Heavy Metal Levels in Ribbon Snakes (Thamnophis sauritus) and Anuran Larvae from the Mobile-Tensaw River Delta, Alabama, USA

Article

Abstract

The Mobile-Tensaw River Delta (MTD) drains more than 75% of the state of Alabama and leads into Mobile Bay and the Northern Gulf of Mexico. Although it is a relatively healthy watershed, the MTD is potentially impacted by inputs of contaminants such as heavy metals. The levels of lead, copper, cadmium, and mercury were measured in whole body samples of Eastern Ribbon Snakes (Thamnophis sauritus) collected from the MTD. Lead, copper, and cadmium levels were also measured in anuran larvae (Rana catesbeiana, R. clamitans, and Hyla cinerea). These organisms were chosen because they are abundant in the MTD and are underrepresented in environmental contaminant biomonitoring studies. Ribbon snakes had significantly lower levels of lead, copper, and cadmium compared to whole body levels in anuran larvae, indicating that these metals were not biomagnifying through upper trophic levels. Copper and mercury levels were significantly correlated with age/growth indices in ribbon snakes. Although detectable levels of all metals were found in anuran larvae and ribbon snakes, these levels appear to be less than body burdens that would be associated with toxic effects. Populations of ribbon snakes in our particular collection sites within the MTD appear to be at minimal risk of exposure to toxic levels of metals. However, the MTD contains low- and high-impact areas, and other populations within this watershed could be at higher risk of exposure to heavy metals. We found the Eastern Ribbon Snake to be an excellent snake model for contaminant biomonitoring because of its abundance, reasonable size, and ease of collection.

References

  1. Aubret F, Bonnet X (2005) Influence of body reserves and eye opacity on foraging behaviours of tiger snakes. J Exp Zool 303A:1075–1084CrossRefGoogle Scholar
  2. Aubret F, Bonnet X, Maumelat S (2005) Tail loss, body condition and swimming performances in tiger snakes, Notechis ater occidentalis. J Exp Zool 303A:894–903CrossRefGoogle Scholar
  3. Bazar MA, Holtzman DA, Adair BM, Gresens SE (2002) Effects of dietary methylmercury in juvenile corn snakes (Elaphe guttata). Abstracts, SETAC 23rd Annual Meeting, Salt Lake City, Utah, November 16–20, P089, p 176Google Scholar
  4. Birdsall CW, Grue CE, Anderson A (1986) Lead concentrations in bullfrog Rana catesbeiana and green frog R. clamitans tadpoles inhabiting highway drainages. Environ Pollut A 40:233–247CrossRefGoogle Scholar
  5. Burger J (1992) Trace elements in pine snake hatchlings: tissue and temporal differences. Arch Environ Contam Toxicol 22:209–213CrossRefGoogle Scholar
  6. Burger J, Campbell KR, Campbell TS, Shukla T, Jeitner C, Gochfeld M (2005) Use of skin and blood as nonlethal indicators of heavy metal contamination in Northern Water Snakes (Nerodia sipedon). Arch Environ Contam Toxicol 49:232–238CrossRefGoogle Scholar
  7. Burger J, Murray S, Gaines KF, Novak JM, Punshon T, Dixon C, Gochfeld M (2006) Element levels in snakes in South Carolina: differences between a control site and exposed site on the Savannah River site Environ Monit Assess 112:35–52CrossRefGoogle Scholar
  8. Campbell KR, Campbell TS (2001) The accumulation and effects of environmental contaminants on snakes: a review. Environ Monit Assess 70:253–301CrossRefGoogle Scholar
  9. Carpenter CC (1952) Comparative ecology of the common garter snake (Thamnophis sirtalis) the ribbon snake (Thamnophis sauritus) and Butler’s garter snake (Thamnophis butleri) Ecol Monogr 22:235–258CrossRefGoogle Scholar
  10. Conant R, Collins JT (1998) Field guide to reptiles and amphibians of Eastern/Central North America 3rd ed. Houghton Mifflin Co., New YorkGoogle Scholar
  11. Dunson WA, Wyman RL, Corbett ES (1992) A symposium on amphibian declines and habitat acidification. J Herpetol 26:349–352CrossRefGoogle Scholar
  12. Ferreira CM, Lombardi JV, Machado-Neto JG, Bueno-Guimarães HM, Soares SRC, Saldiva PHN (2004) Effects of copper oxychloride in Rana catesbeiana tadpoles: toxicological and bioaccumulative aspects. Bull Environ Contam Toxicol 73:465–470CrossRefGoogle Scholar
  13. Gale NL, Wixon BG, Hardie MG, Jennett JC (1973) Aquatic organisms and heavy metals in Missouri’s new lead belt. Water Resour Bull 9:673–688Google Scholar
  14. Gillilland CD, Summer CL, Gillilland MG, Kanna K, Villeneuve DL, Coady KK, Muzzall P, Mehne C, Giesy JP (2001) Organochlorine insecticides, polychlorinated biphenyls, and metals in water, sediment, and green frogs from southwestern. Michigan Chemosphere 44:327–339Google Scholar
  15. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  16. Hall RJ, Mulhern BM (1984) Are anuran amphibians heavy metal accumulators? In: Siegel RA, Hunt LE, Knight JL, Malaret L, Zuschlag NL (eds) Vertebrate ecology and systematics—a tribute to Henry S. Fitch. Museum of Natural History, University of Kansas, Lawrence, Kansas pp 123–133Google Scholar
  17. Heinz GH, Haseltine SD, Hall RJ, Krynitsky AJ (1980) Organochlorine and mercury residues in snakes from pilot and spider islands, Lake Michigan-1978. Bull Environ Contam Toxicol 25:738–743CrossRefGoogle Scholar
  18. Hopkins WA (2000) Reptile toxicology: challenges and opportunities on the last frontier in vertebrate ecotoxicology. Environ Toxicol Chem 19:2391–2393CrossRefGoogle Scholar
  19. Hopkins WA, Congdon J, Ray JK (2000) Incidence and impact of axial malformations in larval bullfrogs (Rana catesbeiana) developing in sites polluted by a coal-burning power plant. Environ Toxicol Chem 19:862–868CrossRefGoogle Scholar
  20. Hopkins WA, Roe JH, Snodgrass JW, Jackson BP, Kling DE, Rowe CL, Congdon JD (2001) Nondestructive indices of trace element exposure in squamate reptiles. Environ Pollut 115:1–7CrossRefGoogle Scholar
  21. Hopkins WA, Roe JH, Snodgrass JW, Staub BP, Jackson BP, Congdon JD (2002) Effects of chronic dietary exposure to trace elements on banded water snakes (Nerodia fasciata). Environ Toxicol Chem 21:906–913CrossRefGoogle Scholar
  22. Hopkins WA, Rowe CL, Congdon JD (1999) Elevated trace element concentrations and standard metabolic rate in banded water snakes, Nerodia fasciata, exposed to coal combustion wastes. Environ Toxicol Chem 18:1258–1263CrossRefGoogle Scholar
  23. Jennett JC, Wixson BG, Lowsley IH, Purushothaman K, Bolter E, Hemphill DD, Gale NL, Tranter WH (1977) Transport and distribution from mining, milling, and smelting operations in a forest ecosystem. In: Boggess WR (ed) Lead in the environment. NSF RANN Program NSF/RA 770214. NSF, Washington, DC, pp 135–178Google Scholar
  24. Loumbourdis NS, Kyriakopoulou-Sklavounou P, Zachariadis G (1999) Effects of cadmium exposure on bioaccumulation and larval growth in the frog Rana ridibunda. Environ Pollut 429–433CrossRefGoogle Scholar
  25. Morel FMM, Kraepiel AML, Amyot M (1998) The chemical cycle and bioaccumulation of mercury. Ann Rev Ecol Syst 29:543–566CrossRefGoogle Scholar
  26. Nelson DH (2004) Aquatic herpetological inventory of the upper Mobile-Tensaw Delta: status report. Final report to the Alabama Department of Conservation and Natural Resources (ADCNR), 11 pagesGoogle Scholar
  27. Niethammer KR, Atkinson RD, Baskett TS, Samson FB (1985) Metals in riparian wildlife of the lead mining district of southeastern Missouri. Arch Environ Contam Toxicol 14:213–223CrossRefGoogle Scholar
  28. Pattee OH, Pain DJ (2003) Lead in the environment. In: Hoffman DJ, Rattner BA, Burton GA Jr, Cairns J Jr (eds) Handbook of ecotoxicology, 2nd ed. Lewis Publishers, Boca Raton, Florida, pp 373–408Google Scholar
  29. Pechmann JHK, Wilbur HW (1994) Putting declining amphibian populations in perspective: natural fluctuations and human impacts. Herpetol 50:65–84Google Scholar
  30. Rainwater TR, Reynolds KD, Canas JE, Cobb GP, Anderson TA, McMurry ST, Smith PN (2005) Organochlorine pesticides and mercury in cottonmouths (Agkistrodon piscivorus) from Northeastern Texas, USA. Environ Toxicol Chem 24:665–673CrossRefGoogle Scholar
  31. Reading CJ (2004) The influence of body condition and prey availability on female breeding success in the smooth snake (Coronella austriaca Laurenti). J Zool 264:61–67CrossRefGoogle Scholar
  32. Rice TM, Blackstone BJ, Nixdorf WL, Taylor DH (1999) Exposure to lead induces hypoxia-like responses in bullfrog larvae (Rana catesbeiana). Environ Toxicol Chem 18:2283–2288CrossRefGoogle Scholar
  33. Rice TM, Oris JT, Taylor DH (2001) Toxicokinetics, available source, and route of entry of lead in fed and food-deprived bullfrog (Rana catesbeiana) larvae. Arch Environ Contam Toxicol 41:450–457CrossRefGoogle Scholar
  34. Rice TM, Oris JT, Taylor DH (2002) Effects on growth and changes in organ distribution of bullfrog larvae exposed to lead throughout metamorphosis. Bull Environ Contam Toxicol 68:8–17Google Scholar
  35. Rossman DA (1963) The colubrid snake genus Thamnophis: a revision of the sauritus group. Bull Florida State Mus 7:99–178Google Scholar
  36. Sparling DW, Lowe TP (1996) Metal concentrations of tadpoles in experimental ponds. Environ Pollut 91:149–159CrossRefGoogle Scholar
  37. Tolkkinen K (2005) Meeting on mercury held: anger, confusion spill out in meeting about mercury. Mobile Register, June 8, p 2Google Scholar
  38. US EPA (United States Environmental Protection Agency) (1989a) EPA Superfund record of decision: Stauffer Chemical Co. (Cold Creek Plant) EPA ID: ALD095688875 OU 01 BUCKS, AL 09/27/1989 EPA/ROD/R04-89/057 http://www.epa.gov/superfund/sites/rods/fulltext/r0489057.pdf
  39. US EPA (United States Environmental Protection Agency) (1989b) EPA Superfund record of decision: Stauffer Chemical Co. (Lemoyne Plant) EPA ID: ALD008161176 OU 01 AXIS, AL 09/27/1989 EPA/ROD/R04-89/053 http://www.epa.gov/superfund/sites/rods/fulltext/r0489053.pdf
  40. US EPA (United States Environmental Protection Agency) (1993) EPA Superfund record of decision: Stauffer Chemical Co. (Lemoyne Plant) EPA ID: ALD008161176 OU 03 AXIS, AL 09/17/1993 EPA/ROD/R04-93/152 http://www.epa.gov/superfund/sites/rods/fulltext/r0493152.pdf
  41. US EPA (United States Environmental Protection Agency) (1994a) Method 3051: Microwave assisted acid digestion of sediments, sludges, soils, and oils. SW-846, Test methods for evaluating solid waste. US EPA, Washington, DC. http://www.epa.gov/epaoswer/hazwaste/test/sw846.htm
  42. US EPA (United States Environmental Protection Agency) (1994b) Method 7471A: Mercury in solid or semisolid waste (manual cold-vapor technique). SW-846, Test methods for evaluating solid waste. US EPA, Washington, DC. http://www.epa.gov/epaoswer/hazwaste/test/sw846.htm
  43. US EPA (United States Environmental Protection Agency) (1995a) EPA superfund record of decision: Stauffer Chemical Co. (Cold Creek Plant) EPA ID: ALD095688875 OU 02 BUCKS, AL 08/16/1995 EPA/ROD/R04-95/237 http://www.epa.gov/superfund/sites/rods/fulltext/r0495237.pdf
  44. US EPA (United States Environmental Protection Agency) (1995b) EPA Superfund Record of Decision: Olin Corp. (McIntosh Plant) EPA ID: ALD008188708 OU 01 MCINTOSH, AL 12/16/1994 EPA/ROD/R04-95/216 http://www.epa.gov/superfund/sites/rods/fulltext/r0495216.pdf
  45. US EPA (United States Environmental Protection Agency) (1999) EPA Superfund record of decision: Stauffer Chemical Co. (Lemoyne Plant) EPA ID: ALD008161176 OU 02 Axis, AL 03/18/1999 EPA/ROD/R04-99/026 http://www.epa.gov/superfund/sites/rods/fulltext/r0499026.pdf
  46. US EPA (United States Environmental Protection Agency) (2005) Current national recommended water quality criteria http://www.epa.gov/waterscience/criteria/wqcriteria.html%23appendxa
  47. Winger PV, Sieckman C, May TW, Johnson WW (1984) Residues of organochlorine insecticides, polychlorinated biphenyls and heavy metals in biota from Apalachicola River, Florida, 1978. J Assoc Off Anal Chem 67:325–333Google Scholar
  48. Wolfe MF, Schwarzbach S, Sulaiman RA (1998) Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146–160CrossRefGoogle Scholar
  49. Wright DA, Welbourn P (2002) Environmental toxicology. Cambridge University Press, Cambridge, UKGoogle Scholar
  50. Yu M-H (2005) Environmental toxicology: biological and health effects of pollutants 2nd ed. Lewis Publishers, Boca Raton, FloridaGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of South AlabamaMobileUSA

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