Academic Journal
Overwintering Strategies Drive Climate Change Impacts on Body Mass in Northern Mammals.
| Τίτλος: | Overwintering Strategies Drive Climate Change Impacts on Body Mass in Northern Mammals. |
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| Συγγραφείς: | Leach O; Department of Biology, Memorial University of Newfoundland and Labrador, St. John's, Newfoundland and Labrador, Canada., Peers MJL; Department of Biology, Memorial University of Newfoundland and Labrador, St. John's, Newfoundland and Labrador, Canada., Earle A; Department of Biology, Memorial University of Newfoundland and Labrador, St. John's, Newfoundland and Labrador, Canada., Majchrzak YN; Department of Biology, Memorial University of Newfoundland and Labrador, St. John's, Newfoundland and Labrador, Canada., Boonstra R; Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada., Boutin S; Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada., Murray DL; Department of Biology, Trent University, Peterborough, Ontario, Canada., Jung TS; Department of Environment, Government of Yukon, Whitehorse, Yukon, Canada.; Department of Renewable Resources, University of Alberta, Edmonton, Alberta, Canada., Gilbert BS; Applied Science and Management, Yukon University, Whitehorse, Yukon, Canada., Kenney AJ; Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada., Wal EV; Department of Biology, Memorial University of Newfoundland and Labrador, St. John's, Newfoundland and Labrador, Canada. |
| Πηγή: | Global change biology [Glob Chang Biol] 2026 Oct; Vol. 32 (10), pp. e71132. |
| Τύπος έκδοσης: | Journal Article |
| Γλώσσα: | English |
| Στοιχεία περιοδικού: | Publisher: Blackwell Pub Country of Publication: England NLM ID: 9888746 Publication Model: Print Cited Medium: Internet ISSN: 1365-2486 (Electronic) Linking ISSN: 13541013 NLM ISO Abbreviation: Glob Chang Biol Subsets: MEDLINE |
| Imprint Name(s): | Publication: Original Publication: Oxford, UK : Blackwell Science, 1995- |
| Ιατρικοί όροι (MeSH): | Arvicolinae*/physiology , Peromyscus*/physiology , Hares*/physiology , Climate Change* , Body Weight*, Animals ; Seasons ; Yukon Territory ; Temperature ; Body Size |
| Περίληψη: | Climate change drives variable shifts in mammalian body sizes, yet the mechanisms underlying this variation remain unclear. Two explanations prevail: (1) higher temperatures reduce thermal constraints, favouring smaller bodies; or (2) warming enhances primary productivity, supporting larger bodies. We propose that species' overwintering strategies, which mitigate exposure to winter temperatures, determine which mechanism predominates. Using ~50 years of body mass data, we tested these hypotheses in three small mammals with contrasting natural histories in the rapidly warming Yukon, Canada. Snowshoe hares (Lepus americanus), exposed to ambient winter conditions, declined in mass over time and responded negatively to temperature and snow. In subnivean species, deer mice (Peromyscus maniculatus) showed no long-term trend but increased body mass with growing degree days, whereas red-backed voles (Clethrionomys rutilus) increased with temperature and snow. The results demonstrate that overwintering ecology mediates climate-driven body mass change, emphasizing the role of natural history in shaping species' responses to warming. (© 2026 John Wiley & Sons Ltd.) |
| References: | Aitchison, C. W. 2001. “The Effect of Snow Cover on Small Animals.” In Snow Ecology: An Interdisciplinary Examination of Snow Covered Ecosystems, edited by H. G. Jones, J. W. Pomeroy, D. A. Walker, and R. W. Hoham, 229–265. Cambridge University Press. Bergmann, C. 1848. Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Vandenhoeck und Ruprecht. Black, H. C. 1965. “An Analysis of a Population of Snowshoe Hares, Lepus americanus washingtonii Baird, in Western Oregon.” Ph.D. thesis, Oregon State University, Corvallis. Blackburn, T. M., K. J. Gaston, and N. Loder. 1999. “Geographic Gradients in Body Size: A Clarification of Bergmann's Rule.” Diversity and Distributions 5, no. 4: 165–174. Blackburn, T. M., P. H. Harvey, and M. D. Pagel. 1990. “Species Number, Population Density and Body Size Relationships in Natural Communities.” Journal of Animal Ecology 59, no. 1: 335–345. Boonstra, R., and C. Krebs. 2006. “Population Limitation of the Northern Red‐Backed Vole in the Boreal Forests of Northern Canada.” Journal of Animal Ecology 75, no. 6: 1269–1284. Boonstra, R., C. J. Krebs, S. B. Gilbert, and S. Schweiger. 2001. “Herbivores—Voles and Mice.” In Ecosystem Dynamics of the Boreal Forest: The Kluane Project, 216–235. Oxford University Press. Boutin, S., C. J. Krebs, R. Boonstra, et al. 1995. “Population Changes of the Vertebrate Community During a Snowshoe Hare Cycle in Canada's Boreal Forest.” Oikos 74, no. 1: 69–80. Boutin, S., and J. E. Lane. 2014. “Climate Change and Mammals: Evolutionary Versus Plastic Responses.” Evolutionary Applications 7, no. 1: 29–41. Brooks, M. E., K. Kristensen, K. J. Van Benthem, et al. 2017. “glmmTMB Balances Speed and Flexibility Among Packages for Zero‐Inflated Generalized Linear Mixed Modeling.” R Journal 9, no. 2: 378–400. Bush, E., and D. S. Lemmen, eds. 2019. Canada's Changing Climate Report, 444. Government of Canada. Calvin, K., D. Dasgupta, G. Krinner, et al. 2023. Climate Change 2023: Synthesis Report. Contribution of Working Groups I, II and III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change, edited by Core Writing Team, H. Lee, and J. Romero. IPCC. ClimateData.ca. Accessed February (2025). Dale, M., S. Francis, C. J. Krebs, and N. Vilis. 2001. “Plan Dynamics—Trees.” In Ecosystem Dynamics of the Boreal Forest: The Kluane Project, 117–135. Oxford University Press. Davy, C. M., V. Von Zuben, P. M. Kukka, B. Gerber, B. G. Slough, and T. S. Jung. 2022. “Rapidly Declining Body Size in an Insectivorous Bat Is Associated With Increased Precipitation and Decreased Survival.” Ecological Applications 32, no. 7: e2639. Dillon, M. E., G. Wang, and R. B. Huey. 2010. “Global Metabolic Impacts of Recent Climate Warming.” Nature 467, no. 7316: 704–706. Eastman, L. M., T. L. Morelli, K. C. Rowe, C. J. Conroy, and C. Moritz. 2012. “Size Increase in High Elevation Ground Squirrels Over the Last Century.” Global Change Biology 18, no. 5: 1499–1508. Ellsworth, E., M. R. Boudreau, K. Nagy, J. L. Rachlow, and D. L. Murray. 2016. “Differential Sex‐Related Winter Energetics in Free‐Ranging Snowshoe Hares (Lepus americanus).” Canadian Journal of Zoology 94, no. 2: 115–121. Fietz, J., F. Langer, and W. Schlund. 2020. “They Like It Cold, but Only in Winter: Climate‐Mediated Effects on a Hibernator.” Functional Ecology 34, no. 10: 2098–2109. Gardner, J. L., A. Peters, M. R. Kearney, L. Joseph, and R. Heinsohn. 2011. “Declining Body Size: A Third Universal Response to Warming?” Trends in Ecology & Evolution 26, no. 6: 285–291. Gienapp, P., C. Teplitsky, J. Alho, J. A. Mills, and J. Merilä. 2008. “Climate Change and Evolution: Disentangling Environmental and Genetic Responses.” Molecular Ecology 17, no. 1: 167–178. Gigliotti, L. C., N. D. Berg, R. Boonstra, et al. 2020. “Latitudinal Variation in Snowshoe Hare (Lepus americanus) Body Mass: A Test of Bergmann's Rule.” Canadian Journal of Zoology 98, no. 2: 88–95. Gilbert, B. S., and C. J. Krebs. 1981. “Effects of Extra Food on Peromyscus and Clethrionomys Populations in the Southern Yukon.” Oecologia 51, no. 3: 326–331. Gilbert, B. S., and C. J. Krebs. 1991. “Population Dynamics of Clethrionomys and Peromyscus in Southwestern Yukon 1973–1989.” Ecography 14, no. 4: 250–259. Hayes, R. D., R. Farnell, R. M. Ward, et al. 2003. “Experimental Reduction of Wolves in the Yukon: Ungulate Responses and Management Implications.” Wildlife Monographs 152: 1–35. Hodges, K., C. J. Krebs, D. Hik, C. Stefan, E. Gillis, and C. Doyle. 2001. “Herbivores – Snowshoe Hare Demography.” In Ecosystem Dynamics of the Boreal Forest: The Kluane Project, 143–177. Oxford University Press. Humphries, M. M., E. K. Studd, A. K. Menzies, and S. Boutin. 2017. “To Everything There Is a Season: Summer‐to‐Winter Food Webs and the Functional Traits of Keystone Species.” Integrative and Comparative Biology 57, no. 5: 961–976. Jolly, S. R., J. H. Gilbert, J. E. Woodford, D. Eklund, and J. N. Pauli. 2024. “Seasonal Dynamics of Small Mammal Populations: Resource Availability and Cold Exposure Interact to Govern Abundance.” Canadian Journal of Zoology 102, no. 12: 907–921. Jones, K. E., J. Bielby, M. Cardillo, et al. 2009. “PanTHERIA: A Species‐Level Database of Life History, Ecology, and Geography of Extant and Recently Extinct Mammals.” Ecology 90: 2648. Jung, T. S., B. G. Slough, C. A. McEwn, and W. G. Johnston. 2021. “Snow Tracking Provides Insights on Hunting Behaviour of Marten (Martes americana).” Mammal Research 66, no. 4: 663–688. Krebs, C. J., and R. Boonstra. 2001. “The Kluane Region.” In Ecosystem Dynamics of the Boreal Forest: The Kluane Project, 11–24. Oxford University Press. Krebs, C. J., R. Boonstra, and S. Boutin. 2018. “Using Experimentation to Understand the 10‐Year Snowshoe Hare Cycle in the Boreal Forest of North America.” Journal of Animal Ecology 87, no. 1: 87–100. Krebs, C. J., S. Boutin, R. Boonstra, et al. 2023. “Long‐Term Monitoring in the Boreal Forest Reveals High Spatio‐Temporal Variability Among Primary Ecosystem Constituents.” Frontiers in Ecology and Evolution 11: 1187222. Krebs, C. J., S. Boutin, and B. S. Gilbert. 1986. “A Natural Feeding Experiment on a Declining Snowshoe Hare Population.” Oecologia 70, no. 2: 194–197. Krebs, C. J., A. J. Kenney, B. S. Gilbert, and R. Boonstra. 2024. “Long‐Term Monitoring of Cycles in Clethrionomys rutilus in the Yukon Boreal Forest.” Integrative Zoology 19, no. 1: 27–36. Lawrence, I. E. 1955. “An Ecological Study of the Snowshoe Hare, Lepus americanus bairdii Hayden, in the Medicine Bow National Forest of Wyoming.” M.Sc. thesis, University of Wyoming, Laramie. Lindenfors, P., J. L. Gittleman, and K. E. Jones. 2007. “Sexual Size Dimorphism in Mammals.” In Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism, edited by D. J. Fairbairn, W. U. Blanckenhorn, and T. Székely, 16–26. Oxford University Press. Lüdecke, D., M. S. Ben‐Shachar, I. Patil, P. Waggoner, and D. Makowski. 2021. “Performance: An R Package for Assessment, Comparison and Testing of Statistical Models.” Journal of Open Source Software 6, no. 60: 3139. Martínez, J. J., L. V. Sommaro, N. S. Vera, M. B. Chiappero, and J. Priotto. 2024. “Contemporary Body Size Variation of Neotropical Rodents: Environmental and Genetic Effects.” Evolutionary Biology 51, no. 1: 166–178. Martins, I. S., F. Schrodt, S. A. Blowes, et al. 2023. “Widespread Shifts in Body Size Within Populations and Assemblages.” Science 381, no. 6662: 1067–1071. Mason, T. H., M. Apollonio, R. Chirichella, S. G. Willis, and P. A. Stephens. 2014. “Environmental Change and Long‐Term Body Mass Declines in an Alpine Mammal.” Frontiers in Zoology 11: 1–14. McMaster, G. S., and W. W. Wilhelm. 1997. “Growing Degree‐Days: One Equation, Two Interpretations.” Agricultural and Forest Meteorology 87, no. 4: 291–300. McNab, B. K. 2010. “Geographic and Temporal Correlations of Mammalian Size Reconsidered: A Resource Rule.” Oecologia 164, no. 1: 13–23. Meiri, S., D. Guy, T. Dayan, and D. Simberloff. 2009. “Global Change and Carnivore Body Size: Data Are Stasis.” Global Ecology and Biogeography 18, no. 2: 240–247. Merritt, J. F., and D. A. Zegers. 2002. “Maximizing Survivorship in Cold: Thermogenic Profiles of Non‐Hibernating Mammals.” Acta Theriologica 47, no. 1: 221–234. Moyes, K., D. H. Nussey, M. N. Clements, et al. 2011. “Advancing Breeding Phenology in Response to Environmental Change in a Wild Red Deer Population.” Global Change Biology 17, no. 7: 2455–2469. Ozgul, A., D. Z. Childs, M. K. Oli, et al. 2010. “Coupled Dynamics of Body Mass and Population Growth in Response to Environmental Change.” Nature 466, no. 7305: 482–485. Ozgul, A., S. Tuljapurkar, T. G. Benton, J. M. Pemberton, T. H. Clutton‐Brock, and T. Coulson. 2009. “The Dynamics of Phenotypic Change and the Shrinking Sheep of St. Kilda.” Science 325, no. 5939: 464–467. Parmesan, C., and G. Yohe. 2003. “A Globally Coherent Fingerprint of Climate Change Impacts Across Natural Systems.” Nature 421: 37–42. Pauli, J. N., B. Zuckerberg, J. P. Whiteman, and W. Porter. 2013. “The Subnivium: A Deteriorating Seasonal Refugium.” Frontiers in Ecology and the Environment 11, no. 5: 260–267. Pecl, G. T., M. B. Araújo, J. D. Bell, et al. 2017. “Biodiversity Redistribution Under Climate Change: Impacts on Ecosystems and Human Well‐Being.” Science 355, no. 6332: eaai9214. Perrin, A., and D. Jolkowski. 2022. Yukon Climate Change Indicators and Key Findings 2022, 126. YukonU Research Centre, Yukon University. Pruitt, W. O. 1960. “Animals in the Snow.” Scientific American 202, no. 1: 60–69. R Core Team. 2024. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R‐project.org/. Réale, D., M. Festa‐Bianchet, and J. Jorgenson. 1999. “Heritability of Body Mass Varies With Age and Season in Wild Bighorn Sheep.” Heredity 83: 526–532. Réale, D., A. G. McAdam, S. Boutin, and D. Berteaux. 2003. “Genetic and Plastic Responses of a Northern Mammal to Climate Change.” Proceedings of the Royal Society of London, Series B: Biological Sciences 270, no. 1515: 591–596. Scott, A. M., J. H. Gilbert, and J. N. Pauli. 2022. “Small Mammal Dynamics in Snow‐Covered Forests.” Journal of Mammalogy 103, no. 3: 680–692. Searing, K. B., M. V. Lomolino, and R. Rozzi. 2023. “Melting Climates Shrink North American Small Mammals.” Proceedings of the National Academy of Sciences of the United States of America 120, no. 50: e2310855120. Sentis, A., S. Bazin, D. S. Boukal, and R. Stoks. 2024. “Ecological Consequences of Body Size Reduction Under Warming.” Proceedings of the Biological Sciences 291, no. 2029: 20241250. Sheridan, J. A., and D. Bickford. 2011. “Shrinking Body Size as an Ecological Response to Climate Change.” Nature Climate Change 1, no. 8: 401–406. Shipley, A. A., and B. Zuckerberg. 2023. “Snow Cover Constrains the Behavioural Flexibility of a Winter‐Adapted Bird.” Ibis 165, no. 4: 1186–1200. Sih, A., M. C. Ferrari, and D. J. Harris. 2011. “Evolution and Behavioural Responses to Human‐Induced Rapid Environmental Change.” Evolutionary Applications 4, no. 2: 367–387. Slatyer, R. A., K. D. Umbers, and P. A. Arnold. 2022. “Ecological Responses to Variation in Seasonal Snow Cover.” Conservation Biology 36, no. 1: e13727. Smith, F. A., J. H. Brown, J. P. Haskell, et al. 2004. “Similarity of Mammalian Body Size Across the Taxonomic Hierarchy and Across Space and Time.” American Naturalist 163, no. 5: 672–691. Sobie, S. R., D. Ouali, C. L. Curry, and F. W. Zwiers. 2024. “Multivariate Canadian Downscaled Climate Scenarios for CMIP6 (CanDCS‐M6).” Geoscience Data Journal 11: 806–824. Stebbins, L. 1971. “Seasonal Variations in Circadian Rhythms of Deer Mice in Northwestern Canada.” Arctic 24: 124–131. Stebbins, L. 1976. “Overwintering of the Red‐Backed Vole at Edmonton, Alberta, Canada.” Journal of Mammalogy 57, no. 3: 554–561. Teplitsky, C., and V. Millien. 2014. “Climate Warming and Bergmann's Rule Through Time: Is There Any Evidence?” Evolutionary Applications 7, no. 1: 156–168. Theriot, M., L. Olson, and H. Lanier. 2024. “Accounting for Age: Uncovering the Nuanced Drivers of Mammal Body‐Size Responses to Climate Change.” Journal of Mammalogy 105: 512–523. Thompson, K. L., B. Zuckerberg, W. P. Porter, and J. N. Pauli. 2018. “The Phenology of the Subnivium.” Environmental Research Letters 13, no. 6: 064037. Thompson, K. L., B. Zuckerberg, W. P. Porter, and J. N. Pauli. 2021. “The Decline of a Hidden and Expansive Microhabitat: The Subnivium.” Frontiers in Ecology and the Environment 19, no. 5: 268–273. Verberk, W. C., D. Atkinson, K. N. Hoefnagel, A. G. Hirst, C. R. Horne, and H. Siepel. 2021. “Shrinking Body Sizes in Response to Warming: Explanations for the Temperature–Size Rule With Special Emphasis on the Role of Oxygen.” Biological Reviews 96, no. 1: 247–268. Villar, C. H., and D. E. Naya. 2018. “Climate Change and Temporal Trends in Body Size: The Case of Rodents.” Oikos 127, no. 8: 1186–1194. Vincent, L. A., X. Zhang, É. Mekis, H. Wan, and E. J. Bush. 2018. “Changes in Canada's Climate: Trends in Indices Based on Daily Temperature and Precipitation Data.” Atmosphere‐Ocean 56, no. 5: 332–349. Visser, M. E., and C. Both. 2005. “Shifts in Phenology due to Global Climate Change: The Need for a Yardstick.” Proceedings of the Royal Society B: Biological Sciences 272, no. 1581: 2561–2569. Whittaker, M. E., and V. G. Thomas. 1983. “Seasonal Levels of Fat and Protein Reserves of Snowshoe Hares in Ontario.” Canadian Journal of Zoology 61, no. 6: 1339–1345. Wickham, H., R. François, L. Henry, K. Müller, and D. Vaughan. 2023. “dplyr: A Grammar of Data Manipulation.” R Package Version 1.1.4. https://github.com/tidyverse/dplyr. Williams, C. M., H. A. L. Henry, and B. J. Sinclair. 2015. “Cold Truths: How Winter Drives Responses of Terrestrial Organisms to Climate Change.” Biological Reviews of the Cambridge Philosophical Society 90, no. 1: 214–235. Wilson, A. J., J. M. Pemberton, J. G. Pilkington, T. H. Clutton‐Brock, D. W. Coltman, and L. E. B. Kruuk. 2007. “Quantitative Genetics of Growth and Cryptic Evolution of Body Size in an Island Population.” Evolutionary Ecology 21, no. 3: 337–356. Yom‐Tov, Y., and S. Yom‐Tov. 2004. “Climatic Change and Body Size in Two Species of Japanese Rodents.” Biological Journal of the Linnean Society 82, no. 2: 263–267. Yom‐Tov, Y., S. Yom‐Tov, and G. Jarrell. 2008. “Recent Increase in Body Size of the American Marten Martes americana in Alaska.” Biological Journal of the Linnean Society 93: 701–707. Yom‐Tov, Y., S. Yom‐Tov, D. MacDonald, and E. Yom‐Tov. 2007. “Population Cycles and Changes in Body Size of the Lynx in Alaska.” Oecologia 152: 239–244. Youngflesh, C., J. F. Saracco, R. B. Siegel, and M. W. Tingley. 2022. “Abiotic Conditions Shape Spatial and Temporal Morphological Variation in North American Birds.” Nature Ecology & Evolution 6: 1860–1870. Zuercher, G. L., D. D. Roby, and E. A. Rexstad. 1999. “Seasonal Changes in Body Mass, Composition, and Organs of Northern Red‐Backed Voles in Interior Alaska.” Journal of Mammalogy 80, no. 2: 443–459. |
| Grant Information: | Natural Sciences and Engineering Research Council of Canada; Polar Knowledge Canada; Weston Family Foundation |
| Contributed Indexing: | Keywords: Bergmann's rule; body mass; boreal forest; climate change; deer mouse; red‐backed vole; snow; snowshoe hare |
| Entry Date(s): | Date Created: 20260930 Date Completed: 20260930 Latest Revision: 20260930 |
| Update Code: | 20260930 |
| DOI: | 10.1111/gcb.71132 |
| PMID: | 42812007 |
| Βάση Δεδομένων: | MEDLINE |
| ISSN: | 1365-2486 |
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| DOI: | 10.1111/gcb.71132 |