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Evolutionary Biology

, Volume 40, Issue 4, pp 562–578 | Cite as

An Intercontinental Analysis of Climate-Driven Body Size Clines in Reptiles: No Support for Patterns, No Signals of Processes

  • Daniel Pincheira-Donoso
  • Shai Meiri
Research Article

Abstract

Climatic gradients impose clinal selection on animal ecological and physiological performance, often promoting geographic body size clines. Bergmann’s rule predicts that body size increases with decreasing environmental temperatures given the need to retain body-heat through adjustments of body-mass-to-surface-area ratio. This prediction generally holds for endotherms, but remains controversial for ectotherms. An alternative interpretation, the ‘resource rule’, suggests that food abundance, primary productivity and precipitation (which, unlike temperature, do not necessarily correlate with geography), drive body size clines. We investigate geographic variation in body size within 65 species of lizards and snakes (squamates) based on an intercontinental dataset (6,500+ specimens belonging to 56 Israeli species, and multiple populations of nine Liolaemus species from Argentina and Chile). Bergmann’s rule is only rarely supported by our data (in four species, 6 %), whereas six species (9 %) follow its converse (hence, it is unsupported in 94 % of cases). Similarly, size increases with resource abundance in only 12 species (18 %). Therefore, although neither of the rules is supported, factors suggested by the resource rule are better predictors of body size than temperature. Surprisingly, we show that some measures of the extent of a species’ climatic envelope do not affect the likelihood of it showing a size-climate relationship. We conclude that negative size-temperature associations are an exception rather than a generality among squamates.

Keywords

Macroecology Bergmann’s rule Resource rule Climatic variability Geographic variation in body size Lizards Snakes Liolaemus 

Notes

Acknowledgments

We thank Erez Maza for invaluable help resolving the correct geographic origin of species in the TAUM, and Anat Feldman and Stanislav Volynchic for valuable discussion. We are also grateful to referee’s and editor’s comments that greatly improved our manuscript. D.P.-D. thanks the Leverhulme Trust and a University of Lincoln Faculty Starting Funding for financial support. D.P.D. dedicates this paper to Natalia Feltrin, a young Argentinean ecologist, and a good friend, who devoted her career to the study of Liolaemus lizards, and who recently passed away in a road accident. Her life was interrupted on her way to her Ph.D viva. Natalia’s work will be greatly remembered and appreciated.

References

  1. Adams, D. C., & Church, J. O. (2008). Amphibians do not follow Bergmann’s rule. Evolution, 62, 413–420.PubMedCrossRefGoogle Scholar
  2. Amarello, M., Nowak, E. M., Taylor, E. N., Schuett, G. W., Repp, R. A., Rosen, P. C., et al. (2010). Potential environmental influences 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, 1443–1449.CrossRefGoogle Scholar
  3. Ashton, K. G., & Feldman, C. R. (2003). Bergmann’s rule in nonavian reptiles: Turtles follow it, lizards and snakes reverse it. Evolution, 57, 1151–1163.PubMedGoogle Scholar
  4. Ashton, K. G., Tracy, M. C., & de Queiroz, A. (2000). Is Bergmann’s rule valid for mammals? American Naturalist, 156, 390–415.CrossRefGoogle Scholar
  5. Bar, A., & Haimovitch, G. (2011). A field guide to reptiles and amphibians of Israel. Israel: Pazbar.Google Scholar
  6. Bergmann, 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. (2003). Macroecology. Concepts and consequences. Oxford: Blackwell.Google Scholar
  8. Blackburn, T. M., Gaston, K. J., & Loder, N. (1999). Geographic gradients in body size: A clarification of Bergmann’s rule. Diversity and Distributions, 5, 165–174.CrossRefGoogle Scholar
  9. Blackburn, T. M., & Ruggiero, A. (2001). Latitude, elevation and body mass variation in Andean passerine birds. Global Ecology and Biogeography, 10, 245–259.CrossRefGoogle Scholar
  10. Blanckenhorn, W. U., & Demont, M. (2004). Bergmann and converse Bergmann latitudinal clines in arthropods: Two ends of a continuum? Integrative and Comparative Biology, 44, 413–424.PubMedCrossRefGoogle Scholar
  11. Cei, J. M. (1993). Reptiles del noroeste, nordeste y este de la Argentina. Herpetofauna de las selvas subtropicales, puna y pampas (p. 947). Torino: Museo Regionale di Scienze Naturali di Torino.Google Scholar
  12. Costa, G. C., Vitt, L. G., Pianka, E. R., Mesquita, D. O., & Colli, G. R. (2008). Optimal foraging constrains macroecological patterns: Body size and dietary niche breadth in lizards. Global Ecology and Biogeography, 17, 670–677.CrossRefGoogle Scholar
  13. Cruz, F. B., Fitzgerald, L. A., Espinoza, R. E., & Schulte, J. A. (2005). The importance of phylogenetic scale in tests of Bergmann’s and Rapoport’s rules: Lessons from a clade of South American lizards. Journal of Evolutionary Biology, 18, 1559–1574.PubMedCrossRefGoogle Scholar
  14. Dayan, T., Tchernov, E., Yom-Tov, Y., & Simberloff, D. (1989). Ecological character displacement in Saharo-Arabian Vulpes: Outfoxing Bergmann’s rule. Oikos, 55, 263–272.CrossRefGoogle Scholar
  15. Dillon, M. E., Frazier, M. R., & Dudley, R. (2006). Into thin air: Physiology and evolution of alpine insects. Integrative and Comparative Biology, 46, 49–61.PubMedCrossRefGoogle Scholar
  16. Espinoza, R. E., Wiens, J. J., & Tracy, C. R. (2004). Recurrent evolution of herbivory in small, cold-climate lizards: Breaking the ecophysiological rules of reptilian herbivory. Proceedings of the National Academy of Sciences, USA, 101, 16819–16824.CrossRefGoogle Scholar
  17. Feldman, A. & Meiri, S. (2013). Length-mass allometry in snakes. Biological Journal of the Linnean Society (In Press).Google Scholar
  18. Frankenberg, E., & Werner, Y. L. (1992). Egg, clutch and maternal sizes in lizards: Intra- and interspecific relations in near-eastern Agamidae and Lacertidae. Herpetological Journal, 2, 7–18.Google Scholar
  19. Goldberg, S. R. (2012a). Reproduction in Kotschy’s gecko Mediodactylus kotschyi (Squamata: Gekkonidae) from the Greek Islands and Israel. Herpetological Bulletin, 119, 15–18.Google Scholar
  20. Goldberg, S. R. (2012b). Reproduction in the desert lacerta, Mesalina guttulata, from Israel (Squamata: Lacertidae). Zoology in the Middle East, 56, 27–38.CrossRefGoogle Scholar
  21. Gur, H., & Gur, M. K. (2012). Is spatial variation in food availability an explanation for a Bergmannian size pattern in a North American hibernating, burrowing mammal? An information-theoretic approach. Journal of Zoology, 287, 104–114.CrossRefGoogle Scholar
  22. 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, 1965–1978.CrossRefGoogle Scholar
  23. Huston, M. A., & Wolverton, S. (2011). Regulation of animal size by NPP, Bergmann’s rule, and related phenomena. Ecological Monographs, 81, 349–405.CrossRefGoogle Scholar
  24. 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, 870–873.PubMedCrossRefGoogle Scholar
  25. Iverson, J. B. (1982). Adaptations to herbivory in Iguanine lizards. In G. M. Burghardt, & A. S. Rand (Eds.), Iguanas of the world. Their behaviour, ecology and conservation. New Jersey: Noyes Publications. (pp. 60–76).Google Scholar
  26. James, F. C. (1970). Geographic size variations in birds and its relationship with climate. Ecology, 51, 365–390.CrossRefGoogle Scholar
  27. King, G. (1996). Reptiles and herbivory. New York: Chapman and Hall.Google Scholar
  28. Labra, A., Pienaar, J., & Hansen, T. F. (2009). Evolution of thermal physiology in Liolaemus lizards: Adaptation, phylogenetic inertia, and niche tracking. American Naturalist, 174, 204–220.PubMedCrossRefGoogle Scholar
  29. Lindsey, C. C. (1966). Body sizes of poikilotherm vertebrates at different latitudes. Evolution, 20, 456–465.CrossRefGoogle Scholar
  30. Lovegrove, B. G. (2000). The zoogeography of mammalian basal metabolic rate. American Naturalist, 156, 201–219.PubMedCrossRefGoogle Scholar
  31. Mayr, E. (1956). Geographical character gradients and climatic adaptation. Evolution, 10, 105–108.CrossRefGoogle Scholar
  32. McNab, B. K. (2010). Geographic and temporal correlations of mammalian size reconsidered: A resource rule. Oecologia, 164, 13–23.PubMedCrossRefGoogle Scholar
  33. Meiri, S. (2008). Evolution and ecology of lizard body sizes. Global Ecology and Biogeography, 17, 724–734.CrossRefGoogle Scholar
  34. Meiri, S. (2010). Length-weight allometries in lizards. Journal of Zoology, 281, 218–226.Google Scholar
  35. Meiri, S. (2011). Bergmann’s rule: What’s in a name? Global Ecology and Biogeography, 20, 203–207.CrossRefGoogle Scholar
  36. Meiri, S., Bauer, A. M., Chirio, L., Colli, G. R., Das, I. Doan, T. M., Feldman, A., Castro-Herrera, F., Novosolov, M., Pafilis, P., Pincheira-Donoso, D., Powney, G., Torres-Carvajal, O., Uetz, P., & Van Damme, R. (2013). Are lizards feeling the heat? A tale of ecology and evolution under two temperatures. Global Ecology and Biogeography (In Press). doi: 10.1111/geb.12053.
  37. Meiri, S., Brown, J. H., & Sibly, R. M. (2012). The ecology of lizard reproductive output. Global Ecology and Biogeography, 21, 592–602.CrossRefGoogle Scholar
  38. Meiri, S., & Dayan, T. (2003). On the validity of Bergmann’s rule. Journal of Biogeography, 30, 331–351.CrossRefGoogle Scholar
  39. Meiri, S., Meijaard, E., Wich, S., Groves, C., & Helgen, K. (2008). Mammals of Borneo—small size on a large island. Journal of Biogeography, 35, 1087–1094.CrossRefGoogle Scholar
  40. Meiri, S., & Thomas, G. H. (2007). The geography of body size—challenges of the interspecific approach. Global Ecology and Biogeography, 16, 689–693.CrossRefGoogle Scholar
  41. Meiri, S., Yom-Tov, Y., & Geffen, E. (2007). What determines conformity to Bergmann’s rule? Global Ecology and Biogeography, 16, 788–794.CrossRefGoogle Scholar
  42. Mendelssohn, H. (1963). On the biology of the venomous snakes in Israel, Part I. Israel Journal of Zoology, 12, 143–170.Google Scholar
  43. O’Brien, R. M. (2007). A caution regarding rules of thumb for variance inflation factors. Quality and Quantity, 41, 673–690.CrossRefGoogle Scholar
  44. Olalla-Tarraga, M. A. (2011). “Nullius in Bergmann” or the pluralistic approach to ecogeographical rules: A reply to Watt et al. (2010). Oikos, 120, 1441–1444.CrossRefGoogle Scholar
  45. 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, 781–793.CrossRefGoogle Scholar
  46. Oufiero, C. E., Adolph, S. C., Gartner, G. E. A., & Garland, T. (2011). Latitudinal and climatic variation in body size and dorsal scale counts in Sceloporus lizards: A phylogenetic perspective. Evolution, 65, 3590–3607.PubMedCrossRefGoogle Scholar
  47. Partridge, L., & Coyne, J. A. (1997). Bergmann’s rule in ectotherms: Is it adaptive? Evolution, 51, 632–635.CrossRefGoogle Scholar
  48. Peters, R. H. (1983). The ecological implications of body size. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  49. 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, 247–253.PubMedCrossRefGoogle Scholar
  50. Pincheira-Donoso, D. (2011). Predictable variation of range-sizes across an extreme environmental gradient in a lizard adaptive radiation: Evolutionary and ecological inferences. PLoS One, 6, e28942.PubMedCrossRefGoogle Scholar
  51. Pincheira-Donoso, D., Bauer, A. M., Meiri, S., & Uetz, P. (2013). Global taxonomic diversity of living reptiles. PLoS One, 8, e59741.PubMedCrossRefGoogle Scholar
  52. Pincheira-Donoso, D., Fox, S. F., Scolaro, J. A., Ibargüengoytía, N., Acosta, J. C., Corbalán, V., et al. (2011). Body size dimensions in lizard ecological and evolutionary research: Exploring the predictive power of mass estimation equations in two Liolaemidae radiations. Herpetological Journal, 21, 35–42.CrossRefGoogle Scholar
  53. Pincheira-Donoso, D., Hodgson, D. J., & Tregenza, T. (2008a). The evolution of body size under environmental gradients in ectotherms: Why should Bergmann’s rule apply to lizards? BMC Evolutionary Biology, 8, 68.PubMedCrossRefGoogle Scholar
  54. Pincheira-Donoso, D., & Núñez, H. (2005). Las especies chilenas del género Liolaemus. Taxonomía, sistemática y evolución. Publicación Ocasional del Museo Nacional de Historia Natural de Chile, 59, 1–487.Google Scholar
  55. Pincheira-Donoso, D., Scolaro, J. A., & Sura, P. (2008b). A monographic catalogue on the systematics and phylogeny of the South American iguanian lizard family Liolaemidae (Squamata, Iguania). Zootaxa, 1800, 1–85.Google Scholar
  56. Pincheira-Donoso, D., Tregenza, T., & Hodgson, D. J. (2007). Body size evolution in South American Liolaemus lizards of the boulengeri clade: A contrasting reassessment. Journal of Evolutionary Biology, 20, 2067–2071.PubMedCrossRefGoogle Scholar
  57. Raia, P., & Meiri, S. (2006). The island rule in large mammals: Paleontology meets ecology. Evolution, 60, 1731–1742.PubMedGoogle Scholar
  58. Roitberg, E. S., Orlova, V. F., Kuranova, V. N., Bulakhova, N. A., Zinenko, O. I., Ljubisavljevic, K., et al. (2011). Inter-observer and intra-observer differences in measuring body length: A test in the common lizard, Zootoca vivipara. Amphibia-Reptilia, 32, 477–484.CrossRefGoogle Scholar
  59. Rosenzweig, M. L. (1968). The strategy of body size in mammalian carnivores. American Midland Naturalist, 80, 299–315.CrossRefGoogle Scholar
  60. Schmidt-Nielsen, K. (1984). Scaling. Why is animal size so important?. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  61. Sears, M. W., & Angilletta, M. J. (2004). Body size clines in Sceloporus lizards: Proximate mechanisms and demographic constraints. Integrative and Comparative Biology, 44, 433–442.PubMedCrossRefGoogle Scholar
  62. Tracy, C. R. (1999). Differences in body size among chuckwalla (Sauromalus obesus) populations. Ecology, 80, 259–271.Google Scholar
  63. Uetz, P. (2012). The Reptile Database. Available at http://www.reptile-database.org. Accessed 31 Mar 2012.
  64. Vezina, A. F. (1985). Empirical relationships between predator and prey size among terrestrial vertebrate predators. Oecologia, 67, 555–565.CrossRefGoogle Scholar
  65. Volynchik, S. (2012). Morphological variability in Vipera palaestinae along an environmental gradient. Asian Herpetological Research, 3, 227–239.CrossRefGoogle Scholar
  66. Waldron, A. (2007). Null models of geographic range size evolution reaffirm its heritability. American Naturalist, 170, 221–231.PubMedCrossRefGoogle Scholar
  67. Watt, C., Mitchell, S., & Salewski, V. (2010). Bergmann’s rule; a concept cluster? Oikos, 119, 89–100.CrossRefGoogle Scholar
  68. Webb, T. J., & Gaston, K. J. (2003). On the heritability of geographic range sizes. American Naturalist, 166, 129–135.Google Scholar
  69. Wilson, A. B. (2009). Fecundity selection predicts Bergmann’s rule in syngnathid fishes. Molecular Ecology, 18, 1263–1272.PubMedCrossRefGoogle Scholar
  70. Yom-Tov, Y. (2003). Body sizes of carnivores commensal with humans have increased over the past 50 years. Functional Ecology, 17, 323–327.CrossRefGoogle Scholar
  71. Yom-Tov, Y., & Geffen, E. (2006). The determination of mammal body size: Ambient temperature or food? Oecologia, 148, 213–218.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Laboratory of Evolutionary Ecology of Adaptations, School of Life SciencesUniversity of LincolnLincoln, LincolnshireUK
  2. 2.Department of ZoologyTel Aviv UniversityTel AvivIsrael

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