Skip to main content

Advertisement

SpringerLink
Log in

Population genetics of the mangrove salt marsh snake, Nerodia clarkii compressicauda, in a linear, fragmented habitat

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The mangrove salt marsh snake (Nerodia clarkii compressicauda) occupies a unique and disappearing habitat in much of coastal southern Florida. Given extensive habitat fragmentation and high predation pressure in open spaces, it seems likely that populations of N. c. compressicauda consist of isolated groups of related individuals. To assess the degree of population subdivision in this species we genotyped a total of 125 individuals from seven locations along the Florida coast at four microsatellite loci. Overall heterozygosity was moderate (57.7%) and somewhat lower than that seen in other snake species. Population subdivision was particularly pronounced with 19 of 21 sample pair-wise ΦST values significantly different from zero and ranging from 0.064 to 0.343 (P ≤ 0.05). About 11 of 39 alleles were private alleles that also tended to be in high frequency in the populations where they occurred (average frequency ~27%). The correlation of genetic and geographic distances was highly significant and positive (r 2 = 0.8733 and P < 0.001) with ΦST increasing by ~0.01 for every 10 km of separation. Overall, salt marsh snake populations appear to be fractured into isolated neighborhoods on the order of 50–80 km. In spite of its apparent local abundance, we believe that N. c. compressicauda is in need of conservation protection. The combination of extremely low dispersal, narrow habitat requirements, and most importantly, extensive habitat alteration resulting from coastal real estate development may mean that N. c. compressicauda is highly susceptible to population extirpation and potentially extinction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig 1
Fig 2

Similar content being viewed by others

References

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidmen JG, Smith JA, Struhl K, Wang-Iverson P, Bonitz SG (1993) Current protocols in molecular biology. Greene Publishing Associates and Wiley-Interscience, New York

    Google Scholar 

  • Barbour RW, Harvey MJ, Hardin JW (1969) Home range, movements, and activity of the eastern worm snake, Carphophis amoenus amoenus. Ecology 50:470–476

    Article  Google Scholar 

  • Birnhak BI, Crowder JP (1974) An evaluation of the extent of vegetative habitat alteration in South Florida, 1943–1970. Ecological Report No. DI-SFEP-74-22 of South Florida Environmental Project, Bureau of Sport Fisheries and Wildlife, United States Department of the Interior, Atlanta, Georgia

  • Blouin-Demers G, Gibbs HL (2003) Isolation and characterization of microsatellite loci in the black rat snake (Elaphe obsolete). Mol Ecol Note 3:98–99

    Article  CAS  Google Scholar 

  • Bonnet X, Naulleau G, Shine R (1999) The dangers of leaving home: dispersal and mortality in snakes. Biol Conserv 89:39–50

    Article  Google Scholar 

  • Brown WS, Parker WS (1976) A ventral scale clipping system for permanently marking snakes (Reptilia, Serpentes). J Herpetol 10:247–249

    Article  Google Scholar 

  • Bureau of Economic and Business Research (1998) Florida statistical abstract. University Presses of Florida, Gainesville

    Google Scholar 

  • Burns EL, Houlden BA (1999) Isolation and characterization of microsatellite markers in the broad-headed snake Hoplocephalus bungaroides. Mol Ecol 8:520–521

    CAS  Google Scholar 

  • Conant R, Collins JT (1991) A field guide to reptiles and amphibians of eastern and central North America, 3rd edn. Houghton Mifflin, Boston

    Google Scholar 

  • Dallas JF (1992) Estimation of microsatellite mutation rates in recombinant inbred strains of mouse. Mamm Gen 5:32–38

    Google Scholar 

  • Dessauer HC, Cadle JE, Lawson R (1987) Patterns of snake evolution suggested by their proteins. Fieldiana: Zoology 34:1–34

    Google Scholar 

  • Dunson WA (1980) The relation of sodium and water balance to survival in sea water of estuarine and freshwater races of the snakes Nerodia fasciata, N. sipedon and N. valida. Copeia 1980:268–280

    Article  Google Scholar 

  • Estoup A, Jarne P, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetic analysis. Mol Ecol 11:1591–1604

    Article  PubMed  CAS  Google Scholar 

  • 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 131:479–491

    PubMed  CAS  Google Scholar 

  • Farnsworth EJ, Ellison AM (1997) The global conservation status of mangroves. Ambio 26:328–334

    Google Scholar 

  • Fosberg FR (1971) Mangroves versus tidal waves. Biol Conserv 4:38–39

    Article  Google Scholar 

  • García-Moreno J, Matocq MD, Roy MS, Geffen E, Wayne RK (1996) Relationships and genetic purity of the endangered Mexican wolf based on analysis of microsatellite loci. Conserv Biol 10:376–389

    Article  Google Scholar 

  • Gartside DF, Rogers JS, Dessauer HC (1977) Speciation with little genetic and morphological differentiation in the ribbon snakes Thamnophis proximus and T. sauritus (Colubridae). Copeia 1977:697–705

    Article  Google Scholar 

  • Gautschi B, Widmer A, Koella J (2000) Isolation and characterization of microsatellite loci in the dice snake (Natrix tessellata). Mol Ecol 9:2191–2193

    PubMed  CAS  Google Scholar 

  • Gibbs HL, Prior KA, Parent C (1998) Characterization of DNA microsatellite loci from a threatened snake: the eastern massasauga rattlesnake (Sistrurus c. catenatus) and their use in population studies. J Hered 89:169–172

    Article  CAS  Google Scholar 

  • Gibbs HL, Prior KA, Weatherhead PJ (1994) Genetic analysis of populations of threatened snake species using RAPD markers. Mol Ecol 3:329–337

    Article  CAS  Google Scholar 

  • 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 6:1123–1132

    Article  PubMed  CAS  Google Scholar 

  • Gibbs HL, Weatherhead PJ (2001) Insights into population ecology and sexual selection in snakes through the application of DNA-based genetic markers. J Hered 92:173–179

    Article  PubMed  CAS  Google Scholar 

  • Gregory PT, Macartney JM, Larsen KW (1987) Activity Patterns. In: Seigel RA, Collins JT, Novak SS (eds) Snakes: ecology and evolutionary biology. MacMillan, New York, pp 396–421

    Google Scholar 

  • Guo S, Thompson E (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  PubMed  CAS  Google Scholar 

  • Hille A, Janssen IAW, Menken SBJ, Schlegel M, Thorpe RS (2002) Heterologous amplification of microsatellite markers from colubroid snakes in European Natricines (Serpentes: Natricinae). J Hered 93:63–66

    Article  PubMed  CAS  Google Scholar 

  • Kandpal RP, Kandpal C, Weissman SM (1994) Construction of libraries enriched for sequence repeats and jumping clones, and hybridization selection for region-specific markers. Proc Natl Acad Sci USA 91:88–92

    Article  PubMed  CAS  Google Scholar 

  • Kautz RS (1993) Trends in Florida wildlife habitat 1936–1987. Fla Sci 56:7–24

    Google Scholar 

  • Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576

    PubMed  CAS  Google Scholar 

  • Kochman HI, Christman SP (1978) Endangered: Atlantic salt marsh snake. In: McDiarmid RW (ed) Rare and endangered biota of Florida, vol 3: amphibians and reptiles. University Presses of Florida, Gainesville

    Google Scholar 

  • Lawson R (1987) Molecular studies of Thamnophiine snakes: I. The phylogeny of the genus Nerodia. J Herpetol 21:140–157

    Article  Google Scholar 

  • Levene H (1949) On a matching problem arising in genetics. Ann Math Stat 20:91–94

    Article  Google Scholar 

  • Lewis RR III, Dunstan FM (1975) Use of spoil islands in re-established mangrove communities in Tampa Bay, Florida. In: Walsh GE, Snedaker S, Teas H (eds) Proceedings of the international symposium on the biological management of mangroves. University of Florida, Gainesville, pp 766–775

    Google Scholar 

  • Lewis RR III, Lewis CS, Fehring, WK, Rodgers JA (1979) Coastal habitat mitigation in Tampa Bay, Florida. In: Proceedings of the mitigation symposium, general technical report RM-65, United States Department of Agriculture, Fort Collins, CO, pp 136–140

  • Lindall WM Jr, Saloman CH (1977) Alteration and destruction of estuaries affecting fisheries resources of the Gulf of Mexico. Mar Fish Rev 39:1262

    Google Scholar 

  • Lougheed SC, Gibbs HL, Prior KA, Weatherhead PJ (1999) Hierarchical patterns of genetic population structure in black rat snakes as revealed by microsatellite DNA markers. Evolution 53:1995–2001

    Article  CAS  Google Scholar 

  • Lowe DW, Matthews JR, Mosely CJ (eds) (1990) The official World Wildlife Fund guide to endangered species of North America, vol 2. Beachum Publishing, Washington, DC

    Google Scholar 

  • Madsen T, Stille B, Shine R (1996) Inbreeding depression in an isolated population of adders Vipera berus. Biol Conserv 75:113–118

    Article  Google Scholar 

  • Manier MK, Arnold SJ (2005) Population genetic analysis identifies source-sink dynamics for two sympatric garter snake species (Thamnophis elegans and Thamnophis sirtalis). Mol Ecol 14:3965–3976

    Article  PubMed  Google Scholar 

  • Mantel NA (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference to microsatellite loci. Genetics 142:1061–1064

    PubMed  CAS  Google Scholar 

  • Miller DE, Mushinsky HR (1990) Foraging ecology and prey size in the mangrove water snake Nerodia fasciata compressicauda. Copeia 1990:1099–1106

    Article  Google Scholar 

  • Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trend Ecol Evol 9:373–374

    Article  Google Scholar 

  • Mushinsky HR, Miller DE (1993) Predation on water snakes: ontogenetic and interspecific considerations. Copeia 1993:660–665

    Article  Google Scholar 

  • Odum WE, McIvor CC (1990) Mangroves. In: Myers RL, Ewel JJ (eds) Ecosystems of Florida. University Presses, Orlando

    Google Scholar 

  • Odum WE, McIvor CC, Smith TJ III (1982) The ecology of the mangroves of South Florida: a community profile. US Fish. Wild. Ser. Tech. Rep., FWS/OBS 81-24

  • Paetkau D, Strobeck C (1994) Microsatellite analysis of genetic variation in black bear populations. Mol Ecol 3:489–495

    Article  PubMed  CAS  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  PubMed  CAS  Google Scholar 

  • Patterson SG (1986) Mangrove community boundary interpretation and detection of areal changes in Marco Island, Florida: application of digital image processing and remote sensing techniques. US Fish Wild Serv Biol Rep No 86(10)

  • Pettus D (1963) Salinity and subspeciation in Natrix sipedon. Copeia 1963:449–504

    Article  Google Scholar 

  • Prosser MR, Gibbs HL, Weatherhead PJ (1999) Microgeographic population genetic structure in the northern water snake, Nerodia sipedon sipedon detected using microsatellite DNA loci. Mol Ecol 8:329–333

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  • Robertson AI, Alongi DM (1992) Tropical mangrove ecosystems: coastal and estuarine studies, vol 41. American Geophysical Union

  • Rohlf FJ, Schnell GD (1971) An investigation of the isolation-by-distance model. Am Nat 105:295–324

    Article  Google Scholar 

  • Rose FL, Selcer KW (1989) Genetic divergence of the allopatric populations of Nerodia harteri. J Herpetol 23:261–267

    Article  Google Scholar 

  • Sattler PW, Guttman SI (1976) An electrophoretic analysis of Thamnophis sirtalis from Western Ohio. Copeia 1976:352–356

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin version 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland

    Google Scholar 

  • Scott IAW, Hayes CM, Keogh JS, Webb JK (2001) Isolation and characterization of novel microsatellite markers from the Australian tiger snakes (Elapidae: Notechis) and amplification in the closely related genus Hoplocephalus. Mol Ecol Note 1:117–119

    Article  CAS  Google Scholar 

  • Sellers JC, Trauth SE, Wit LC (1980) A method of caudal blood collection in lizards. J Herpetol 14:185–187

    Article  Google Scholar 

  • Severance EG, Szmant AM, Karl SA (2004) Microsatellite loci isolated form the Caribbean coal, Montastraea annularis. Mol Ecol Note 4:74–76

    Article  CAS  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Slatkin M, Excoffier L (1996) Testing for linkage disequilibrium in genotypic data using the EM algorithm. Heredity 76:377–383

    Article  PubMed  Google Scholar 

  • Thompson JS, Crother BI (1998) Allozyme variation among disjunct populations of the Florida green watersnake (Nerodia floridana). Copeia 1998:715–719

    Article  Google Scholar 

  • Vogler AP, DeSalle R (1992) Diagnosing units of conservation management. Conserv Biol 8:354–363

    Article  Google Scholar 

  • Waples RS (1991) Definition of a “species” under the Endangered Species Act: application to Pacific salmon. National Ocean and Atmospheric Administration Technical Memorandum, NMFS-F/NWC 194, Northwest Fisheries Science Center, Seattle, WA

  • Waples RS (1995) Evolutionary significant units and the conservation of biological diversity under the Endangered Species Act. In: Nielson JL (ed) Evolution and the aquatic ecosystem: defining unique units in population conservation. Symposium 17 American Fisheries Society, Bethesda, Maryland, pp 8–27

    Google Scholar 

  • Ward RD, Skibinski DOF, Woodwark M (1992) Protein heterozygosity, protein structure, and taxonomic differentiation. Evol Biol 26:73–159

    CAS  Google Scholar 

  • World Resources Institute (1996) World resources 1996–1997. Oxford University Press, New York

    Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

P. Delis, E. Sutton, P. Kwiatkowski, T. Lamb, P. Moler, A. Summers, and D. Wilson assisted with sample collections. A. Bass, M. Cattell, C. Curtis, K. Hayes, C. Puchulutegui, T. Schwartz, E. Severance, and J. T. Streelman provided laboratory and data analysis assistance. An early version of this manuscript benefited from comments by M. Tringali and two anonymous reviewers. Funding for this project was provided, in part, by NSF grant DEB 98-06905 and DEB 03-21924 to SAK, a Florida Fish and Wildlife Conservation Commission Non-game Wildlife Program grant to SAK, HRM, KPJ, and a grant from the Theodore Roosevelt Memorial Fund of the American Museum of Natural History to KPJ. This is SOEST contribution No. 7085 and HIMB contribution No. 1268.

Author information

Authors and Affiliations

  1. Department of Natural Sciences, University of Virginia’s College at Wise, Wise, VA, 24293, USA

    Kevin P. Jansen

  2. Department of Biology, SCA 110, University of South Florida, 4202 East Fowler Ave, Tampa, FL, 33620, USA

    Henry R. Mushinsky

  3. Hawaii Institute of Marine Biology, University of Hawaii, Manoa, P.O. Box 1346, Kaneohe, HI, 96744, USA

    Stephen A. Karl

Authors
  1. Kevin P. Jansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Henry R. Mushinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen A. Karl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephen A. Karl.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jansen, K.P., Mushinsky, H.R. & Karl, S.A. Population genetics of the mangrove salt marsh snake, Nerodia clarkii compressicauda, in a linear, fragmented habitat. Conserv Genet 9, 401–410 (2008). https://doi.org/10.1007/s10592-007-9352-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-007-9352-9

Keywords

Search

Navigation