Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2024-0067
Animal Reproduction (AR)
REVIEW ARTICLE

Effects of heat stress on reproduction and gene expression in sheep

Galma Boneya Arero; Ozge Ozmen

Downloads: 3
Views: 418

Abstract

Small ruminant farming plays a pivotal role in agriculture, especially in developing countries due to sheep's diverse functions and capacity to acclimate to varying temperatures. This review comprehensively explored the impact of rising temperatures on reproductive processes, reproductive function encoding gene expression, and sheep's ability to adapt to heat stress. Several mechanisms contribute to sheep's resilience to heat stress, encompassing morphological, behavioral, physiological, and genetic adaptations. It has been shown that heat stress compromises fertility by affecting follicular development, ovulation rate, estrous behavior, rates of conception, embryonic survival, and fetal development, while also disrupting sperm production and motility, and increasing the incidence of structurally abnormal sperm in males. Estimates suggested that heat stress may reduce conception rates from 20% to 27%. Essential genes encoding the Gonadotrophin-releasing hormone, Follicle-stimulating hormone receptor, Luteinizing hormone receptor, Estradiol receptor, progesterone receptor, and Inhibin play a critical role in elucidating how heat stress impacts the reproductive performance of sheep. Furthermore, the resilience of sheep in facing heat stress adversities is associated with a specific heat shock factor. When an animal is under heat stress, Heat shock factors get activated and stimulate the production of Heat Shock Proteins (HSPs). Emphasis should be given to identifying specific genes and candidate genes that confer protection against heat stress and conducting comprehensive research to unravel how sheep adapt to demanding local climatic conditions to enhance production and profitability, improve animal welfare, and for genetic conservation and breeding programs.

Keywords

heat stress, reproduction, adaptation, genes, sheep

References

Aguiar LH, Hyde KA, Pedroza GH, Denicol AC. Heat stress impairs in vitro development of preantral follicles of cattle. Anim Reprod Sci. 2020;213:106277. http://doi.org/10.1016/j.anireprosci.2020.106277. PMid:31987328.

Ahmad SF, Mehrotra A, Charles S, Ganai NA. Analysis of selection signatures reveals important insights into the adaptability of high-altitude Indian sheep breed Changthangi. Gene. 2021;799:145809. http://doi.org/10.1016/j.gene.2021.145809. PMid:34224833.

Allendorf FW, Hohenlohe PA, Luikart G. Genomics and the future of conservation genetics. Nat Rev Genet. 2010;11(10):697-709. http://doi.org/10.1038/nrg2844. PMid:20847747.

Alves MBR, Andrade AFC, Arruda RP, Batissaco L, Florez-Rodriguez SA, Oliveira BMM, Torres MA, Lançoni R, Ravagnani GM, Prado Filho RR, Vellone VS, Losano JDA, Franci CR, Nichi M, Celeghini ECC. Recovery of normal testicular temperature after scrotal heat stress in rams assessed by infrared thermography and its effects on seminal characteristics and testosterone blood serum concentration. Theriogenology. 2016;86(3):795-805. http://doi.org/10.1016/j.theriogenology.2016.02.034. PMid:27045627.

Amitha JP, Krishnan G, Bagath M, Sejian V, Bhatta R. Heat stress impact on the expression patterns of different reproduction related genes in Malabari goats. Theriogenology. 2019;131:169-76. http://doi.org/10.1016/j.theriogenology.2019.03.036. PMid:30978567.

Archana PR, Aleena J, Pragna P, Vidya MK, Niyas APA, Bagath M. Role of heat shock proteins in livestock adaptation to heat stress. J Dairy Vet Anim Res. 2017;5(1):127.

Aslan M, Demir E, Karslı T. Microsatellite diversity and restriction enzyme-based polymorphisms of MHC loci in some native Turkish goats. J Agric Sci. 2022;28(4):626-34.

Attia NES. Physiological, hematological and biochemical alterations in heat stressed goats. Benha Vet Med J. 2016;31(2):56-62. http://doi.org/10.21608/bvmj.2016.31261.

Bakheit SA, Ibrahim IE, El Shafei IM, Musa MA. Research article effects of water deprivation and environmental temperature on physiological performance of sudanese desert goats. J Sci Eng Res. 2017;4(4):243-50. http://doi.org/10.3390/ijms19072144.

Bartels A, Han Q, Nair P, Stacey L, Gaynier H, Mosley M, Huang QQ, Pearson JK, Hsieh TF, An YC, Xiao W. Dynamic DNA methylation in plant growth and development. Int J Mol Sci. 2018;19(7):2144. http://doi.org/10.3390/ijms19072144. PMid:30041459.

Belhadj Slimen I, Najar T, Ghram A, Abdrrabba M. Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. J Anim Physiol Anim Nutr (Berl). 2016;100(3):401-12. http://doi.org/10.1111/jpn.12379. PMid:26250521.

Berihulay H, Abied A, He X, Jiang L, Ma Y. Adaptation mechanisms of small ruminants to environmental heat stress. Animals (Basel). 2019;9(3):75. http://doi.org/10.3390/ani9030075. PMid:30823364.

Bodin L, Di Pasquale E, Fabre S, Bontoux M, Monget P, Persani L, Mulsant P. A novel mutation in the bone morphogenetic protein 15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in Lacaune sheep. Endocrinology. 2007;148(1):393-400. http://doi.org/10.1210/en.2006-0764. PMid:17038554.

Bowles D, Carson A, Isaac P. Genetic distinctiveness of the Herdwick sheep breed and two other locally adapted hill breeds of the UK. PLoS One. 2014;9(1):e87823. http://doi.org/10.1371/journal.pone.0087823. PMid:24489968.

Cao YH, Xu SS, Shen M, Chen ZH, Gao L, Lv FH, Xie XL, Wang XH, Yang H, Liu CB, Zhou P, Wan PC, Zhang YS, Yang JQ, Pi WH, Hehua E, Berry DP, Barbato M, Esmailizadeh A, Nosrati M, Salehian-Dehkordi H, Dehghani-Qanatqestani M, Dotsev AV, Deniskova TE, Zinovieva NA, Brem G, Štěpánek O, Ciani E, Weimann C, Erhardt G, Mwacharo JM, Ahbara A, Han JL, Hanotte O, Miller JM, Sim Z, Coltman D, Kantanen J, Bruford MW, Lenstra JA, Kijas J, Li MH. Historical introgression from wild relatives enhanced climatic adaptation and resistance to pneumonia in sheep. Mol Biol Evol. 2021;38(3):838-55. http://doi.org/10.1093/molbev/msaa236. PMid:32941615.

Chedid M, Jaber LS, Giger-Reverdin S, Duvaux-Ponter C, Hamadeh SK. Water stress in sheep raised under arid conditions. Can J Anim Sci. 2014;94(2):243-57. http://doi.org/10.4141/cjas2013-188.

Chen HY, Shen H, Jia B, Zhang YS, Wang XH, Zeng XC. Differential gene expression in ovaries of Qira black sheep and Hetian sheep using RNA-Seq technique. PLoS One. 2015;10(3):e0120170. http://doi.org/10.1371/journal.pone.0120170. PMid:25790350.

Chu MX, Liu ZH, Jiao CL, He YQ, Fang L, Ye SC, Chen GH, Wang JY. Mutations in BMPR-IB and BMP-15 genes are associated with litter size in small-tailed Han sheep (Ovis aries). J Anim Sci. 2007;85(3):598-603. http://doi.org/10.2527/jas.2006-324. PMid:17040942.

Collier RJ, Collier JL, Rhoads RP, Baumgard LH. Invited review: genes involved in the bovine heat stress response. J Dairy Sci. 2008;91(2):445-54. http://doi.org/10.3168/jds.2007-0540. PMid:18218730.

Collier RJ, Gebremedhin K, Macko AR, Roy KS. Genes involved in the thermal tolerance of livestock. In: Sejian V, Naqvi SMK, Ezeij R, Lakritz J, Lal R, editors. Environmental stress and amelioration in livestock production. Berlin: Springer; 2012. p. 379–410. http://doi.org/10.1007/978-3-642-29205-7_14.

Das R, Sailo L, Verma N, Bharti P, Saikia J, Kumar R. Impact of heat stress on health and performance of dairy animals: A review. Vet World. 2016;9(3):260-8. http://doi.org/10.14202/vetworld.2016.260-268. PMid:27057109.

De K, Kumar D, Balaganur K, Naqvi SMK. Effect of environmental factors on estrus synchronization and artificial insemination success in farmers flock in sheep under semi‐arid tropical region. Reprod Domest Anim. 2020;55(7):777-84. http://doi.org/10.1111/rda.13683. PMid:32291822.

de La Salles AYF, Batista LF, de Souza BB, da Silva AF, de Barros Correia ÉL. Growth and reproduction hormones of ruminants subjected to heat stress. J Anim Behav Biometeorol. 2020;5(1):7-12. http://doi.org/10.14269/2318-1265/jabb.v5n1p7-12.

de Simoni Gouveia JJ, Paiva SR, McManus CM, Caetano AR, Kijas JW, Faco O, Azevedo HC, de Araujo AM, de Souza CJH, Yamagishi MEB, Carneiro PLS, Braga Lôbo RN, de Oliveira SMP, da Silva MVGB. Genome-wide search for signatures of selection in three major Brazilian locally adapted sheep breeds. Livest Sci. 2017;197:36-45. http://doi.org/10.1016/j.livsci.2017.01.006.

Dobson H, Fergani C, Routly JE, Smith RF. Effects of stress on reproduction in ewes. Anim Reprod Sci. 2012;130(3–4):135-40. http://doi.org/10.1016/j.anireprosci.2012.01.006. PMid:22325927.

Dovolou E, Giannoulis T, Nanas I, Amiridis GS. Heat stress: a serious disruptor of the reproductive physiology of dairy cows. Animals (Basel). 2023;13(11):1846. http://doi.org/10.3390/ani13111846. PMid:37889768.

Farshad A, Yousefi A, Moghaddam A, Khalili B. Seasonal changes in serum testosterone, LDH concentration and semen characteristics in Markhoz goats. Asian-Australas J Anim Sci. 2012;25(2):189-93. http://doi.org/10.5713/ajas.2011.11179. PMid:25049550.

Fernández ME, Goszczynski DE, Lirón JP, Villegas-Castagnasso EE, Carino MH, Ripoli MV, Rogberg-Muñoz A, Posik DM, Peral-García P, Giovambattista G. Comparison of the effectiveness of microsatellites and SNP panels for genetic identification, traceability and assessment of parentage in an inbred Angus herd. Genet Mol Biol. 2013;36(2):185-91. http://doi.org/10.1590/S1415-47572013000200008. PMid:23885200.

Fogarty NM. A review of the effects of the Booroola gene (FecB) on sheep production. Small Rumin Res. 2009;85(2–3):75-84. http://doi.org/10.1016/j.smallrumres.2009.08.003.

Gandhi RS, Arjava Sharma AS. Conservation of livestock diversity in India under current scenario. Indian Dairym. 2016;68(2):102-7.

Garner JB, Douglas ML, Williams SRO, Wales WJ, Marett LC, Nguyen TTT, Reich CM, Hayes BJ. Genomic selection improves heat tolerance in dairy cattle. Sci Rep. 2016;6(1):34114. http://doi.org/10.1038/srep34114. PMid:27682591.

Gebreselassie G, Berihulay H, Jiang L, Ma Y. Review on genomic regions and candidate genes associated with economically important production and reproduction traits in sheep (Ovies aries). Animals (Basel). 2019;10(1):33. http://doi.org/10.3390/ani10010033. PMid:31877963.

Gootwine E. Mini review: breeding Awassi and Assaf sheep for diverse management conditions. Trop Anim Health Prod. 2011;43(7):1289-96. http://doi.org/10.1007/s11250-011-9852-y. PMid:21512726.

Gupta M, Kumar S, Dangi SS, Jangir BL. Physiological, biochemical and molecular responses to thermal stress in goats. Int J Livest Res. 2013;3(2):27-38. http://doi.org/10.5455/ijlr.20130502081121.

Hamilton TRS, Siqueira AFP, Castro LS, Mendes CM, Delgado JC, Assis PM, Mesquita LP, Maiorka PC, Nichi M, Goissis MD, Visintin JA, Assumpção MEODÁ. Effect of heat stress on sperm DNA: protamine assessment in ram spermatozoa and testicle. Oxid Med Cell Longev. 2018;2018(1):5413056. http://doi.org/10.1155/2018/5413056. PMid:29765499.

Hanrahan JP, Gregan SM, Mulsant P, Mullen M, Davis GH, Powell R, Galloway SM. Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol Reprod. 2004;70(4):900-9. http://doi.org/10.1095/biolreprod.103.023093. PMid:14627550.

Hansen PJ. Exploitation of genetic and physiological determinants of embryonic resistance to elevated temperature to improve embryonic survival in dairy cattle during heat stress. Theriogenology. 2007;68(Suppl 1):S242-9. http://doi.org/10.1016/j.theriogenology.2007.04.008. PMid:17482669.

Herman AP, Romanowicz K, Tomaszewska‐Zaremba D. Effect of LPS on reproductive system at the level of the pituitary of anestrous ewes. Reprod Domest Anim. 2010;45(6):e351-9. http://doi.org/10.1111/j.1439-0531.2009.01577.x. PMid:20345594.

Hooda OK, Upadhyay RC. Physiological responses, growth rate and blood metabolites under feed restriction and thermal exposure in kids. J Stress Physiol Biochem. 2014;10(2):214-27.

Hooper LM, Payton RR, Rispoli LA, Saxton AM, Edwards JL. Impact of heat stress on germinal vesicle breakdown and lipolytic changes during in vitro maturation of bovine oocytes. J Reprod Dev. 2015;61(5):459-64. http://doi.org/10.1262/jrd.2014-168. PMid:26120041.

Indu S, Sejian V, Naqvi SMK. Impact of simulated heat stress on growth, physiological adaptability, blood metabolites and endocrine responses in Malpura ewes under semiarid tropical environment. Anim Prod Sci. 2014;55(6):766-76. http://doi.org/10.1071/AN14085.

Júnior CAC, Lucci CM, Peripolli V, Silva AF, Menezes AM, Morais SRL. Effects of testicle insulation on seminal traits in rams: preliminary study. Small Rumin Res. 2015;130:157-65. http://doi.org/10.1016/j.smallrumres.2015.06.014.

Kaushik R, Dige MS, Rout PK. Molecular characterization and expression profiling of ENOX2 gene in response to heat stress in goats. Cell Dev Biol. 2016;5(2):1-5. http://doi.org/10.4172/2168-9296.1000176.

Khan A, Dou J, Wang Y, Jiang X, Khan MZ, Luo H, Usman T, Zhu H. Evaluation of heat stress effects on cellular and transcriptional adaptation of bovine granulosa cells. J Anim Sci Biotechnol. 2020;11(1):25. http://doi.org/10.1186/s40104-019-0408-8. PMid:32095238.

Kim ES, Elbeltagy AR, Aboul-Naga AM, Rischkowsky B, Sayre B, Mwacharo JM, Rothschild MF. Multiple genomic signatures of selection in goats and sheep indigenous to a hot arid environment. Heredity. 2016;116(3):255-64. http://doi.org/10.1038/hdy.2015.94. PMid:26555032.

Kiyma Z, Alexander BM, Van Kirk EA, Murdoch WJ, Hallford DM, Moss GE. Effects of feed restriction on reproductive and metabolic hormones in ewes. J Anim Sci. 2004;82(9):2548-57. http://doi.org/10.2527/2004.8292548x. PMid:15446470.

Kleemann DO, Walker SK. Fertility in South Australian commercial Merino flocks: relationships between reproductive traits and environmental cues. Theriogenology. 2005;63(9):2416-33. http://doi.org/10.1016/j.theriogenology.2004.09.052. PMid:15910923.

Koluman N, Boga M, Silanikove N, Gorgulu M. Performance and eating behaviour of crossbred goats in Mediterranean climate of Turkey. Rev Bras Zootec. 2016;45(12):768-72. http://doi.org/10.1590/s1806-92902016001200006.

Krishnan G, Bagath M, Pragna P, Vidya MK, Aleena J, Archana PR, Sejian V, Bhatta R. Mitigation of the heat stress impact in livestock reproduction. Theriogenology. 2017;8:8-9.

Kumar D, De K, Sejian V, Naqvi SMK. Impact of climate change on sheep reproduction. Sheep Prod Adapt to Clim Chang. 2017;71:93. http://doi.org/10.1007/978-981-10-4714-5_3.

Kumar D, Yadav B, Choudhury S, Kumari P, Madan AK, Singh SP, Rout PK, Ramchandran N, Yadav S. Evaluation of adaptability to different seasons in goat breeds of semi-arid region in India through differential expression pattern of heat shock protein genes. Biol Rhythm Res. 2018;49(3):466-78. http://doi.org/10.1080/09291016.2017.1377984.

Lima CJG, Cardoso SC, Lemos EFL, Zingler E, Capanema C, Menezes LD, Vogado G, Dos Santos BT, de Moraes OL, Duarte EF, de Brito VN, Latronico AC, Lofrano-Porto A. Mutational analysis of the genes encoding rfamide‐related peptide‐3, the human orthologue of gonadotrophin‐inhibitory hormone, and its receptor (GPR 147) in patients with gonadotrophin‐releasing hormone‐dependent pubertal disorders. J Neuroendocrinol. 2014;26(11):817-24. http://doi.org/10.1111/jne.12207. PMid:25180599.

Liu Q, Pan Z, Wang X, Hu W, Di R, Yao Y, Chu M. Progress on major genes for high fecundity in ewes. Front Agric Sci Eng. 2014;1(4):282-90. http://doi.org/10.15302/J-FASE-2014042.

López R, Pinto-Santini L, Perozo D, Pineda J, Oliveros I, Chacón T, Rossini M, Ríos de Álvarez L. Confort térmico y crecimiento de corderas West African pastoreando con y sin acceso a sombra artificial. Arch Zootec. 2015;64(246):139-46. http://doi.org/10.21071/az.v64i246.388.

Luo E, Stephens SBZ, Chaing S, Munaganuru N, Kauffman AS, Breen KM. Corticosterone blocks ovarian cyclicity and the LH surge via decreased kisspeptin neuron activation in female mice. Endocrinology. 2016;157(3):1187-99. http://doi.org/10.1210/en.2015-1711. PMid:26697722.

Mahgoub O, Kadim IT, Al-Dhahab A, Bello RB, Al-Amri IS, Ali AAA and Khalaf S. An assessment of Omani native sheep fiber production and quality characteristics. J Agric Mar Sci. 2010;15:9-14.

Marai IFM, El-Darawany AA, Fadiel A, Abdel-Hafez MAM. Physiological traits as affected by heat stress in sheep: a review. Small Rumin Res. 2007;71(1–3):1-12. http://doi.org/10.1016/j.smallrumres.2006.10.003.

Marai IFM, El-Darawany AA, Fadiel A, Abdel-Hafez MAM. Reproductive performance traits as affected by heat stress and its alleviation in sheep. Trop Subtrop Agroecosystems. 2008;8(3):209-34.

Maurya VP, Naqvi SMK, Mittal JP. Effect of dietary energy level on physiological responses and reproductive performance of Malpura sheep in the hot semi-arid regions of India. Small Rumin Res. 2004;55(13):11722. http://doi.org/10.1016/j.smallrumres.2003.12.008.

Maurya VP, Sejian V, Kumar D, Naqvi SMK. Biological ability of Malpura rams to counter heat stress challenges and its consequences on production performance in a semi-arid tropical environment. Biol Rhythm Res. 2018;49(3):479-93. http://doi.org/10.1080/09291016.2017.1381451.

Maurya VP, Sejian V, Kumar D, Naqvi SMK. Effect of induced body condition score differences on sexual behavior, scrotal measurements, semen attributes and endocrine responses in Malpura rams under hot semi‐arid environment. J Anim Physiol Anim Nutr (Berl). 2010;94(6):e308-17. http://doi.org/10.1111/j.1439-0396.2010.01012.x. PMid:20626503.

Maya-Soriano MJ, Taberner E, López-Béjar M. Retinol improves in vitro oocyte nuclear maturation under heat stress in heifers. Zygote. 2013;21(4):377-84. http://doi.org/10.1017/S0967199412000135. PMid:22785151.

Mazinani M, Rude B. Population, world production and quality of sheep and goat products. Am J Anim Vet Sci. 2020;15(4):291-9. http://doi.org/10.3844/ajavsp.2020.291.299.

McManus C, Paludo GR, Louvandini H, Gugel R, Sasaki LCB, Paiva SR. Heat tolerance in Brazilian sheep: physiological and blood parameters. Trop Anim Health Prod. 2009;41(1):95-101. http://doi.org/10.1007/s11250-008-9162-1. PMid:19052907.

McManus CM, Faria DA, Lucci CM, Louvandini H, Pereira SA, Paiva SR. Heat stress effects on sheep: are hair sheep more heat resistant? Theriogenology. 2020;155:157-67. http://doi.org/10.1016/j.theriogenology.2020.05.047. PMid:32679441.

McNatty KP, Galloway SM, Wilson T, Smith P, Hudson NL, O’Connell A, Bibby AH, Heath DA, Davis GH, Hanrahan JP, Juengel JL. Physiological effects of major genes affecting ovulation rate in sheep. Genet Sel Evol. 2005;37(Suppl. 1):S25-38. http://doi.org/10.1186/1297-9686-37-S1-S25. PMid:15601593.

Mondal S, Mor A, Reddy IJ, Nandi S, Gupta PSP. Heat stress induced alterations in prostaglandins, ionic and metabolic contents of sheep endometrial epithelial cells in vitro. Biomed J Sci Tech Res. 2017;1(4):1-5. http://doi.org/10.26717/BJSTR.2017.01.000384.

Mwacharo JM, Kim ES, Elbeltagy AR, Aboul-Naga AM, Rischkowsky BA, Rothschild MF. Genomic footprints of dryland stress adaptation in Egyptian fat-tail sheep and their divergence from East African and western Asia cohorts. Sci Rep. 2017;7(1):17647. http://doi.org/10.1038/s41598-017-17775-3. PMid:29247174.

Neves MLMW, Azevedo M, da Costa LAB, Guim A, Leite AM, Chagas JC. Níveis críticos do índice de conforto térmico para ovinos da raça Santa Inês criados a pasto no agreste do Estado de Pernambuco. Acta Sci Anim Sci. 2009;31(2):169-75. http://doi.org/10.4025/actascianimsci.v31i2.3766.

Niyas PAA, Chaidanya K, Shaji S, Sejian V, Bhatta R. Adaptation of livestock to environmental challenges. J Vet Sci Med Diagn. 2015;4(3):2. http://doi.org/10.4172/2325-9590.1000146.

Nyboe Andersen A, Nelson SM, Fauser BCJM, García-Velasco JA, Klein BM, Arce JC, Tournaye H, De Sutter P, Decleer W, Petracco A, Borges E, Barbosa CP, Havelock J, Claman P, Yuzpe A, Višnová H, Ventruba P, Uher P, Mrazek M, Andersen AN, Knudsen UB, Dewailly D, Leveque AG, La Marca A, Papaleo E, Kuczynski W, Kozioł K, Anshina M, Zazerskaya I, Gzgzyan A, Bulychova E, Verdú V, Barri P, García-Velasco JA, Fernández-Sánchez M, Martin FS, Bosch E, Serna J, Castillon G, Bernabeu R, Ferrando M, Lavery S, Gaudoin M, Nelson SM, Fauser BCJM, Klein BM, Helmgaard L, Mannaerts B, Arce J-C. Individualized versus conventional ovarian stimulation for in vitro fertilization: a multicenter, randomized, controlled, assessor-blinded, phase 3 noninferiority trial. Fertil Steril. 2017;107(2):387-396.e4. http://doi.org/10.1016/j.fertnstert.2016.10.033. PMid:27912901.

Ozawa M, Tabayashi D, Latief TA, Shimizu T, Oshima I, Kanai Y. Alterations in follicular dynamics and steroidogenic abilities induced by heat stress during follicular recruitment in goats. Reproduction. 2005;129(5):621-30. http://doi.org/10.1530/rep.1.00456. PMid:15855625.

Pérez RV, Macías Cruz U, Avendaño Reyes L, Correa-Calderón A, López Baca MDLÁ, Lara Rivera AL. Impacto del estrés por calor en la producción de ovinos de pelo. Revisión. Rev Mex Cienc Pecu. 2020;11(1):205-22. http://doi.org/10.22319/rmcp.v11i1.4923.

Pineda MH, Dooley MP. McDonald’s veterinary endocrinology and reproduction. Iowa: Iowa State Press; 2003.

Pöhland R, Souza-Cácares MB, Datta TK, Vanselow J, Martins MIM, Silva WAL, Cardoso CJT, Melo-Sterza FA. Influence of long-term thermal stress on the in vitro maturation on embryo development and Heat Shock Protein abundance in zebu cattle. Anim Reprod. 2020;17(3):e20190085. http://doi.org/10.1590/1984-3143-ar2019-0085. PMid:33029207.

Rana MS, Hashem MA, Akhter S, Habibullah M, Islam MH, Biswas RC. Effect of heat stress on carcass and meat quality of indigenous sheep of Bangladesh. Bangladesh J Anim Sci. 2014;43(2):147-53. http://doi.org/10.3329/bjas.v43i2.20717.

Rasooli A, Jalali MT, Nouri M, Mohammadian B, Barati F. Effects of chronic heat stress on testicular structures, serum testosterone and cortisol concentrations in developing lambs. Anim Reprod Sci. 2010;117(1–2):55-9. http://doi.org/10.1016/j.anireprosci.2009.03.012. PMid:19428197.

Rathwa SD, Vasava AA, Pathan MM, Madhira SP, Patel YG, Pande AM. Effect of season on physiological, biochemical, hormonal, and oxidative stress parameters of indigenous sheep. Vet World. 2017;10(6):650-4. http://doi.org/10.14202/vetworld.2017.650-654. PMid:28717317.

Renaudeau D, Collin A, Yahav S, De Basilio V, Gourdine JL, Collier RJ. Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal. 2012;6(5):707-28. http://doi.org/10.1017/S1751731111002448. PMid:22558920.

Romero RD, Montero Pardo A, Montaldo HH, Rodríguez AD, Hernández Cerón J. Differences in body temperature, cell viability, and HSP-70 concentrations between Pelibuey and Suffolk sheep under heat stress. Trop Anim Health Prod. 2013;45(8):1691-6. http://doi.org/10.1007/s11250-013-0416-1. PMid:23677527.

Romo-Barron CB, Diaz D, Portillo-Loera JJ, Romo-Rubio JA, Jimenez-Trejo F, Montero-Pardo A. Impact of heat stress on the reproductive performance and physiology of ewes: a systematic review and meta-analyses. Int J Biometeorol. 2019;63(7):949-62. http://doi.org/10.1007/s00484-019-01707-z. PMid:30888508.

Rossi M. Analysis of poplar plants responses to environmental stress conditions. 2017 [cited 2024 May 19]. Available from: https://hdl.handle.net/11695/79757.

Sawyer G, Narayan EJ. A review on the influence of climate change on sheep reproduction. In: Narayan E, editor. Comparative Endocrinology of Animals. Local, Australia: Intech; 2019. p. 10. http://doi.org/10.5772/intechopen.86799.

Scholtz MM, McManus C, Leeuw KJ, Louvandini H, Seixas L, Melo CD, Theunissen A, Neser FWC. The effect of global warming on beef production in developing countries of the southern hemisphere. Nat Sci (Irvine Calif). 2013;5(1):106-19. http://doi.org/10.4236/ns.2013.51A017.

Seixas L, de Melo CB, Tanure CB, Peripolli V, McManus C. Heat tolerance in Brazilian hair sheep. Asian-Australas J Anim Sci. 2017;30(4):593-601. http://doi.org/10.5713/ajas.16.0191. PMid:27282972.

Sejian V, Bagath M, Krishnan G, Rashamol VP, Pragna P, Devaraj C, Bhatta R. Genes for resilience to heat stress in small ruminants: A review. Small Rumin Res. 2019;173:42-53. http://doi.org/10.1016/j.smallrumres.2019.02.009.

Sejian V, Bhatta R, Gaughan J, Malik PK, Naqvi SMK, Lal R, editors. Sheep production adapting to climate change. Singapore: Springer; 2017a. Adapting sheep production to climate change; p. 1-29. http://doi.org/10.1007/978-981-10-4714-5.

Sejian V, Bhatta R, Gaughan J, Malik PK, Naqvi SMK, Lal R, editors. Sheep production adapting to climate change. Singapore: Springer; 2017b. Sheep production adapting to climate change, p. 1-29. http://doi.org/10.1007/978-981-10-4714-5.

Sejian V, Bhatta R, Gaughan JB, Dunshea FR, Lacetera N. Adaptation of animals to heat stress. Animal. 2018;12(s2):s431-44. http://doi.org/10.1017/S1751731118001945. PMid:30139399.

Sejian V, Maurya VP, Kumar K, Naqvi SMK. Effect of multiple stresses (thermal, nutritional, and walking stress) on the reproductive performance of Malpura ewes. Vet Med Int. 2012a;2012:471760. http://doi.org/10.1155/2012/471760. PMid:22448337.

Sejian V, Maurya VP, Kumar K, Naqvi SMK. Effect of multiple stresses on growth and adaptive capability of Malpura ewes under semi-arid tropical environment. Trop Anim Health Prod. 2012b;45(1):107-16. http://doi.org/10.1007/s11250-012-0180-7. PMid:23011669.

Sejian V, Maurya VP, Naqvi SMK. Adaptability and growth of Malpura ewes subjected to thermal and nutritional stress. Trop Anim Health Prod. 2010a;42(8):1763-70. http://doi.org/10.1007/s11250-010-9633-z. PMid:20571921.

Sejian V, Maurya VP, Naqvi SMK. Adaptive capability as indicated by endocrine and biochemical responses of Malpura ewes subjected to combined stresses (thermal and nutritional) in a semi-arid tropical environment. Int J Biometeorol. 2010b;54(6):653-61. http://doi.org/10.1007/s00484-010-0341-1. PMid:20607306.

Sejian V, Maurya VP, Naqvi SMK. Effect of thermal, nutritional and combined (thermal and nutritional) stresses on growth and reproductive performance of Malpura ewes under semi-arid tropical environment. J Anim Physiol Anim Nutr (Berl). 2011;95:252-8. http://doi.org/10.1111/j.1439-0396.2010.01048.x. PMid:20796074.

Sheikh AA, Bhagat R, Islam ST, Dar RR, Sheikh SA, Wani JM. Effect of climate change on reproduction and milk production performance of livestock: a review. J Pharmacogn Phytochem. 2017;6(6):2062-4.

Shilja S, Sejian V, Bagath M, Mech A, David CG, Kurien EK, Varma G, Bhatta R. Adaptive capability as indicated by behavioral and physiological responses, plasma HSP70 level, and PBMC HSP70 mRNA expression in Osmanabadi goats subjected to combined (heat and nutritional) stressors. Int J Biometeorol. 2016;60(9):1311-23. http://doi.org/10.1007/s00484-015-1124-5. PMid:26698161.

Shinde AK, Sejian V. Sheep husbandry under changing climate scenario in India: an overview. Indian J Anim Sci. 2013;83(10):998-1008.

Singh KM, Singh S, Ganguly I, Ganguly A, Nachiappan RK, Chopra A, Narula HK. Evaluation of Indian sheep breeds of arid zone under heat stress condition. Small Rumin Res. 2016;141:113-7. http://doi.org/10.1016/j.smallrumres.2016.07.008.

Singh KM, Singh S, Ganguly I, Nachiappan RK, Ganguly A, Venkataramanan R, Chopra A, Narula HK. Association of heat stress protein 90 and 70 gene polymorphism with adaptability traits in Indian sheep (Ovis aries). Cell Stress Chaperones. 2017;22(5):675-84. http://doi.org/10.1007/s12192-017-0770-4. PMid:28265807.

Slimen IB, Chniter M, Najar T, Ghram A. Meta-analysis of some physiologic, metabolic and oxidative responses of sheep exposed to environmental heat stress. Livest Sci. 2019;229:179-87. http://doi.org/10.1016/j.livsci.2019.09.026.

Solórzano-Montilla J, Pinto-Santini L, Camacaro-Calvete S, Vargas-Guzmán D, Ríos-de Álvarez L. Effect of the presence of shade in sheep grazing areas. 2. Animal activity. Pastos Forrajes. 2018;41(1):39-46.

Stamperna K, Giannoulis T, Dovolou E, Kalemkeridou M, Nanas I, Dadouli K, Moutou K, Mamuris Z, Amiridis GS. The effects of heat shock protein 70 addition in the culture medium on the development and quality of in vitro produced heat shocked bovine embryos. Animals (Basel). 2021;11(12):3347. http://doi.org/10.3390/ani11123347. PMid:34944122.

van Wettere WHEJ, Kind KL, Gatford KL, Swinbourne AM, Leu ST, Hayman PT, Kelly JM, Weaver AC, Kleemann DO, Walker SK. Review of the impact of heat stress on reproductive performance of sheep. J Anim Sci Biotechnol. 2021;12(1):26. http://doi.org/10.1186/s40104-020-00537-z. PMid:33583422.

Wang H, Zhang L, Cao J, Wu M, Ma X, Liu Z, Liu R, Zhao F, Wei C, Du L. Genome-wide specific selection in three domestic sheep breeds. PLoS One. 2015;10(6):e0128688. http://doi.org/10.1371/journal.pone.0128688.

Webb RJ, Bains H, Cruttwell C, Carroll J. Gap-junctional communication in mouse cumulus-oocyte complexes: implications for the mechanism of meiotic maturation. Reproduction. 2002;123(1):41-52. http://doi.org/10.1530/rep.0.1230041. PMid:11869185.

Wei S, Shen X, Gong Z, Deng Y, Lai L, Liang H. FSHR and LHR expression and signaling as well as maturation and apoptosis of cumulus-oocyte complexes following treatment with FSH receptor binding inhibitor in sheep. Cell Physiol Biochem. 2017;43(2):660-9. http://doi.org/10.1159/000480650. PMid:28942449.

Wojtas K, Cwynar P, Kołacz R. Effect of thermal stress on physiological and blood parameters in merino sheep. Bull Vet Inst Pulawy. 2014;58(2):283-8. http://doi.org/10.2478/bvip-2014-0043.

Wolfenson D, Roth Z, Meidan R. Impaired reproduction in heat-stressed cattle: basic and applied aspects. Anim Reprod Sci. 2000;60:535-47. http://doi.org/10.1016/S0378-4320(00)00102-0. PMid:10844222.

Yan Z, Wang Z, Zhang Q, Yue S, Yin B, Jiang Y, Shi K. Identification of whole‐genome significant single nucleotide polymorphisms in candidate genes associated with body conformation traits in Chinese Holstein cattle. Anim Genet. 2020;51(1):141-6. http://doi.org/10.1111/age.12865. PMid:31633203.

Yang JI, Li WR, Lv FH, He SG, Tian SL, Peng WF, Sun YW, Zhao YX, Tu XL, Zhang M, Xie XL, Wang YT, Li JQ, Liu YG, Shen ZQ, Wang F, Liu GJ, Lu HF, Kantanen J, Han JL, Li MH, Liu MJ. Whole-genome sequencing of native sheep provides insights into rapid adaptations to extreme environments. Mol Biol Evol. 2016;33(10):2576-92. http://doi.org/10.1093/molbev/msw129. PMid:27401233.

Zhang L, Duan C, Guo Y, Zhang Y, Liu Y. Inhibition of prolactin promotes secondary skin follicle activation in cashmere goats. J Anim Sci. 2021;99(4):79. http://doi.org/10.1093/jas/skab079. PMid:33693756.

Zhu B, Walker SK, Oakey H, Setchell BP, Maddocks S. Effect of paternal heat stress on the development in vitro of preimplantation embryos in the mouse. Andrologia. 2004;36(6):384-94. http://doi.org/10.1111/j.1439-0272.2004.00635.x. PMid:15541055.
 


Submitted date:
05/19/2024

Accepted date:
01/17/2025

67d2d057a953954cca2b5d03 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections