Australian Snakes Do Not Follow Bergmann’s Rule

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. 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.

    Google Scholar 

  2. 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.

    Article  Google Scholar 

  3. Ashton, K. G. (2001). Body size variation among mainland populations of the western rattlesnake (Crotalus viridis). Evolution, 55(12), 2523–2533.

    CAS  PubMed  Article  Google Scholar 

  4. 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.

    PubMed  Article  Google Scholar 

  5. Beaupre, S. J. (1995). Effects of geographically variable thermal environment on bioenergetics of mottled rock rattlesnakes. Ecology, 76, 1655–1665.

    Article  Google Scholar 

  6. Bergmann, K. G. L. C. (1847). Ueber die Verhaltnisse der Warmeokonomie der thiere zu ihrer grosse. Gottinger studien, 3, 595–708.

    Google Scholar 

  7. 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.

    Article  Google Scholar 

  8. Blackburn, T. M., & Hawkins, B. A. (2004). Bergmann’s rule and the mammal fauna of northern North America. Ecography, 27(6), 715–724.

    Article  Google Scholar 

  9. 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.

    Article  Google Scholar 

  10. Boback, S. M., & Guyer, C. (2003). Empirical evidence for an optimal body size in snakes. Evolution, 57(2), 345–351.

    PubMed  Article  Google Scholar 

  11. 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.

    Article  Google Scholar 

  12. Boyce, M. S. (1979). Seasonality and patterns of natural selection for life histories. The American Naturalist, 114(4), 569–583.

    Article  Google Scholar 

  13. Cardillo, M. (2002). Body size and latitudinal gradients in regional diversity of New World birds. Global Ecology and Biogeography, 11(1), 59–65.

    Article  Google Scholar 

  14. Case, T. J. (1978). A general explanation for insular body size trends in terrestrial vertebrates. Ecology, 59, 1–18.

    Article  Google Scholar 

  15. 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.

    Article  Google Scholar 

  16. ESRI (Environmental Systems Resource Institute). (2009). ArcGIS 9.3.1. Redlands, CA: ESRI.

  17. 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.

    Google Scholar 

  18. Feldman, A., & Meiri, M. (2013). Length–mass allometry in snakes. Biological Journal of the Linnean Society, 108(1), 161–172.

    Article  Google Scholar 

  19. 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.

    Article  Google Scholar 

  20. 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.

    Article  Google Scholar 

  21. 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.

    Article  Google Scholar 

  22. 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.

    Google Scholar 

  23. 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.

    Article  Google Scholar 

  24. 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.

    Article  Google Scholar 

  25. 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.

    Article  Google Scholar 

  26. Huston, M. A., & Wolverton, S. (2011). Regulation of animal size by eNPP, Bergmann’s rule, and related phenomena. Ecological Monographs, 81(3), 349–405.

    Article  Google Scholar 

  27. 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.

    CAS  PubMed  Article  Google Scholar 

  28. James, F. C. (1970). Geographic size variation in birds and its relationship to climate. Ecology, 51, 365–390.

    Article  Google Scholar 

  29. 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.

    CAS  Article  Google Scholar 

  30. King, R. B. (1989). Body size variation among island and mainland snake populations. Herpetologica, 45, 84–88.

    Google Scholar 

  31. 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.

    Article  Google Scholar 

  32. 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.

    Google Scholar 

  33. Lindsey, C. C. (1966). Body sizes of poikilotherms vertebrates at different latitudes. Evolution, 20, 456–465.

    Article  Google Scholar 

  34. 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.

    Article  Google Scholar 

  35. Mayr, E. (1956). Geographical character gradients and climatic adaptation. Evolution, 10(1), 105–108.

    Article  Google Scholar 

  36. 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.

    Article  Google Scholar 

  37. McNab, B. K. (1971). On the ecological significance of Bergmann’s rule. Ecology, 52, 845–854.

    Article  Google Scholar 

  38. McNab, B. K. (2010). Geographic and temporal correlations of mammalian size reconsidered: A resource rule. Oecologia, 164(1), 13–23.

    PubMed  Article  Google Scholar 

  39. 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.

    PubMed Central  PubMed  Article  Google Scholar 

  40. Meiri, S. (2010). Length-weight allometries in lizards. Journal of Zoology, 281(3), 218–226.

    Google Scholar 

  41. Meiri, S. (2011). Bergmann’s Rule—What’s in a name? Global Ecology and Biogeography, 20(1), 203–207.

    Article  Google Scholar 

  42. Meiri, S., & Dayan, T. (2003). On the validity of Bergmann’s rule. Journal of Biogeography, 30(3), 331–351.

    Article  Google Scholar 

  43. 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.

    Article  Google Scholar 

  44. Meiri, S., & Thomas, G. (2007). The geography of body size—Challenges of the interspecific approach. Global Ecology and Biogeography, 16(6), 689–693.

    Article  Google Scholar 

  45. Millar, J. S., & Hickling, G. J. (1990). Fasting endurance and the evolution of mammalian body size. Functional Ecology, 4(1), 5–12.

    Article  Google Scholar 

  46. 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.

  47. 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.

    Article  Google Scholar 

  48. 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.

    PubMed  Article  Google Scholar 

  49. 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.

  50. Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401(6756), 877–884.

    CAS  PubMed  Article  Google Scholar 

  51. 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.

    Article  Google Scholar 

  52. 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.

    Google Scholar 

  53. 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.

    PubMed  Article  Google Scholar 

  54. 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.

    PubMed Central  PubMed  Article  Google Scholar 

  55. 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.

    Google Scholar 

  56. R Development Core Team. (2013). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  57. Rambaut, A. (2010). FigTree, version 1.3.1. Edinburgh: Institute of Evolutionary Biology, University of Edinburgh.

  58. Ray, C. (1960). The application of Bergmann’s and Allen’s rules to the poikilotherms. Journal of Morphology, 106(1), 85–108.

    CAS  PubMed  Article  Google Scholar 

  59. Rensch, B. (1938). Some problems of geographical variation and species formation. Proceedings of the Linnean Society of London, 150, 275–285.

    Article  Google Scholar 

  60. Rosenzweig, M. L. (1968). The strategy of body size in mammalian carnivores. American Midland Naturalist, 80, 299–315.

    Article  Google Scholar 

  61. 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.

  62. Schwaner, T. D., & Sarre, S. D. (1990). Body size and sexual dimorphism in mainland and island tiger snakes. Journal of Herpetology, 24, 320–322.

    Article  Google Scholar 

  63. Seebacher, F., & Shine, R. (2004). Evaluating thermoregulation in reptiles: The fallacy of the inappropriately applied method. Physiological and Biochemical Zoology, 77(4), 688–695.

    PubMed  Article  Google Scholar 

  64. Shelomi, R. (2012). Where are we now? Bergmann’s rule sensu lato in insects. The American Naturalist, 180(4), 511–519.

    PubMed  Article  Google Scholar 

  65. Shine, R. (1991). Australian snakes: A natural history. Sydney: Reed New Holland.

    Google Scholar 

  66. 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.

    CAS  PubMed  Article  Google Scholar 

  67. 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.

    Article  Google Scholar 

  68. 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.

    CAS  PubMed  Article  Google Scholar 

  69. 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.

    Article  Google Scholar 

  70. 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.

    Article  Google Scholar 

  71. Uetz, P. (2013). The reptile database. http://reptile-database.reptarium.cz.

  72. Ulrich, W., & Fiera, C. (2010). Environmental correlates of body size distributions of European springtails (Hexapoda: Collembola). Global Ecology and Biogeography, 19(6), 905–915.

    Article  Google Scholar 

  73. Volynchik, S. (2012). Morphological variability in Vipera palaestinae along an environmental gradient. Asian Herpetological Research, 3(3), 227–239.

    Article  Google Scholar 

  74. Watt, C., Mitchell, S., & Salewski, V. (2010). Bergmann’s rule; a concept cluster? Oikos, 119(1), 89–100.

    Article  Google Scholar 

  75. Webb, J. K., & Shine, R. (1998). Thermoregulation by a nocturnal elapid snake (Hoplocephalus bungaroides) in southeastern Australia. Physiological Zoology, 71(6), 680–692.

    CAS  PubMed  Google Scholar 

  76. 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.

    Article  Google Scholar 

  77. Wilson, S., & Swan, G. (2010). A complete guide to reptiles of Australia (3rd ed.). Sydney: New Holland.

    Google Scholar 

  78. 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.

    Article  Google Scholar 

  79. 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.

    PubMed  Article  Google Scholar 

Download references

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

Affiliations

Authors

Corresponding author

Correspondence to Anat Feldman.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 24 kb)

Supplementary material 2 (DOCX 38 kb)

Rights and permissions

Reprints 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

Download citation

Keywords

  • Snakes
  • Bergmann’s Rule
  • Body size
  • Body mass
  • Activity time
  • Habitat use
  • Thermoregulation