, 159:617 | Cite as

Global richness patterns of venomous snakes reveal contrasting influences of ecology and history in two different clades

  • Levi Carina TerribileEmail author
  • Miguel Ángel Olalla-Tárraga
  • Ignacio Morales-Castilla
  • Marta Rueda
  • Rosa M. Vidanes
  • Miguel Ángel Rodríguez
  • José Alexandre Felizola Diniz-Filho
Community Ecology - Original Paper


Recent studies addressing broad-scale species richness gradients have proposed two main primary drivers: contemporary climate and evolutionary processes (differential balance between speciation and extinction). Here, we analyze the global richness patterns of two venomous snake clades, Viperidae and Elapidae. We used ordinary least squares multiple regression (OLS) and partial regression analysis to investigate to what extent actual evapotranspiration (AET; summarizing current environmental conditions) and biogeographical regions (representing evolutionary effects) were associated with species richness. For viperids, AET explained 45.6% of the variance in richness whereas the effect of this variable for elapids was almost null (0.5%). On the other hand, biogeographic regions were the best predictors of elapid richness (56.5%), against its relatively small effect (25.9%) in viperid richness. Partial regressions also revealed similar patterns for independent effects of climate and history in both clades. However, the independent historical effect in Elapidae decreased from 45.2 to 17.8% when we excluded Australia from the analyses, indicating that the strong historical effect that had emerged for the global richness pattern was reflecting the historical process of elapid radiation into Australia. Even after excluding Australia, the historical signal in elapid richness in the rest of the globe was still significant and much higher than that observed in viperid richness at a global scale (2.7% after controlling for AET effects). Differences in the evolutionary age of these two clades can be invoked to explain these contrasting results, in that viperids probably had more time for diversification, generating richness responses to environmental gradients, whereas the pattern of distribution of elapid richness can be more directly interpreted in an evolutionary context. Moreover, these results show the importance of starting to adopt deconstructive approaches to species richness, since the driving factors of these patterns may vary from group to group according to their evolutionary history.


Evolutionary history Latitudinal gradient Snakes Species richness Water energy hypothesis 



We thank B. Hawkins and an anonymous reviewer for useful suggestions. L. C. T. thanks the Universidad de Alcalá at Alcalá de Henares for their hospitality during the preparation of the data and the CAPES (PDEE-CAPES Process: 5142/06-7) for the financial support. Work by J. A. F. D.-F. is supported by a CNPQ researcher fellowship. The Spanish Ministry of Education and Science has supported M. Á. R., R. M. V. and M. R. (grant: CGL2006-03000/BOS to M. Á. R.), as well as M. Á. O.-T. (FPU fellowship: AP2005-0636), and I. M.-C. (FPI fellowship: BES-2007-16314).

Supplementary material

442_2008_1244_MOESM1_ESM.doc (102 kb)
Supplementary Material S1 (DOC 102 kb)


  1. Alvarado-Díaz J, Campbell JA (2004) A new montane rattlesnake (Viperidae) from Michoacán, Mexico. Herpetologica 60:281–286CrossRefGoogle Scholar
  2. Ananjeva NB, Orlov NL, Khalikov RG, Darevsky IS, Ryabov SA, Barabanov AV (2006) The reptiles of Northen Eurasia: taxonomic diversity, distribution, conservation status. Pensoft, SofiaGoogle Scholar
  3. Araújo MB, Nogués-Bravo D, Diniz-Filho JAF, Haywood AM, Valdes PJ, Rahbek C (2008) Quaternary climate changes explain diversity among reptiles and amphibians. Ecography 31:8–15CrossRefGoogle Scholar
  4. Arnold EN (2002) A field guide to the reptiles and amphibians of Britain and Europe. Harper Collins, LondonGoogle Scholar
  5. Arnold EN, Ovenden DW (2002) Reptiles and Amphibians of Europe. Princeton University Press, PrincetonGoogle Scholar
  6. Avery RA, Bedford JD, Newcombe CP (1982) The role of thermoregulation in lizard biology: predatory efficiency in a temperate diurnal basker. Behav Ecol Sociobiol 11:261–267CrossRefGoogle Scholar
  7. Branch B (1988) Field guide to the snakes and other reptiles of Southern Africa, 1st edn. Struik, Cape TownGoogle Scholar
  8. Branch B (1998) Field guide to snakes and other reptiles of Southern Africa, 3rd edn. Curtis, FloridaGoogle Scholar
  9. Broadley DG, Doria CT (2003) Snakes of Zambia: an atlas and field guide. Chimaira, Frankfurt am MainGoogle Scholar
  10. Buckley LB, Jetz W (2007) Environmental and historical constraints on global patterns of amphibian richness. Proc R Soc B 274:1167–1173PubMedCrossRefGoogle Scholar
  11. Campbell JA, Lamar WW (2004) The venomous reptiles of the Western Hemisphere, vol I and II. Cornell University Press, New YorkGoogle Scholar
  12. Castoe TA, Parkinson CL (2006) Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Mol Phylogenet Evol 39:91–110PubMedCrossRefGoogle Scholar
  13. Castoe TA, Smith EN, Brown RM, Parkinson CL (2007) Higher-level phylogeny of Asian and American coralsnakes, their placement within the Elapidae (Squamata), and the systematic affinities of the enigmatic Asian coralsnake Hemibungarus calligaster (Wiegmann, 1834). Zool J Linn Soc 151:809–831Google Scholar
  14. Ceballos G, Ehrlich PR (2006) Global mammal distributions, biodiversity hotspots, and conservation. Proc Natl Acad Sci USA 103:19374–19379PubMedCrossRefGoogle Scholar
  15. Cherlin VA (1981) The new saw-scaled viper Echis multisquamatus sp. nov. from south-western and Middle Asia (in Russian). Trudy Zool Inst 101:92–95Google Scholar
  16. Costa GC, Nogueira C, Machado RB, Colli GR (2007) Squamate richness in the Brazilian Cerrado and its environmental–climatic associations. Diversity Distrib 13:714–724CrossRefGoogle Scholar
  17. Cox CB (2001) The biogeographic regions reconsidered. J Biogeogr 28:511–523CrossRefGoogle Scholar
  18. Currie DJ (1991) Energy and large-scale patterns of animal- and plant-species richness. Am Nat 137:27–49CrossRefGoogle Scholar
  19. Diniz-Filho JAF, Bini LM, Hawkins BA (2003) Spatial autocorrelation and red herrings in geographical ecology. Global Ecol Biogeogr 12:53–64CrossRefGoogle Scholar
  20. Dobiey M, Vogel G (2007) Venomous snakes of Africa. Chimaira, Frankfurt am MainGoogle Scholar
  21. Dormann CF, McPherson J, Araújo MB, Bivand R, Bolliger J, Carl G, Davies RG, Hirzel A, Jetz W, Kissling WD, Kühn I, Ohlemüller R, Peres-Neto P, Reineking B, Schröder B, Schurr FM, Wilson R (2007) Methods to account for spatial autocorrelation in the analysis of distributional species data: a review. Ecography 30:609–628CrossRefGoogle Scholar
  22. Francis AP, Currie DJ (1998) Global patterns of tree species richness in moist forests: another look. Oikos 81:598–602CrossRefGoogle Scholar
  23. Geniez P, Tynié A (2005) Discovery of a population of the critically engangered Vipera darevskii Vedmederja, Orlov and Tuniyev 1986 in Turkey, with new elements on its identification (Reptilia: Squamata: Viperidae). Herpetozoa 18:25–33Google Scholar
  24. Glazier DS (1987) Energetics and taxonomic patterns of species diversity. Syst Zool 36:62–71CrossRefGoogle Scholar
  25. Grenyer R, Orme CDL, Jackson SF, Thomas GH, Davies RG, Davies TJ, Jones KE, Olson VA, Ridgely RS, Rasmussen PC, Ding T-S, Bennett PM, Blackburn TM, Gaston KJ, Gittleman JL, Owens IPF (2006) Global distribution and conservation of rare and threatened vertebrates. Nature 444:93–96PubMedCrossRefGoogle Scholar
  26. Hawkins BA, Porter EE (2003) Relative influences of current and historical factors on mammal and bird diversity patterns in deglaciated North America. Global Ecol Biogeogr 12:475–481CrossRefGoogle Scholar
  27. Hawkins BA, Field R, Cornell HV, Currie DJ, Guégan J-F, Kaufman DM, Kerr JT, Mittelbach GG, Oberdorff T, O’Brien EM, Porter EE, Turner JRG (2003a) Energy, water, and broad-scale geographic patterns of species richness. Ecology 84:3105–3117CrossRefGoogle Scholar
  28. Hawkins BA, Porter EE, Diniz-Filho JAF (2003b) Productivity and history as predictors of the latitudinal diversity gradient of terrestrial birds. Ecology 84:1608–1623CrossRefGoogle Scholar
  29. Hawkins BA, Diniz-Filho JAF, Soeller SA (2005) Water links the historical and contemporary components of the Australian bird diversity gradient. J Biogeogr 32:1035–1042CrossRefGoogle Scholar
  30. Hawkins BA, Diniz-Filho JAF, Jaramillo CA, Soeller SA (2007a) Climate, niche conservatism, and the global bird diversity gradient. Am Nat 170:S16–S27PubMedCrossRefGoogle Scholar
  31. Hawkins BA, Diniz-Filho JAF, Bini LM, Marco P, Blackburn TM (2007b) Red herrings revisited: spatial autocorrelation and parameter estimation in geographical ecology. Ecography 30:375–384Google Scholar
  32. Hawkins BA, Albuquerque FS, Araújo MB, Beck J, Bini LM, Cabrero-Sañudo FJ, Castro-Parga I, Diniz-Filho JAF, Ferrer-Castán D, Field R, Gómez JF, Hortal J, Kerr JT, Kitching JF, León-Cortés JL, Lobo JMD, Montoya D, Moreno JC, Olalla-Tárraga MÁ, Pausas JG, Qian H, Rahbek C, Rodríguez MÁ, Sanders NJ, Williams P (2007c) A global evaluation of metabolic theory as an explanation for terrestrial species richness gradients. Ecology 88:1877–1888PubMedCrossRefGoogle Scholar
  33. Heise PJ, Maxson LR, Dowling HG, Hedges SB (1995) Higher-level snake phylogeny inferred from mitochondrial DNA sequences of 12s rRNA and 16s rRNA genes. Mol Biol Evol 12:259–265PubMedGoogle Scholar
  34. Hortal J, Rodríguez J, Nieto-Díaz M, Lobo JM (2008) Regional and environmental effects on the species richness of mammal assemblages. J Biogeogr 35:1202–1214CrossRefGoogle Scholar
  35. von Humboldt A (1808) Ansichten der Natur mit wissenschaftlichen Erlauterungen. Cotta, TübingenGoogle Scholar
  36. Hutchinson GE (1959) Homage to Santa Rosalia, or why are these so many kinds of animals? Am Nat 93:145–159CrossRefGoogle Scholar
  37. IUCN, Conservation International, Nature Serve (2006) Global amphibian assessment., version 1.1. Downloaded on 15 October 2006
  38. Jablonski D, Roy K, Valentine JW (2006) Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient. Science 314:102–106PubMedCrossRefGoogle Scholar
  39. Kelly CMR, Barker NP, Villet MH (2003) Phylogenetics of advanced snakes (Caenophidia) based on four mitochondrial genes. Syst Biol 54:439–449CrossRefGoogle Scholar
  40. Keogh JS (1998) Molecular phylogeny of elapid snakes and a consideration of their biogeographic history. Biol J Linn Soc 63:177–203CrossRefGoogle Scholar
  41. Khan S (2002) Venomous terrestrial snakes of Pakistan. In: Accessed on 3 April 2007
  42. Kissling WD, Carl G (2008) Spatial autocorrelation and the selection of simultaneous autoregressive models. Global Ecol Biogeogr 17:59–71CrossRefGoogle Scholar
  43. Knight A, Mindell DP (1994) On the phylogenetic relationship of Colubrinae, Elapidae, and Viperidae and the evolution of front-fanged venom systems in snakes. Copeia 1994:1–9CrossRefGoogle Scholar
  44. Kreft H, Jetz W (2007) Global patterns and determinants of vascular plant diversity. Proc Natl Acad Sci USA 104:5925–5930PubMedCrossRefGoogle Scholar
  45. Kuch U, Müller L, Mödden C, Mebs D (2006) Snake fangs from the Lower Miocene of Germany: evolutionary stability of perfect weapons. Naturwissenschaften 93:84–87PubMedCrossRefGoogle Scholar
  46. Lamoreux JF, Morrison JC, Ricketts TH, Olson DM, Dinerstein E, McKnight MW, Shugart HH (2006) Global tests of biodiversity concordance and the importance of endemism. Nature 440:212–214PubMedCrossRefGoogle Scholar
  47. Latham RE, Ricklefs RE (1993) Global patterns of tree species richness in moist forests: energy–diversity theory does not account for variation in species richness. Oikos 67:325–333CrossRefGoogle Scholar
  48. Latifi M (1991) The snakes of Iran. Society for the study of Amphibians and Reptiles, OxfordGoogle Scholar
  49. Lavin-Murcio PA, Dixon JR (2004) A new species of coral snake (Serpentes, Elapidae) from the Sierra de Tamaulipas, Mexico. Phyllomedusa 3:3–7Google Scholar
  50. Legendre P, Legendre L (1998) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  51. Lenk P, Kalyabina S, Wink M, Joger U (2001) Evolutionary relationships among the true vipers (Reptilia: Viperidae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 19:94–104PubMedCrossRefGoogle Scholar
  52. Mallow D, Ludwig D, Nilson G (2003) True vipers: natural history and toxinology of old world vipers. Krieger, FloridaGoogle Scholar
  53. Marquet PA, Fernández M, Navarrete SA, Valdovinos C (2004) Diversity emerging: toward a deconstruction of biodiversity patterns. In: Lomolino M, Heaney LR (eds) Frontiers of biogeography: new directions in the geography of nature. Sinauer, Massachusetts, pp 191–209Google Scholar
  54. Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM, Bush MB, Harrison SP, Hurlbert AH, Knowlton N, Lessios HA, McCain CM, McCune AR, McDade LA, McPeek MA, Near TJ, Price TD, Ricklefs RE, Roy K, Sax DF, Schluter D, Sobel JM, Turelli M (2007) Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Lett 10:315–331PubMedCrossRefGoogle Scholar
  55. Montoya D, Rodriguez MA, Zavala MA, Hawkins BA (2007) Contemporary richness of holarctic trees and the historical pattern of glacial retreat. Ecography 30:173–182Google Scholar
  56. O’Brien ME (2006) Biological relativity to water–energy dynamics. J Biogeogr 33:1868–1888CrossRefGoogle Scholar
  57. Oberdoff T, Guégan J-F, Hugueny B (1995) Global scale patterns of fish species richness in rivers. Ecography 18:345–352CrossRefGoogle Scholar
  58. Olalla-Tárraga MA, Rodríguez MA, Hawkins BA (2006) Broad-scale patterns of body size in squamate reptiles of Europe and North America. J Biogeogr 33:781–793CrossRefGoogle Scholar
  59. Orlov NL, Tuniyev BF (1990) Three species in the Vipera kaznakowi complex (Eurosiberian group) in the Caucasus: their present distribution, possible genesis, and phylogeny. Asiat Herpetol Res 3:1–36Google Scholar
  60. Orme CDL, Davies RG, Burgess M, Eigenbrod F, Pickup N, Olson V, Webster AJ, Ding T-S, Rasmussen PC, Ridgely RS, Stattersfield AJ, Bennett PM, Blackburn TM, Gaston KJ, Owens IPF (2005) Global hotspots of species richness are not congruent with endemism or threat. Nature 436:1016–1019PubMedCrossRefGoogle Scholar
  61. Owen JG (1989) Patterns of herpetofaunal species richness: relation to temperature, precipitation, and variance in elevation. J Biogeogr 16:141–150CrossRefGoogle Scholar
  62. Pearman PB, Guisan A, Broennimann O, Randin CF (2007) Niche dynamics in space and time. Trends Ecol Evol 23:149–158CrossRefGoogle Scholar
  63. Peterson AT, Soberón J, Sánchez-Cordero V (1999) Conservatism of ecological niches in evolutionary time. Science 285:1265–1267PubMedCrossRefGoogle Scholar
  64. Pianka ER (1966) Latitudinal gradients in species diversity: a review of concepts. Am Nat 100:33–46CrossRefGoogle Scholar
  65. Rage J-C, Buffetaut E, Buffetaut-Tong H, Chaimanee Y, Ducrocq S, Jaeger J-J, Sutetthorn V (1992) A colubrid snake in the late Eocene of Thailand: the oldest known Colubridae (Reptilia, Serpentes). C R Acad sci 2:1085–1089Google Scholar
  66. Rangel TFLVB, Diniz-Filho JAF, Bini LM (2006) Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Global Ecol Biogeogr 15:321–327CrossRefGoogle Scholar
  67. Rangel TFLVB, Diniz-Filho JAF, Colwell RK (2007) Species richness and evolutionary niche dynamics: a spatial Pattern-oriented simulation experiment. Am Nat 170:602–616PubMedCrossRefGoogle Scholar
  68. Reed RN (2003) Interspecific patterns of species richness, geographic range size, and body size among New World venomous snakes. Ecography 26:107–117CrossRefGoogle Scholar
  69. Renjifo JM, Lundberg M (2003) Una especie nuevo de serpiente coral (Elapidae, Micrurus), de la region de Urra, municipio de Tierra Alta, Cordoba, noroccidente de Colombia. Rev Acad Colombiana Cienc Exact Fis Natur 27:141–144Google Scholar
  70. Ricklefs RE (2003) Global diversification rates of passerine birds. Proc R Soc B 270:2285–2291PubMedCrossRefGoogle Scholar
  71. Ricklefs RE (2006) Evolutionary diversification and the origin of the diversity–environment relationship. Ecology 87:S3–S13PubMedCrossRefGoogle Scholar
  72. Rodríguez MÁ, Belmontes JA, Hawkins BA (2005) Energy, water and large-scale patterns of reptile and amphibian species richness in Europe. Acta Oecol 28:65–70CrossRefGoogle Scholar
  73. Rodríguez MÁ, Olalla-Tárraga MÁ, Hawkins BA (2008) Bergmann’s rule and the geography of mammal body size in the Western Hemisphere. Global Ecol Biogeogr 17:274–283CrossRefGoogle Scholar
  74. Sanders KL, Lee MSY (2008) Molecular evidence for a rapid late-Miocene radiation of Australasian venomous snakes (Elapidae, Colubroidea). Mol Phylogenet Evol 46:1180–1188Google Scholar
  75. Scanlon JD, Lee MSY (2004) Phylogeny of Australasian venomous snakes (Colubroidea, Elapidae, Hydrophiinae) based on phenotypic and molecular evidence. Zool Scrip 33:335–366CrossRefGoogle Scholar
  76. Schall JJ, Pianka ER (1978) Geographical trends in the numbers of species. Science 201:679–686PubMedCrossRefGoogle Scholar
  77. Shine R, Madsen T (1996) Is thermoregulation unimportant for most reptiles? An example using water pythons (Liasis fuscus) in tropical Australia. Physiol Zool 69:252–269Google Scholar
  78. Spawls S, Howell K, Drewes R, Ashe J (2004) A field guide to the reptiles of East Africa. Black, LondonGoogle Scholar
  79. Svenning J-C, Borchsenius F, Bjorholm S, Balslev H (2008) High tropical net diversification drives the New World latitudinal gradient in palm (Arecaceae) species richness. J Biogeogr 35:394–406CrossRefGoogle Scholar
  80. Szyndlar Z, Rage J-C (1999) Oldest fossil vipers (Serpentes: Viperidae) from the Old World. Kaupia 8:9–20Google Scholar
  81. Tuniyev BS, Ostrovskikh SV (2001) Two new species of vipers of “kaznakovi” complex (Ophidia, Viperinae) from the Western Caucasus. Russ J Herpetol 8:117–126Google Scholar
  82. Uetz P (2007) The reptile database. Accessed on 10 May 2007
  83. Vidal N, Hedges SB (2002) Higher-level relationships of caenophidian snakes inferred from four nuclear and mitochondrial genes. C R Biol 325:987–995PubMedCrossRefGoogle Scholar
  84. Vidal N, Delmas AS, David P, Cruaud C, Couloux A, Hedges SB (2007) The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes. C R Biol 330:182–187PubMedCrossRefGoogle Scholar
  85. Vogel G (2006) Venomous snakes of Asia. Chimaira, Frankfurt am MainGoogle Scholar
  86. Whittaker RJ, Nogués-Bravo D, Araújo MB (2007) Geographical gradients of species richness: a test of the water–energy conjecture of Hawkins et al. (2003) using European data for five taxa. Global Ecol Biogeogr 16:76–89CrossRefGoogle Scholar
  87. Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecology and species richness. Trends Ecol Evol 19:639–644PubMedCrossRefGoogle Scholar
  88. Wiens JJ, Graham CH, Moen DS, Smith SA, Reeder TW (2006a) Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity. Am Nat 168:579–596PubMedCrossRefGoogle Scholar
  89. Wiens JJ, Brandley MC, Reeder TW (2006b) Why does a trait evolve multiple times within a clade? Repeated evolution of snakelike body form in squamate reptiles. Evolution 60:114–123Google Scholar
  90. Willig MR, Kaufman DM, Stevens RD (2003) Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annu Rev Ecol Evol Syst 34:273–309CrossRefGoogle Scholar
  91. Wilson S, Swan G (2003) Reptiles of Australia. Princeton University Press, PrincetonGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Levi Carina Terribile
    • 1
    • 3
    Email author
  • Miguel Ángel Olalla-Tárraga
    • 2
  • Ignacio Morales-Castilla
    • 2
  • Marta Rueda
    • 2
  • Rosa M. Vidanes
    • 2
  • Miguel Ángel Rodríguez
    • 2
  • José Alexandre Felizola Diniz-Filho
    • 3
  1. 1.Programa de Pós-Graduação em Biologia AnimalUniversidade de BrasíliaBrasíliaBrazil
  2. 2.Department of EcologyUniversity of AlcalaAlcalá de HenaresSpain
  3. 3.Departamento de Biologia Geral, ICBUniversidade Federal de GoiásGoiâniaBrazil

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