Abstract
The skin plays an important role in thermoregulation. Identification of genes on the skin that contribute to increased heat tolerance can be used to select animals with the best performance in warm environments. Our objective was to identify candidate genes associated with the heat stress response in the skin of Santa Ines sheep. A group of 80 sheep assessed for thermotolerance was kept in a climatic chamber for 8 days at a stress level temperature of 36 °C (10 am to 04 pm) and a maintenance temperature of 28 °C (04 pm to 10 am). Two divergent groups, with seven animals each, were formed after ranking them by thermotolerance using rectal temperature. From skin biopsy samples, total RNA was extracted, quantified, and used for RNA-seq analysis. 15,989 genes were expressed in sheep skin samples, of which 4 genes were differentially expressed (DE; FDR < 0.05) and 11 DE (FDR 0.05–0.177) between the two divergent groups. These genes are involved in cellular protection against stress (HSPA1A and HSPA6), ribosome assembly (28S, 18S, and 5S ribosomal RNA), and immune response (IGHG4, GNLY, CXCL1, CAPN14, and SAA-4). The candidate genes and main pathways related to heat tolerance in Santa Ines sheep require further investigation to understand their response to heat stress in different climatic conditions and under solar radiation. It is essential to verify whether these genes and pathways are present in different breeds and to understand the relationship between heat stress and other genes identified in this study.
Similar content being viewed by others
References
Al-Dawood A (2017) Acute phase proteins as indicators of stress in Baladi goats from Jordan. Acta Agric Scand A Anim Sci 67:58–65. https://doi.org/10.1080/09064702.2017.1363815
Atanackovic D, Nierhaus A, Neumeier M, Hossfeld DK, Hegewisch-Becker S (2002) 41.8 degrees C whole body hyperthermia as an adjunct to chemotherapy induces prolonged T cell activation in patients with various malignant diseases. Cancer Immunol Immunother 51:603–613
Bagath M, Krishnan G, Devaraj C, Rashamol VP, Pragna P, Lees AM, Sejian V (2019) The impact of heat stress on the immune system in dairy cattle: a review. Res Vet Sci 126:94–102. https://doi.org/10.1016/j.rvsc.2019.08.011
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful ppproach to multiple testing. J R Stat Soc Series B (methodological) 57(1):289–300. https://doi.org/10.1111/J.2517-6161.1995.TB02031.X
Bharati J, Dangi SS, Mishra SR, Chouhan VS, Verma V, Shankar O, Bharti MK, Paul A, Mahato DK, Rajesh G, Singh G, Maurya VP, Bag S, Kumar P, Sarkar M (2017) Expression analysis of Toll like receptors and interleukins in Tharparkar cattle during acclimation to heat stress exposure. J Therm Biol 65:48–56. https://doi.org/10.1016/j.jtherbio.2017.02.002
Borges TJ, Wieten L, Van Herwijnen MJ, Broere F, Van der Zee R, Bonorino C, Van Eden W (2012) The anti-inflammatory mechanisms of Hsp70. Front Immunol 4:95. https://doi.org/10.3389/fimmu.2012.00095
Cafe LM, Robinson DL, Ferguson DM, McIntyre BL, Geesink GH, Greenwood PL (2011) Cattle temperament: persistence of assessments and associations with productivity, efficiency, carcass and meat quality traits. J Anim Sci 89(5):1452–1465. https://doi.org/10.2527/jas.2010-3304
Cantet JM, Yu Z, Ríus AG (2021) Heat stress-mediated activation of immune-inflammatory pathways. Antibiotics (basel) 10:1285. https://doi.org/10.3390/antibiotics10111285
Carabaño MJ, Ramón M, Menéndez-Buxadera A, Molina A, Díaz C (2019) Selecting for heat tolerance. Anim Front 9:1. https://doi.org/10.1093/af/vfy033
Chakraborti S, Alam MN, Paik D, Shaikh S, Chakraborti T (2012) Implications of calpains in health and diseases. Indian J Biochem Biophys 49:316–328
Chensue SW (2006) Chemokines, CXC | CXCL1 (GRO1)–CXCL3 (GRO3). In: Laurent GJ, Shapiro SD (eds) Encyclopedia of respiratory medicine. Academic Press, Cambridge, Massachusetts, pp 407–410 https://doi.org/10.1016/B0-12-370879-6/00469-5
Cheruiyot EK, Haile-Mariam M, Cocks BG, MacLeod IM, Xiang R, Pryce JE (2021) New loci and neuronal pathways for resilience to heat stress in cattle. Sci Rep 11:16619. https://doi.org/10.1038/s41598-021-95816-8
Davis BP, Stucke EM, Khorki ME, Litosh VA, Rymer JK, Rochman M, Travers J, Kottyan LC, Rothenberg ME (2016) Eosinophilic esophagitis-linked calpain 14 is an IL-13-induced protease that mediates esophageal epithelial barrier impairment. JCI Insight 1:e86355. https://doi.org/10.1172/jci.insight.86355
De Buck M, Gouwy M, Wang JM, Van Snick J, Opdenakker G, Struyf S, Van Damme J (2016) Structure and expression of different serum amyloid A (SAA) variants and their concentration-dependent functions during host insults. Curr Med Chem 23:1725–1755. https://doi.org/10.2174/0929867323666160418114600
Diehl S, Rincón M (2002) The two faces of IL-6 on Th1/Th2 differentiation. Mol Immunol 39(9):531–536. https://doi.org/10.1016/S0161-5890(02)00210-9
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut F, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. J Bioinform 29(1):15–21. https://doi.org/10.1093/bioinformatics/bts635
Duque GA, Descoteaux A (2014) Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol 5:491. https://doi.org/10.3389/fimmu.2014.00491
EustáquioFilho A, Teodoro SM, Chaves MA, Santos PEF, Silva MWR, Murta RM, Carvalho GGP, Souza LEB (2011) Thermal comfort zone of Santa Ines sheep based on physiological responses. Rev Bras Zootec 40(8):1807–1814
Ferreira F, Campos WE, Carvalho AU, Pires MFA, Martinez ML, Silva MVGB, Verneque RS, Silva PF (2009) Taxa de sudação e parâmetros histológicos de bovinos submetidos ao estresse calórico. Arq Bras Med Vet Zootec 61:763–768
Flick K, Kaiser P (2012) Protein degradation and the stress response. Semin Cell Dev Biol 23:515–522. https://doi.org/10.1016/j.semcdb.2012.01.019
Fulda S, Gorman AM, Hori O, Samali A (2010) Cellular stress responses: cell survival and cell death. Int J Biol 2010:214074. https://doi.org/10.1155/2010/214074
Ganesan S, Volodina O, Pearce SC, Gabler NK, Baumgard LH, Rhoads RP, Selsby JT (2017) Acute heat stress activated inflammatory signaling in porcine oxidative skeletal muscle. Physiol Rep 5:e13397. https://doi.org/10.14814/phy2.13397
Garner JB, Chamberlain AJ, Vander Jagt C, Nguyen TTT, Mason BA, Marett LC, Leury BJ, Wales WJ, Hayes BJ (2020) Gene expression of the heat stress response in bovine peripheral white blood cells and milk somatic cells in vivo. Sci Rep 10:19181. https://doi.org/10.1038/s41598-020-75438-2
Gebremedhin KG, Hillman PE, Lee CN, Collier RJ, Willard ST, Arthington JD, Brown-Brandl TM (2008) Sweating rates of dairy cows and beef heifers in hot conditions. Trans ASABE 51:2167–2178. https://doi.org/10.13031/2013.25397
Gerashchenko MV, Lobanov AV, Gladyshev VN (2012) Genome-wide ribosome profiling reveals complex translational regulation in response to oxidative stress. Proc Natl Acad Sci U S A 109(43):17394–17399. https://doi.org/10.1073/pnas.1120799109
Ghoshal K, Jacobh ST (1996) Heat shock selectively inhibits ribosomal RNA gene transcription and down-regulates E1BF/Ku in mouse lymphosarcoma cells Kalpana. Biochem J 317:689–695
Hassan FU, Nawaz A, Rehman MS, Ali MA, Dilshad SMR, Yang C (2019) Prospects of HSP70 as a genetic marker for thermo-tolerance and immuno-modulation in animals under climate change scenario. Anim Nutr 5:340–350. https://doi.org/10.1016/j.aninu.2019.06.005
Herbut P, Angrecka S, Godyń D, Hoffmann G (2019) The physiological and productivity effects of heat stress in cattle-a review. Annals Anim Sci 19(3):579–593. https://doi.org/10.2478/aoas-2019-0011
Hu H, Li X (2007) Transcriptional regulation in eukaryotic ribosomal protein genes. Genomics 90(4):421–423. https://doi.org/10.1016/j.ygeno.2007.07.003
Inbaraj S, Sejian V, Bagath M, Bhatta R (2016) Impact of heat stress on immune responses of livestock: a review. J Trop Agric Sci 39:459–482
Iwaniec J, Robinson GP, Garcia CK, Murray KO, de Carvalho L, Clanton TL, Laitano O (2021) Acute phase response to exertional heat stroke in mice. Exp Physiol 106(1):222–232. https://doi.org/10.1113/EP088501
Jonak C, Klosner G, Trautinger F (2009) Significance of heat shock proteins in the skin upon UV exposure. Front Biosci 14:4758–4768
Kapila N, Sharma A, Kishore A, Sodhi M, Tripathi PK, Ashok KM, Manishi M (2018) Correction: impact of heat stress on cellular and transcriptional adaptation of mammary epithelial cells in riverine buffalo (Bubalus Bubalis). PLoS One 13:e0191380. https://doi.org/10.1371/journal.pone.0157237
Kaufman JD, Seidler Y, Bailey HR, Whitacre L, Bargo F, Lüersen K, Rimbach G, Pighetti GM, Ipharraguerre IR, Ríus AG (2021) A postbiotic from Aspergillus oryzae attenuates the impact of heat stress in ectothermic and endothermic organisms. Sci Rep 11:6407. https://doi.org/10.1038/s41598-021-85707-3
Kim J, Suh Y, Chang K (2021) Interleukin-17 induced by cumulative mild stress promoted depression-like behaviors in young adult mice. Mol Brain 14:11. https://doi.org/10.1186/s13041-020-00726-x
Korbecki J, Barczak K, Gutowska I, Chlubek D, Baranowska-Bosiacka I (2022) CXCL1: gene, promoter, regulation of expression, mRNA stability, regulation of activity in the intercellular space. Int J Mol Sci 23:792. https://doi.org/10.3390/ijms23020792
Leite JHGM, Da Silva RG, Asensio LAB, de Sousa JER, da Silva WST, da Silva WE, Façanha DAE (2020) Coat color and morphological hair traits influence on the mechanisms related to the heat tolerance in hair sheep. Int J Biometeorol 64:2185–2194. https://doi.org/10.1007/s00484-020-02014-8
Liao Y, Wang J, Jaehnig EJ, Shi Z, Zhang B (2019) WebGestalt 2019: gene set analysis toolkit with revamped UIs and APIs. Nucleic Acids Res 47(W1):W199–W205. https://doi.org/10.1093/nar/gkz401
Liberman N, O’Brown ZK, Earl AS, Boulias K, Gerashchenko MV, Wang SY, Fritsche C, Fady P, Dong A, Gladyshev VN, Greer EL (2020) N6-adenosine methylation of ribosomal RNA affects lipid oxidation and stress resistance. Sci Adv 6:eaaz4370
Logan AC, Somero GN (2011) Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper). Am J Physiol 300(6):R1373–R1383
Luna-Nevárez G, Kelly AC, Camacho LE, Limesand SW, Reyna-Granados JR, Luna-Nevarez P (2020) Discovery and validation of candidate SNP markers associated to heat stress response in pregnant ewes managed inside a climate-controlled chamber. Trop Anim Health Prod 52:3457–3466. https://doi.org/10.1007/s11250-020-02379-3
Luna-Nevárez G, Pendleton AL, Luna-Ramirez RI, Limesand SW, Reyna-Granados JR, Luna-Nevárez P (2021) Genome-wide association study of a thermo-tolerance indicator in pregnant ewes exposed to an artificial heat-stressed environment. J Therm Biol 101:103095. https://doi.org/10.1016/j.jtherbio.2021.103095
Macías-Cruz U, Gastélum MA, Álvarez FD, Correa A, Díaz R, Meza-Herrera CA, Mellado M, Avendaño-Reyes L (2016) Effects of summer heat stress on physiological variables, ovulation and progesterone secretion in Pelibuey ewes under natural outdoor conditions in an arid region. Anim Sci J 87(3):354–360. https://doi.org/10.1111/asj.12430
Maibam U, Hoodaa OK, Sharmab PS, Mohantyc AK, Singha SV, Upadhyay RC (2017) Expression of HSP70 genes in skin of zebu (Tharparkar) and crossbred (Karan Fries) cattle during different seasons under tropical climatic conditions. J Therm Biol 63:58–64
McManus C, Dallago BSL, Lehugeur C, Ribeiro LA, Hermuche P, Guimarães RF, CarvalhoJúnior OA, Paiva SR (2016) Patterns of heat tolerance in different sheep breeds in Brazil. Small Rumin Res 144:290–299. https://doi.org/10.1016/j.smallrumres.2016.10.004
McManus CM, Faria DA, Lucci CM, Louvandini H, Pereira SA, Paiva SR (2020) Heat stress effects on sheep: are hair sheep more heat resistant? Theriogenol 155:157–167. https://doi.org/10.1016/j.theriogenology.2020.05.047
Morrison SF, Nakamura K (2011) Central neural pathways for thermoregulation. Front Biosci 16:74–104
Mota-Rojas D, Titto CG, Orihuela A, Martínez-Burnes J, Gómez-Prado J, Torres-Bernal F, Flores-Padilla K, Carvajal-de la Fuente V, Wang D (2021) Physiological and behavioral mechanisms of thermoregulation in mammals. Animals 11(6):1733. https://doi.org/10.3390/ani11061733
Mwacharo JM, Kim E, Elbeltagy A, Aboul Naga M, Rischkowsky B, Rothschild MF (2016) Genome wide scans reveal multiple selection sweep regions in indigenous sheep (Ovis Aries) from a hot arid tropical environment. In Proceedings of the plant and animal genome conference XXIV, San Diego, CA, USA, pp 9–13
Noonan EJ, Place RF, Giardina C, Hightower LE (2007) Hsp70B′ regulation and function. Cell Stress Chaperones Winter 12:393–402. https://doi.org/10.1379/csc-278e.1
Normanton M, Marti LC (2013) Current data on IL-17 and Th17 cells and implications for graft versus host disease. Einstein 11:237–246
Panniers R (1994) Translational control during heat shock. Biochimie 76:737–747
Pantoja MHA, Campos JCD, Almeida DHS, Negrão JA, Mourão GB, Pereira AMF, Titto CG (2022) Influence of successive heat waves on the thermoregulatory responses of pregnant and non-pregnant ewes. J Therm Biol 111:103420. https://doi.org/10.1016/j.jtherbio.2022.103420
Park DS, Gu BH, Park YJ, Joo SS, Lee S, Kim S, Kim ET, Kim DH, Lee SS, Lee SJ, Kim B, Kim M (2021) Dynamic changes in blood immune cell composition and function in Holstein and Jersey steers in response to heat stress. Cell Stress Chaperones 26:705–720. https://doi.org/10.1007/s12192-021-01216-2
Pezeshki A, Stordeur P, Wallemacq H, Schynts F, Stevens M, Boutet P, Peelman LJ, Spiegeleer B, Duchateau L, Bureau F, Burvenich C (2011) Variation of inflammatory dynamics and mediators in primiparous cows after intramammary challenge with Escherichia coli. Vet Res 42:1–10. https://doi.org/10.1186/1297-9716-42-15
Ponomarenko M, Stepanenko I, Kolchanov N (2013) Heat shock proteins. In: Maloy S, Hughes K (eds) Brenner’s Encyclopedia of genetics, 2nd edn. Academic Press, Cambridge, Massachusetts, pp.402–405. https://doi.org/10.1016/B978-0-12-374984-0.00685-9
Pulido-Rodríguez LF, Titto CG, Bruni GA, Froge GA, Fuloni MF, Payan-Carrera R, Henrique FL, Geraldo ANAPM, Pereira AMF (2021) Effect of solar radiation on thermoregulatory responses of Santa Inês sheep and their crosses with wool and hair Dorper sheep. Small Rumin Res 202:10647
Rawash RAA, Sharaby MA, Hassan GEA, Elkomy AE, Hafez EE, Hafsa SHA, Salem MMI (2022) Expression profiling of HSP 70 and interleukins 2, 6 and 12 genes of Barki sheep during summer and winter seasons in two different locations. Int J Biometeorol 66:2047–2053. https://doi.org/10.1007/s00484-022-02339-6
Raza SHA, Hassanin AA, Dhshan AIM, Dhshan AIM, Abdelnour SA, Khan R, Mei C, Zan L (2021) In silico genomic and proteomic analyses of three heat shock proteins (HSP70, HSP90-a, and HSP90-b) in even-toed ungulates. Electron J Biotechnol 53:61–70
Ribeiro ELA, González-García E (2016) Indigenous sheep breeds in Brazil: potential role for contributing to the sustainability of production systems. Trop Anim Health Prod 48:1305–1313
Ríus AG, Kaufman JD, Li MM, Hanigan MD, Ipharraguerre IR (2022) Physiological responses of Holstein calves to heat stress and dietary supplementation with a postbiotic from Aspergillus oryzae. Sci Rep 12:1587. https://doi.org/10.1038/s41598-022-05505-3
Robinson DW (1969) Preliminary observations on the heat tolerance of shorn and nutritionally depleted sheep in a tropical environment. Br Vet J 125(3):112–120. https://doi.org/10.1016/s0007-1935(17)49058-0
Romanovsky AA (2014) Skin temperature: its role in thermoregulation. Acta Physiol 210:498–507. https://doi.org/10.1111/apha.12231
Sadis S, Hickey E, Weber LA (1988) Effect of heat shock on RNA metabolism in HeLa cells. J Cell Physiol 135:377–386. https://doi.org/10.1002/jcp.1041350304
Salama AAK, Caja G, Hamzaoui S, Badaoui B, Castro-Costa A, Façanha DAE, Guilhermino MM, Bozzi R (2014) Different levels of response to heat stress in dairy goats. Small Rumin Res 121(1):73–79. https://doi.org/10.1016/j.smallrumres.2013.11.021
Scheffler TL (2022) Connecting heat tolerance and tenderness in Bos indicus influenced cattle. Animals 12:220. https://doi.org/10.3390/ani12030220
Silva WE, Leite JHGM, de Sousa JER, Costa WP, da Silva WST, Guilhermino MM, Asensio LAB, Façanha DAE (2017) Daily rhythmicity of the thermoregulatory responses of locally adapted brazilian sheep in a semiarid environment. Int J Biometeorol 61:1221–1231. https://doi.org/10.1007/s00484-016-1300-2
Singh M, More T, Rai AK (1980) Heat tolerance of different genetic groups of sheep exposed to elevated temperature conditions. J Agric Sci 94(01):63. https://doi.org/10.1017/s0021859600027908
Singh AK, Upadhyay RC, Malakar DV, Kumar S, Devi R (2013) Role of animal skin in thermoregulation. In: Upadhyay RC, Sirohi S, Singh AK (eds) Climate resilient livestock and production system. Intech Printers and Publishers, India, pp 50–61
Slimen IB, Najar T, Ghram A, Abdrrabba M (2016) Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. J Anim Physiol Anim Nutr 100:401–412. https://doi.org/10.1111/jpn.12379
Smekalova EM, Gerashchenko MV, O’Connor PBF, Whittaker CA, Kauffman KJ, Fefilova AS, Zatsepin TS, Bogorad RL, Baranov PV, Langer R, Gladyshev VN, Anderson DG, Koteliansky V (2020) In vivo RNAi-mediated eIF3m knockdown affects ribosome biogenesis and transcription but has limited impact on mRNA-specific translation. Mol Therm Nucleic Acids 19:252–266. https://doi.org/10.1016/j.omtn.2019.11.009
Song JH, Kim KJ, Choi SY, Koh EJ, Park J, Lee BY (2019) Korean ginseng extract ameliorates abnormal immune response through the regulation of inflammatory constituents in Sprague Dawley rat subjected to environmental heat stress. J Ginseng R 43:252–260. https://doi.org/10.1016/j.jgr.2018.02.003
Souil E, Capon A, Mordon S, Dinh-Xuan AT, Polla BS, Bachelet M (2001) Treatment with 815-nm diode laser induces long-lasting expression of 72-kDa heat shock protein in normal rat skin. Br J Dermatol 144:260–266
Srikanth K, Kwon A, Lee E, Chung H (2017) Characterization of genes and pathways that respond to heat stress in Holstein calves through transcriptome analysis. Cell Stress Chaperones 22:29–42. https://doi.org/10.1007/s12192-016-0739-8
Swanson RM, Tait RG, Galles BM, Duffy EM, Schmidt TB, Petersen JL, Yates DT (2020) Heat stress-induced deficits in growth, metabolic efficiency, and cardiovascular function coincided with chronic systemic inflammation and hypercatecholaminemia in ractopamine-supplemented feedlot lambs. J Anim Sci 98:skaa168. https://doi.org/10.1093/jas/skaa168
Temim S, Chagneau AM, Peresson R, Tesseraud S (2000) Chronic heat exposure alters protein turnover of three different skeletal muscles in finishing broiler chickens fed 20 or 25% Protein Diets. J Nutr 130(4):813–819. https://doi.org/10.1093/jn/130.4.813
Titto CG, Veríssimo CJ, Pereira AMF, Geraldo AM, Katiki LM, Titto EAL (2016) Thermoregulatory response in hair sheep and shorn wool sheep. Small Rumin Res 144:341–345. https://doi.org/10.1016/j.smallrumres.2016.10.015
Yang JI, Li WR, Lv FH, He SG, Tian SL, Peng WF, Sun YW, ZhaoYX TuXL, 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 (2016) Whole-genome sequencing of native sheep provides insights into rapid adaptations to extreme environments. Mol Boil Evol 33(10):2576–2592
Zenobia C, Hajishengallis G (2015) Basic biology and role of interleukin-17 in immunity and inflammation. Periodontol 2000 69:142–159. https://doi.org/10.1111/prd.12083
Zhou X, Tron VA, Li G, Trotter MJ (1998) Heat shock transcription factor-1 regulates heat shock protein-72 expression in human keratinocytes exposed to ultraviolet B light. J Invest Dermatol 3:194–198
Funding
This work was supported by FAPESP (grant number 2019/12604–4; fellowship number 2019/22226–7 and 2021/07178–6) and by the Coordination for the Improvement of Higher Education Personnel (CAPES) (Financial Code 001), and National Council for Scientific and Technological Development (Financial Code 444874/2020–8), Brazil.
Author information
Authors and Affiliations
Contributions
CGT: conceptualization, formal analysis, investigation, resources, writing — original draft, writing — review and editing, project administration, and funding acquisition. MHAP: conceptualization, formal analysis, investigation, resources, writing — original draft, writing — review and editing, and supervision. HF: conceptualization and writing — original draft. KKSD: investigation. FJN: formal analysis, and writing — original draft. GBM: formal analysis and writing — original draft. MDP: writing — original draft and writing — review and editing. RM: writing — review and editing. LLC: writing — original draft.
Corresponding author
Ethics declarations
Ethics approval
The experiment was approved by the Ethics Committee on Animal Experimentation (CEUA/FZEA/USP Declaration 7498130919), considering the legal and ethical issues of the interventions performed.
Competing interests
The authors declare no competing interests.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
de Andrade Pantoja, M.H., Poleti, M.D., de Novais, F.J. et al. Skin transcriptomic analysis reveals candidate genes and pathways associated with thermotolerance in hair sheep. Int J Biometeorol 68, 435–444 (2024). https://doi.org/10.1007/s00484-023-02602-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-023-02602-4