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Mammalian body size is determined by interactions between climate, urbanization, and ecological traits

  • 1.

    Gould, S. J. Allometry and size in ontogeny and phylogeny. Biol. Rev. 41, 587–638 (1966).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 2.

    Brown, J. H. & Maurer, B. A. Body size, ecological dominance and Cope’s rule. Nature 324, 248–250 (1986).

    Article 

    Google Scholar 

  • 3.

    Brown, J. H., Marquet, P. A. & Taper, M. L. Evolution of body size: consequences of an energetic definition of fitness. Am. Nat. 142, 573–584 (1993).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 4.

    Peters, R. H. The ecological implications of body size. Cambridge University Press. (1983).

  • 5.

    White, E. P., Ernest, S. K. M., Kerkhoff, A. J. & Enquist, B. J. Relationship between body size and abundance in ecology. Trends Ecol. Evo 22, 323–330 (2007).

    Article 

    Google Scholar 

  • 6.

    Yom-Tov, Y. & Geffen, E. Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls. Biol. Rev. 86, 531–541 (2011).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 7.

    Bergmann, C. About the relationships between heat conservation and body size of animals. Goett. Stud. (original Ger.) 1, 595–708 (1847).

    Google Scholar 

  • 8.

    Ashton, K. G., Tracy, M. C. & de Queiroz, A. Is Bergmann’s rule valid for mammals? Am. Nat. 156, 390–415 (2000).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 9.

    Meiri, S. & Dayan, T. On the validity of Bergmann’s rule. J. Biogeogr. 30, 331–351 (2003).

    Article 

    Google Scholar 

  • 10.

    Riemer, K., Guralnick, R. P. & White, E. P. No general relationship between mass and temperature in endothermic species. elife 7, e27166 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 11.

    Alroy, J. A multispecies overkill simulation of the end- Pleistocene megafaunal mass extinction. Science 292, 1893–1896 (2001).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 12.

    Pineda-Munoz, S., Evans, A. & Alroy, J. The relationship between diet and body mass in terrestrial mammals. Paleobiology 42, 659–669 (2016).

    Article 

    Google Scholar 

  • 13.

    Tomassini, A., Colangelo, P., Agnelli, P., Jones, G. & Russo, D. Cranial size has increased over 133 years in a common bat, Pipistrellus kuhlii: a response to changing climate or urbanization? J. Biogeogr. 41, 944–953 (2014).

    Article 

    Google Scholar 

  • 14.

    Fischer, J. D., Cleeton, S. H., Lyons, T. P. & Miller, J. R. Urbanization and the predation paradox: the role of trophic dynamics in structuring vertebrate communities. Bioscience 62, 809–818 (2012).

    Article 

    Google Scholar 

  • 15.

    Ives, C. D. et al. Cities are hotspots for threatened species. Glob. Ecol. Biogeogr. 25, 117–126 (2016).

    Article 

    Google Scholar 

  • 16.

    Oke, T. R. The energetic basis of the urban heat island. Q. J. R. Meteorol. Soc. 108, 1–24 (1882).

    Google Scholar 

  • 17.

    Blackburn, T. M. & Hawkins, B. A. Bergmann’s rule and the mammal fauna of northern North America. Ecography 27, 715–724 (2004).

    Article 

    Google Scholar 

  • 18.

    Gardner, J. L., Peters, A., Kearney, M. R., Joseph, L. & Heinsohn, R. Declining body size: a third universal response to warming? Trends Ecol. Evol. 26, 285–291 (2011).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 19.

    Rapacciuolo, G. et al. The signature of human pressure history on the biogeography of body mass in tetrapods. Glob. Ecol. Biogeogr. 26, 1022–1034 (2017).

    Article 

    Google Scholar 

  • 20.

    Weeks, B. C. et al. Shared morphological consequences of global warming in North American migratory birds. Ecol. Lett. 23, 316–325 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 21.

    Merckx, T. et al. Body‐size shifts in aquatic and terrestrial urban communities. Nature 558, 113–116 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 22.

    Magura, T., Ferrante, M. & Lövei, G. L. Only habitat specialists become smaller with advancing urbanization. Glob. Ecol. Biogeor. 29, 1978–1987 (2020).

    Article 

    Google Scholar 

  • 23.

    Pergams, O. R. W. & Lacy, R. C. Rapid morphological and genetic change in Chicago-area Peromyscus. Mol. Ecol. 17, 450–463 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 24.

    McKinney, M. L. Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst. 11, 161–176 (2008).

    Article 

    Google Scholar 

  • 25.

    McNab, B. K. Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 164, 13–23 (2010).

    PubMed 
    Article 

    Google Scholar 

  • 26.

    Schmidt, N. M. & Jensen, P. M. Changes in mammalian body length over 175 years – adaptations to a fragmented landscape? Conserv. Ecol. 72, 6 (2003).

    Google Scholar 

  • 27.

    Schmidt, N. M. & Jensen, P. M. Concomitant patterns in avian and mammalian body length changes in Denmark. Ecol. Soc. 10, 5 (2005).

    Article 

    Google Scholar 

  • 28.

    Nowak, R. M. Walker’s mammals of the world. Baltimore: The Johns Hopkins University Press. (1999).

  • 29.

    Lindstedt, S. L. & Boyce, M. S. Seasonality, fasting endurance, and body size in mammals. Am. Nat. 125, 873–878 (1985).

    Article 

    Google Scholar 

  • 30.

    McCain, C. M. & King, S. R. B. Body size and activity times mediate mammalian responses to climate change. Glob. Change Biol. 20, 1760–1769 (2014).

    Article 

    Google Scholar 

  • 31.

    Naya, D. E., Naya, H. & Cook, J. Climate change and body size trends in aquatic and terrestrial endotherms: does habitat matter? PLoS ONE 12, e0183051 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 32.

    Johnson, G. E. Hibernation in mammals. Q. Rev. Biol. 6, 439–461 (1931).

    Article 

    Google Scholar 

  • 33.

    Terrien, J., Perret, M. & Aujard, F. Behavioral thermoregulation in mammals: a review. Front. Biosci. 16, 1428–1444 (2011).

    Article 

    Google Scholar 

  • 34.

    Kuussaari, M. et al. Butterfly species’ responses to urbanization: differing effects of human population density and built-up area. Urban Ecosyst. 24, 515–527 (2021).

    Article 

    Google Scholar 

  • 35.

    McNab, B. K. Food habits, energetics, and the population biology of mammals. Am. Nat. 116, 106–124 (1980).

    Article 

    Google Scholar 

  • 36.

    Guralnick, R., Hantak, M. M., Li, D. & McLean, B. S. Body size trends in response to climate and urbanization in the widespread North American deer mouse, Peromyscus maniculatus. Sci. Rep. 10, 8882 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 37.

    Robinette, W. L., Baer, C. H., Pillmore, R. E. & Knittle, C. E. Effects of nutritional change on captive mule deer. J. Wildl. Manag. 37, 312–326 (1973).

    Article 

    Google Scholar 

  • 38.

    Beckmann, J. P. & Berger, J. Using black bears to test ideal-free distribution models experimentally. J. Mammal. 84, 594–606 (2003).

    Article 

    Google Scholar 

  • 39.

    Liow, L. H., Fortelius, M., Lintulaakso, K., Mannila, H. & Stenseth, N. C. Lower extinction risk in sleep-or-hide mammals. Am. Nat. 173, 264–272 (2009).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 40.

    Eastman, L. M., Morelli, T. L., Rowe, K. C., Conroy, C. J. & Moritz, C. Size increase in high elevation ground squirrels over the last century. Glob. Change Biol. 18, 1499–1508 (2012).

    Article 

    Google Scholar 

  • 41.

    Cardillo, M. et al. Multiple causes of high extinction risk in large mammal species. Science 309, 1239–1241 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 42.

    Huey, R. B. et al. Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos. Trans. R. Soc. B 367, 1665–1679 (2012).

    Article 

    Google Scholar 

  • 43.

    Scheffers, B. R., Edward, D. P., Diesmos, A., William, S. E. & Evans, T. A. Microhabitats reduce animal’s exposure to climate extremes. Glob. Change Biol. 20, 495–503 (2014).

    Article 

    Google Scholar 

  • 44.

    Smith, F. A., Betancourt, J. L. & Brown, J. H. Evolution of body size in the woodrat over the past 25,000 years of climate change. Science 270, 2012–2014 (1995).

    CAS 
    Article 

    Google Scholar 

  • 45.

    Sheridan, J. A. & Bickford, D. Shrinking body size as an ecological response to climate change. Nat. Clim. Change 1, 401–406 (2011).

    Article 

    Google Scholar 

  • 46.

    Gohli, J. & Voje, K. L. An interspecific assessment of Bergmann’s rule in 22 mammalian families. BMC Evolut. Biol. 16, 222 (2016).

    Article 

    Google Scholar 

  • 47.

    Babinska-Werka, J. Food of the striped field mouse in different types of urban areas. Acta Theriol. 26, 285–299 (1981).

    Article 

    Google Scholar 

  • 48.

    Brown, J. S., Kotler, B. P. & Porter, W. P. How foraging allometries are resource dynamics could explain Bergmann’s rule and the body-size diet relationship in mammals. Oikos 126, 224–230 (2017).

    Article 

    Google Scholar 

  • 49.

    Santini, L. et al. One strategy does not fit all: Determinants of urban adaptation in mammals. Ecol. Lett. 22, 365–376 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 50.

    Nielsen, S. E. et al. Environmental, biological and anthropogenic effects on grizzly bear body size: temporal and spatial considerations. BMC Ecol. 13, 31 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 51.

    Dahirel, M., De Cock, M., Vantieghem, P. & Bonte, D. Urbanization-driven changes in web building and body size in an orb web spider. J. Anim. Ecol. 88, 79–91 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 52.

    Hart, M. A. & Sailor, D. J. Quantifying the influence of land-use and surface characteristics on spatial variability in the urban heat island. Theor. Appl. Climatol. 95, 397–406 (2009).

    Article 

    Google Scholar 

  • 53.

    Yom-Tov, Y. Body sizes of carnivores commensal with humans have increased over the past 50 years. Funct. Ecol. 17, 323–327 (2003).

    Article 

    Google Scholar 

  • 54.

    Bateman, P. W. & Fleming, P. A. Big city life: carnivores in urban environments. J. Zool. 287, 1–23 (2012).

    Article 

    Google Scholar 

  • 55.

    Metcalfe, N. B. & Ure, S. E. Diurnal variation in flight performance and hence potential predation risk in small birds. Proc. R. Soc. B Biol. Sci. 261, 395–400 (1995).

    Article 

    Google Scholar 

  • 56.

    Kullberg, C., Fransson, T. & Jakobsson, S. Impaired predator evasion in fat blackcaps (Sylvia atricapilla). Proc. R. Soc. B Biol. Sci. 263, 1671–1675 (1996).

    Article 

    Google Scholar 

  • 57.

    Downes, S. Trading heat and food for safety: costs of predator avoidance in a lizard. Ecology 82, 2870–2881 (2001).

    Article 

    Google Scholar 

  • 58.

    Macleod, R., Gosler, A. G. & Cresswell, W. Diurnal mass gain strategies and perceived predation risk in the great tit Parus major. J. Anim. Ecol. 74, 956–964 (2005).

    Article 

    Google Scholar 

  • 59.

    Harris, S. E. & Munshi-South, J. Signatures of positive selection and local adaptation to urbanization in white-footed mice (Peromyscus leucopus). Mol. Ecol. 26, 6336–6350 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 60.

    Ordeñana, M. A. et al. Effects of urbanization on carnivore species distribution and richness. J. Mammal. 91, 1322–1331 (2010).

    Article 

    Google Scholar 

  • 61.

    Croci, S., Butet, A. & Clergeau, P. Does urbanization filter birds on the basis of their biological traits? Condor 110, 223–240 (2008).

    Article 

    Google Scholar 

  • 62.

    Jokimäki, J., Suhonen, J., Jokimäki-Kaisanlahti, M.-L. & Carbó-Ramirez, P. Effects of urbanization on breeding birds in European towns: Impacts of species traits. Urban Ecosyst. 19, 1565–1577 (2016).

    Article 

    Google Scholar 

  • 63.

    Jung, K. & Threlfall, C. G. Trait-dependent tolerance of bats to urbanization: a global meta-analysis. Proc. R. Soc. B Biol. Sci. 285, 20181222 (2018).

    Article 

    Google Scholar 

  • 64.

    Parsons, A. W. et al. Mammal communities are larger and more diverse in moderately developed areas. eLife 7, e38012 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 65.

    Fuller, A., Mitchell, D., Maloney, S. K. & Hetem, R. S. Towards a mechanistic understanding of the responses of large terrestrial mammals to heat and aridity associated with climate change. Clim. Change Resp. 3, 10 (2016).

    Article 

    Google Scholar 

  • 66.

    Ruf, T. & Geiser, F. Daily torpor and hibernation in birds and mammals. Biol. Rev. 90, 891–926 (2015).

    PubMed 
    Article 

    Google Scholar 

  • 67.

    Suggitt, A. J. et al. Extinction risk from climate change is reduced by microclimatic buffering. Nat. Clim. Change 8, 713–717 (2018).

    Article 

    Google Scholar 

  • 68.

    Riddell, E. A. et al. Exposure to climate drives stability or collapse of desert mammal and bird communities. Science 371, 633–636 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 69.

    Law, C. J., Slater, G. J. & Mehta, R. S. Shared extremes by ectotherms and endotherms: body elongation in mustelids is associated with small size and reduced limbs. Evolution 73, 735–749 (2019).

    PubMed 
    Article 

    Google Scholar 

  • 70.

    Freckleton, R. P., Harvey, P. H. & Pagel, M. Bergmann’s rule and body size in mammals. Am. Nat. 161, 821–825 (2003).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 71.

    Nengovhela, A., Denys, C. & Taylor, P. J. Life history and habitat do not mediate temporal changes in body size due to climate warming in rodents. PeerJ 8, 9792 (2020).

    Article 

    Google Scholar 

  • 72.

    Merckx, T., Kaiser, A. & Van Dyck, H. Increased body size along urbanization gradients at both community and intraspecific level in macro-moths. Glob. Change Biol. 24, 3837–3848 (2018).

    Article 

    Google Scholar 

  • 73.

    Ohlberger, J. Climate warming and ectotherm body size – from individual physiology to community ecology. Funct. Ecol. 27, 991–1001 (2013).

    Article 

    Google Scholar 

  • 74.

    Grimm, N. B. et al. Global change and the ecology of cities. Science 319, 756–760 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 75.

    Seto, K. C., Güneralp, B. & Hutyra, L. R. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc. Natl Acad. Sci. USA 109, 16083–16088 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 76.

    Christensen, J. H. et al. Climate Phenomena and their Relevance for Future Regional Climate Change in Climate Change 2013: The Physical Science Basis. Contribution Working Group I Fifth Assess. Rep. Intergovernmental Panel Clim. Change 1–6, 1217–1308 (2013). pp.

    Google Scholar 

  • 77.

    Guralnick, R. & Constable, H. VertNet: creating a data-sharing community. Bioscience 60, 258–259 (2010).

    Article 

    Google Scholar 

  • 78.

    National Ecological Observatory Network. Data Products: DP1.10072.001. Provisional data downloaded from http://data.neonscience.org on May 10, 2019. Battelle, Boulder, CO, USA. (2019).

  • 79.

    Calhoun, J. B. North American census of small mammals. Release no. 1. Announcement of program. Rodent ecology program. Johns Hopkins University Pres. (1948).

  • 80.

    Calhoun, J. B. North American census of small mammals. Release no. 2. Annual report of census made in 1948. Rodent ecology program. Johns Hopkins University Press. (1949).

  • 81.

    Calhoun, J. B. North American census of small mammals. Release no. 3. Annual report of census made in 1949. Roscoe B. Jackson Memorial Laboratory. (1950).

  • 82.

    Calhoun, J. B. North American census of small mammals. Release no. 4. Annual report of census made in 1950. Roscoe B. Jackson Memorial Laboratory. (1951).

  • 83.

    Calhoun, J. B. Population dynamics of vertebrates. Compilations of research data. Release no. 5. 1951 Annual report – North American census of small mammals. U.S. Department of Health, Education, and Welfare, Public Health Service, National Institute of Mental Health. (1956).

  • 84.

    Calhoun, J. B. & Arata, A. A. Population dynamics of vertebrates. Compilations of research data. Release no. 6. 1952 Annual report – North American census of small mammals. U.S. Department of Health, Education, and Welfare, Public Health Service, National Institute of Mental Health. (1957).

  • 85.

    Calhoun, J. B. & Arata, A. A. Population dynamics of vertebrates. Compilations of research data. Release no. 7. 1953 Annual report – North American census of small mammals. U.S. Department of Health, Education, and Welfare, Public Health Service, National Institute of Mental Health. (1957).

  • 86.

    Calhoun, J. B. & Arata, A. A. Population dynamics of vertebrates. Compilations of research data. Release no. 8. 1954 Annual report – North American census of small mammals. U.S. Department of Health, Education, and Welfare, Public Health Service, National Institute of Mental Health. (1957).

  • 87.

    Calhoun, J. B. & Arata, A. A. Population dynamics of vertebrates. Compilations of research data. Release no. 9. 1955 and 1956 Annual report – North American census of small mammals and certain summaries for the years 1948–1956. U.S. Department of Health, Education, and Welfare, Public Health Service, National Institute of Mental Health. (1957).

  • 88.

    Guralnick, R. P. et al. The Importance of digitized biocollections as a source of trait data and a new VertNet resource. Database 2016, baw158 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 89.

    Laney, C. & Lunch, C. neonUtilities: utilities for working with NEON data. R package version 1.3.1. https://cran.r-project.org/web/packages/neonUtilities. (2019).

  • 90.

    Chapman, A. D. & Wieczorek, J. Guide to best practices for georeferencing. Global Biodiversity Information Facility. (2006).

  • 91.

    Wieczorek, J., Guo, Q., Boureau, C. & Wieczorek, C. Georeferencing calculator. http://manisnet.org/gci2.html. (2001).

  • 92.

    R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, https://www.R-project.org/. (2021).

  • 93.

    Tiwari, V. & Kashikar, A. OutlierDetection: Outlier Detection. R package version 0.1.1. https://cran.r-project.org/web/packages/OutlierDetection/index.html. (2019).

  • 94.

    Fang, Y. & Jawitz, J. W. High-resolution reconstruction of the United States human population distribution, 1790 to 2010. Sci. Data 5, 180067 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 95.

    Venter, O. et al. Global Human Footprint maps for 1993 and 2009. Sci. Data 3, 10067 (2016).

    Article 

    Google Scholar 

  • 96.

    Li, D., Stucky, B. J., Deck, J., Baiser, B. & Guralnick, R. P. The effect of urbanization on plant phenology depends on regional temperature. Nat. Ecol. Evol. 3, 1661–1667 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 97.

    Li, D. et al. Climate, urbanization, and species traits interactively drive flowering duration. Glob. Change Biol. 27, 892–903 (2021).

    Article 

    Google Scholar 

  • 98.

    PRISM Climate Group. PRISM climate data. Available at https://prism.oregonstate.edu. (2020).

  • 99.

    Upham, N. S., Esselstyn, J. A. & Jetz, W. Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLOS Biol. 17, e3000494 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 100.

    Bates, D., Maechler, M., Bolker, B. & Walker, S. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7. (2014).

  • 101.

    Brown, James H. Macroecology. University of Chicago Press. (1995).

  • 102.

    Smith, F. A. et al. Similarity of mammalian body size across the taxonomic hierarchy and across space and time. Am. Nat. 163, 672–691 (2004).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 103.

    Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: Tests in Linear Mixed Effects Models. J. Stat. Softw. 82, 1–26 (2017).

    Article 

    Google Scholar 

  • 104.

    Barton, K. Package ‘MuMIn’. Model selection and model averaging based on information criteria. R package version 3.2.4. http://cran.r-project.org/web/packages/MuMIn/index.html. (2012).

  • 105.

    Li, D., Dinnage, R., Helmus, M. & Ives, A. phyr: An R package for phylogenetic species‐distribution modelling in ecological communities. Methods Ecol. Evol. 11, 1455–1463 (2020).

    Article 

    Google Scholar 

  • 106.

    Ives, A. R. & Li, D. rr2: an R package to calculate R2s for regression models. J. Open Source Softw. 3, 1028 (2018).

    Article 

    Google Scholar 


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