Sleep in the wild: the importance of individual effects and environmental conditions on sleep behaviour in wild boar

. 2024 May ; 291 (2023) : 20232115. [epub] 20240529

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38808449

Sleep serves vital physiological functions, yet how sleep in wild animals is influenced by environmental conditions is poorly understood. Here we use high-resolution biologgers to investigate sleep in wild animals over ecologically relevant time scales and quantify variability between individuals under changing conditions. We developed a robust classification for accelerometer data and measured multiple dimensions of sleep in the wild boar (Sus scrofa) over an annual cycle. In support of the hypothesis that environmental conditions determine thermoregulatory challenges, which regulate sleep, we show that sleep quantity, efficiency and quality are reduced on warmer days, sleep is less fragmented in longer and more humid days, while greater snow cover and rainfall promote sleep quality. Importantly, this longest and most detailed analysis of sleep in wild animals to date reveals large inter- and intra-individual variation. Specifically, short-sleepers sleep up to 46% less than long-sleepers but do not compensate for their short sleep through greater plasticity or quality, suggesting they may pay higher costs of sleep deprivation. Given the major role of sleep in health, our results suggest that global warming and the associated increase in extreme climatic events are likely to negatively impact sleep, and consequently health, in wildlife, particularly in nocturnal animals.

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Anafi RC, Kayser MS, Raizen DM. 2019. Exploring phylogeny to find the function of sleep. Nat. Rev. Neurosci. 20, 109-116. (10.1038/s41583-018-0098-9) PubMed DOI

Besedovsky L, Lange T, Haack M. 2019. The sleep-immune crosstalk in health and disease. Physiol. Rev. 99, 1325-1380. (10.1152/physrev.00010.2018) PubMed DOI PMC

Manzar MD, Zannat W, Hussain ME. 2014. Sleep and physiological systems: a functional perspective. Biol. Rhythm Res. 46, 195-206. (10.1080/09291016.2014.966504) DOI

Medic G, Wille M, Hemels ME. 2017. Short- and long-term health consequences of sleep disruption. Nat. Sci. Sleep 9, 151-161. (10.2147/NSS.S134864) PubMed DOI PMC

Xie L, et al. 2013. Sleep drives metabolite clearance from the adult brain. Science 342, 373-377. (10.1126/science.1241224) PubMed DOI PMC

Klinzing JG, Niethard N, Born J. 2019. Mechanisms of systems memory consolidation during sleep. Nat. Neurosci. 22, 1598-1610. (10.1038/s41593-019-0467-3) PubMed DOI

Johnsson RD, Connelly F, Gaviraghi Mussoi J, Vyssotski AL, Cain KE, Roth TC, Lesku JA. 2022. Sleep loss impairs cognitive performance and alters song output in Australian magpies. Sci. Rep. 12, 6645. (10.1038/s41598-022-10162-7) PubMed DOI PMC

Wild CJ, Nichols ES, Battista ME, Stojanoski B, Owen AM. 2018. Dissociable effects of self-reported daily sleep duration on high-level cognitive abilities. Sleep 41, zsy182. (10.1093/sleep/zsy182) PubMed DOI PMC

Sabia S, Dugravot A, Léger D, Ben Hassen C, Kivimaki M, Singh-Manoux A. 2022. Association of sleep duration at age 50, 60, and 70 years with risk of multimorbidity in the UK: 25-year follow-up of the Whitehall II cohort study. PLoS Med. 19, e1004109. (10.1371/journal.pmed.1004109) PubMed DOI PMC

Kushida CA. 2004. Sleep deprivation: basic science, physiology, and behaviour. In Lung biology in health and disease (ed. Lenfant C). Boca Raton, FL: CRC Press.

Capellini I, Preston BT, Mcnamara P, Barton RA, Nunn CL. 2010. Ecological constraints on mammmalian sleep architecture. In Evolution of sleep, pp. 12-33. Cambridge, UK: Cambridge University Press.

Campbell SS, Tobler I. 1984. Animal sleep: a review of sleep duration across phylogeny. Neurosci. Biobehav. Rev. 8, 269-300. (10.1016/0149-7634(84)90054-x) PubMed DOI

Capellini I, Barton RA, McNamara P, Preston BT, Nunn CL. 2008. Phylogenetic analysis of the ecology and evolution of mammalian sleep. Evolution 62, 1764-1776. (10.1111/j.1558-5646.2008.00392.x) PubMed DOI PMC

Capellini I, Nunn CL, McNamara P, Preston BT, Barton RA. 2008. Energetic constraints, not predation, influence the evolution of sleep patterning in mammals. Funct. Ecol. 22, 847-853. (10.1111/j.1365-2435.2008.01449.x) PubMed DOI PMC

Dingemanse NJ, Wolf M. 2013. Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim. Behav. 85, 1031-1039. (10.1016/j.anbehav.2012.12.032) DOI

van Dongen HPA, Vitellaro KM, Dinges DF. 2005. Individual differences in adult human sleep and wakefulness: leitmotif for a research agenda. Sleep 28, 479-498. (10.1093/sleep/28.4.479) PubMed DOI

Samson DR, Crittenden AN, Mabulla IA, Mabulla AZP. 2017. The evolution of human sleep: technological and cultural innovation associated with sleep-wake regulation among Hadza hunter-gatherers. J. Hum. Evol. 113, 91-102. (10.1016/j.jhevol.2017.08.005) PubMed DOI

Lyamin O, Pryaslova J, Lance V, Siegel J. 2005. Continuous activity in cetaceans after birth. Nature 435, 1177-1177. (10.1038/4351177a) PubMed DOI PMC

Gravett N, Bhagwandin A, Sutcliffe R, Landen K, Chase MJ, Lyamin OI, Siegel JM, Manger PR. 2017. Inactivity/sleep in two wild free-roaming African elephant matriarchs: does large body size make elephants the shortest mammalian sleepers? PLoS ONE 12, e0171903. (10.1371/journal.pone.0171903) PubMed DOI PMC

Ternman E, Nilsson E, Nielsen PP, Pastell M, Hanninen L, Agenas S. 2019. Rapid eye movement sleep time in dairy cows changes during the lactation cycle. J. Dairy Sci. 102, 5458-5465. (10.3168/jds.2018-15950) PubMed DOI

Harding EC, Franks NP, Wisden W. 2020. Sleep and thermoregulation. Curr. Opin. Physiol. 15, 7-13. (10.1016/j.cophys.2019.11.008) PubMed DOI PMC

Downs CT, Awuah A, Jordaan M, Magagula L, Mkhize T, Paine C, Raymond-Bourret E, Hart LA. 2015. Too hot to sleep? Sleep behaviour and surface body temperature of Wahlberg's epauletted fruit bat. PLoS ONE 10, e0119419. (10.1371/journal.pone.0119419) PubMed DOI PMC

Dewasmes G, Maho YL, Groscolas R, Robin J, Vardon G, Libert J. 2001. Effects of weather on activity and sleep in brooding king penguins (Aptenodytes patagonicus). Polar Biol. 24, 508-511. (10.1007/s003000100249) DOI

Reyes KR, Patel UA, Nunn CL, Samson DR. 2021. Gibbon sleep quantified: the influence of lunar phase and meteorological variables on activity in Hylobates moloch and Hylobates pileatus. Primates 62, 749-759. (10.1007/s10329-021-00920-y) PubMed DOI

Loftus JC, Harel R, Núñez CL, Crofoot MC. 2022. Ecological and social pressures interfere with homeostatic sleep regulation in the wild. eLife 11, e73695. (10.7554/eLife.73695) PubMed DOI PMC

Mitchell D, Snelling EP, Hetem RS, Maloney SK, Strauss WM, Fuller A. 2018. Revisiting concepts of thermal physiology: predicting responses of mammals to climate change. J. Anim. Ecol. 87, 956-973. (10.1111/1365-2656.12818) PubMed DOI

LeGates TA, Fernandez DC, Hattar S. 2014. Light as a central modulator of circadian rhythms, sleep and affect. Nat. Rev. Neurosci. 15, 443-454. (10.1038/nrn3743) PubMed DOI PMC

Yetish G, Kaplan H, Gurven M, Wood B, Pontzer H, Manger PR, Wilson C, McGregor R, Siegel JM. 2015. Natural sleep and its seasonal variations in three pre-industrial societies. Curr. Biol. 25, 2862-2868. (10.1016/j.cub.2015.09.046) PubMed DOI PMC

Samson DR, Crittenden AN, Mabulla IA, Mabulla AZP, Nunn CL. 2018. Does the moon influence sleep in small-scale societies? Sleep Health 4, 509-514. (10.1016/j.sleh.2018.08.004) PubMed DOI

Nunn CL, McNamara P, Capellini I, Preston BT, Barton RA. 2009. Primate sleep in phylogenetic perspective. In Evolution of sleep: phylogenetic and functional perspectives (eds McNamara P, Barton RA, Nunn CL). Cambridge, UK: Cambridge University Press.

Olejarz A, Faltusová M, Börger L, Güldenpfennig J, Jarský V, Ježek M, Mortlock E, Silovský V, Podgórski T. 2023. Worse sleep and increased energy expenditure yet no movement changes in sub-urban wild boar experiencing an influx of human visitors (anthropulse) during the COVID-19 pandemic. Sci. Total Environ. 879, 163106. (10.1016/j.scitotenv.2023.163106) PubMed DOI PMC

Lesku JA, Bark RJ, Martinez-Gonzalez D, Rattenborg NC, Amlaner CJ, Lima SL. 2008. Predator-induced plasticity in sleep architecture in wild-caught Norway rats (Rattus norvegicus). Behav. Brain Res. 189, 298-305. (10.1016/j.bbr.2008.01.006) PubMed DOI

Podgórski T, Baś G, Jędrzejewska B, Sönnichsen L, Śnieżko S, Jędrzejewski W, Okarma H. 2013. Spatiotemporal behavioral plasticity of wild boar (Sus scrofa) under contrasting conditions of human pressure: primeval forest and metropolitan area. J. Mammal. 94, 109-119. (10.1644/12-MAMM-A-038.1) DOI

Lo Martire V, Caruso D, Palagini L, Zoccoli G, Bastianini S. 2020. Stress & sleep: a relationship lasting a lifetime. Neurosci. Biobehav. Rev. 117, 65-77. (10.1016/j.neubiorev.2019.08.024) PubMed DOI

Williams HJ, et al. 2020. Optimizing the use of biologgers for movement ecology research. J. Anim. Ecol. 89, 186-206. (10.1111/1365-2656.13094) PubMed DOI PMC

Wilson RP, Shepard ELC, Liebsch N. 2008. Prying into the intimate details of animal lives: use of a daily diary on animals. Endangered Species Res. 4, 123-137. (10.3354/esr00064) DOI

Robert S, Dallaire A. 1986. Polygraphic analysis of the sleep-wake states and the REM sleep periodicity in domesticated pigs (Sus scrofa). Physiol. Behav. 37, 289-293. (10.1016/0031-9384(86)90235-0) PubMed DOI

Ruckebusch Y. 1972. The relevance of drowsiness in the circadian cycle of farm animals. Anim. Behav. 20, 637-643. (10.1016/S0003-3472(72)80136-2) PubMed DOI

Skinner JE, Mohr DN, Kellaway P. 1975. Sleep-stage regulation of ventricular arrhythmias in the unanesthetized pig. Circ. Res. 37, 342-349. (10.1161/01.RES.37.3.342) PubMed DOI

Kuipers M, Whatson TS. 1979. Sleep in piglets: an observational study. Appl. Anim. Ethol. 5, 145-151. (10.1016/0304-3762(79)90085-3) DOI

Bonnet MH. 2004. Sleep fragmentation. In Sleep deprivation: basic science, physiology, and behaviour (ed. Kushida CA), pp. 103-117. Boca Raton, FL: CRC Press.

Stepanski EJ. 2002. The effect of sleep fragmentation on daytime function. Sleep 25, 268-276. (10.1093/sleep/25.3.268) PubMed DOI

Cox DTC, Gaston KJ. 2023. Cathemerality: a key temporal niche. Biol. Rev. 99, 329-2347. (10.1111/brv.13024) PubMed DOI

Gordigiani L, Viviano A, Brivio F, Grignolio S, Lazzeri L, Marcon A, Mori E. 2022. Carried away by a moonlight shadow: activity of wild boar in relation to nocturnal light intensity. Mamm. Res. 67, 39-49. (10.1007/s13364-021-00610-6) DOI

Brivio F, Grignolio S, Brogi R, Benazzi M, Bertolucci C, Apollonio M. 2017. An analysis of intrinsic and extrinsic factors affecting the activity of a nocturnal species: the wild boar. Mammal. Biol. 84, 73-81. (10.1016/j.mambio.2017.01.007) DOI

Thurfjell H, Spong G, Ericsson G. 2014. Effects of weather, season, and daylight on female wild boar movement. Acta Theriologica 59, 467-472. (10.1007/s13364-014-0185-x) DOI

Drimaj J, Kamler J, Hošek M, Plhal R, Mikulka O, Zeman J, Drápela K. 2020. Reproductive potential of free-living wild boar in Central Europe. Eur. J. Wildl. Res. 66, 75. (10.1007/s10344-020-01416-8) DOI

Shepard E, et al. 2008. Identification of animal movement patterns using tri-axial accelerometry. Endanger. Species Res. 10, 47-60. (10.3354/esr00084) DOI

Watanabe YY, Rutz C. 2022. Accelerometer-based analyses of animal sleep patterns. eLife 11, e77349. (10.7554/eLife.77349) PubMed DOI PMC

Shepard ELC, Wilson RP, Halsey LG, Quintana F, Gómez Laich A, Gleiss AC, Liebsch N, Myers AE, Norman B. 2008. Derivation of body motion via appropriate smoothing of acceleration data. Aquat. Biol. 4, 235-241. (10.3354/ab00104) DOI

Qasem L, Cardew A, Wilson A, Griffiths I, Halsey LG, Shepard ELC, Gleiss AC, Wilson R. 2012. Tri-axial dynamic acceleration as a proxy for animal energy expenditure; should we be summing values or calculating the vector? PLoS ONE 7, e31187. (10.1371/journal.pone.0031187) PubMed DOI PMC

Jarský V, Palátová P, Riedl M, Zahradník D, Rinn R, Hochmalová M. 2022. Forest attendance in the times of COVID-19: a case study on the example of the Czech Republic. Int. J. Environ. Res. Public Health 19, 2529. (10.3390/ijerph19052529) PubMed DOI PMC

Hertel AG, Niemelä PT, Dingemanse NJ, Mueller T. 2020. A guide for studying among-individual behavioral variation from movement data in the wild. Mov. Ecol. 8, 30. (10.1186/s40462-020-00216-8) PubMed DOI PMC

R Core Team. 2022. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Bürkner P-C. 2018. Advanced Bayesian multilevel modeling with the R package brms. R J. 10, 395-411. (10.32614/RJ-2018-017) DOI

Stan Development Team. 2022. Stan modeling language users guide and reference manual, 2.30 edn.

Bridger D, Bonner SJ, Briffa M. 2015. Individual quality and personality: bolder males are less fecund in the hermit crab Pagurus bernhardus. Proc. R. Soc. B 282, 20142492. (10.1098/rspb.2014.2492) PubMed DOI PMC

Gelman A, Jakulin A, Pittau MG, Su Y-S. 2008. A weakly informative default prior distribution for logistic and other regression models. Ann. Appl. Stat. 2, 1360-1383.

Gelman A, Carlin J, Stern H, Rubin D. 2013. Bayesian data analysis, vol. 3. New York, NY: Chapman & Hall/CRC.

Brogi R, Apollonio M, Brivio F, Merli E, Grignolio S. 2022. Behavioural syndromes going wild: individual risk-taking behaviours of free-ranging wild boar. Anim. Behav. 194, 79-88. (10.1016/j.anbehav.2022.09.013) DOI

Stillfried M, Gras P, Busch M, Börner K, Kramer-Schadt S, Ortmann S. 2017. Wild inside: urban wild boar select natural, not anthropogenic food resources. PLoS ONE 12, e0175127. (10.1371/journal.pone.0175127) PubMed DOI PMC

Harding EC, Franks NP, Wisden W. 2019. The temperature dependence of sleep. Front. Neurosci. 13, 336. (10.3389/fnins.2019.00336) PubMed DOI PMC

Gaudiano L, Pucciarelli L, Frassanito AG, Mori E, Morimando F, Silvestri FM, Sorino R, Viviano A, Corriero G. 2022. Spatio-temporal behaviour of female wild boar in an agro-forestry–pastoral landscape of Southern Italy. Mammal Res. 67, 163-172. (10.1007/s13364-022-00617-7) DOI

Verzuh TL, Hall LE, Cufaude T, Knox L, Class C, Monteith KL. 2021. Behavioural flexibility in a heat-sensitive endotherm: the role of bed sites as thermal refuges. Anim. Behav. 178, 77-86. (10.1016/j.anbehav.2021.05.020) DOI

Galland BC, Peebles CM, Bolton DPG, Taylor BJ. 1993. Sleep state organization in the developing piglet during exposure to different thermal stimuli. Sleep 16, 610-619. (10.1093/sleep/16.7.610) PubMed DOI

Sumova A, Sladek M, Polidarova L, Novakova M, Houdek P. 2012. Circadian system from conception till adulthood. Prog. Brain Res. 199, 83-103. (10.1016/B978-0-444-59427-3.00005-8) PubMed DOI

Keuling O, Stier N, Roth M. 2008. How does hunting influence activity and spatial usage in wild boar Sus scrofa L.? Eur. J. Wildl. Res. 54, 729-737. (10.1007/s10344-008-0204-9) DOI

Festa-Bianchet M, Cote SD, Hamel S, Pelletier F. 2019. Long-term studies of bighorn sheep and mountain goats reveal fitness costs of reproduction. J. Anim. Ecol. 88, 1118-1133. (10.1111/1365-2656.13002) PubMed DOI

Harshman LG, Zera AJ. 2007. The cost of reproduction: the devil in the details. Trends Ecol. Evol. 22, 80-86. (10.1016/j.tree.2006.10.008) PubMed DOI

Tucker MA, et al. 2023. Behavioral responses of terrestrial mammals to COVID-19 lockdowns. Science 380, 1059-1064. (10.1126/science.abo6499) PubMed DOI

Dammhahn M, Dingemanse NJ, Niemelä PT, Réale D. 2018. Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life history. Behav. Ecol. Sociobiol. 72, 62. (10.1007/s00265-018-2473-y) DOI

Anderson L, Camus MF, Monteith KM, Salminen TS, Vale PF. 2022. Variation in mitochondrial DNA affects locomotor activity and sleep in Drosophila melanogaster. Heredity 129, 225-232. (10.1038/s41437-022-00554-w) PubMed DOI PMC

Tobler I. 1995. Is sleep fundamentally different between mammalian species? Behav. Brain Res. 69, 35-41. (10.1016/0166-4328(95)00025-O) PubMed DOI

Mortlock E, Silovský V, Güldenpfennig J, Faltusová M, Olejarz A, Börger L, Ježek M, Jennings DJ, Capellini I. 2024. Sleep in the wild: the importance of individual effects and environmental conditions on sleep behaviour in wild boar. Figshare. (10.6084/m9.figshare.c.7204012) PubMed DOI PMC

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