Skip to main content
Log in

Nondestructive indices of mercury exposure in three species of turtles occupying different trophic niches downstream from a former chloralkali facility

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Turtles are useful for studying bioaccumulative pollutants such as mercury (Hg) because they have long life spans and feed at trophic levels that result in high exposure to anthropogenic chemicals. We compared total Hg concentrations in blood and toenails of three species of turtles (Chelydra serpentina, Sternotherus odoratus, and Graptemys geographica) with different feeding ecologies from locations up- and downstream of a superfund site in Virginia, USA. Mercury concentrations in turtle tissues were low at the reference site (average ± 1SE: blood = 48 ± 6 ng g−1; nail = 2,464 ± 339 ng g−1 FW) but rose near the contamination source to concentrations among the highest ever reported in turtles [up to 1,800 ng g−1 (blood) and 42,250 ng g−1 (nail) FW]. Tissue concentrations remained elevated ~130 km downstream from the source compared to reference concentrations. Tissue Hg concentrations were higher for C. serpentina and S. odoratus than G. geographica, consistent with the feeding ecology and our stable isotope (δ13C and δ15N) analyses of these species. In addition, we suggest that toenails were a better indication of Hg exposure than blood, probably because this keratinized tissue represents integrated exposure over time. Our results demonstrate that downstream transport of Hg from point sources can persist over vast expanses of river thereby posing potential exposure risks to turtles, but relative exposure varies with trophic level. In addition, our study identifies turtle toenails as a simple, cost-efficient, and minimally invasive tissue for conservation-minded sampling of these long-lived vertebrates.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Albers PH, Sileo L, Mulhern BM (1986) Effects of environmental contamination on snapping turtles of a tidal wetland. Arch Environ Contam Toxicol 15:39–109

    Article  CAS  Google Scholar 

  • Barr JF (1986) Population dynamics of the common loon (Gavia immer) associated with mercury-contaminated waters in northwestern Ontario. Canadian Wildlife Service Occasional paper no. 56

  • Bearhop S, Waldron S, Thompson D, Furness R (2000) Bioamplification of mercury in great skua Catharacta skua chicks: The influence of trophic status as determined by stable isotope signatures of blood and feathers. Mar Pollut Bull 40:181–185

    Article  CAS  Google Scholar 

  • Bearhop S, Furness R, Hilton GM, Votier SC, Waldron S (2003) A forensic approach to understanding diet and habitat use from stable isotope analysis of (avian) claw material. Funct Ecol 17:270–275

    Article  Google Scholar 

  • Bergeron CM, Husak JF, Unrine JM, Romanek CS, Hopkins WA (2007) Influence of feeding ecology on blood mercury concentrations in four species of turtles. Environ Toxicol Chem 26:1733–1741

    Article  CAS  Google Scholar 

  • Bergeron CM, Bodinof CM, Unrine JM, Hopkins WA (2010a) Mercury accumulation along a contamination gradient and nondestructive indices of exposure in amphibians. Environ Toxicol Chem 29:980–988

    Article  CAS  Google Scholar 

  • Bergeron CM, Bodinof CM, Unrine JM, Hopkins WA (2010b) Bioaccumulation and maternal transfer of mercury and selenium in amphibians. Environ Toxicol Chem 29:989–997

    Article  CAS  Google Scholar 

  • Bergeron CM, Hopkins WA, Todd BD, Hepner MJ, Unrine JM (2011) Interactive effects of maternal and dietary mercury exposure have latent and lethal consequences for amphibian larvae. Environ Sci Technol 45:3781–3787

    Article  CAS  Google Scholar 

  • Bonzongo JC, Lyons WB, Hines ME, Warwick JJ, Faganeli J, Horvat M, Lechler PJ, Miller JR (2002) Mercury in surface waters of three mine-dominated river systems: Idrija River, Slovenia; Carson River, Nevada; and Madeira River, Brazilian Amazon. Geochem Explor Environ Anal 2:111–119

    Article  CAS  Google Scholar 

  • Carter LJ (1977) Chemical-plants leave unexpected legacy for two Virginia rivers. Science 198:1015–1020

    Article  CAS  Google Scholar 

  • Congdon JD, Greene JL, Brooks RJ (2008) Reproductive and nesting ecology of female snapping turtles. In: Steyermark AC, Finkler MS, Brooks RJ (eds) Biology of the Snapping Turtle (Chelydra serpentina). Johns Hopkins University Press, Baltimore, pp 123–134

    Google Scholar 

  • Cristol DA, Brasso RL, Condon AM, Fovargue RE, Friedman SL, Hallinger KK, Monroe AP, White AE (2008) The movement of aquatic mercury through terrestrial food webs. Science 320:335

    Article  CAS  Google Scholar 

  • Day RD, Christopher SJ, Becker PR, Whitaker DW (2005) Monitoring mercury in the loggerhead sea turtle, Caretta caretta. Environ Sci Technol 39:437–446

    Article  CAS  Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  CAS  Google Scholar 

  • Drevnick PE, Sandheinrich MB (2003) Effects of dietary methylmercury on reproductive endocrinology of fathead minnows. Environ Sci Technol 37:4390–4396

    Article  CAS  Google Scholar 

  • Eisler R (2006) Mercury hazards to living organisms. CRC Press, Boca Raton

    Book  Google Scholar 

  • Ernst CH, Lovich JE, Barbour RW (1994) Turtles of the United States and Canada. Smithsonian Institute Press, Washington, DC

    Google Scholar 

  • Evers DC, Kaplan JD, Meyer MW, Reaman PS, Braselton WE, Major A, Burgess N, Scheuhammer AM (1998) Geographical trend in mercury measured in common loon feathers and blood. Environ Toxicol Chem 17:173–183

    Article  CAS  Google Scholar 

  • Evers DC, Burgess NM, Champoux L, Hoskins B, Major A, Goodale WM, Taylor RJ, Poppenga R, Daigle T (2005) Patterns and interpretation of mercury exposure in freshwater avian communities in northeastern North America. Ecotoxicology 14:193–221

    Article  CAS  Google Scholar 

  • Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, déjà vu amphibians. Bioscience 50:653–666

    Article  Google Scholar 

  • Golet WJ, Haines TA (2001) Snapping turtles (Chelydra serpentina) as monitors for mercury contamination of aquatic environments. Environ Monit Assess 71:211–220

    Article  CAS  Google Scholar 

  • Hallinger KK, Cornell KL, Brasso RL, Cristol DA (2011) Mercury exposure and survival in free-living swallows (Tachycineta bicolor). Ecotoxicology 20:39–46

    Article  CAS  Google Scholar 

  • Hammerschmidt CR, Sandheinrich MB, Wiener JG, Rada RG (2002) Effects of dietary methylmercury on reproduction of fathead minnows. Environ Sci Technol 36:877–883

    Article  CAS  Google Scholar 

  • Heinz GH (1996) Mercury poisoning in wildlife. In: Fairbrother AL, Locke LN, Hoff GL (eds) Noninfectious diseases of wildlife, 2nd edn. Iowa State University Press, Ames, pp 118–127

    Google Scholar 

  • Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR, Kondrad SL, Erwin CA (2009) Species differences in the sensitivity of avian embryos to methylmercury. Arch Environ Contam Toxicol 56:129–138

    Article  CAS  Google Scholar 

  • Helwig DD, Hora ME (1983) Polychlorinated biphenyl, mercury, and cadmium concentrations in Minnesota snapping turtles. Bull Environ Contam Toxicol 30:186–190

    Article  CAS  Google Scholar 

  • Hildebrand SG, Strand RH, Huckabee JW (1980) Mercury accumulation in fish and invertebrates of the North Fork Holston River, Virginia and Tennessee. J Environ Qual 9:393–400

    Article  CAS  Google Scholar 

  • Hill WR, Stewart AJ, Napolitano GE (1996) Mercury speciation and bioaccumulation in lotic primary producers and primary consumers. Can J Fish Aquat Sci 53:812–819

    Article  CAS  Google Scholar 

  • Hobson KA, Clark RG (1993) Turnover of 13C in cellular and plasma fractions of blood: implications for nondestructive sampling in avian dietary studies. Auk 110:638–641

    Article  Google Scholar 

  • Hobson KA, Clark RG (1994) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188

    Article  Google Scholar 

  • Hopkins WA (2006) Use of tissue residues in reptile ecotoxicology: a call for integration and experimentalism. In: Gardner S, Oberdorster E (eds) New perspectives: toxicology and the environment, vol 3., Reptile toxicologyTaylor and Francis Publishers, London, pp 35–62

    Google Scholar 

  • Hopkins WA (2007) Amphibians as models for studying environmental change. Inst Lab Anim Res J 48:270–277

    CAS  Google Scholar 

  • Hopkins WA, Rowe CL (2010) Interdisciplinary and hierarchical approaches for studying the effects of metals and metalloids on amphibians. In: Sparling D, Linder G, Bishop CA (eds) Ecotoxicology of amphibians and reptiles, 2nd edn. SETAC Press, Pensacola, pp 325–336

    Chapter  Google Scholar 

  • 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 115:1–7

    Article  CAS  Google Scholar 

  • Hopkins WA, Snodgrass JW, Baionno JA, Roe JH, Staub BP, Jackson BP (2005) Functional relationships among selenium concentrations in the diet, target tissues, and nondestructive tissue samples of two species of snakes. Environ Toxicol Chem 24:344–351

    Article  CAS  Google Scholar 

  • Hopkins WA, Hopkins LB, Unrine J, Snodgrass J, Elliot J (2007) Mercury concentrations in tissues of osprey from the Carolinas, USA. J Wildl Manage 71:1819–1829

    Article  Google Scholar 

  • Iverson JB (1982) Biomass in turtle populations—a neglected subject. Oecologia 55:69–76

    Article  Google Scholar 

  • Jackson BP, Hopkins WA, Baionno JA (2003) Laser ablation-ICP-MS analysis of micro-dissected tissue: a conservation-minded approach to assessing contaminant exposure. Environ Sci Technol 37:2511–2515

    Article  CAS  Google Scholar 

  • Kenyon LO, Landry AM, Gill GA (2001) Trace metal concentrations in blood of the Kemp’s Ridley sea turtle (Lepidochelys kempii). Chelonian Conserv Biol 4:128–135

    Google Scholar 

  • Meyers-Schöne L, Walton BT (1994) Turtles as monitors of chemical contaminants in the environment. Rev Environ Contam Toxicol 135:93–153

    Article  Google Scholar 

  • Meyers-Schöne L, Shugart LR, Beauchamp JJ, Walton BT (1993) Comparison of two fresh-water turtle species as monitors of radionuclide and chemical contamination—DNA-damage and residue analysis. Environ Toxicol Chem 12:1487–1496

    Article  Google Scholar 

  • Mitchell JC (1994) The reptiles of Virginia. Smithsonian Institute Press, Washington, DC

    Google Scholar 

  • Obbard ME (1980) Nesting migrations of the snapping turtle (Chelydra serpentina). Herpetologica 36:158–162

    Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Rimmer CC, McFarland KP, Evers DC, Miller EK, Aubry Y, Busby D, Taylor RJ (2005) Mercury concentrations in Bicknell’s thrush and other insectivorous passerines in montane forests of northeastern North America. Ecotoxicology 14:223–240

    Article  CAS  Google Scholar 

  • Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36:12–18

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: principles and practice of statistics in biological research. W.H. Freeman, New York

    Google Scholar 

  • Southworth GR, Peterson MJ, Bogle MA (2004) Bioaccumulation factors for mercury in stream fish. Environ Pract 6:135–143

    Google Scholar 

  • Tan SW, Meiller JC, Mahaffey KR (2009) The endocrine effects of mercury in humans and wildlife. Crit Rev Toxicol 39:228–269

    Article  CAS  Google Scholar 

  • Thompson DR, Furness RW (1989) The chemical form of mercury stored in South Atlantic seabirds. Environ Pollut 60:305–317

    Article  CAS  Google Scholar 

  • Turnquist MA, Driscoll CT, Schulz KL, Schlaepfer MA (2011) Mercury concentrations in snapping turtles (Chelydra serpentina) correlate with environmental and landscape characteristics. Ecotoxicology 20:1599–1608

    Article  CAS  Google Scholar 

  • USEPA (1991) Determination of mercury in tissues by cold vapor atomic absorption spectrometry. EPA/600/4-91/010

  • USEPA (2002) Method 1631, Revision E: Mercury in water by oxidation, purge and trap, and cold vapor atomic fluorescence spectrometry. EPA-821-R-02-019

  • Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066

    Article  CAS  Google Scholar 

  • Wada H, Cristol DA, McNabb FMA, Hopkins WA (2009) Suppressed adrenocortical responses and triiodothyronine levels in tree swallow (Tachycineta bicolor) nestlings near a Hg-contaminated river. Environ Sci Technol 43:6031–6038

    Article  CAS  Google Scholar 

  • Watras CJ, Bloom NS (1992) Mercury and methylmercury in individual zooplankton—implications for bioaccumulation. Limnol Oceanogr 37:1313–1318

    Article  Google Scholar 

  • Wiener JG, Spry DJ (1996) Toxicological significance of mercury in freshwater fish. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife: interpreting tissue concentrations. Lewis Publishers, Boca Raton, pp 297–340

    Google Scholar 

  • Wolfe MF, Schwarzbach S, Sulaiman RA (1998) Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146–160

    Article  CAS  Google Scholar 

  • Young-Morgan & Associates (1990) An assessment of mussel communities in the North Fork Holston River. Prepared for: Olin Corporation, pp 1–22

Download references

Acknowledgments

J. Schmerfeld, G. Heffinger, K. Tom, M. Newman, D. Evers, D. Yates, G. Schoenholtz, and S. Folsom provided valuable assistance during the project. We thank the landowners along the NFHR for their cooperation. Collection of animals was in conformance with appropriate permits in Virginia and Tennessee and sample methods were in compliance with Virginia Polytechnic Institute and State University’s animal care and use protocols. This research was primarily supported by contract #501817M754 from the US Fish and Wildlife Service, but was also supported by startup funds to WAH.

Conflict of interest

The authors declare that they have no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to William A. Hopkins.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hopkins, W.A., Bodinof, C., Budischak, S. et al. Nondestructive indices of mercury exposure in three species of turtles occupying different trophic niches downstream from a former chloralkali facility. Ecotoxicology 22, 22–32 (2013). https://doi.org/10.1007/s10646-012-0999-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-012-0999-8

Keywords

Navigation