Impact of heat stress on growth rate， serum antioxidant properties， and rumen flora in weaned lambs

doi:10.11686/cyxb2022249

Abstract

Abstract:

Heat stress （HS） has affected the efficiency and development of the sheep industry. This study investigated the growth performance， serum antioxidant properties， and rumen microbiota in weaned lambs under HS conditions using an environmental control chamber. Twelve weaned lambs were randomly allocated into two groups and raised in two chambers with one lamb per pen. The chamber of the control group was maintained at 21.5 ℃ and 60% humidity， while the HS chamber was maintained at 33.5 ℃ and 60% humidity. The entire experiment lasted for 14 days， and the growth rate， serum antioxidant enzyme activities， heat stress proteins （HSP）， and rumen flora diversity were measured at the end of the experiment. It was found that： 1） Under HS conditions， the daily feed intake and daily weight gain of lambs decreased （P<0.05） by 28.38% and 41.12%， respectively， compared with those in control group， while the feed/gain （F/G） increased by 33.13%. 2） The serum antioxidant properties of lambs decreased under HS conditions. The total antioxidant capacity， catalase， or superoxide dismutase （SOD） activity decreased （ P<0.05） under HS， while the levels of malondialdehyde increased （P≤0.05）. Moreover， compared with the control group， the serum HSP content in the HS group increased （P<0.05） by 1.19 times for HSP60， 1.47 times for HSP70， and 1.39 times for HSP90. 3） The diversity and abundance of rumen flora were affected by the HS conditions； The Shannon index and Simpson index both decreased （P<0.05）， while the relative abundance of Bacteroidetes or Proteobacteria increased （P<0.05）. In particular， Bacteroidetes abundance increased by 76.47% compared with the control group. However， the abundance of Actinobacteria or Firmicutes decreased （P<0.05）. In addition， under HS， the abundance of Prevotella_1 in the rumen increased by 326.28% （P<0.05）， and the abundance of Selemonas_1 decreased by 84.21% （P<0.05）， compared with the control. In summary， HS affected growth rate， serum antioxidant properties， and rumen microbe community structure of the lambs. The results from this study provide data to help understand and relieve sheep affected by HS in commercial production.

Key words: lamb, heat stress, growth performance, antioxidant performance, flora

Ai-yu LIU, Chao WANG, Zhan-jun WU, Shou-pei ZHAO, Li-chen ZHAO, Xiao-yu LI, Wei-tao ZHANG, Le-tian WANG, Yu-hong GAO. Impact of heat stress on growth rate， serum antioxidant properties， and rumen flora in weaned lambs[J]. Acta Prataculturae Sinica, 2023, 32(4): 173-182.

Figures/Tables 7

References 44

1	Yerou H， Belgherbi B， Homrani A. Impact of heat stress on holstein breeding performance conducted in a semiarid Mediterranea climate. Genetics and Biodiversity Journal， 2021， 5（2）： 116-126.
2	Zhong S. Temperature and humidity index （THI）-induced rumen bacterial community changes in goats. Xianyang： Northwest A&F University， 2019.
	钟书. 温湿度指数（THI）介导山羊瘤胃细菌群落的变化. 咸阳：西北农林科技大学， 2019.
3	He Z Y， Meng Z， Jiang A D， et al. Research progress on the effect of heat stress on mutton sheep production. Chinese Journal of Animal Science， 2022， 58（5）： 59-64.
	何志勇，孟祝，蒋澳迪，等. 热应激对肉羊生产的影响研究进展. 中国畜牧杂志， 2022， 58（5）： 59-64.
4	Zhang C. Comparative study on the effects of damp-heat stress on production performance， rumen fermentation and blood biochemical indexes of Tibetan sheep and goats. Chengdu： Sichuan Agricultural University， 2016.
	张灿. 湿热应激对藏绵羊和山羊生产性能、瘤胃发酵及血液生化指标影响的比较研究. 成都：四川农业大学， 2016.
5	Das R， Sailo L， Verma N， et al. Impact of heat stress on health and performance of dairy animals： A review. Veterinary World， 2016， 9（3）： 260-268.
6	Salama A A K， Caja G， Hamzaouis， et al. Different levels of response to heat stress in dairy goats. Small Ruminant Research， 2014， 121（1）： 73-79.
7	Zhang Y F， Qi Z L. Mechanism of oxidative stress in body under heat stress. Chinese Journal of Animal Nutrition， 2017， 29（9）： 3051-3058.
	张轶凤，齐智利. 热应激条件下机体发生氧化应激的机制. 动物营养学报， 2017， 29（9）： 3051-3058.
8	Rea K， Dinan T G， Cryan J F. The microbiome： A key regulator of stress and neuroinflammation. Neurobiol Stress， 2016， 4： 23-33.
9	Cholewinska P， Gorniak W， Wojnarowski K. Impact of selected environmental factors on microbiome of the digestive tract of ruminants. BMC Veterinary Research， 2021， 17： 25.
10	Aschenbach J R， Zebeli Q， Patra A K， et al. Symposium review： The importance of the ruminal epithelial barrier for a healthy and productive cow. Journal of Dairy Science， 2019， 102（2）： 1866-1882.
11	Chen S， Wang J， Peng D， et al. Exposure to heat-stress environment affects the physiology， circulation levels of cytokines， and microbiome in dairy cows. Journal of Archaeological Science-Reports， 2018， 8： 14606.
12	Wang J P， Wang J Q， Bu D P. Expression of heat shock protein in the blood of dairy cows in summer. Chinese Journal of Veterinary Medicine， 2014， 34（8）： 1289-1293.
	王建平，王加启，卜登攀. 夏季奶牛血液中热休克蛋白的表达量. 中国兽医学报， 2014， 34（8）： 1289-1293.
13	Mertz W. Chramium occurrence and function in biological systems. Physilogical Reviews， 1969， 2： 163-239.
14	Alhidary I A， Shini S， Al Jassim R A M， et al. Effects of selenium and vitamin E on performance， physiological response， and selenium balance in heat-stressed sheep. Journal of Animal Science， 2015， 93（2）： 576-588.
15	Aida. Harm of heat stress to sheep and prevention strategies. Modern Animal Husbandry Science and Technology， 2020（9）： 162-163.
	阿依达尔. 热应激对羊的危害及预防策略. 现代畜牧科技， 2020（9）： 162-163.
16	Peng X K， Zhao T， Huang X Y， et al. Effects of acute heat stress on blood biochemistry indices and expression of HSP70 family genes in blood lymphocytes in goats. Acta Veterinaria et Zootechnica Sinica， 2019， 50（6）： 1219-1229.
	彭孝坤，赵天，黄晓瑜，等. 急性热应激对山羊血液生化指标及血淋巴细胞热休克蛋白70家族基因表达的影响. 畜牧兽医学报， 2019， 50（6）： 1219-1229.
17	Xia D， Yang S J， Liu T Z. Seasonal variation of blood antioxidant enzymes in holstein cows. Journal of Domestic Animal Ecology， 2006， 27（1）： 56-59.
	夏东，杨淑晶，刘铁铮. 奶牛血液抗氧化酶活性的季节变化. 家畜生态学报， 2006， 27（1）： 56-59.
18	Ahmad H， Tian J， Wang J， et al. Effects of dietary sodium selenite and selenium yeast on antioxidant enzyme activities and oxidative stability of chicken breast meat. Journal of Agricultural and Food Chemistry， 2012， 60（29）： 7111-7120.
19	Sindhu R K， Ehdaie A， Farmand F， et al. Expression of catalase and glutathione peroxidase in renal insufficiency. Biochimica et Biophysica Acta， 2005， 1743（1/2）： 86-92.
20	Akyol O， Yanik M， Elyas H， et al. Association between Ala-9Val polymorphism of Mn-SOD gene and schizophrenia. Progress in Neuro-Psychopharmacology & Biological Psychiatry， 2005， 29（1）： 123-131.
21	Daren A， Adamczyk P， Bladzinski P， et al. Humor perception in schizophrenia appears to be related to disorganization syndrome. Comprehensive Psychiatry， 2020， 96： 152149.
22	Peng X K， Hu J H， Zhang E P. Effects of heat stress on physiological and biochemical indexes and expression levels of miRNA in peripheral blood of beef cattle， sheep and goats. Journal of Domestic Animal Ecology， 2018， 39（3）： 1-7.
	彭孝坤，胡建宏，张恩平. 热应激对肉牛和肉羊生理生化指标及外周血miRNA表达水平的影响. 家畜生态学报， 2018， 39（3）： 1-7.
23	Shi L L， Wang Z Q， Xu Y Q， et al. Effects of heat stress on serum immune and antioxidative indexes and relative expression of related genes in sheep. Chinese Journal of Animal Nutrition， 2020， 32（11）： 5275-5284.
	石璐璐，王哲奇，徐元庆，等. 热应激对绵羊血清免疫和抗氧化指标及相关基因相对表达量的影响. 动物营养学报， 2020， 32（11）： 5275-5284.
24	Li Q， Wan G， Peng C， et al. Effect of probiotic supplementation on growth performance，intestinal morphology， barrier integrity， and inflammatory response in broilers subjected to cyclic heat stress. Tropical Animal Science Journal， 2020， 91（1）： e13433.
25	Liu F， Yin J， Du M， et al. Heat-stress-induced damage to porcine small intestinal epithelium associated with downregulation of epithelial growth factor signaling. Journal of Animal Science， 2009， 87： 1941-1949.
26	Gao D Y， Lian W S， Kang T T， et al. Effect of high temperature environment on serum biochemical indexes and HSP70， HSP90 mRNA expression in jejunal tissue of Tongcheng pig. Chinese Journal of Animal Science， 2020， 56（10）： 112-116.
	高登营，连维思，康亭亭，等. 高温环境对通城猪血清生化指标及空肠组织HSP70与HSP90 mRNA表达的影响. 中国畜牧杂志， 2020， 56（10）： 112-116.
27	Porto M L， Givsiez P E N， Saraiva E P， et al. Glutamic acid improves body weight gain and intestinal morphology of broiler chickens submitted to heat stress. Brazilian Journal of Poultry Science， 2015， 17： 355-362.
28	Kpodo K R， Duttlinger A W， Radcliffe J S， et al. Time course determination of the effects of rapid and gradual cooling after acute hyperthermia on body temperature and intestinal integrity in pigs. Journal of Thermal Biology， 2020， 87： 102481.
29	Pearce S C， Mani V， Boddicker R L， et al. Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs. PLoS One， 2013， 8： e70215.
30	Pearce S C， Main V， Weber T E， et al. Heat stress and reduced plane of nutrition decreases intestinal integrity and function in pigs. Journal of Animal Science， 2013， 91： 5183-5193.
31	Salles M S V， Zanetti M A， Salles F A， et al. Changes in ruminal fermentation and mineral serum level in animals kept in high temperature environments. Revista Brasileira de Zootecnia， 2010， 39（4）： 883-890．
32	Du R， Jin H， Wang B H， et al. Dietary probiotics affect gastrointestinal microflora and metabolites and consequently improves meat quality in Sunit lambs. Food Science， 2020， 41（11）： 14-21.
33	Liu C， He Y Q， Xu N N， et al. Effect of compound probiotics on performance and ruminal microflora of dairy cows in mid- and late-lactation. Chinese Journal of Animal Science， 2020， 56（4）： 115-121.
	刘程，何韵秋，徐宁宁，等. 复合益生菌对泌乳中后期奶牛生产性能和瘤胃菌群的影响. 中国畜牧杂志， 2020， 56（4）： 115-121.
34	Pang K Y， Dai D W， Yang Y K， et al. Effects of different feeding methods on rumen fermentation parameters and microbial flora of yak. Chinese Journal of Animal Nutrition， 2022， 34（3）： 1667-1682.
	庞凯悦，戴东文，杨英魁，等. 不同饲养方式对牦牛瘤胃发酵参数及微生物菌群的影响. 动物营养学报， 2022， 34（3）： 1667-1682.
35	Li S G， Chen G J， Li X D， et al. Effects of hybrid paper mulberry silage on rumen microflora of Wuchuan white goat. China Feed， 2022（1）： 114-120.
	李世歌，陈光吉，李小冬，等. 杂交构树青贮对务川白山羊瘤胃微生物区系的影响. 中国饲料， 2022（1）： 114-120.
36	Kim S H， Ramos S C， Valencia R A， et al. Heat stress： Effects on rumen microbes and host physiology， and strategies to alleviate the negative impacts on lactating dairy cows. Frontiers in Microbiology， 2022， 13： 804562.
37	Zhen Y G， Chen X， Piao G H， et al. Effects of the combination of Aspergillus oryzae culture and yeast culture on the diversity of sheep rumen flora. Chinese Journal of Animal Science， 2018， 54（6）： 96-100.
	甄玉国，陈雪，朴光赫，等. 米曲霉培养物与酵母培养物组合对绵羊瘤胃菌群多样性的影响. 中国畜牧杂志， 2018， 54（6）： 96-100.
38	Luo H X， Yang Y， Xie X L. Analysis of gut microbial community in lambs with diarrhea and healthy lambs. Advances in Animal Medicine， 2017， 38（12）： 86-90.
	罗海霞，杨易，谢秀兰. 腹泻羔羊与健康羔羊肠道微生物群落分析. 动物医学进展， 2017， 38（12）： 86-90.
39	Mao S Y， Zhang M L， Liu J H， et al. Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle： Membership and potential function. Journal of Diary Science， 2015， 5： 16116.
40	Li H， Wang Y， Gao J， et al. Effects of heat stress on rumen microbiota and its relationship with performance of dairy cows. Chinese Journal of Animal Nutrition， 2019， 31（10）： 4458-4463.
	李晗，王宇，高景，等. 热应激对瘤胃微生物的影响及其与奶牛生产性能的关系. 动物营养学报， 2019， 31（10）： 4458-4463.
41	Tajima K， Nonaka I， Higuchi K， et al. Influence of high temperature and humidity on rumen bacterial diversity in Holstein heifers. Anaerobe， 2007， 13（2）： 57-64.
42	Xu P. Effects of supplementary feeding on growth performance， blood indexes and rumen flora of grazing calves. Hohhot： Inner Mongolia Agricultural University， 2021.
	徐萍. 补饲对放牧犊牛生长性能、血液指标及瘤胃菌群的影响. 呼和浩特：内蒙古农业大学， 2021.
43	Wu X Z， Gao Y X， Ou H L， et al. Isolation and characterization of Selenomonas ruminantium from the rumen of dairy cows. Progress in Veterinary Medicine， 2008（10）： 25-28.
	武心镇，高玉霞，欧海龙，等. 奶牛瘤胃中反刍兽月形单胞菌的分离鉴定. 动物医学进展， 2008（10）： 25-28.
44	Ma F T. Effects of honeysuckle extract on production performance， antioxidant properties and rumen microflora structure in heat-stressed dairy cows. Beijing： Chinese Academy of Agricultural Sciences， 2020.
	马峰涛. 金银花提取物对热应激奶牛生产性能、抗氧化性能和瘤胃微生物菌群结构的影响. 北京：中国农业科学院， 2020.

原料 Ingredient	含量Content （%）	养分Nutrient	含量Content
花生秧Peanut vine	18.50	代谢能 Metabolic energy^3）（MJ·kg^-1）	11.79
羊草Chinese wildrye	19.00	粗蛋白质CP （%）	14.35
玉米Corn	32.20	酸性洗涤纤维ADF （%）	20.14
豆粕Soybean meal	20.00	中性洗涤纤维NDF （%）	26.45
麸皮Bran	8.00	钙 Ca （%）	0.55
小苏打NaHCO₃	0.70	磷 P （%）	0.32
盐NaCl	0.80
多种维生素Multivitamin^1）	0.20
矿物质微量元素Mineral trace elements^2）	0.60
合计Total	100.00

原料 Ingredient	含量Content （%）	养分Nutrient	含量Content
花生秧Peanut vine	18.50	代谢能 Metabolic energy^3）（MJ·kg^-1）	11.79
羊草Chinese wildrye	19.00	粗蛋白质CP （%）	14.35
玉米Corn	32.20	酸性洗涤纤维ADF （%）	20.14
豆粕Soybean meal	20.00	中性洗涤纤维NDF （%）	26.45
麸皮Bran	8.00	钙 Ca （%）	0.55
小苏打NaHCO₃	0.70	磷 P （%）	0.32
盐NaCl	0.80
多种维生素Multivitamin^1）	0.20
矿物质微量元素Mineral trace elements^2）	0.60
合计Total	100.00

项目Item	热应激组Heat stress	对照组Control	P值P-value	标准误差SE
总抗氧化能力T-AOC （U·mL^-1）	9.800	11.100	0.001	0.253
超氧化物歧化酶SOD （U·mL^-1）	52.860	55.000	0.029	0.753
丙二醛MDA （nmol·mL^-1）	1.670	1.230	0.050	0.167
谷胱甘肽过氧化物酶GSH-Px （μmol·L^-1）	7.230	7.510	0.057	0.119
过氧化氢酶CAT （U·mL^-1）	6.850	12.320	0.000	0.581

项目Item	热应激组Heat stress	对照组Control	P值P-value	标准误差SE
总抗氧化能力T-AOC （U·mL^-1）	9.800	11.100	0.001	0.253
超氧化物歧化酶SOD （U·mL^-1）	52.860	55.000	0.029	0.753
丙二醛MDA （nmol·mL^-1）	1.670	1.230	0.050	0.167
谷胱甘肽过氧化物酶GSH-Px （μmol·L^-1）	7.230	7.510	0.057	0.119
过氧化氢酶CAT （U·mL^-1）	6.850	12.320	0.000	0.581

[1]	Qian-long YANG, Qian-qian WEI, De-hui ZHAO, Xiao-lan GUO, Tie-tao ZHANG, Xiao-xu WANG, Kun BAO, Kai-ying WANG. Effects of dietary rumen-protected cysteine on growth performance， nutrient apparent digestibility and serum biochemical indexes of sika deer during weight gain [J]. Acta Prataculturae Sinica, 2023, 32(2): 148-159.
[2]	Juan-juan ZHAO, Da-lu CHE, Wei-ting GUO, Wei-tao ZHANG, Lian-chao LIU, Li-chen ZHAO, Yu-hong GAO, Xin-sheng SUN, Xue-mei LI, Yuan WANG. Effect of a Chinese medicine formula on the performance and physiological and blood biochemical parameters of hybrid Small-Tail Han sheep under heat stress [J]. Acta Prataculturae Sinica, 2022, 31(5): 178-189.
[3]	Xun-gang WANG, Xiao-ling ZHANG, Tian-wei XU, Yuan-yue GENG, Lin-yong HU, Na ZHAO, Hong-jin LIU, Sheng-ping KANG, Shi-xiao XU. Effects of dietary protein levels on ruminal fungal community structure and function in Tibetan sheep [J]. Acta Prataculturae Sinica, 2022, 31(2): 182-191.
[4]	Ning ZHAO, Hui-ling MA, Ran ZHANG, Jin-qing ZHANG, Yi SHI. Regulatory effects of butanediol on the expression level of endogenous hormones and related genes in creeping bentgrass under heat stress [J]. Acta Prataculturae Sinica, 2022, 31(12): 118-132.
[5]	Yang FAN, Wei-biao QI, Chong-miao ZHU, Yu-yang YIN, Sheng-yong MAO. Effects of fermented soybean residues on growth performance， apparent nutrient digestibility， meat quality and serum biochemical indexes of Hu sheep [J]. Acta Prataculturae Sinica, 2022, 31(11): 86-93.
[6]	Yu-jie FAN, Hua-zhe SI, Xiao-xu WANG, Qian-long YANG, Xin-yu ZHANG, Wei ZHONG, Kai-ying WANG. Effects of arginine level on rumen flora population structure and fermentation in weaning sika deer [J]. Acta Prataculturae Sinica, 2022, 31(10): 154-166.
[7]	Jun-hong HUO, Kang ZHAN, Qiu-sheng HUANG, Xiao-jun ZHONG, Jin-shun ZHAN, Xue-bing YAN. Effects of different concentration∶roughage ratios on growth performance， serum biochemical indices and ruminal fermentation of Nubian goats [J]. Acta Prataculturae Sinica, 2021, 30(6): 151-161.
[8]	Jing-ting LAN, Rui REN, Rui ZHOU, Hong-wei DAI, Wen-xiu SHU, Kai ZHU, Lue-yu WANG, Hong-wei XU, Rong-xin ZANG. Effects of feeding fermented cauliflower residue on growth performance， serum biochemical indices， intestinal tissue morphology and economic returns of nursery pigs [J]. Acta Prataculturae Sinica, 2021, 30(6): 180-189.
[9]	Xiao-jun SUO, Nian ZHANG, Qian-ping YANG, Hu TAO, Qi XIONG, Xiao-feng LI, Feng ZHANG, Ming-xin CHEN. Effects of peanut vine and alfalfa meal on weight gain performance， internal organ development， and blood indexes of Boer×Macheng crossbred goats [J]. Acta Prataculturae Sinica, 2021, 30(5): 146-154.
[10]	Sheng-jing SHI, Jun GAO, Chun-xia WANG, Zhen JIANG, Xue-lin CHEN. Analysis of the floristic diversity of vascular plants in Duoer National Nature Reserve， Gansu [J]. Acta Prataculturae Sinica, 2021, 30(4): 140-149.
[11]	Hong LI, Shu-zhen SONG, Liang-shuang GAO, Xia LANG, Li-shan LIU, Xu-yin GONG, Yu-bing WEI, Jian-ping WU. Effects of feeding level on the gastrointestinal development， rumen fermentation and rumen microbiota in Altay sheep [J]. Acta Prataculturae Sinica, 2021, 30(4): 180-190.
[12]	Sheng-wei ZHANG, Xiao-ping WANG, Zhan-hai ZHANG, You-ji MA, Shuang-bao GUN, Qiao-li YANG, Xiao-li GAO, Bao-jun ZHANG. Effects of Broussonetia papyrifera silage on growth performance， serum biochemical indexes and meat quality of Dorper×Hu crossbred sheep [J]. Acta Prataculturae Sinica, 2021, 30(3): 89-99.
[13]	Jian-bo ZHANG, KAO Ren-qing DING, Ze-yi LIANG, Ahmad Anum-ali, Mei DU, Juan-shan ZHENG, Xue-zhi DING. Effect of early nutrition intervention on rumen microflora development in young ruminants [J]. Acta Prataculturae Sinica, 2021, 30(2): 199-211.
[14]	Mei XIONG, Ji-rong QIAO, Yang YANG, Feng ZHANG, Jia-hua ZHENG, Jian-xin WU, Meng-li ZHAO. Stocking rate effects on stoichiometric characteristics of the steppe grassland pioneer species Stipabreviflora and its underlying soil [J]. Acta Prataculturae Sinica, 2021, 30(2): 212-219.
[15]	Chen WU, Zhi-hao YAO, Wen-qing MEI, Yu-yan FENG, Qu CHEN, Ying-dong NI. Effects of vitamin B complex on intestinal microflora composition and gut epithelial structure in growing goats [J]. Acta Prataculturae Sinica, 2021, 30(11): 170-180.