Abstract
Bergmann’s Rule (i.e., the tendency of body size to increase with decreasing environmental temperature) was originally explained by a mechanism that is unique to endotherms. Nevertheless, geographic variation of body size of ectotherms, including snakes, is increasingly studied, and some claim that the rule should apply to ectotherms, or to thermoregulating ectotherms. Such studies usually focus on assemblages or on species in a region, but mostly ignore species’ ecological and biological traits when seeking biogeographic patterns. We examined the relationship between environmental temperatures and body size of 146 Australian snake species. We examined this relationship while considering the effects of ecological traits (activity time and habitat use), climatic variables which are thought to influence snake body size, and shared ancestry. Our finding suggest that Bergmann’s Rule is not a valid generalization across species of Australian snakes. Furthermore, ecological traits greatly influence the relationship between snake body size and environmental temperature. Body size of fossorial species decreases with environmental temperature, whereas body size of nocturnal, surface active species increases. Body size of diurnal, surface active species is not related to environmental temperature. Our results indicate that lumping all species in a clade together is misleading, and that ecological traits profoundly affect the geographic variation of snake body size. Though environmental temperature generally does not exert a strong selective force on snake body size, this relationship differs for taxa exhibiting different ecological traits.
Similar content being viewed by others
References
Alexander, G. (2007). Thermal biology of the Southern African Python (Python natalensis): Does temperature limit its distribution? In R. W. Henderson & R. Powell (Eds.), Biology of the boas and pythons (pp. 51–70). Eagle Mountain, UT: Eagle Mountain.
Amarello, M., Novak, E. M., Taylor, E. N., Schuett, G. W., Repp, R. A., Rosen, P. C., et al. (2010). Potential environmental influence on variation in body size and sexual size dimorphism among Arizona populations of the western diamond-backed rattlesnake (Crotalus atrox). Journal of Arid Environments, 74(11), 1443–1449.
Ashton, K. G. (2001). Body size variation among mainland populations of the western rattlesnake (Crotalus viridis). Evolution, 55(12), 2523–2533.
Ashton, K. G., & Feldman, C. R. (2003). Bergmann’s rule in nonavian reptiles: Turtles follow it, lizards and snakes reverse it. Evolution, 57(5), 1151–1163.
Beaupre, S. J. (1995). Effects of geographically variable thermal environment on bioenergetics of mottled rock rattlesnakes. Ecology, 76, 1655–1665.
Bergmann, K. G. L. C. (1847). Ueber die Verhaltnisse der Warmeokonomie der thiere zu ihrer grosse. Gottinger studien, 3, 595–708.
Blackburn, T. M., Gaston, K. J., & Loder, N. (1999). Geographic gradients in body size: A clarification of Bergmann’s rule. Diversity and Distribution, 5(4), 165–174.
Blackburn, T. M., & Hawkins, B. A. (2004). Bergmann’s rule and the mammal fauna of northern North America. Ecography, 27(6), 715–724.
Blouin-Demers, G., Prior, K. A., & Weatherhead, P. J. (2002). Comparative demography of black rat snakes (Elaphe obsoleta) in Ontario and Maryland. Journal of Zoology, 256(1), 1–10.
Boback, S. M., & Guyer, C. (2003). Empirical evidence for an optimal body size in snakes. Evolution, 57(2), 345–351.
Bonnet, X., Pearson, D., Ladyman, M., Lourdais, O., & Bradshaw, D. (2002). ‘Heaven’ for serpents? A mark-recapture study of tiger snakes (Notechis scutatus) on Carnac Island, Western Australia. Austral Ecology, 27(4), 442–450.
Boyce, M. S. (1979). Seasonality and patterns of natural selection for life histories. The American Naturalist, 114(4), 569–583.
Cardillo, M. (2002). Body size and latitudinal gradients in regional diversity of New World birds. Global Ecology and Biogeography, 11(1), 59–65.
Case, T. J. (1978). A general explanation for insular body size trends in terrestrial vertebrates. Ecology, 59, 1–18.
Cvetkovic, D., Tomasevic, N., Ficetola, G. F., Crnobrnja-Isailovic, J., & Miaud, C. (2009). Bergmann’s rule in amphibians: Combining demographic and ecological parameters to explain body size variation among populations in the common toad Bufo bufo. Journal of Zoological Systematics and Evolutionary Research, 47(2), 171–180.
ESRI (Environmental Systems Resource Institute). (2009). ArcGIS 9.3.1. Redlands, CA: ESRI.
Fearn, S., Schwarzkopf, L., Shine, R. (2005). Giant snakes in tropical forests: A field study of the Australian scrub python, Morelia kinghorni. Wildlife Research 32(2), 193–201.
Feldman, A., & Meiri, M. (2013). Length–mass allometry in snakes. Biological Journal of the Linnean Society, 108(1), 161–172.
Finkler, M. S., & Claussen, D. L. (1999). Influence of temperature, body size, and inter-individual variation on forced and voluntary swimming and crawling speeds in Nerodia sipedon and Regina septemvittata. Journal of Herpetology, 33, 62–71.
Fisher, J. A. D., Frank, K. T., & Leggett, W. C. (2010). Global variation in marine fish body size and its role in biodiversity—ecosystem functioning. Marine Ecology Progress Series, 405, 1–13.
Franca, F. G. R., Mesquita, D. O., Nogueira, C. C., & Araujo, A. F. B. (2008). Phylogeny and ecology determine morphological structure in a snake assemblage in the Central Brazilian Cerrado. Copeia, 2008(1), 23–38.
Gaston, K. J., & Chown, S. L. (2013). Macroecological patterns in insect body size. In F. A. Smith & S. K. Lyons (Eds.), Body size: Linking pattern and process across space, time and taxonomic group (pp. 13–61). Chicago: University of Chicago Press.
Hedges, S. B. (1985). The influence of size and phylogeny on life history variation in reptiles: A response to Stearns. The American Naturalist, 126(2), 258–260.
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25(15), 1965–1978.
Huey, R. B., Peterson, C. R., Arnold, S. J., & Porter, W. P. (1989). Hot rocks and not-so-hot rocks: Retreat-site selection by garter snakes and its thermal consequences. Ecology, 70(4), 931–944.
Huston, M. A., & Wolverton, S. (2011). Regulation of animal size by eNPP, Bergmann’s rule, and related phenomena. Ecological Monographs, 81(3), 349–405.
Imhoff, M. L., Bounoua, L., Ricketts, T., Loucks, C., Harriss, R., & Lawrence, W. T. (2004). Global patterns in human consumption of net primary production. Nature, 429(6994), 870–873.
James, F. C. (1970). Geographic size variation in birds and its relationship to climate. Ecology, 51, 365–390.
Kearney, M., Shine, R., & Porter, W. P. (2009). The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proceedings of the National Academy of Sciences, 106(10), 3835–3840.
King, R. B. (1989). Body size variation among island and mainland snake populations. Herpetologica, 45, 84–88.
Kubota, U., Loyola, R. D., Almeida, A. M., Carvalho, D. A., & Lewinsohn, T. M. (2007). Body size and host range co-determine the altitudinal distribution of Neotropical tephritid flies. Global Ecology and Biogeography, 16(5), 632–639.
Lillywhite, H. B. (1987). Temperature, energetic, and physiological ecology. In R. A. Seigal, J. T. Collins, & S. S. Novak (Eds.), Snakes: Ecology and evolutionary biology (pp. 422–477). New York: Macmillan.
Lindsey, C. C. (1966). Body sizes of poikilotherms vertebrates at different latitudes. Evolution, 20, 456–465.
Martins, M., Araujo, M. S., Sawaya, R. J., & Nunes, R. (2001). Diversity and evolution of macrohabitat use, body size and morphology in a monophyletic group of Neotropical pitvipers (Bothrops). Journal of Zoology, 254(4), 529–538.
Mayr, E. (1956). Geographical character gradients and climatic adaptation. Evolution, 10(1), 105–108.
McGill, B. J., Enquist, B. J., Weiher, E., & Westoby, M. (2006). Rebuilding community ecology from functional traits. Trends in Ecology & Evolution, 21(4), 178–185.
McNab, B. K. (1971). On the ecological significance of Bergmann’s rule. Ecology, 52, 845–854.
McNab, B. K. (2010). Geographic and temporal correlations of mammalian size reconsidered: A resource rule. Oecologia, 164(1), 13–23.
Meik, J. M., Lawing, A. M., & Pires-daSilva, A. (2010). Body size evolution in insular speckled rattlesnakes (Viperidae: Crotalus mitchellii). PLoS One, 5(3), e9524.
Meiri, S. (2010). Length-weight allometries in lizards. Journal of Zoology, 281(3), 218–226.
Meiri, S. (2011). Bergmann’s Rule—What’s in a name? Global Ecology and Biogeography, 20(1), 203–207.
Meiri, S., & Dayan, T. (2003). On the validity of Bergmann’s rule. Journal of Biogeography, 30(3), 331–351.
Meiri, S., Meijaard, E., Wich, S., Groves, C., & Helgen, K. (2008). Mammals of Borneo—Small size on a large island. Journal of Biogeography, 35(6), 1087–1094.
Meiri, S., & Thomas, G. (2007). The geography of body size—Challenges of the interspecific approach. Global Ecology and Biogeography, 16(6), 689–693.
Millar, J. S., & Hickling, G. J. (1990). Fasting endurance and the evolution of mammalian body size. Functional Ecology, 4(1), 5–12.
Olalla-Tarraga, M. A. (2011). “Nullius in Bergmann” or the pluralistic approach to ecogeographical rules: A reply to Watt et al. (2010). Oikos, 120(10), 1441–1444.
Olalla-Tarraga, M. A., Rodriguez, M. A., & Hawkins, B. A. (2006). Broad-scale patterns of body size in squamate reptiles of Europe and North America. Journal of Biogeography, 33(5), 781–793.
Olson, V., Davies, R. G., Orme, C. D. L., Thomas, G. H., Meiri, S., Blackburn, T. M., et al. (2009). Global biogeography and ecology of body size in birds. Ecology Letters, 12(3), 249–259.
Orme, C. D. L., Freckleton, R. P., Thomas, G. H., Petzoldt, T., Fritz, S. A., & Isaac, N. (2011). Caper: Comparative analyses of phylogenetics and evolution in R. http://cran.r-project.org/web/packages/caper/index.html.
Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401(6756), 877–884.
Pearson, D., Shine, R., & Williams, A. (2003). Thermal biology of large snakes in cool climates: A radio-telemetric study of carpet pythons (Morelia spilota imbricata) in south-western Australia. Journal of Thermal Biology, 28(2), 117–131.
Peterson, C. R., Gibson, A. R., & Dorcas, M. E. (1993). Snake thermal ecology: The causes and consequences of body-temperature variation. In R. A. Seigal & J. T. Collins (Eds.), Snakes: Ecology and behavior (pp. 241–314). New York: McGraw-Hill.
Pincheira-Donoso, D. (2010). The balance between predictions and evidence and the search for universal macroecological patterns: Taking Bergmann’s rule back to its endothermic origin. Theory in Biosciences, 129(4), 247–253.
Pincheira-Donoso, D., Hodgson, D. J., & Tregenza, T. (2008). The evolution of body size under environmental gradients in ectotherms: Why should Bergmann’s rule apply to lizards? BMC Evolutionary Biology, 8(1), 68.
Pincheira-Donoso, D., & Meiri, S. (2013). An intercontinental analysis of climate-driven body size clines in reptiles: No support for patterns, no signals of processes. Evolutionary Biology,. doi:10.1007/s11692-013-9232-9.
R Development Core Team. (2013). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
Rambaut, A. (2010). FigTree, version 1.3.1. Edinburgh: Institute of Evolutionary Biology, University of Edinburgh.
Ray, C. (1960). The application of Bergmann’s and Allen’s rules to the poikilotherms. Journal of Morphology, 106(1), 85–108.
Rensch, B. (1938). Some problems of geographical variation and species formation. Proceedings of the Linnean Society of London, 150, 275–285.
Rosenzweig, M. L. (1968). The strategy of body size in mammalian carnivores. American Midland Naturalist, 80, 299–315.
Schwaner, T. D. (1989). A field study of thermoregulation in black tiger snakes (Notechis ater niger: Elapidae) on the Franklin Islands, South Australia. Herpetologica, 45(4), 393–401.
Schwaner, T. D., & Sarre, S. D. (1990). Body size and sexual dimorphism in mainland and island tiger snakes. Journal of Herpetology, 24, 320–322.
Seebacher, F., & Shine, R. (2004). Evaluating thermoregulation in reptiles: The fallacy of the inappropriately applied method. Physiological and Biochemical Zoology, 77(4), 688–695.
Shelomi, R. (2012). Where are we now? Bergmann’s rule sensu lato in insects. The American Naturalist, 180(4), 511–519.
Shine, R. (1991). Australian snakes: A natural history. Sydney: Reed New Holland.
Shine, R., Harlow, P. S., Elphick, M. J., Olsson, M. M., & Mason, R. T. (2000). Conflicts between courtship and thermoregulation: The thermal ecology of amorous male garter snakes (Thamnophis sirtalis parietalis, Colubridae). Physiological and Biochemical Zoology, 73(4), 508–516.
Shine, R., Sun, L. X., Kearney, M., & Fitzgerald, M. (2002). Thermal correlates of foraging-site selection by Chinese pit-vipers (Gloydius shedaoensis, Viperidae). Journal of Thermal Biology, 27(5), 405–412.
Sinervo, B., Mendez-De-La-Cruz, F., Miles, D. B., Heulin, B., Bastiaans, E., Villagrán-Santa Cruz, M., et al. (2010). Erosion of lizard diversity by climate change and altered thermal niches. Science, 328(5980), 894–899.
Spotila, J. R., Lommen, P. W., Bakken, G. S., & Gates, D. M. (1973). A mathematical model for body temperatures of large reptiles: Implications for dinosaur ecology. The American Naturalist, 107, 391–404.
Terribile, L. C., Olalla-Tarraga, M. A., Diniz-Filho, J. A. F., & Rodriguez, M. A. (2009). Ecological and evolutionary components of body size: Geographic variation of venomous snakes at the global scale. Biological Journal of the Linnean Society, 98(1), 94–109.
Uetz, P. (2013). The reptile database. http://reptile-database.reptarium.cz.
Ulrich, W., & Fiera, C. (2010). Environmental correlates of body size distributions of European springtails (Hexapoda: Collembola). Global Ecology and Biogeography, 19(6), 905–915.
Volynchik, S. (2012). Morphological variability in Vipera palaestinae along an environmental gradient. Asian Herpetological Research, 3(3), 227–239.
Watt, C., Mitchell, S., & Salewski, V. (2010). Bergmann’s rule; a concept cluster? Oikos, 119(1), 89–100.
Webb, J. K., & Shine, R. (1998). Thermoregulation by a nocturnal elapid snake (Hoplocephalus bungaroides) in southeastern Australia. Physiological Zoology, 71(6), 680–692.
Whitaker, P. B., & Shine, R. (2002). Thermal biology and activity patterns of the eastern brown snake (Pseudonaja textilis): A radiotelemetric study. Herpetologica, 58(4), 436–452.
Wilson, S., & Swan, G. (2010). A complete guide to reptiles of Australia (3rd ed.). Sydney: New Holland.
Winne, C., Ryan, Y. J., Leiden, Y., & Dorcas, M. E. (2001). Evaporative water loss in two Natricine snakes, Nerodia fasciata and Seminatrix pygaea. Journal of Herpetology, 35(1), 129–133.
Yom-Tov, Y., & Geffen, E. (2011). Recent spatial and temporal changes in body size of terrestrial vertebrates: Probable causes and pitfalls. Biological Reviews, 86(2), 531–541.
Acknowledgments
We thank Yuval Itescu, Miguel Angel Olalla-Tarraga, Daniel Pincheira-Donoso, Xavier Bonnet and an anonymous referee for insightful comments on an earlier draft of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Feldman, A., Meiri, S. Australian Snakes Do Not Follow Bergmann’s Rule. Evol Biol 41, 327–335 (2014). https://doi.org/10.1007/s11692-014-9271-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11692-014-9271-x