, Volume 143, Issue 6, pp 705–716 | Cite as

Genetic diversity and genetic structure of an endemic Mexican Dusky Rattlesnake (Crotalus triseriatus) in a highly modified agricultural landscape: implications for conservation

  • Armando Sunny
  • Octavio Monroy-Vilchis
  • Martha M. Zarco-González
  • Germán David Mendoza-Martínez
  • Daniel Martínez-Gómez


It is necessary to determine genetic diversity of fragmented populations in highly modified landscapes to understand how populations respond to land-use change. This information will help guide future conservation and management strategies. We conducted a population genetic study on an endemic Mexican Dusky Rattlesnake (Crotalus triseriatus) in a highly modified landscape near the Toluca metropolitan area, in order to provide crucial information for the conservation of this species. There was medium levels of genetic diversity, with a few alleles and genotypes. We identified three genetically differentiated clusters, likely as a result of different habitat cover type. We also found evidence of an ancestral genetic bottleneck and medium values of effective population size. Inbreeding coefficients were low and there was a moderate gene flow. Our results can be used as a basis for future research and C. triseriatus conservation efforts, particularly considering that the Trans-Mexican Volcanic Belt is heavily impacted by destructive land-use practices.


Microsatellites Endemic species Conservation Rattlesnake Habitat fragmentation Conservation genetics 



We thank the following people for their help with field work: Andrea González-Fernández, Juan Carlos Guido-Patiño, Víctor Muñoz-Mora, Giovany Arturo González-Desales and Carlos Reyna-Valencia. We thank Víctor Ávila Akerberg for valuable comments and English editing. We thank the editor and two anonymous reviewers for their comments. AS is grateful to the graduate program “Ciencias Agropecuarias y Recursos Naturales” of the Autonomous University of the State of Mexico and for scholarships received from CONACYT (356612) and COMECYT.

Compliance with ethical standards

Conflict of interest and ethical approval

The authors declare that they have no conflict of interest. The manipulation of rattlesnakes was conducted with the approval of the ethics committee of Universidad Autónoma del Estado de México.

Supplementary material

10709_2015_9868_MOESM1_ESM.doc (912 kb)
Supplementary material 1 (DOC 913 kb)


  1. Aldridge RD, Duvall D (2002) Evolution of the mating season in the pitvipers of North America. Herpetological Monographs 16:1–25CrossRefGoogle Scholar
  2. Allendorf FW, Ryman N (2002) The role of genetics in population viability analysis. In: Beissinger SR, McCollough DR (eds) Population viability analysis. University of Chicago Press, Chicago, pp 50–85Google Scholar
  3. Andrews KM, Gibbons JW (2005) How do highways influence snake movement? Behavioral responses to roads and vehicles. Copeia 2005:772–782CrossRefGoogle Scholar
  4. Aresco MJ (2005) Mitigation measures to reduce highway mortality of turtles and other herpetofauna at a north Florida lake. J Wildl Manage 69:549–560CrossRefGoogle Scholar
  5. Ávila Cervantes J (2011) Análisis de la estructura y diversidad genética de cuatro poblaciones de Crotalus molossus nigrescens. Master’s Thesis, Facultad de Ciencias, UNAM, México. Accessed 11 Feb 2014Google Scholar
  6. Beaman KR, Hayes WK (2008) Rattlesnakes: Research trends and annotated checklist. In: Hayes WK, Beaman KR, Caldwell MD, Bush SP (eds) The biology of rattlesnakes. Loma Linda University Press, Loma Linda, pp 5–16Google Scholar
  7. Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029PubMedCentralPubMedGoogle Scholar
  8. Beck DD (1995) Ecology and energetics of three sympatric rattlesnake species in the Sonoran Desert. J Herpetol 29:211–223CrossRefGoogle Scholar
  9. Beerli P (2008) Migrate version 3.0: a maximum likelihood and Bayesian estimator of gene flow using the coalescent. Accessed 13 Nov 2014
  10. Beerli P (2009) How to use migrate or why are markov chain monte carlo programs dificult to use? In: Bertorelle G, Bruford MW, Haue HC, Rizzoli A, Vernesi C (eds) Population genetics for animal conservation, vol 17., Conservation BiologyCambridge University Press, Cambridge, pp 42–79Google Scholar
  11. Beerli P (2012) Migrate documentation. Accessed 17 Aug 2015
  12. Belkenhol N, Waits LP (2009) Molecular road ecology: exploring the potential of genetics for investigating transportation impacts on wildlife. Mol Ecol 18:4151–4164CrossRefGoogle Scholar
  13. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B 57:289–300Google Scholar
  14. Blouin-Demers G, Weatherhead PJ (2001a) Habitat use by black rat snakes (Elaphe obsolete obsoleta) in fragmented forests. Ecology 82:2882–2896CrossRefGoogle Scholar
  15. Blouin-Demers G, Weatherhead PJ (2001b) An experimental test of the link between foraging, habitat selection and thermoregulation in black rat snake, Elaphe obsolete obsoleta. J Anim Ecol 70:1006–1013CrossRefGoogle Scholar
  16. Booth W, Schuett GW (2011) Molecular genetic evidence for alternative reproductive strategies in North American pitvipers (Serpentes: Viperidae): long-term sperm storage and facultative parthenogenesis. Biol J Linn Soc Lond 104:934CrossRefGoogle Scholar
  17. Bryson RW Jr, Riddle BR (2012) Tracing the origins of widespread highland species: a case of Neogene diversification across the Mexican sierras in an endemic lizard. Biol J Linn Soc 105:382–394CrossRefGoogle Scholar
  18. Bryson RW, Murphy RW, Lathrop A, Lazcano-Villareal D (2011) Evolutionary drivers of phylogeographical diversity in the highlands of Mexico: a case study of the Crotalus triseriatus species group of montane rattlesnakes. J Biogeogr 38:697–710CrossRefGoogle Scholar
  19. Bryson RW, Linkem CW, Dorcas ME, Lathrop A, Jones JM, Alvarado-Díaz J, Grünwald CI, Murphy RW (2014) Multilocus species delimitation in the Crotalus triseriatus species group (Serpentes: Viperidae: Crotalinae) with the description of two new species. Zootaxa 3:475–496CrossRefGoogle Scholar
  20. Bushar LM, Reinert HK, Gelbert L (1998) Genetic variation and gene flow within and between local populations of the timber rattlesnake, Crotalus horridus. Copeia 2:411–422CrossRefGoogle Scholar
  21. Campbell JA, Lamar WW (2004) The venomous reptiles of the western hemisphere, vol II. Comstock/Cornell University Press, IthacaGoogle Scholar
  22. Canseco-Márquez L, Mendoza-Quijano F (2007) Crotalus triseriatus In: IUCN 2013 IUCN Red List of Threatened Species, Version, 20132. www.iucnredlistorg. Downloaded on 05 May 2014Google Scholar
  23. Castellano MJ, Valone TJ (2006) Effects of livestock removal and perennial grass recovery on the lizards of a desertified arid grassland. J Arid Environ 66:87–95CrossRefGoogle Scholar
  24. Challenger, A (1998) Utilización y conservación de los ecosistemas terrestres de México. Pasado, presente y futuro. CONABIO, Instituto de Biología, Agrupación Sierra Madre, MéxicoGoogle Scholar
  25. Clark RW, Brown WS, Stechert R, Zamudio KR (2008) Integrating individual behaviour and landscape genetics: the population structure of timber rattlesnake hibernacula. Mol Ecol 17:719–730PubMedGoogle Scholar
  26. Clark RW, Brown WS, Stechert R, Zamudio KR (2010) Roads, interrupted dispersal, and genetic diversity in Timber Rattlesnakes. Conserv Biol 24:1059–1069CrossRefPubMedGoogle Scholar
  27. Clark RW, Schuett GW, Repp RA, Amarello M, Smith CF et al (2014) Mating systems, reproductive success, and sexual selection in secretive species: a case study of the western diamond-backed rattlesnake, Crotalus atrox. PLoS ONE 9(3):e90616. doi: 10.1371/journal.pone.0090616 PubMedCentralCrossRefPubMedGoogle Scholar
  28. CONAPO (2010) Delimitación de las zonas metropolitanas de México.
  29. Cournet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent populations bottleneck from allele frequency data. Genetics 144:2001–2014Google Scholar
  30. Dixon MD (2011) Population genetic structure and natal philopatry in the widespread North American bat Myotis lucifugus. J Mammal 92:1343–1351CrossRefGoogle Scholar
  31. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator 2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214CrossRefPubMedGoogle Scholar
  32. Doonan TJ, Slade NA (1995) Effects of supplemental food on population dynamics of cotton rats, Sigmodon hispidus. Ecology 76:814–826CrossRefGoogle Scholar
  33. Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  34. Eldridge MD, Kinnear JE, Zenger KR, McKenzie LM, Spencer PB (2004) Genetic diversity in remnant mainland and ‘‘pristine’’ island populations of three endemic Australian macropodids (Marsupialia): Macropus eugenii, Lagorchestes hirsutus and Petrogale lateralis. Conserv Genet 5:325–338CrossRefGoogle Scholar
  35. England PR, Cornuet JM, Berthier P, Tallmon DA, Luikart G (2005) Estimating effective population size from linkage disequilibrium: severe bias in small samples. Conserv Genet 7:3003–3008Google Scholar
  36. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  37. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedCentralPubMedGoogle Scholar
  38. Figueroa-Rangel BL, Willis KJ, Olvera-Vargas M (2010) Cloud forest dynamics in the Mexican Neotropics during the last 1300 years. Glob Change Biol 16:1689–1704CrossRefGoogle Scholar
  39. Flores-Villela V, Canseco-Márquez L (2004) Nuevas especies y cambios taxonómicos para la herpetofauna de México. Acta Zool Mex Nueva 20:115–144Google Scholar
  40. Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675CrossRefGoogle Scholar
  41. Galicia L, García-Romero A (2007) Land use and land cover change in highland temperate forests in the Izta-Popo National Park, central Mexico. Mt Res Dev 27:48–57CrossRefGoogle Scholar
  42. Gasca-Pineda J, Cassaigne I, Alonso RA, Eguiarte LE (2013) Effective population size, genetic variation, and their relevance for conservation: the bighorn sheep in Tiburon island and comparisons with managed artiodactyls. PLoS ONE 8(10):e78120. doi: 10.1371/journal.pone.0078120 PubMedCentralCrossRefPubMedGoogle Scholar
  43. Gibbs HL, Prior KA, Weatherhead PJ, Johnson G (1997) Genetic structure of populations of the threatened eastern massasauga rattlesnake, Sistrurus c. catenatus: evidence from microsatellite DNA markers. Mol Ecol 6:1123–1132CrossRefPubMedGoogle Scholar
  44. Goldberg CS, Edwards T, Kaplan ME, Goode M (2003) PCR primers for microsatellite loci in the tiger rattlesnake (Crotalus tigris, Viperidae). Mol Ecol Notes 3:539–541CrossRefGoogle Scholar
  45. Greene HW, May PG, Hardy DL, Sciturro JM, Farrell TM (2002) Parental behavior in vipers. In: Schuett GW, Höggren M, Douglas ME, Greene HW (eds) Biology of the Vipers. Eagle Mountain Publishing, Eagle Mountain, UtahGoogle Scholar
  46. Hammer Ø (2015) PAST: Paleontological Statistics software package for education and data analysis. Palaeontol Electron 4(1).
  47. Holycross AT, Douglas ME (2007) Geographic isolation, genetic divergence, and ecological non-exchangeability define ESUs in a threatened sky-island rattlesnake. Biol Conserv 134:142–154CrossRefGoogle Scholar
  48. Holycross AT, Douglas ME, Higbee JR, Bogden RH (2002) Isolation and characterization of microsatellite loci from a threatened rattlesnake (New Mexico Ridge-nosed Rattlesnake, Crotalus willardi obscurus). Mol Ecol Notes 2:537–539CrossRefGoogle Scholar
  49. Hoss SK, Guyer C, Smith LL, Schuett GW (2010) Multiscale influences of landscape composition and configuration on the spatial ecology of eastern diamond-backed rattlesnakes (Crotalus adamanteus). J Herpetol 44:110–123CrossRefGoogle Scholar
  50. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332PubMedCentralCrossRefPubMedGoogle Scholar
  51. Huey RB (1982) Temperature, physiology, and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of the reptilia. Physiology C. Physiological ecology, vol 12. Academic Press, New York, pp 25–91Google Scholar
  52. Jansen KP, Mushinsky HR, Karl SA (2008) Population genetics of the mangrove salt marsh snake, Nerodia clarkii compressicauda, in a linear fragmented habitat. Conserv Genet 9:401–410CrossRefGoogle Scholar
  53. Jiménez-Velázquez G (2013) Estructura y composición de la herpetofauna asociada a humedales en un paisaje urbano-agrícola del Eje Neovolcánico. Master’s Thesis, Facultad de Ciencias, Universidad Autónoma de Querétaro, México. Accessed 11 Feb 2014
  54. Kalinowski S, Wagner AP, Taper ML (2006) ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579CrossRefGoogle Scholar
  55. Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064CrossRefGoogle Scholar
  56. Kohn MH, York EC, Kanradt DA, Haught G, Sauvajot RM, Wayne RK (1999) Estimating population size by genotyping feces. Proc R Soc Lond B Biol Sci 266:657–663CrossRefGoogle Scholar
  57. León-Paniagua L, Navarro-Sigüenza AG, Hernández-Baños BE, Morales JC (2007) Diversification of the arboreal mice of the genus Habromys (Rodentia: Cricetidae: Neotominae) in the Mesoamerican highlands. Mol Phylogenet Evol 42:653–664CrossRefPubMedGoogle Scholar
  58. Lougheed SC, Gibbs HL, Prior KA, Weatherhead PJ (1999) Hierarchical patterns of genetic population structure in black rat snakes (Elaphe obsoleta obsoleta) as revealed by microsatellite DNA analysis. Evolution 5319:95–2001Google Scholar
  59. Luna I, Morrone JJ, Espinosa D (2007) Biodiversidad de la Faja Volcánica Transmexicana. UNAM, D. F. MéxicoGoogle Scholar
  60. Martin FD, Wike LD, Paddock LS (2000) Role of edge effect on small mammal populations in a forest fragment. Department of Energy Technical Report, Savannah River Ecology Lab, Aiken, SCGoogle Scholar
  61. Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25:1982–1983CrossRefPubMedGoogle Scholar
  62. McCormack JE, Peterson AT, Bonaccorso E, Smith TB (2008) Speciation in the highlands of Mexico: genetic and phenotypic divergence in the Mexican jay (Aphelocoma ultramarina). Mol Ecol 17:2505–2521CrossRefPubMedGoogle Scholar
  63. Mittermeier RA, Goettsch de Mittermeier C (1992) La importancia de la diversidad biológica de México. In: Sarukhán J, Dirzo R (eds) México ante los retos de la biodiversidad. CONABIO, México, pp 63–73Google Scholar
  64. Monroy-Vilchis O, Cabrera L, Suárez P, Zarco-González M, Rodríguez-Soto C, Urios V (2008) Uso tradicional de vertebrados silvestres en la Sierra Nanchititla, México. Interciencia 33:08–313Google Scholar
  65. Navarro-Sigüenza AG, Peterson AT, Nyari A, García-Deras G, García-Moreno J (2008) Phylogeography of the Buarremon brush-finch complex (Aves Emberizidae) in Mesoamerica. Mol Phylogenet Evol 47:21–35CrossRefPubMedGoogle Scholar
  66. Nei M (1972) Genetic distance between populations. Am Nat 106:283–292CrossRefGoogle Scholar
  67. Neuwald JL (2010) Population isolation exacerbates conservation genetic concerns in the endangered Amargosa vole, Microtus californicus scirpensis. Biol Conserv 143:2028–2038CrossRefGoogle Scholar
  68. Nomura T (2008) Estimation of effective number of breeders from molecular coancestry of single cohort sample. Evol Appl 1:462–474PubMedCentralCrossRefPubMedGoogle Scholar
  69. Oyler-McCance SJ, John J, Parker JM, Anderson SH (2005) Characterization of microsatellite loci isolated in midget faded rattlesnake (Crotalus viridis concolor). Mol Ecol Notes 5:452–453CrossRefGoogle Scholar
  70. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  71. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  72. Ponce-Reyes R, Reynoso-Rosales VH, Watson JEM, VanDerWal J, Fuller RA, Pressey RL, Possingham HP (2012) Vulnerability of cloud forest reserves in Mexico to climate change. Nat Clim Change 2:448–452CrossRefGoogle Scholar
  73. Pozarowski K, Bryan DS, Bosse R, Watson E, Herrmann H-W (2012) Development of polymorphic microsatellite loci for the rattlesnake species Crotalus atrox, C. cerastes and C. scutulatus (Viperidae: Crotalinae) and cross species amplification of microsatellite markers in Crotalus and Sistrurus species. Conserv Genet Resour 4:955–961CrossRefGoogle Scholar
  74. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  75. Prosser ML, Gibbs HL, Weatherhead PJ, Brown GP (2000) Genetic analysis of the mating system and opportunity for sexual selection in northern water snakes (Nerodia sipedon). Behav Ecol 13:800–807CrossRefGoogle Scholar
  76. Rasband WS (2012) ImageJ. U.S. National Institutes of Health, Bethesda, Maryland, USA. Scholar
  77. Raymond M, Rousset F (1995) GENEPOP v 12: population genetics software for exact test and ecumenicism. J Hered 86:248–249Google Scholar
  78. Ribeiro R, Santos X, Sillero N, Carretero MA, Llorente GA (2009) Biodiversity and land uses at a regional scale: Is agriculture the biggest threat for reptile assemblages? Acta Oecol 35:327–334CrossRefGoogle Scholar
  79. Rosen PC, Lowe CH (1994) Highway mortality of snakes in the Sonoran Desert of southern Arizona. Biol Conserv 68:143–148CrossRefGoogle Scholar
  80. Ruiz-Sanchez E, Specht CD (2013) Influence of the geological history of the Trans-Mexican Volcanic Belt on the diversification of Nolina parviflora (Asparagaceae: Nolinoideae). J Biogeogr 40:1336–1347CrossRefGoogle Scholar
  81. Sarukhán J, Koleff P, Carabias J, Soberon J. Dirzo R et al (2009) Capital Natural de México. Síntesis Conocimiento actual, evaluación y perspectivas de la sustentabilidad. Comision Nacional para el Uso y Conocimiento de la Biodiversidad. MéxicoGoogle Scholar
  82. Schuett GW (1992) Is long-term sperm storage an important component of the reproductive biology of temperate pitvipers? In: Campbell JA, Brodie ED Jr (eds) Biology of the pitvipers. Selva, Tyler, pp 169–184Google Scholar
  83. Sever DM, Hamlett WC (2001) Female sperm storage in reptiles. J Exp Zool 182:724–738Google Scholar
  84. Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417CrossRefGoogle Scholar
  85. Shine R, Lemaster M, Wall M, Langkilde T, Mason R (2004) Why did the snake cross the road? Effects of roads on movement and location of mates by garter snakes (Thamnophis sirtalis parietalis). Ecol Soc 9:9Google Scholar
  86. Souza AM, Pires RC, Borges VS, Eterovick PC (2015) Road mortality of the herpetofauna in a Cerrado ecosystem, central Brazil. Herpetol J 25(3):141–148Google Scholar
  87. Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc Series B 64:479–498CrossRefGoogle Scholar
  88. Sunny A, Monroy-Vilchis O, Fajardo V, Aguilera-Reyes U (2014a) Genetic diversity and structure of an endemic and critically endangered stream river salamander (Caudata: Ambystoma leorae) in Mexico. Conserv Genet 15:49–59CrossRefGoogle Scholar
  89. Sunny A, Monroy-Vilchis O, Reyna-Valencia C, Zarco-González MM (2014b) Microhabitat types promote the genetic structure of a micro-endemic and critically endangered mole salamander (Ambystoma leorae) of Central Mexico. PLoS ONE 9:e103595. doi: 10.1371/journalpone0103595 PubMedCentralCrossRefPubMedGoogle Scholar
  90. Uetz P, Hošek J (eds) The reptile database. Accessed 13 Aug 2015
  91. Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17:2566–2580CrossRefPubMedGoogle Scholar
  92. Valière N (2002) GIMLET: a computer program for analyzing genetic individual identification data. Mol Ecol Notes 10:1046–1048Google Scholar
  93. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  94. Vargas-Rodríguez YL, Platt WJ, Vázquez-García JA, Boqiun G (2010) Selecting relict montane cloud forests for conservation priorities: the case of western Mexico. Nat Areas J 30:156–174CrossRefGoogle Scholar
  95. Vázquez-Domínguez E, Vega R (2006) ¿Dónde estamos y hacia dónde vamos en el conocimiento genético de los mamíferos mexicanos? In: Vázquez-Domínguez E, Hafner DJ (eds) Genética y mamíferos mexicanos: presente y futuro. New México Museum of Natural History and Science, New Mexico, pp 67–73Google Scholar
  96. Vázquez-Domínguez E, Surárez-Atilano M, Booth W, González-Baca C, Cuarón AD (2012) Genetic evidence of a recent successful colonization of introduced species on islands: Boa constrictor imperator on Cozumel Island. Biol Invasions 14:2101–2116CrossRefGoogle Scholar
  97. Vázquez-Domínguez E, Mendoza-Martínez A, Orozco-Lugo L, Cuarón AD (2013) High dispersal and generalist habits of the bat Artibeus jamaicensis on Cozumel Island, Mexico: an assessment using molecular genetics. Acta Chiropt 15:411–421CrossRefGoogle Scholar
  98. Villarreal X, Bricker J, Reinert HK, Gelbert L, Bushar LM (1996) Isolation and characterization of microsatellite loci for use in population genetic analysis in the timber rattlesnake, Crotalus horridus. J Hered 87:152–155CrossRefPubMedGoogle Scholar
  99. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  100. White D, Minotti PG, Barczak MJ, Sifneos JC, Freemark KE, Santelmann MV, Steinitz CF, Kiester AR, Preston EM (1997) Assessing risks to biodiversity from future landscape change. Conserv Biol 11:349–360CrossRefGoogle Scholar
  101. Yanes M, Velasco JM, Suarez F (1995) Permeability of roads and railways to vertebrates: the importance of culverts. Biol Conserv 71:217–222CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Armando Sunny
    • 1
  • Octavio Monroy-Vilchis
    • 1
  • Martha M. Zarco-González
    • 1
  • Germán David Mendoza-Martínez
    • 2
  • Daniel Martínez-Gómez
    • 2
  1. 1.Centro de Investigación en Ciencias Biológicas AplicadasUniversidad Autónoma del Estado de MéxicoTolucaMexico
  2. 2.Departamento de Producción Agrícola y AnimalUniversidad Autónoma Metropolitana XochimilcoCol. Villa QuietudMexico

Personalised recommendations