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The Alapahoochee watershed microgeographic structure and its potential influence on metal concentrations and genetic structure in the Florida cottonmouth, Agkistrodon piscivorus conanti, within the watershed

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Abstract

This study examines the microgeographic structure of the Alapahoochee watershed, part of the Suwannee River basin, south-central GA, USA, and relates it to variations in liver metal concentrations and genetic structure of the Florida cottonmouth, Agkistrodon piscivorus conanti. One objective was to determine if liver metal concentrations in A. piscivorus differ between Grand Bay and Mud creeks, which form the watershed’s upper portion. Grand Bay Creek is relatively pristine, whereas Mud Creek is polluted with various metals. Genetic analyses were used to assess possible migration patterns between the creeks indicating whether the basin possesses a single population or two populations. Collections occurred in 2008 and 2009. Specimens were captured, euthanized, or collected as road kills, and liver metal concentrations were analyzed and DNA extracted. No differences in metal concentrations were detected between the creeks, except for nickel in females. Metal concentrations in A. piscivorus were not significantly different between males and females nor show a relationship to body size. Genetic analyses were limited to three primer sets, which amplified informative loci. Locus, CH4B, was highly divergent between the putative populations and particularly informative. Genetic structure indicates potential population isolation within the two creeks. Results suggest that two distinct A. piscivorus populations were present and those populations did not differ in their liver metal concentrations (exception being nickel), despite the differences in environmental metal concentrations in the areas. These findings provide new insight into metal accumulation and detoxification in these animals.

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References

  • ASIH Guidelines. (2004). Http://www.asih.org/sites/default/files/documents/Resources/guidelinesherpsresearch2004.pdf. Accessed 1 Sep 2017.

  • Barnett, J., Bechler, D. L., Denizman, C., Grable, J., Nienow, J., Turco, J., Tietjen, W., & Wood, G. L. (2007). Watershed restoration action strategy development in the Alapahoochee River watershed. Nonpoint Source Management Program, Section 319 Report. Environmental Protection Division, Department of Natural Resources, Georgia, USA.

  • Bechler, D. L. (2006). A survey and analysis of fish diversity in the Alapahoochee River of South Georgia (abstract). Annual Meeting of Georgia Academy of Science, 24–25 March 2006. Georgia Journal of Science 64, (1), 28–29.

  • Bechler, D. L., & Salter, J. S. (2013). The status of the blackbanded sunfish and other species of concern in the state of Georgia. Final report, Non-Game Division, Georgia Department of Natural Resources, Social Circle, Georgia, Submission date 18 December 2013.

  • Bechler, D. L., Hightower, P., Rousey, J., & Smith, M. E. (2014). The use of nest-traps to study behavior, population structure and life history of Procambarus spiculifer. Freshwater Crayfish, 20(1), 7–16.

    Article  Google Scholar 

  • Burbrink, F. T., & Guiher, T. J. (2015). Considering gene flow when using coalescent methods to delimit lineages of North American pitvipers of the genus Agkistrodon. Zoological Journal of the Linnean Society, 173(2), 505–526. https://doi.org/10.1111/zoj.12211.

    Article  Google Scholar 

  • Burger, J., Campbell, K. R., Murray, S., Campbell, T. S., Gaines, K. F., Jeitner, C., Shukla, T., Burke, S., & Gochfeld, M. (2007). Metal levels in blood, muscle and liver of water snakes (Nerodia spp.) from New Jersey, Tennessee and South Carolina. Science of the Total Environment, 373(2), 556–563.

    Article  CAS  Google Scholar 

  • Burger, J., Gochfeld, M., Jeitner, C., Zappalorti, R., Pittfield, T., & DeVito, E. (2017). Arsenic, cadmium, chromium, lead, mercury and selenium concentrations in pine snakes (Pituophis melanoleucus) from the New Jersey Pine Barrens. Archives of Environmental Contamination and Toxicology, 72(4), 586–595. https://doi.org/10.1007/s00244-017-0398-5.

    Article  CAS  Google Scholar 

  • Burkett, R. D. (1966). Natural history of cottonmouth moccasin, Agkistrodon piscivorus (reptilia). In E. Raymond Hall, H. S. Fitch, & F. B. Cross (Eds.), University of Kansas Publications, Museum of Natural History. 17(9) (pp. 435–491). Lawrence: University of Kansas.

    Google Scholar 

  • Campbell, K. R., & Campbell, T. S. (2001). The accumulation and effects of environmental contaminants on snakes: a review. Environmental Monitoring and Assessment, 70, 253–301.

    Article  CAS  Google Scholar 

  • Campbell, J. A., & Lamar, W. W. (1989). The venomous reptiles of Latin America. Ithaca: Cornell University Press.

    Google Scholar 

  • Campbell, K. R., Campbell, T. S., & Burger, J. (2005). Heavy metal concentrations in northern water snakes (Nerodia sipedon) from East Fork Poplar Creek and the Little River, East Tennessee, USA. Archives of Environmental Contamination and Toxicology, 49(2), 239–248.

    Article  CAS  Google Scholar 

  • Chaney, J. C., & Bechler, D. L. (2006). The occurrence and distribution of Heterandria formosa (Teleostei, Poeciliidae) in Lowndes County, Georgia. https://digitalcommons.gaacademy.org/cgi/viewcontent.cgi?article=1281&context=gjs. Accessed 1 Sep 2017.

  • Cikrt, M. (1981). Biliary excretion of metals. In Industrial and environmental xenobiotics (pp. 17–36). Berlin: Springer.

    Chapter  Google Scholar 

  • Clark, A. (2006). Using microsatellite loci to determine the fine scale genetic structure of a complex of timber rattlesnake (Crotalus horridus) dens in northeastern New York. Unpublished master’s thesis, University of Florida.

  • Conant, R., & Collins, J. T. (1998). A guide to reptiles and amphibians: eastern and central North America (vol. 12). Houghton Mifflin Harcourt.

  • Cross, C. L. (2002). Agkistrodon piscivorus piscivorus (eastern cottonmouth) diet. Herpetological Review, 33(1), 55–56.

    Google Scholar 

  • Dai, Z., Amatya, D. M., Sun, G., Li, C., Trettin, C. C., & Li, H. (2008). Modeling the effect of land use change on hydrology of a forested watershed in coastal South Carolina. Journal, USDA Publications. https://www.srs.fs.usda.gov/pubs/33891 & http://tigerprints.clemson.edu/cgi/viewcontent.cgi?article=1208&context=scwrc. Accessed 1 Sep 2017.

  • DeVault, T. L., & Krochmal, A. R. (2002). Scavenging by snakes: an examination of the literature. Herpetologica, 58(4), 429–436. https://doi.org/10.1655/0018-0831(2002)058[0429:SBSAEO]2.0.CO;2.

  • Douglas, M. E., Douglas, M. R., Schuett, G. W., & Porras, L. W. (2009). Climate change and evolution of the New World pitviper genus Agkistrodon (Viperidae). Journal of Biogeography, 36(6), 1164–1180. https://doi.org/10.1111/j.1365-2699.2008.02075.x.

    Article  Google Scholar 

  • Durso, A. M., Willson, J. D., & Winne, C. T. (2011). Needles in haystacks: estimating detection probability and occupancy of rare and cryptic snakes. Biological Conservation, 144(5), 1508–1515.

    Article  Google Scholar 

  • Eskew, E. A., Willson, J. D., & Winne, C. T. (2009). Ambush site selection and ontogenetic shifts in foraging strategy in a semi-aquatic pit viper, the eastern cottonmouth. Journal of Zoology, 277(2), 179–186. https://doi.org/10.1111/j.1469-7998.2008.00527.x.

    Article  Google Scholar 

  • ESRI. (2016). http://www.esri.com/?q=esri&form=EDGSPH&mkt=en-us&httpsmsn=1&refig=2fe7173d36d34613ad78aef05dc7adb2&sp=1&http%3A%2F%2Fwww.esri.com%2F=. Accessed 1 Sep 2017.

  • ESRI. (2017). ARCGIS blog. Using and citing Esri data. https://blogs.esri.com/esri/arcgis/2010/12/03/using-and-citing-esri-data/. Accessed 1 Sep 2017.

  • Georgia Department of Natural Resources. (2018). Wildlife Regulations & the Georgia Teacher. http://www.georgiawildlife.com/wildlife-and-the-classroom. Accessed 1 Jan 2017.

  • Gibbons, J. W. (2003). Terrestrial habitat: a vital component for herpetofauna of isolated wetlands. Wetlands, 23(3), 630–635. https://doi.org/10.1672/0277-5212(2003)023[0630:THAVCF]2.0.CO;2.

  • Gibbs, H. L., & Weatherhead, P. J. (2001). Insights into population ecology and sexual selection in snakes through the application of DNA-based genetic markers. Journal of Heredity, 92(2), 173–179.

    Article  CAS  Google Scholar 

  • Glaudas, X., Andrews, K. M., Willson, J. D., & Gibbons, J. W. (2007). Migration patterns in a population of cottonmouths (Agkistrodon piscivorus) inhabiting an isolated wetland. Journal of Zoology, 271(2), 119–124.

    Article  Google Scholar 

  • Gloyd, H. K., & Conant, R. (1990). Snakes of the Agkistrodon complex: a monographic review. Society for the Study of Amphibians and Reptiles: St. Louis.

    Google Scholar 

  • Google Earth. (2016).https://www.google.com/earth/. Google Inc. (“Google”), 1600 Amphitheatre Parkway, Mountain View, CA 94043, United States.

  • Google Maps. (2016). https://www.google.com/maps/@34.7345825,-85.4787907,13z. Google Inc. (“Google”), 1600 Amphitheatre Parkway, Mountain View, CA 94043, United States.

  • Grillitsch, B., & Schiesari, L. (2010). The ecotoxicology of metals in reptiles. Ecotoxicology of Amphibians and Reptiles, 337.

  • Guiher, T. J., & Burbrink, F. T. (2008). Demographic and phylogeographic histories of two venomous North American snakes of the genus Agkistrodon. Molecular Phylogenetics and Evolution, 48(2), 543–553. https://doi.org/10.1016/j.ympev.2008.04.008.

    Article  CAS  Google Scholar 

  • Hightower, P. W., & Bechler, D. L. (2012). The life history of the crayfish Procambarus spiculifer in the Alapahoochee River. Freshwater Crayfish, 19(1), 77–89.

    Article  Google Scholar 

  • Jarvis, T. A., Lockhart, J. M., Loughry, W. J., & Bielmyer, G. (2013). Metal accumulation in wild nine-banded armadillos. Ecotoxicology, 22, 1053–1062.

    Article  CAS  Google Scholar 

  • Jiang, Z. J., Castoe, T. A., Austin, C. C., Burbrink, F. T., Herron, M. D., McGuire, J. A., & Pollock, D. D. (2007). Comparative mitochondrial genomics of snakes: extraordinary substitution rate dynamics and functionality of the duplicate control region. BMC Evolutionary Biology, 7(1), 123.

    Article  Google Scholar 

  • Kirkley, J. A. (2014). Biogeography and population genetic structure of the cottonmouth, Agkistrodon piscivorus, in the Alapahoochee watershed. Master’s thesis, Valdosta State University.

  • Knight, R. A. (1991). Molecular systematics of the Agkistrodon complex (Doctoral dissertation, Texas Tech University).

  • Kofron, C. P. (1978). Foods and habitats of aquatic snakes (Reptilia, Serpentes) in a Louisiana swamp. Journal of Herpetology, 12, 543–554. http://www.jstor.org/stable/1563360.

    Article  Google Scholar 

  • Kofron, C. P. (1979). Reproduction of aquatic snakes in south-central Louisiana. Herpetologica, 44–50.

  • LiCOR® Biosciences. (2011a). SagaGT™ software. Lincoln, NE.

  • LiCOR® Biosciences. (2011b). LiCOR® reagents: sizing standards. https://licor.secure.force.com/catalog/LI_ProductListMain?categoryID=a0d6000000T9QdAAKandstore=bio.

  • Lillywhite, H. B., Sheehy III, C. M., & McCue, M. (2002). Scavenging behaviors of cottonmouth snakes at island bird rookeries. Herpetological Review, 33, 259–261.

    Google Scholar 

  • Lillywhite, H. B., Sheehy, C. M., & Zaidan, F. (2008). Pitviper scavenging at the intertidal zone: an evolutionary scenario for invasion of the sea. Bioscience, 58(10), 947–955.

    Article  Google Scholar 

  • Lillywhite, H. B., Pfaller, J. B., & Sheehy, C. M. (2015). Feeding preferences and responses to prey in insular neonatal Florida cottonmouth snakes. Journal of Zoology, 297(2), 156–163. https://doi.org/10.1016/S1095-6433(02)00344-6.

    Article  Google Scholar 

  • Lockhart, J.M., Siddiqui, S., Loughry, W.J., Bielmyer-Fraser, G.K. (2016). Metal accumulation in wild-caught opossums. Environmental Monitoring and Assessment 188, 1-10.

    Article  CAS  Google Scholar 

  • Lougheed, S. C., Gibbs, H. L., Prior, K. A., & Weatherhead, P. J. (2000). A comparison of RAPD versus microsatellite DNA markers in population studies of the massasauga rattlesnake. Journal of Heredity, 91(6), 458–463.

    Article  CAS  Google Scholar 

  • Luiselli, L. (2006). Broad geographic, taxonomic and ecological patterns of interpopulation variation in the dietary habits of snakes. Web Ecology, 6(1), 2–16.

    Article  Google Scholar 

  • McCleary, R. J. R. (2009). Evolution of venom variation in the Florida cottonmouth, Agkistrodon piscivorus conanti (Doctoral dissertation, University of Florida).

  • Palmer Drought Index. (2017). National Climatic Data Center, National Oceanic and Atmospheric Administration, USA. http://www.ncdc.noaa.gov/oa/climate/research/prelim/drought/palmer.html. Accessed 1 Sep 2017.

  • Parkinson, C. L. (1999). Molecular systematics and biogeographical history of pitvipers as determined by mitochondrial ribosomal DNA sequences. Copeia, 1999, 576–586. https://doi.org/10.2307/1447591.

    Article  Google Scholar 

  • Parkinson, C. L., Zamudio, K. R., & Greene, H. W. (2000). Phylogeography of the pitviper clade Agkistrodon: historical ecology, species status, and conservation of cantils. Molecular Ecology, 9(4), 411–420.

    Article  CAS  Google Scholar 

  • Prosser, M. R., Gibbs, L., Weatherhead, H., & Weatherhead, P. J. (1999). Microgeographic population genetic structure in the northern water snake, Nerodia sipedon sipedon detected using microsatellite DNA loci. Molecular Ecology, 8(2), 329–333.

    Article  CAS  Google Scholar 

  • Raymond, M., & Rousset, F. (1995). GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86(3), 248–249.

    Article  Google Scholar 

  • Rezaie-Atagholipour, M., Riyahi-Bakhtiari, A., Chee Kong Yap, M. C., Ghaffari, S., Ebrahimi-Sirizi, Z., & Ghezellou, P. (2012). Metal concentrations in selected tissues and main prey species of the annulated sea snake (Hydrophis cyanocinctus) in the Hara Protected Area, northeastern coast of the Persian Gulf, Iran. Marine Pollution Bulletin 64(2) 416–421.

    Article  CAS  Google Scholar 

  • Riekerk, H., & Korhnak, L. V. (2000). The hydrology of cypress wetlands in Florida pine flatwoods. Wetlands, 20(3), 448–460. https://doi.org/10.1672/0277-5212(2000)020[0448:THOCWI]2.0.CO;2.

  • Roark, A. W. (2003). Comparative genetic analysis in insular and mainland populations of the Florida cottonmouth, Agkistrodon piscivorus conanti. Doctoral dissertation, University of Florida.

  • Roe, J. H., Kingsbury, B. A., & Herbert, N. R. (2003). Wetland and upland use patterns in semi-aquatic snakes: implications for wetland conservation. Wetlands, 23(4), 1003–1014.

    Article  Google Scholar 

  • Roe, J. H., Gibson, J., & Kingsbury, B. A. (2006). Beyond the wetland border: estimating the impact of roads for two species of water snakes. Biological Conservation, 130(2), 161–168.

    Article  Google Scholar 

  • Roth, E. D. (2005). Spatial ecology of a cottonmouth (Agkistrodon piscivorus) population in east Texas. Journal of Herpetology, 39(2), 308–312.

    Article  Google Scholar 

  • Rousset, F. (2008). Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8(1), 103–106.

    Article  Google Scholar 

  • Shine, R. (1977). Habitats, diets, and sympatry in snakes: a study from Australia. Canadian Journal of Zoology, 55(7), 1118–1128.

    Article  Google Scholar 

  • Shine, R., Cogger, H. G., Reed, R. R., Shetty, S., & Bonnet, X. (2003a). Aquatic and terrestrial locomotor speeds of amphibious sea-snakes (Serpentes, Laticaudidae). Journal of Zoology, 259(3), 261–268.

    Article  Google Scholar 

  • Shine, R., Shine, T., & Shine, B. (2003b). Intraspecific habitat partitioning by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae): the effects of sex, body size, and colour pattern. Biological Journal of the Linnean Society, 80(1), 1–10.

    Article  Google Scholar 

  • Slip, D. J., & Shine, R. (1988). Habitat use, movements and activity patterns of free-ranging diamond pythons, Morelia spilota spilota (Serpentes, Boidae)—a radiotelemetric study. Wildlife Research, 15(5), 515–531.

    Article  Google Scholar 

  • Smith, P. W. (1961). The amphibians and reptiles of Illinois. Bulletin Illinois Natural History Survey, 28, 1–298.

    Google Scholar 

  • Sparling, D. W., Linder, G., Bishop, C. A., & Krest, S. K. (Eds.). (2010). Ecotoxicology of amphibians and reptiles (2nd ed.). Pensacola: SETAC.

    Google Scholar 

  • Sun, G., McNulty, S. G., Shepard, J. P., Amatya, D. M., Riekerk, H., Comerford, N. B., ... & Swift, L. (2001). Effects of timber management on the hydrology of wetland forests in the southern United States. Forest Ecology and Management, 143(1), 227–236. https://doi.org/10.1016/S0378-1127(00)00520-X.

  • Thomason, R. K., Loughry, W.J., Lockhart, J.M., & Bielmyer-Fraser, G.K. (2016). Metal accumulation in bobcats in the Southeastern United States. Environmental Monitoring and Assessment 188, 565-574.

    Article  Google Scholar 

  • Trauth, S. E., & McAllister, C. T. (1995). Vertebrate prey of selected Arkansas snakes. Journal of the Arkansas Academy of Science, 49(1), 188–192.

    Google Scholar 

  • Turner, B., Elder, J., & Laughlin, T. (1989). DNA fingerprinting of fishes: a general method using oligonucleoide probes. DNA Fingerprint News, 1, 15–16.

    Google Scholar 

  • Valdes, A. M., Slatkin, M., & Freimer, N. B. (1993). Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics, 133(3), 737–749.

    CAS  Google Scholar 

  • Vincent, S. E., Herrel, A., & Irschick, D. J. (2004). Sexual dimorphism in head shape and diet in the cottonmouth snake (Agkistrodon piscivorus). Journal of Zoology, 264(1), 53–59.

    Article  Google Scholar 

  • Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 1984, 1358–1370.

    Google Scholar 

  • Wharton, C. H. (1966). Reproduction and growth in the cottonmouth, Agkistrodon piscivorous Lacepede, of Cedar Keys, Florida. Copeia, 1996, 149–161.

    Article  Google Scholar 

  • Willson, J. D., Winne, C. T., Dorcas, M. E., & Gibbons, J. W. (2006). Post-drought responses of semi-aquatic snakes inhabiting an isolated wetland: insights on different strategies for persistence in a dynamic habitat. Wetlands, 26(4), 1071–1078. https://doi.org/10.1672/0277-5212(2006)26[1071,PROSSI]2.0.CO;2.

  • Wright, S. (1978). Evolution and the genetics of populations: a treatise in four volumes: vol. 4: variability within and among natural populations (pp. 590). Chicago: University of Chicago Press.

  • Wright, C. (2013). Bridges sites as refuges for fishes. Master’s thesis, Valdosta, Georgia: Valdosta State University.

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Acknowledgements

Harvey B. Lilywhite is acknowledged for serving on the master’s thesis committee of the primary author. Jeremy Davis is thanked for providing access to his family’s holdings on the west side of Grand Bay Swamp. Tayler Jarvis is thanked for help in analyzing metal concentrations. Langdale Forestry Company is thanked for providing access to the west side of Mud Swamp. Grand Bay Hunting Club (now closed) is thanked for providing access to Site 6 north of Howell road.

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  1. Wiregrass Georgia Technical College, 4809 Val Tech Road, Valdosta, GA, 31602, USA

    Joseph Ashley Kirkly

  2. Department of Chemistry, Jacksonville University, Jacksonville, FL, 32211, USA

    Gretchen K. Bielmyer-Fraser

  3. Department of Biology, Valdosta State University, Valdosta, GA, 31698, USA

    John F. Elder

  4. Cloudland, USA

    David L. Bechler

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Kirkly, J.A., Bielmyer-Fraser, G.K., Elder, J.F. et al. The Alapahoochee watershed microgeographic structure and its potential influence on metal concentrations and genetic structure in the Florida cottonmouth, Agkistrodon piscivorus conanti, within the watershed. Environ Monit Assess 190, 220 (2018). https://doi.org/10.1007/s10661-018-6579-5

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