Ages [J]. Scientia Agricultura Sinica, 2021, 54(6): 1270-1279.
[6] YANG NingZhi,LI Ting,WANG Yan,CHEN Zhuo,MA YiCheng,REN QiangLin,LIU JiaJia,YANG HuiGuo,YAO Gang. Comparison of Growth Physiology and Gut Microbiota Between Healthy and Diarrheic Lambs in Pre- and Post-Weaning Period [J]. Scientia Agricultura Sinica, 2021, 54(2): 422-434.
[7] Min LIU,Yulin FANG. Effects of Heat Stress on Physiological Indexes and Ultrastructure of Grapevines [J]. Scientia Agricultura Sinica, 2020, 53(7): 1444-1458.
[8] ZHANG AiJing,LI LinQiong,WANG PengJie,GAO YuLong. Effects of Heat Stress on Cell Membrane and Membrane Protein of Escherichia coli [J]. Scientia Agricultura Sinica, 2020, 53(5): 1046-1057.
[9] YUAN XiongKun,JIANG LiLi,TAO ShiYu,ZANG JianJun,WANG JunJun. Research Progresses on Sensitive Index System of Heat Stress in Sows [J]. Scientia Agricultura Sinica, 2020, 53(22): 4691-4699.
[10] Shuang XING,JingHai FENG. Effects of Lactobacillus Supplements on Growth Performance of Broilers: A Meta-Analysis [J]. Scientia Agricultura Sinica, 2020, 53(1): 183-190.
[11] YANG YuYan,WANG XueJie,ZHANG MinHong,FENG JingHai. The Upper Limit Temperature of Thermoneutral Zone Estimated by the Changes of Temperature and Respiration Rate of the Broilers [J]. Scientia Agricultura Sinica, 2019, 52(3): 550-557.
[12] HU LiRong, KANG Ling, WANG ShuHui, LI Wei, YAN XinYi, LUO HanPeng, DONG GangHui, WANG XinYu, WANG YaChun, XU Qing. Effects of Cold and Heat Stress on Milk Production Traits and Blood Biochemical Parameters of Holstein Cows in Beijing Area [J]. Scientia Agricultura Sinica, 2018, 51(19): 3791-3799.
[13] HAN JiaLiang, LIU JianXin, LIU HongYun. Effect of Heat Stress on Lactation Performance in Dairy Cows [J]. Scientia Agricultura Sinica, 2018, 51(16): 3162-3170.
[14] FAN XiaoRui, ZHANG Zhen, XI HuaMing, LIANG YaJun, HE JunPing. Effect of Heat Stress on the Expression of Cyt-C and Caspase-3 in Boar Testis [J]. Scientia Agricultura Sinica, 2017, 50(5): 924-931.
[15] YANG Huan, SHEN Xin, LU DaLei, LU WeiPing. Effects of Heat Stress Durations at Grain Formation Stage on Grain Yield and Starch Quality of Waxy Maize [J]. Scientia Agricultura Sinica, 2017, 50(11): 2071-2082.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!