Skip to main content
SpringerLink
Log in

Select metal and metalloid surveillance of free-ranging Eastern box turtles from Illinois and Tennessee (Terrapene carolina carolina)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The Eastern box turtle (Terrapene carolina carolina) is a primarily terrestrial chelonian distributed across the eastern US. It has been proposed as a biomonitor due to its longevity, small home range, and reliance on the environment to meet its metabolic needs. Plasma samples from 273 free-ranging box turtles from populations in Tennessee and Illinois in 2011 and 2012 were evaluated for presence of heavy metals and to characterize hematologic variables. Lead (Pb), arsenic (As), zinc (Zn), chromium (Cr), selenium (Se), and copper (Cu) were detected, while cadmium (Cd) and silver (Ag) were not. There were no differences in any metal detected among age class or sex. However, Cr and Pb were higher in turtles from Tennessee, while As, Zn, Se, and Cu were higher in turtles from Illinois. Seasonal differences in metal concentrations were observed for Cr, Zn, and As. Health of turtles was assessed using hematologic variables. Packed cell volume was positively correlated with Cu, Se, and Pb in Tennessee. Total solids, a measure of plasma proteins, in Tennessee turtles were positively correlated with Cu and Zn. White blood cell count, a measure of inflammation, in Tennessee turtles was negatively correlated with Cu and As, and positively correlated with Pb. Metals are a threat to human health and the health of an ecosystem, and the Eastern Box Turtle can serve as a monitor of these contaminants. Differences established in this study can serve as baseline for future studies of these or related populations.

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

  • Allender MC (2012) Characterizing the epidemiology of Ranavirus in North American chelonians: diagnosis, surveillance, pathogenesis, and Therapy. PhD Dissertation, University of Illinois

  • Beresford WA, Donovan MP, Henninger JM, Waalkes MP (1981) Lead in the bone and soft tissues of box turtles caught near smelters. Bull Environ Contam Toxicol 27:349–352

    Article  CAS  Google Scholar 

  • Borkowski R (1997) Lead poisoning and intestinal perforations in a snapping turtle (Chelydra serpentine) due to fishing gear ingestion. J Zoo Wildl Med 28:109–113

    CAS  Google Scholar 

  • Burger J, Carruth-Hinchey C, Ondroff J, McMahon M, Gibbons JW, Gochfeld M (1998) Effects of lead on behavior, growth, and survival of hatchling slider turtles. J Toxicol Environm Health Part A 55:495–502

    Article  CAS  Google Scholar 

  • Burger J, Jeitner C, Schneider L, Vogt R, Gochfeld M (2010) Arsenic, cadmium, chromium, lead, mercury, and selenium levels in blood of four species on turtles from the Amazon in Brazil. J Toxicol Environ Health Part A 73:33–40

    Article  CAS  Google Scholar 

  • Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer, New York

    Book  Google Scholar 

  • Chaffin K, Norton TM, Gilardi K, Poppenga R, Jensen JB, Moler P, Cray C, Dierenfeld ES, Chen T, Oliva M, Origgi FC, Gibbs S, Mazarro L, Mazet J (2008) Health assessment of free-ranging alligator snapping turtles (Macrochelys temminickii) in Georgia and Florida. J Wildl Dis 44:670–686

    Article  CAS  Google Scholar 

  • Davidson C (2004) Declining downwind: amphibian population declines in California and historical pesticide use. Ecol Appl 14:1892–1902

    Article  Google Scholar 

  • Dodd CK (2001) North American box turtles: a natural history. University of Oklahoma Press, Norman

    Google Scholar 

  • Fitzgerald K, Vera R (2006) Reported toxicities in reptiles. In: Mader D (ed) Reptile Medicine and Surgery. Elsevier Publishing, St. Louis, pp 1068–1080

    Chapter  Google Scholar 

  • Friend M, Franson JC (1999) Lead. In: Ciganovich (ed) Field manual of wildlife diseases. USGS Biology Resources Division, Washington, pp 317–334

    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, Deja Vu Amphibians. Bioscience 50:653–666

    Article  Google Scholar 

  • Golden NH, Rattner BA (2003) Ranking terrestrial vertebrate species for utility in biomonitoring and vulnerability to environmental contaminants. Rev Environ Contam Toxicol 176:67–136

    Google Scholar 

  • Grillitsch B, Schiesari L (2010) The ecotoxicology of metals in reptiles. In: Sparling D, Linder G, Bishop CA, Krest SK (eds) Ecotoxicology of Amphibians and Reptiles, 2nd edn. CRC Press, Boca Raton, pp 337–448

    Chapter  Google Scholar 

  • Guthrie RK, Cherry DS (1979) Trophic level accumulation of heavy metals in a coal ash basin drainage system. Water Res Bull 25:244–248

    Article  Google Scholar 

  • Harmata AR, Restani M (2013) Lead, mercury, selenium, and other trace elements in tissues of golden eagles from southwestern Montanta, USA. J Wildl Dis 49:114–124

    Article  CAS  Google Scholar 

  • Hays KA, McBee K (2010) Population demographics of red-eared slider turtles (Trachemys scripta) from the Tar Creek superfund site. J Herpetol 44:441–446

    Article  Google Scholar 

  • Hopkins WA, Mendonca MT, Rowe CL, Congdon JD (1998) Elevated trace element concentrations in southern toads, Bufo terrestris, exposed to coal combustion waste. Arch Environ Contam Toxicol 35:325–329

    Article  CAS  Google Scholar 

  • Jacobson ER, Gaskin JM, Brown MB, Harris RK, Gardiner CH, LaPointe JL, Adams HP, Reggiardo C (1991) Chronic upper respiratory tract disease of free-ranging desert tortoises (Xerobates agassizii). J Wildl Dis 27:296–316

    Article  CAS  Google Scholar 

  • Ley-Quinonez C, Zavala-Norzagaray AA, Espinosa-Carreon TL, Peckham H, Marquez-Herrera C, Campos-Villegas L, Aguirre AA (2011) Baseline heavy metals and metalloid values in blood of loggerhead turtles (Caretta caretta) from Baja California Sur, Mexico. Mar Pollut Bull 62:1979–1983

    Article  CAS  Google Scholar 

  • Martinez-Lopez E, Sousa AR, Maria-Mojica P, Gomez-Ramirez P, Guilhermino L, Garcia-Fernandez AJ (2010) Blood δ-ALAD, lead, and cadmium concentrations in spur-thighed tortoises (Testudo graeca) from southeastern Spain and northern Africa. Ecotoxicology 19:670–677

    Article  CAS  Google Scholar 

  • Pellalo-Martinez NA, Ilizaliturri-Hernandez CA, Espinosa-Reyes G, Carrizales-Yanez L, Gonzalez-Mille DJ (2011) Assessment of exposure to lead in humans and turtles living in an industrial site in Coatzacoalcos Veracruz, Mexico. Bull Environ Contam Toxicol 86:642–645

    Article  Google Scholar 

  • Rocke TE, Samuel MD (1991) Effects of lead shot ingestion on selected cells of the mallard immune system. J Wildl Dis 27:1–9

    Article  CAS  Google Scholar 

  • Rose BMR, Allender MC (2011) Health assessment of wild Eastern box turtles (Terrapene carolina carolina) in East Tennessee. J Herpetol Med Surg 21:107–112

    Article  Google Scholar 

  • Rowe CL, Kinney OM, Fiori AP, Congdon JD (1996) Oral deformities in tadpoles (Rana catesbeiana) associated with coal ash deposition: effects on grazing ability and growth. Freshw Biol 36:723–730

    Article  Google Scholar 

  • Sleeman J (2008) Use of wildlife rehabilitation centers as monitors of ecosystem health. In: Fowler ME, Miller RE (eds) Zoo and wild animal medicine, current therapy 6. Saunders Elsevier, St. Louis, pp 97–104

    Chapter  Google Scholar 

  • Smith PN, Cobb GP, Godard-Codding C, Hoff D, McMurry ST, Rainwater TR, Reynolds KD (2007) Contaminant exposure in terrestrial vertebrates. Environ Poll 150:41–64

    Article  CAS  Google Scholar 

  • Sparling DW, Fellers GM, McConnell LL (2001) Pesticides and amphibian population declines in California, USA. Environ Toxicol Chem 20:1591–1595

    Article  CAS  Google Scholar 

  • Van Dijk PP (2011) Terrapene carolina. IUCN red list of threatened species. IUCN, Cambridge

    Google Scholar 

  • Yu S, Halbrook RS, Sparling DW, Colombo R (2011) Metal accumulation and evaluation of effects in a freshwater turtle. Ecotoxicology 20:1801–1812

    Article  CAS  Google Scholar 

  • Yu S, Halbrook RS, Sparling DW (2013) Correlation between heavy metals and turtle abundance in ponds near the Paducah gaseous diffusion plant, Kentucky USA. Arch Environ Contam Toxicol 65:555–566

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank students of CRESO and University of Illinois College of Veterinary Medicine for assistance with sample collection and Gerald Bargren and Yakov Lavorsky of the Illinois Sustainable Technology Center for assistance with chemical analysis.

Conflict of interest

The authors declare that they have no conflict of interest.

Statement of Human and Animal Rights

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This article does not contain any studies with human participants performed by any of the authors.

Informed Consent

There were no human subjects, thus informed consent is not applicable for this study.

Author information

Authors and Affiliations

  1. Department of Comparative Bioscience, College of Veterinary Medicine, University of Illinois, Urbana, 61802, USA

    Matthew C. Allender & Bishap Patel

  2. Illinois Sustainability Technology Center, Prairie Research Institute, 1 E. Hazelwood Dr., Champaign, 61820, USA

    Elizabeth L. Luber & John W. Scott

  3. Clinch River Environmental Studies Organization, Oak Ridge, TN, USA

    John Byrd

  4. Illinois Natural History Survey, Prairie Research Institute, University of Illinois, Champaign, 61820, USA

    Matthew C. Allender, Michael J. Dreslik & Christopher A. Phillips

Authors
  1. Matthew C. Allender
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael J. Dreslik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bishap Patel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elizabeth L. Luber
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John Byrd
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christopher A. Phillips
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. John W. Scott
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew C. Allender.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Allender, M.C., Dreslik, M.J., Patel, B. et al. Select metal and metalloid surveillance of free-ranging Eastern box turtles from Illinois and Tennessee (Terrapene carolina carolina). Ecotoxicology 24, 1269–1278 (2015). https://doi.org/10.1007/s10646-015-1498-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-015-1498-5

Keywords

Search

Navigation