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The Ecology of Morphology: The Ecometrics of Locomotion and Macroenvironment in North American Snakes

  • A. Michelle Lawing
  • Jason J. Head
  • P. David Polly
Chapter
Part of the Springer Earth System Sciences book series (SPRINGEREARTH)

Abstract

Morphological traits that have a functional relationship with the environment can be used to study relationships between organisms and environments through time and across space. Dynamics of the trait-environment complex can be studied with ecometrics in individuals, in populations, and in communities. We explored how closely correlated three skeletal traits are with substrate use, and thus macrohabitat, among communities of snakes with the goal of better understanding how climate and macrovegetation might affect snake assemblages. Substrate use explained a large part of the variance in mean length-to-width ratio of vertebrae (R 2 = 0.66), PC1 of vertebral shape of a mid trunk vertebra (R 2 = 0.46), and relative tail length (R 2 = 0.71). Furthermore, mean relative tail length in snake assemblages across North America is strongly associated with ecoregions and vegetation cover (R 2 = 0.65 and 0.47, respectively). The close relationship with macrovegetation makes relative tail length a useful tool for predicting how snake assemblages will change as climates and biomes change across space or through time. This “ecometric” approach provides a medium-scale link between data collected from ecological studies over decades to data assembled from the fossil record over thousands, tens of thousands, or even millions of years. We show how historical vegetation changes between the early twentieth and twenty-first centuries at five preserves in North America resulted in ecometric changes that parallel the geographic distribution of relative tail length in snake communities across North America.

Keywords

Climate Community morphology Ecometrics Ecomorphology Geographic variation Paleoenvironment Serpentes Taxon-free Vertebrae 

Notes

Acknowledgments

Matthew Rowe, Laura Scheiber, and Susan Spencer at the William R. Adams Zooarchaeology Lab, Indiana University, Ron Richards at the Indiana State Museum, Eileen Westwig at the American Museum of Natural History, Phil Myers at the University of Michigan, Kevin DeQueiroz and George Zug at the Smithsonian Institution, Kevin Seymour at the Royal Ontarioi Museum, Colin McCarthy and David Gower at the Natural History Museum, London, Christopher J. Bell at the University of Texas at Austin, Heidi Price-Thomas at Queen Mary, University of London, Carl Franklin and Jonathan Campbell at University of Texas at Arlington and Bill Stanley and Harold Voris at the Field Museum of Natural History provided specimens in their care. Christopher J. Bell, Jussi Eronen, Mikael Fortelius, Robert Guralnick, Anne Hereford, Steve Le Comber, Norman Macleod, Jesse Meik, and Eric Smith discussed or assisted with parts of this work. This work was supported by Indiana University and a grant from the US National Science Foundation (EAR-0843935) and is a contribution to the Integrated Climate Change Biology programme (iCCB) of the International Union of Biological Sciences (IUBS). Early data collection was supported by a NSF Biological Informatics Postdoctoral Fellowship to JJH (NSF 98–162, 0204082).

References

  1. Adalsteinsson SA, Branch WA, Trape S, Vitt LJ, Hedges SB (2009) Molecular phylogeny, classification, and biogeography of snakes of the family Leptotyphlopidae (Reptilia, Squamata). Zootaxa 2244:1–50Google Scholar
  2. Bailey RG (1998) Ecoregions map of North America. US Forest Serv Misc Publ 1548:1–10Google Scholar
  3. Bailey RG (2005) Identifying ecoregion boundaries. Environ Manage 34:S14–S16CrossRefGoogle Scholar
  4. Barnosky AD, Kaplan MH, Carrasco MA (2004) Assessing the effect of Middle Pleistocene climate change on Marmota populations from the Pit Locality. In: Barnosky AD (ed) Biodiversity response to climate change in the Middle Pleistocene. University of California Press, BerkeleyGoogle Scholar
  5. Blain H-A, Bailon S, Cuenca-Bescós G, Bennàsar M, Rofes J, López-García JM, Huguet R, Arsuaga JL, Castro JMBd, Carbonell E (2010) Climate and environment of the earliest West European hominins inferred from amphibian and squamate reptile assemblages: Sima del Elefante Lower Red Unit, Atapuerca, Spain. Quaternary Sci Rev 29:3034–3044CrossRefGoogle Scholar
  6. Böhme M, Ilg A, Ossig A, Küchenhoff H (2006) New method to estimate paleoprecipitation using fossil amphibians and reptiles and the middle and late Miocene precipitation gradients in Europe. Geology 34:425–428CrossRefGoogle Scholar
  7. Brodman R, Cortwright S, Resetar A (2002) Historical changes of reptiles and amphibians of northwest Indiana fish and wildlife properties. Am Midl Nat 147:135–144CrossRefGoogle Scholar
  8. Burbrink FT (2005) Inferring the phylogenetic position of Boa constrictor among the Boinae. Mol Phylogenet Evol 34:167–180CrossRefGoogle Scholar
  9. Busby WH, Parmelee JR (1996) Historical changes in a herpetofaunal assemblage in the Flint Hills of Kansas. Am Midl Nat 135:81–91CrossRefGoogle Scholar
  10. Castoe TA, Parkinson CL (2006) Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Mol Phylogenet Evol 39:91–110CrossRefGoogle Scholar
  11. Caumul R, Polly PD (2005) Phylogenetic and environmental components of morphological variation: skull, mandible, and molar shape in marmots (Marmota, Rodentia). Evolution 59:2460–2472Google Scholar
  12. Crother BI (1999) Phylogenetic relationships among West Indian Xenodontine snakes (Serpentes; Colubridae) with comments on the phylogeny of some mainland Xenodontines. Contemporary Herpetology 2:1–4Google Scholar
  13. Damuth JD, Jablonski D, Harris RM, Potts R, Stucky RK, Sues HD, Weishampel DB (1992) Taxon-free characterization of animal communities. In: Beherensmeyer AK, Damuth JD, diMichele WA, Potts R, Sues HD, Wing SL (eds) Terrestrial ecosystems through time: evolutionary paleoecology of terrestrial plants and animals. University of Chicago Press, ChicagoGoogle Scholar
  14. Dryden IL, Mardia KV (1998) Statistical Shape Analysis. John Wiley and Sons, New YorkGoogle Scholar
  15. Emerson BC, Gillespie RG (2008) Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol Evol 23:619–630CrossRefGoogle Scholar
  16. Eronen JT, Polly PD, Fred M, Damuth J, Frank DC, Mosbrugger V, Scheidegger C, Stenseth NC, Fortelius M (2010a) Ecometrics: the traits that bind the past and present together. Integr Zool 5:88–101CrossRefGoogle Scholar
  17. Eronen JT, Puolamäki K, Liu L, Lintulaakso K, Damuth J, Janis C, Fortelius M (2010b) Precipitation and large herbivorous mammals I: estimates from present-day communities. Evol Ecol Res 12:217–233Google Scholar
  18. Eronen JT, Puolamäki K, Liu L, Lintulaakso K, Damuth J, Janis C, Fortelius M (2010c) Precipitation and large herbivorous mammals II: applications to fossil data. Evol Ecol Res 12:235–248Google Scholar
  19. Fischer AG (1960) Latitudinal variations in organic diversity. Evolution 14:64–81CrossRefGoogle Scholar
  20. Fitch HS (2006) Collapse of a fauna: reptiles and turtles of the University of Kansas natural history reservation. J Kans Herpetol 17:10–13Google Scholar
  21. Fortelius M, Eronen J, Jernvall J, Liu LP, Pushkina D, Rinne J, Tesakov A, Vislobokova I, Zhang ZQ, Zhou LP (2002) Fossil mammals resolve regional patterns of Eurasian climate change over 20 million years. Evol Ecol Res 4:1005–1016Google Scholar
  22. Franca FGR, Mesquita DO, Nogueira CC, Araujo AFB (2008) Phylogeny and ecology determine morphological structure in a snake assemblage in the Central Brazilian Cerrado. Copeia 1:23–38CrossRefGoogle Scholar
  23. Garland T, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292Google Scholar
  24. Gower JC (1975) Generalized Procrustes analysis. Psychometrika 40:33–51CrossRefGoogle Scholar
  25. Guyer C, Donnelly MA (1990) Length–Mass relationships among an assemblage of tropical snakes in Costa Rica. J Trop Ecol 6:65–76CrossRefGoogle Scholar
  26. Head JJ (2010) Climatic inferences from extant and fossil reptiles: toward a metabolic paleothermometer. AGU fall meeting abstracts, vol #B51F-0412. Smithsonian/NASA Astrophysics Data SystemGoogle Scholar
  27. Head JJ, Bloch JI, Hastings AK, Bourque JR, Cadena EA, Herrera FA, Polly PD, Jaramillo CA (2009) Giant boid snake from the Palaeocene neotropics reveals hotter past equatorial temperatures. Nature 457:715–718CrossRefGoogle Scholar
  28. Helmus MR, Savage K, Diebel MW, Maxted JT, Ives AR (2007) Separating the determinants of phylogenetic community structure. Ecol Lett 10:917–925CrossRefGoogle Scholar
  29. Holm PA (2008) Phylogenetic biology of the burrowing snake tribe Sonorini (Colubridae). University of Arizona, TusconGoogle Scholar
  30. Hossack BR, Corn PS, Pilliod DS (2005) Lack of significant changes in the herpetofauna of Theodore Roosevelt National Park, North Dakota, since the 1920s. Am Midl Nat 154:423–432CrossRefGoogle Scholar
  31. Jablonski D (2008) Species selection: theory and data. Annu Rev Ecol Evol Syst 39:501–524CrossRefGoogle Scholar
  32. Jadin RC, Gutberlet RL, Smith EN (2010) Phylogeny, evolutionary morphology, and hemipenis descriptions of the Middle American jumping pitvipers (Serpentes: Crotalinae: Atropoides). J Zool Syst Evol Res 48:360–365CrossRefGoogle Scholar
  33. Janis CM, Fortelius M (1988) On the means whereby mammals achieve increased functional durability of their dentitions, with special reference to limiting factors. Biol Rev Camb Philos Soc 63:197–230CrossRefGoogle Scholar
  34. Jenks GF (1977) Optimal data classification for choropleth maps. University of Kansas Department of Geography Occasional Papers 2:1–24Google Scholar
  35. Johnson RG (1955) The adaptive and phylogenetic significance of vertebral form in snakes. Evolution 9:367–388CrossRefGoogle Scholar
  36. King RB (2008) Sexual dimorphism in snake tail length: sexual selection, natural selection, or morphological constraint? Biol J Linn Soc 38:133–154CrossRefGoogle Scholar
  37. Kozak KH, Larson A, Bonett RM, Harmon LJ (2005) Phylogenetic analysis of ecomorphological divergence, community structure, and diversification rates in dusky salamanders (Plethodontidae: Desmognathus). Evolution 59:2000–2016Google Scholar
  38. Kraft NJB, Cornwell WK, Webb CO, Ackerly DD (2007) Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat 170:271–283CrossRefGoogle Scholar
  39. Lawing AM, Polly PD (2011) Pleistocene climate, phylogeny, and climate envelope models: an integrative approach to better understand species’ response to climate change. PLoS One 16:e28554CrossRefGoogle Scholar
  40. Lawson R, Slowinski JB, Crother BI, Burbrink FT (2005) Phylogeny of the Colubroidea (Serpentes): new evidence from mitochondrial and nuclear genes. Mol Phylogenet Evol 37:581–601CrossRefGoogle Scholar
  41. Lindell LE (1994) The evolution of vertebral number and body size in snakes. Funct Ecol 8:708–719CrossRefGoogle Scholar
  42. Lindsey AA, Crankshaw WB, Qadir SA (1965) Soil relations and distribution map of the vegetation of presettlement Indiana. Bot Gazette 126:155–163CrossRefGoogle Scholar
  43. Little SA, Kembel SW, Wilf P (2010) Paleotemperature proxies from leaf fossils reinterpreted in light of evolutionary history. PLoS One 5:e15161CrossRefGoogle Scholar
  44. Maguire KC, Stigall AL (2009) Using ecological niche modeling for quantitative biogegoraphic analysis: a case study of Miocene and Pliocene Equinae in the Great Plains. Paleobiology 35:587–611CrossRefGoogle Scholar
  45. Makarieva AM, Gorshkov VG, Li BL (2005) Gigantism, temperature and metabolic rate in terrestrial poikilotherms. Proc R Soc B Biol Sci 272:2325–2328CrossRefGoogle Scholar
  46. 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 pitvipers (Bothrops). J Zool 254:529–538CrossRefGoogle Scholar
  47. Matthews E (1983) Global vegetation and land use: new high-resolution data bases for climate studies. J Clim Appl Meteorol 22:474–487CrossRefGoogle Scholar
  48. Matthews E (1984) Prescription of land-surface boundary conditions in GISS GCM II: a simple method based on high-resolution vegetation datasets NASA TM-86096. National Aeronautics and Space Administration, Washington, DCGoogle Scholar
  49. Maurer BA (1999) Untangling ecological complexity: the macroscopic perspective. University of Chicago Press, ChicagoGoogle Scholar
  50. McGill B (2010) Matters of scale. Science 328:575CrossRefGoogle Scholar
  51. Mosbrugger V, Utescher T, Dilcher DL (2005) Cenozoic continental climatic evolution of Central Europe. Proc Natl Acad Sci USA 102:14964–14969CrossRefGoogle Scholar
  52. Mullin SJ, Seigel RA (2009) Sankes: ecology and conservation. Cornell University Press, IthacaGoogle Scholar
  53. Myers CE, Lieberman BS (2010) Sharks that pass in the night: using geographical information systems to investigate competition in the Cretaceous Western Interior Seaway. Proc R Soc B Biol Sci 278:681–689CrossRefGoogle Scholar
  54. Olalla-Tarraga MA, Rodriguez MA, Hawkins BA (2006) Broad-scale patterns of body size in squamate reptiles of Europe and North America. J Biogeogr 33:781–793CrossRefGoogle Scholar
  55. Polly PD (2003) Paleophylogeography: the tempo of geographic differentiation in marmots (Marmota). J Mammal 84:369–384CrossRefGoogle Scholar
  56. Polly PD (2010) Tiptoeing through the trophics: geographic variation in carnivoran locomotor ecomorphology in relation to environment. In: Goswami A, Friscia A (eds) Carnivoran evolution: new views on phylogeny, form, and function. Cambridge studies in morphology and molecules: new paradigms in evolutionary biology. Cambridge University Press, CambridgeGoogle Scholar
  57. Polly PD, Eronen JT (2011) Mammal associations in the Pleistocene of Britain: implications of ecological niche modelling and a method for reconstrucing palaeoclimate. In: Ashton N, Lewis SG, Stringer C (eds) The ancient human occupation of Britain. Elsevier, New YorkGoogle Scholar
  58. Polly PD, Eronen JT, Fred M, Dietl GP, Mosbrugger V, Scheidegger C, Frank DC, Damuth J, Stenseth NC, Fortelius M (2011) History matters: ecometrics and integrative climate change biology. Proc R Soc B Biol Sci 278:1131–1140CrossRefGoogle Scholar
  59. Prentice IC, Cramer W, Harrison SP, Leemans R, Monserud RA, Solomon AM (1992) A global biome model based on palent physiology and dominance, soil properties and climate. J Biogeogr 19:117–134CrossRefGoogle Scholar
  60. Pyron RA, Burbrink FT, Colli GR, Montes de Oca AN, Vitt LJ, Kuczynski CA, Wiens JJ (2011) The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Mol Phylogenet Evol 58:329–342CrossRefGoogle Scholar
  61. Reading CJ, Luiselli LM, Akani GC, Bonet X, Amori G, Ballouard JM, Filippi E, Naulleau G, Pearson D, Rugiero L (2010) Are snake populations in widespread decline? Biol Lett 6:777–780CrossRefGoogle Scholar
  62. Ricklefs RE, Miles DB (1994) Ecological and evolutionary inferences form morphology: an ecological perspective. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, ChicagoGoogle Scholar
  63. Rodríguez MA, 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
  64. Rohlf FJ, Slice D (1990) Extentions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59CrossRefGoogle Scholar
  65. Row LW, Hastings DA (1994) TerrainBase worldwide digital terrain data (release 1.0). National Oceanic and Atmospheric Administration, National Geophysical Data Center, BoulderGoogle Scholar
  66. Sanders KL, Mumpuni AH, Head JJ, Gower DJ (2010) Phylogeny and divergence times of filesnakes (Acrochordus): inferences from morphology, fossils and three molecular loci. Mol Phylogenet Evol 56:857–867CrossRefGoogle Scholar
  67. Scheiter S, Higgins SI (2009) Impacts of climate change on the vegetation of Africa: an adptive dynamic vegetation modelling approach. Global Change Biol 15:2224–2246CrossRefGoogle Scholar
  68. Sigala Rodríguez JJ, Greene HW (2009) Landscape change and conservation priorities: Mexican herpetofaunal perspectives at local and regional scales. Revista Mexicana de Biodiversidad 80:231–240Google Scholar
  69. Slowinski JB, Lawson R (2002) Snake phylogeny: evidence from nuclear and mitochondrial genes. Mol Phylogenet Evol 24:194–202CrossRefGoogle Scholar
  70. Sneath PH (1967) Trend-surface analysis of transformation grids. J Zool 151:65–122CrossRefGoogle Scholar
  71. Svenning J-C, Flojgaard C, Marske KA, Nógues Bravo D, Normand S (2011) Applications of species distribution modeling to paleobiology. Quaternary Sci Rev 30:2930–2947CrossRefGoogle Scholar
  72. Tingley MW, Beissinger SR (2009) Detecting range shifts from historical species occurrences: new perspectives on old data. Trends Ecol Evol 24:625–633CrossRefGoogle Scholar
  73. Varela S, Lobo JM, Hortal J (2011) Using species distribution models in paleobiogeography: a matter of data, predictors and concepts. Palaeogeogr Palaeoclimat Palaeoecol 310:451–463CrossRefGoogle Scholar
  74. Vidal N, Kindl SG, Wong A, Hedges SB (2000) Phylogenetic relationships of xenodontine snakes inferred from 12S and 16S ribosomal RNA sequences. Mol Phylogenet Evol 14:389–402CrossRefGoogle Scholar
  75. Webb JK, Shine R (1998) Using thermal ecology to predict retreat-site selection by an endangered snake species. Biol Conserv 86:233–242CrossRefGoogle Scholar
  76. Webb CT, Hoeting JA, Ames GM, Pyne MI, Poff NL (2010) A structure and dynamic framework to advance traits-based theory and prediction in ecology. Ecol Lett 13:267–283CrossRefGoogle Scholar
  77. Wiens JA, Bachelet D (2010) Matching the multiple scales of conservation with the multiple scales of climate change. Conserv Biol 24:51–62CrossRefGoogle Scholar
  78. Wiens JJ, Brandley MC, Reeder TW (2006) Why does a trait evolve multiple times within a clade? repeated evolution of snakelike body form in squamate reptiles. Evolution 60:123–141Google Scholar
  79. Wilcox TP, Zwickl DJ, Heath TA, Hillis DM (2002) Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Mol Phylogenet Evol 25:361–371CrossRefGoogle Scholar
  80. Williams JW, Blois JL, Shuman BN (2011) Extrinsic and instrinsic forcing of abrupt ecological change: case studies from the late Quaternary. J Ecol 99:664–677CrossRefGoogle Scholar
  81. Willis KJ, Gillson L, Brncic TM, Figueroa-Rangel BL (2005) Providing baselines for biodiversity measurement. Trends Ecol Evol 20:107–108CrossRefGoogle Scholar
  82. Willmott KM, Legates DR (1998) Global air temperature and precipitation: regridded monthly and annual climatologies (version 2.01). Center for Climatic Research, University of Delaware, NewarkGoogle Scholar
  83. Wilson JA, Dhananjay MM, Peters SE, Head JJ (2010) Predation upon hatchling dinosaurs by a new snake from the late cretaceous of India. PLoS Biol 8:e1000322CrossRefGoogle Scholar
  84. Wolfe JA (1979) Temperature parameters of humid to mesic forests of Eastern Asia and relation to forests of other regions in the Northern Hemisphere and Australasia. US Geol Survey Prof Pap 1106:1–37Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • A. Michelle Lawing
    • 1
  • Jason J. Head
    • 2
  • P. David Polly
    • 3
  1. 1.Department of Geological Sciences and BiologyIndiana UniversityBloomingtonUSA
  2. 2.Department of Earth and Atmospheric SciencesUniversity of Nebraska-LincolnLincolnUSA
  3. 3.Department of Geological SciencesIndiana UniversityBloomingtonUSA

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