Evolutionary Ecology

, Volume 25, Issue 2, pp 531–546 | Cite as

Ventral and sub-caudal scale counts are associated with macrohabitat use and tail specialization in viperid snakes

Original Paper

Abstract

Viperids are a species rich clade of snakes that vary greatly in both morphology and ecology. Many species in the family express tail specializations used for defensive warnings, prey lures, and stability during locomotion and striking. To examine the relationships among ecology, behavior, and vertebral number in the family Viperidae, morphological data (maximum total length and the number of pre-cloacal and caudal vertebrae), macrohabitat use, and tail specialization for 157 viperids were gleaned from published sources. A composite tree topology was constructed from multiple published viperid phylogenies for independent contrasts analysis. The number of vertebrae was strongly correlated with the total length of the snake. Results of both non-phylogenetic and phylogenetically corrected analysis showed that macrohabitat use did not strongly influence total snake length. However, the number of vertebrae per unit length did vary among species according to macrohabitat. Specifically, vertebral density increased with increasing arboreality. Overall, viperids showed a positive correlation between the number of caudal and pre-cloacal vertebrae, but separately rattlesnakes had a significant negative correlation. Species with prehensile tails and those that caudal lure had the most caudal vertebrae. The increased caudal segments of prehensile and luring tails likely improve performance when grasping small vegetation for support or imitating invertebrate prey. These results illustrate that vertebral number is a primary characteristic involved in the diversification of viper species and ecology.

Keywords

Caudal luring Ecomorphology Rattle Snake Tail Vertebrae Viperidae 

References

  1. Albert JS (2007) Phylogenetic character reconstruction. In: Kaas JH (ed) Evolution of nervous systems, vol. I. History of ideas, basic concepts, and developmental mechanisms. Academic Press, Oxford, pp 41–54Google Scholar
  2. Alexander AA, Gans C (1966) The pattern of dermal-vertebral correlation in snakes and amphisbaenians. Zoologische Mededlingen 41:171–190Google Scholar
  3. Arnold SJ, Bennett AF (1988) Behavioral variation in natural populations. V.Morphological correlates of locomotion in the garter snake Thamnophis radix. Biol J Linn Soc 34:175–190CrossRefGoogle Scholar
  4. Astley HC, Jayne BC (2007) Effects of perch diameter and incline on the kinematics, performance and modes of arboreal locomotion of corn snakes (Elaphe guttata). J Exp Biol 210:3862–3872CrossRefPubMedGoogle Scholar
  5. Blackburn TM, Gaston KJ (1998) Some methodological issues in macroecology. Am Nat 151:68–83CrossRefPubMedGoogle Scholar
  6. Bonnet X, Naulleau G, Shine R, Lourdais O (2001) Short-term versus long-term effects of food intake on reproductive output in a viviparous snake, Vipera aspis. Oikos 92:297–308CrossRefGoogle Scholar
  7. Calder WA III (1984) Size, function, and life history. Harvard University Press, CambridgeGoogle Scholar
  8. Campbell JA, Lamar WL (2004) The venomous reptiles of the western hemisphere, vol. I and II. Cornell University Press, New YorkGoogle Scholar
  9. Castoe TA, Parkinson CL (2006) Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Mol Phylo Evol 39:91–110CrossRefGoogle Scholar
  10. Costa GC, Vitt LJ, Pianka ER, Mesquita DO, Colli GR (2008) Optimal foraging constrains macroecological patterns: body size and dietary niche breadth in lizards. Glob Ecol Biog 17:670–677CrossRefGoogle Scholar
  11. Diniz-Filho JAF, Tôrres NM (2002) Phylogenetic comparative methods and the geographic range size—body size relationship in New World terrestrial carnivore. Evol Ecol 16:351–367CrossRefGoogle Scholar
  12. Dohm MR, Garland TJ (1993) Quantitative genetics of scale counts in the garter snake Thamnophis sirtalis. Copeia 1993:987–1002CrossRefGoogle Scholar
  13. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  14. Gasc JP, Gans C (1990) Tests on locomotion of the elongate and limbless lizard Anguis fragilis (Squamata: Anguidae). Copeia 1990:1055–1067CrossRefGoogle Scholar
  15. Goin JJ, Williams TH, Donohoe CJ (2008) Variation of vertebral number in juvenile Oncorhynchus mykiss in relation to upstream distance from the ocean. Environ Biol Fish 82:207–213CrossRefGoogle Scholar
  16. Gomez C, Pourquié O (2009) Developmental control of segment numbers in vertebrates. J Exp Zool (Mol Dev Evol) 312B:533–544CrossRefGoogle Scholar
  17. Gomez C, Özbudak EM, Wunderlich J, Baumann D, Lewis J, Pourquié O (2008) Control of segment number in vertebrate embryos. Nature 454:335–339CrossRefPubMedGoogle Scholar
  18. Greene HW, Campbell JA (1972) Notes on the use of caudal lures in arboreal green pitvipers. Herpetologica 28:32–34Google Scholar
  19. Grismer LL, Grismer JL, McGuire JA (2006) A new species of pitviper of the genus Popeia (Squamata: Viperidae) from Pulau Tioman, Pahang, West Malaysia. Zootaxa 1305:1–19Google Scholar
  20. Gutberlet RL Jr, Harvey MB (2004) The evolution of New World venomous snakes. In: Campbell JA, Lamar WL (eds) The venomous reptiles of the western hemisphere, vol. II. Cornell University Press, New York, pp 634–682Google Scholar
  21. Guyer C, Donnelly MA (1990) Length-mass relationships among an assemblage of tropical snakes in Costa Rica. J Trop Ecol 6:65–76CrossRefGoogle Scholar
  22. Jayne BC (1982) Comparative morphology of the semispinalis-spinalis muscle of snakes and correlations with locomotion and constriction. J Morph 172:83–96CrossRefGoogle Scholar
  23. Jayne BC (1985) Swimming in constricting (Elaphe g. guttata) and nonconstricting (Nerodia fasciata pictiventris) colubrid snakes. Copeia 1985:195–208CrossRefGoogle Scholar
  24. Jayne BC (1988) Muscular mechanisms of snake locomotion: an electromyographic study of the sidewinding and concertina modes of Crotalus cerastes, Nerodia fasciata, and Elaphe obsoleta. J Exp Biol 140:1–33PubMedGoogle Scholar
  25. Jayne BC, Riley MA (2007) Scaling of the axial morphology and gap-bridging ability of the brown tree snake, Boiga irregularis. J Exp Biol 210:1148–1160CrossRefPubMedGoogle Scholar
  26. Kelley KC, Arnold SJ, Gladstone J (1997) The effects of substrate and vertebral number on locomotion in the garter snake Thamnophis elegans. Funct Ecol 11:189–198CrossRefGoogle Scholar
  27. Klauber LM (1972) Rattlesnakes. Their habits, life histories and influence on mankind. University of California Press, CaliforniaGoogle Scholar
  28. Kuch U, Gumprecht A, Melaun C (2007) A new species of temple pitviper (Tropidolaemus Wagler, 1830) from Indonesia (Squamata: Viperidae: Crotalinae). Zootaxa 1446:1–20Google Scholar
  29. Lenk P, Kalyabina S, Wink M, Joger U (2001) Evolutionary relationships among the true vipers (Reptilia: Viperidae) inferred from mitochondrial DNA sequences. Mol Phylo Evol 19:94–104CrossRefGoogle Scholar
  30. Lillywhite HB, Henderson RW (1993) Behavioral and functional ecology of arboreal snakes. In: Seigel RA, Collins JT (eds) Snakes: ecology and behavior. The Blackburn Press, Caldwell, pp 1–48Google Scholar
  31. Lillywhite HB, LaFrentx JR, Lin YC, Tu MC (2000) The cantilever abilities of snakes. J Herpetol 34:523–528CrossRefGoogle Scholar
  32. Lindell LE (1994) The evolution of vertebral number and body size in snakes. Funct Ecol 8:708–719CrossRefGoogle Scholar
  33. Lindell LE, Forsman A, Merilã J (1993) Variation in number of ventral scales in snakes: effects on body size, growth rate and survival in the adder, Vipera berus. J Zool 230:101–115CrossRefGoogle Scholar
  34. Losos JB (1990) Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: an evolutionary analysis. Ecol Monogr 60:369–388CrossRefGoogle Scholar
  35. Losos JB (1999) Uncertainty in the reconstruction of ancestral character states and limitations on the use of phylogenetic comparative methods. Anim Behav 58:1319–1324CrossRefPubMedGoogle Scholar
  36. Losos JB, Ricklefs R (2009) Adaptation and diversification on islands. Nature 457:830–837CrossRefPubMedGoogle Scholar
  37. Lourdais O, Shine R, Bonnet X, Guillon M, Naulleau G (2004) Climate affects embryonic development in a viviparous snake, Vipera aspis. Oikos 104:551–560CrossRefGoogle Scholar
  38. Loveridge A (1945) Reptiles of the Pacific world. The MacMillan Company, New YorkGoogle Scholar
  39. Maddison WP, Maddison DR (2004) Mesquite: a modular system for evolutionary analysis. Ver 1.12. http://mesquiteproject.org
  40. Maddison WP, Maddison DR (2005) MacClade, analysis of phylogeny and character evolution, version 4.07. Sunderland Associates, Inc, Sunderland, MAGoogle Scholar
  41. Madsen T, Shine R (2000) Silver spoons and snake body sizes: prey availability early in life influences long-term growth rates of free-ranging pythons. J Anim Ecol 69:952–958CrossRefGoogle Scholar
  42. Mallow D, Ludwig D, Nilson G (2003) True vipers: natural history and toxinology of old world vipers. Krieger Publishing Co, MalabarGoogle Scholar
  43. Mao S (1993) Common terrestrial venomous snakes of Taiwan. Special Publication no. 5 National Museum of Natural Science, TaichungGoogle Scholar
  44. Martínez-Freiría F, Santos X, Pleguezuelos JM, Lizana M, Brito JC (2009) Geographical patterns of morphological variation and environmental correlations in contact zones: a multi-scale approach using two Mediterranean vipers (Serpentes). J Zool Syst Evol Res 47:357–367CrossRefGoogle Scholar
  45. Martins M, Araujo MS, Sawaya RJ, Nunes R (2001) Diversity and evolution of macrohabitat use, body size, and morphology in a monophyletic group of Neotropical pitvpers (Bothrops). J Zool 254:529–538CrossRefGoogle Scholar
  46. Mattingly WB, Jayne BC (2004) Resource use in arboreal habitats: structure affects locomotion of four ecomorphs of Anolis lizards. Ecology 85:1111–1124CrossRefGoogle Scholar
  47. Moon BR, LaDuc TJ, Dudley R, Chang A (2002) A twist to the rattlesnake tail. In: Aerts P, D’Août K, Herrel A, Van Damme R (eds) Topics in functional and ecological vertebrate morphology. Shaker Publishing, Maastricht, pp 63–76Google Scholar
  48. Norberg UM (1994) Wing design, flight performance, and habitat use in bats. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 205–239Google Scholar
  49. Osgood DW (1978) Effect of temperature on the development of meristic characters in Natrix fasciata. Copeia 1978:33–37CrossRefGoogle Scholar
  50. Pizzatto L, Marques OAV, Martins M (2007) Ecomorphology of boine snakes with emphasis on South American forms. In: Henderson RW, Powell R (eds) Biology of the boas and pythons. Eagle Mountain Publishing, Eagle Mountain, pp 35–48Google Scholar
  51. Rabatsky AM, Waterman JM (2005) Ontogenetic shifts and sex differences in caudal luring in the dusky pygmy rattlesnake, Sistrurus miliarius barbouri. Herpetologica 61:87–91CrossRefGoogle Scholar
  52. Sanders KL, Malhotra A, Gumprecht A, Thorpe RS, Kuch U (2004) Popeia inornata, a new species of pitviper from west Malaysia (Squamata: Viperidae: Crotalinae). Russ J Herp 11:171–184Google Scholar
  53. Shifley ET, VanHorn KM, Perez-Balaguer A, Franklin JD, Weinstein M, Cole SE (2008) Oscillatory lunatic frine activity is crucial for segmentation of the anterior but no posterior skeleton. Development 135:899–908CrossRefPubMedGoogle Scholar
  54. Shine R (1991) Why do larger snakes eat larger prey items. Funct Ecol 5:493–502CrossRefGoogle Scholar
  55. Shine R (2000) Vertebral numbers in male and female snakes: the roles of natural, sexual, and fecundity selection. J Evol Biol 13:455–465CrossRefGoogle Scholar
  56. Swain DP (1992) The functional basis of natural selection for vertebral traits of larvae in the stickleback Gasterosteus aculeatus. Evolution 46:987–997CrossRefGoogle Scholar
  57. Van Damme R, Vanhooydonck B (2002) Speed versus manoeuvrability: association between vertebral number and habitat structure in lacertid lizards. J Zool 258:327–334CrossRefGoogle Scholar
  58. Wüster W, Peppin L, Pook CE, Walker DE (2009) A nesting in vipers: phylogeny and historical biogeography of the Viperidae (Squamata: Serpentes). Mol Phylo Evol 49:445–459CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of BiologyUniversity of Louisiana at LafayetteLafayetteUSA

Personalised recommendations