Conservation Genetics

, Volume 8, Issue 3, pp 599–606 | Cite as

Impact of urban fragmentation on the genetic structure of the eastern red-backed salamander

  • Sarah Noël
  • Martin Ouellet
  • Patrick Galois
  • François-Joseph Lapointe
Original Paper


Urban development is a major cause of habitat loss and fragmentation. Few studies, however, have dealt with fragmentation in an urban landscape. In this paper, we examine the genetic structure of isolated populations of the eastern red-backed salamander (Plethodon cinereus) in a metropolitan area. We sampled four populations located on a mountain in the heart of Montréal (Québec, Canada), which presents a mosaic of forested patches isolated by roads, graveyards and buildings. We assessed the genetic structure of these populations using microsatellite loci and compared it to the genetic structure of four populations located in a continuous habitat in southern Québec. Our results indicate that allelic richness and heterozygosity are lower in the urban populations. Exact differentiation tests and pairwise F ST also show that the populations found in the fragmented habitat are genetically differentiated, whereas populations located in the continuous habitat are genetically homogeneous. These results raise conservation concerns for these populations as well as for rare or threatened species inhabiting urban landscapes.


Conservation genetics Habitat fragmentation Microsatellites Plethodon cinereus Urbanization 



We would like to thank D. Fournier, P. Graillon, S. Marquis, M.-J. Morin, R. Pétel, É. Richard and N. Tessier for their contribution to this study and all members of the Laboratoire d’Écologie Moléculaire et Évolution for their comments on an earlier draft of this manuscript. This study was supported by the Direction des sports, des parcs et des espaces verts de la Ville de Montréal, the Parc national du Mont-Mégantic, Amphibia-Nature, a NSERC scholarship to S. Noël and NSERC grant no. 0155251 to F.-J. Lapointe. Our sampling protocol was approved by the Comité de déontologie de l’expérimentation des animaux of the Université de Montréal.


  1. Adams FD (1903) The Monteregian Hills – a Canadian petrographical province. J Geol 2:239–282CrossRefGoogle Scholar
  2. Andersen LW, Fog K, Damgaard C (2004) Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea). Proc Biol Sci 271:1293–1302PubMedCrossRefGoogle Scholar
  3. Beebee TJC, Flower RJ, Stevenson AC, Patrick ST, Appleby PG, Fletcher C, Marsh C, Natkanski J, Rippey B, Battarbee RW (1990) Decline of the natterjack toad Bufo calamita in Britain: paleoecological, documentary and experimental evidence for breeding site acidification. Biol Conserv 53:1–20CrossRefGoogle Scholar
  4. Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci USA 95:9031–9036PubMedCrossRefGoogle Scholar
  5. Berry O, Tocher MD, Sarre SD (2004) Can assignment tests measure dispersal? Mol Ecol 13:551–561PubMedCrossRefGoogle Scholar
  6. Blaustein AR, Kiesecker JM, Chivers DP, Hokit DG, Marco A, Belden LK, Hatch A (1998) Effects of ultraviolet radiation on amphibians: field experiments. Am Zool 38:799–812Google Scholar
  7. Bonin J, Desroches J-F, Ouellet M, Leduc A (1999) Les forêts anciennes: refuges pour les salamandres. Nat Can 123(1):13–18Google Scholar
  8. Brown JL (1965) Stability of color phase ratio in populations of Plethodon cinereus. Copeia 1965:95–98CrossRefGoogle Scholar
  9. Burton TM, Likens GE (1975) Salamander populations and biomass in the Hubbard Brook Experimental Forest, New Hampshire. Copeia 1975:541–546CrossRefGoogle Scholar
  10. Connors LM, Cabe PR (2003) Isolation of dinucleotide microsatellite loci from red-backed salamander (Plethodon cinereus). Mol Ecol Notes 3:131–133CrossRefGoogle Scholar
  11. Czech B, Krausman PR, Devers PK (2000) Economic associations among causes of species endangerment in the United States. BioScience 50:593–601CrossRefGoogle Scholar
  12. deMaynadier PG, Hunter Jr ML (1998) Effects of sylvicultural edges on the distribution and abundance of amphibians in Maine. Conserv Biol 12:340–352CrossRefGoogle Scholar
  13. Dodd Jr CK, Smith LL (2003) Habitat destruction and alteration: historical trends and future prospects for amphibians. In: Semlitsch RD (ed) Amphibian conservation. Smithsonian Institution, Washington, DC, pp 94–112Google Scholar
  14. Dyrkacz S (1981) Recent instances of albinism in North American amphibians and reptiles. Society for the Study of Amphibians and Reptiles Herpetological Circular No. 11Google Scholar
  15. Ehman H, Cogger H (1985) Australia’s endangered herpetofauna: a review of criteria and policies. In: Grigg GC, Shine R, Ehmann HFW (eds) Biology of Australasian frogs and reptiles. Royal Zoological Society of New South Wales, Sydney, pp 435–447Google Scholar
  16. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  17. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Ann Rev Ecol Syst 34:487–515CrossRefGoogle Scholar
  18. Fahrig L, Pedlar JH, Pope SE, Taylor PD, Wegner JF (1995) Effect of road traffic on amphibian density. Biol Conserv 73:177–182CrossRefGoogle Scholar
  19. Forman RTT, Alexander LE (1998) Roads and their major ecological effects. Ann Rev Ecol Syst 29:207–231CrossRefGoogle Scholar
  20. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508CrossRefGoogle Scholar
  21. Gibbs JP (1998a) Distribution of woodland amphibians along a forest fragmentation gradient. Landsc Ecol 13:263–268CrossRefGoogle Scholar
  22. Gibbs JP (1998b) Genetic structure of redback salamander Plethodon cinereus populations in continuous and fragmented forests. Biol Conserv 86:77–81CrossRefGoogle Scholar
  23. Goudet J (2002) FSTAT, a software to estimate and test gene diversities and differentiation statistics from codominant markers (version Available from
  24. Green DM (1997) Perspectives on amphibian population declines: defining the problem and searching for answers. Herpetol Conserv 1:291–308Google Scholar
  25. Greer AEJ (1973) Adaptative significance of the color phases of the red-backed salamander. Yearb Am Philos Soc 1973:308–309Google Scholar
  26. Grover MC (1998) Influence of cover and moisture on abundances of the terrestrial salamanders Plethodon cinereus and Plethodon glutinosus. J Herpetol 32:489–497CrossRefGoogle Scholar
  27. Highton R (1959) The inheritance of the color phases of Plethodon cinereus. Copeia 1959:33–37CrossRefGoogle Scholar
  28. Highton R (1977) Comparison of microgeographic variation in morphological and electrophoretic traits. In: Hecht M, Steer W, Wallace B (eds) Evolutionary biology. Plenum Publishing, New York, pp 397–436Google Scholar
  29. Highton R, Webster TP (1976) Geographic protein variation and divergence in populations of the salamander Plethodon cinereus. Evolution 30:33–45CrossRefGoogle Scholar
  30. Hitchings SP, Beebee TJC (1997) Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations: implications for biodiversity conservation. Heredity 79:117–127PubMedCrossRefGoogle Scholar
  31. Hitchings SP, Beebee TJC (1998) Loss of genetic diversity and fitness in common toad (Bufo bufo) populations isolated by inimical habitat. J Evol Biol 11:269–283CrossRefGoogle Scholar
  32. Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755PubMedCrossRefGoogle Scholar
  33. Hyde EJ, Simons TR (2001) Sampling plethodontid salamanders: sources of variability. J Wildl Manage 65:624–632CrossRefGoogle Scholar
  34. Jaeger RG (1979) Seasonal spatial distributions of the terrestrial salamander Plethodon cinereus. Herpetologica 35:90–93Google Scholar
  35. Kimberling DN, Ferreira AR, Shuster SM, Keim P (1996) RAPD marker estimation of genetic structure among isolated northern leopard frog populations in the south-western USA. Mol Ecol 5:521–529PubMedCrossRefGoogle Scholar
  36. Kleeberger SR, Werner JK (1982) Home range and homing behavior of Plethodon cinereus in northern Michigan. Copeia 1982:409–415Google Scholar
  37. Knapp RA, Matthews KR (2000) Non-native fish introductions and the decline of the mountain yellow-legged frog from within protected areas. Conserv Biol 14:428–438CrossRefGoogle Scholar
  38. Kolozsvary MB, Swihart RK (1999) Habitat fragmentation and the distribution of amphibians: patch and landscape correlates in farmland. Can J Zool 77:1288–1299CrossRefGoogle Scholar
  39. Kucken DJ, Davis JS, Petranka JW, Smith CK (1994) Anakeesta stream acidification and metal contamination-effects on a salamander community. J Environ Qual 23:1311–1317CrossRefGoogle Scholar
  40. Kuhn J (1987) Strabentod der Erdkrote (Bufo bufo L.) Verlustquoten und Verkehrsaufkommen, Verhalten auf der Straße. Beiheft Veroffentlichungen Naturschutz Landschaftspflege Baden-Wurttemberg 41:175–176Google Scholar
  41. Lacy R (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158CrossRefGoogle Scholar
  42. Larson A, Wake DB, Yanev KP (1984) Measuring gene flow among populations having high-levels of genetic fragmentation. Genetics 106:293–308PubMedGoogle Scholar
  43. Lotter F, Scott Jr NJ (1977) Correlation between climate and distribution of the color morphs of the salamander Plethodon cinereus. Copeia 1977:681–690Google Scholar
  44. Marsh DM, Beckman NG (2004) Effects of forest roads on the abundance and activity of terrestrial salamanders. Ecol Appl 14:1882–1891Google Scholar
  45. Marsh DM, Thakur KA, Bulka KC, Clarke LB (2004) Dispersal and colonization through open fields by a terrestrial, woodland salamander. Ecology 85:3396–3405Google Scholar
  46. Miller JR, Hobbs RJ (2002) Conservation where people live and work. Conserv Biol 16:330–337CrossRefGoogle Scholar
  47. Muralidharan K, Wakeland EK (1993) Concentration of primer and template qualitatively affects products in random-amplified polymorphic DNA PCR. Biotechniques 14:362–364PubMedGoogle Scholar
  48. Murphy NR, Hellwig RJ (1996) Improved nucleic acid organic extraction through use of a unique gel barrier material. Biotechniques 21:934–936PubMedGoogle Scholar
  49. Ouellet M, Galois P, Pétel R, Fortin C (2005a) Les amphibiens et les reptiles des collines montérégiennes: enjeux et conservation. Nat Can 129(1):42–49Google Scholar
  50. Ouellet M, Mikaelian I, Pauli BD, Rodrigue J, Green DM (2005b) Historical evidence of widespread chytrid infection in North American amphibian populations. Conserv Biol 19:1431–1440CrossRefGoogle Scholar
  51. Pabijan M, Babik W, Rafinski J (2005) Conservation units in north-eastern populations of the Alpine newt (Triturus alpestris). Conserv Genet 6:307–312CrossRefGoogle Scholar
  52. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  53. Petranka J (1998) Salamanders of the United States and Canada. Smithsonian Institution, Washington, DCGoogle Scholar
  54. Pfingsten RA, Walker CF (1978) Some nearly all black populations of Plethodon cinereus (Amphibia, Urodela, Plethodontidae) in northern Ohio. J Herpetol 12:163–167CrossRefGoogle Scholar
  55. Piry S, Alapetite A, Cornuet J-M., Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first generation migrants detection. J Hered 95:536–539PubMedCrossRefGoogle Scholar
  56. Pounds JA, Fogden MPL, Campbell JH (1999) Biological response to climate change on a tropical mountain. Nature 398:611–615CrossRefGoogle Scholar
  57. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Nat Acad Sci USA 94:9197–9201PubMedCrossRefGoogle Scholar
  58. Raymond M, Rousset F (1995) Genepop (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  59. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  60. Reed DH, Hobbs GR (2004) The relationship between population size and temporal variability in population size. Anim Conserv 7:1–8CrossRefGoogle Scholar
  61. Reed HD (1908) A note on the coloration of Plethodon cinereus. Am Nat 42:460–465CrossRefGoogle Scholar
  62. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  63. Rieseberg LH (1996) Homology among RAPD fragments in interspecific comparisons. Mol Ecol 5:99–105Google Scholar
  64. Rosen M (1971) An erythristic Plethodon cinereus cinereus from Ste Foy, Portneuf county, Québec. Can Field-Nat 85:326–327Google Scholar
  65. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  66. Schierwater B, Ender A (1993) Different thermostable DNA-polymerases may amplify different RAPD products. Nucleic Acids Res 21:4647–4648PubMedCrossRefGoogle Scholar
  67. Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. Department of Anthropology, University of Geneva, GenevaGoogle Scholar
  68. Statistics Canada (2000) Human activity and the environment. Report 11-509-F. Statistics Canada, OttawaGoogle Scholar
  69. Tait CJ, Daniels CB, Hill RS (2005) Changes in species assemblages within the Adelaide Metropolitan Area, Australia, 1836–2002. Ecol Appl 15:346–359Google Scholar
  70. Thurow G (1961) A salamander color variant associated with glacial boundaries. Evolution 15:281–287CrossRefGoogle Scholar
  71. United Nations Population Division (2004) World urbanization prospects: the 2003 revision. United Nations Department of Economic and Social Affairs, New YorkGoogle Scholar
  72. Vos CC, Antonisse-De Jong AG, Goedhart PW, Smulders MJM (2001) Genetic similarity as a measure for connectivity between fragmented populations of the moor frog (Rana arvalis). Heredity 86:598–608PubMedCrossRefGoogle Scholar
  73. Wasser PM, Strobeck C (1998) Genetic signatures of interpopulation dispersal. Trends Ecol Evol 13:43–44CrossRefGoogle Scholar
  74. Welsh J, McClelland M (1990) Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res 18:7213–7218PubMedCrossRefGoogle Scholar
  75. Wilcove DS, McLellan CH, Dobson AP (1986) Habitat fragmentation in the temperate zone. In: Soulé ME (ed) Conservation biology. Sinauer, Sunderland, pp 237–256Google Scholar
  76. Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535PubMedCrossRefGoogle Scholar
  77. Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418CrossRefGoogle Scholar
  78. Zeisset I, Beebee TJC (2003) Population genetics of a successful invader: the marsh frog Rana ridibunda in Britain. Mol Ecol 12:639–646PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Sarah Noël
    • 1
  • Martin Ouellet
    • 2
  • Patrick Galois
    • 2
  • François-Joseph Lapointe
    • 1
  1. 1.Département de sciences biologiquesUniversité de MontréalMontréalCanada
  2. 2.Amphibia-NatureMontréalCanada

Personalised recommendations