Skip to main content

Advertisement

SpringerLink
Log in

Modeling Hematologic and Biochemical Parameters with Spatiotemporal Analysis for the Free-Ranging Eastern Box Turtle (Terrapene carolina carolina) in Illinois and Tennessee, a Potential Biosentinel

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Box turtles are long-lived, inhabit both aquatic and terrestrial habitats, and have relatively small home ranges making them a suitable candidate as a sentinel. To characterize their changes in response to environmental health, assessment of observed variation of this species is required. Thus, a comparative health assessment was employed in 825 Eastern box turtles in east central Illinois and Oak Ridge, Tennessee, to establish a baseline health assessment with regard to sex, age class, season, and location, identify temporal trends, and map parameters. Hematological and plasma biochemical variables measured included packed cell volume, total solids, white blood cell and differential counts, calcium, phosphorus, aspartate aminotransferase, bile acids, creatine kinase, and uric acid. These variables were reduced to four principle components that explained 68.8 % of the cumulative variance. The top model included the main effects of year, location, and sex, but no interactions. Spatial analysis of turtles in Tennessee demonstrated increased WBC and decreased PCV in 2011 associated with a clear-cut silviculture site. The results of this health assessment can serve as a baseline of population health in future studies and aid in the utility of this species as a sentinel.

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

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.

  • Anderson NL, Wack RF, Hatcher R (1997) Hematology and clinical chemistry reference ranges for clinically normal, captive New Guinea snapping turtle (Elseya novaeguineae) and the effects of temperature, sex, and sample type. Journal of Zoo and Wildlife Medicine 28:394–403.

    CAS  PubMed  Google Scholar 

  • Andreani G, Carpene E, Cannavacciuolo A, DiGirolamo N, Ferlizza E, Isani G (2014) Reference values for hematology and plasma biochemistry variables, and protein electrophoresis of healthy Hermann’s tortoises (Testudo hermanni ssp.). Veterinary Clinical Pathology 43:573–583.

    Article  PubMed  Google Scholar 

  • Bagamian KH, Skrypnk A, Rodina Y, Bezymennyi M, Nevolko O, Skrypnk V, Blackburn JK (2014) Serological Anthrax surveillance in wild boar (Sus scrofa) in Ukraine. Vector-Borne and Zoonotic Diseases 14:618–620.

    Article  PubMed  Google Scholar 

  • Blanvillain G, Schwenter JA, Day RD, Point D, Christopher SJ, Roumillat WA, Owens DW (2007) Diamondback terrapins, Malaclemys terrapin, as a sentinel species for monitoring mercury pollution of estuarine systems in South Carolina and Georgia, USA. Environmental Toxicology and Chemistry 26:1441–1450.

    Article  CAS  PubMed  Google Scholar 

  • Boonyapisitsopa S, Chaiyawong S, Nonthabenjawan N, Jairak W, Prakairungnamthip D, Bunpapong N, Amonsin A (2016) Sentinel model for influenza A virus monitoring in free-grazing ducks in Thailand. Veterinary Microbiology 182:35–43.

    Article  PubMed  Google Scholar 

  • Brown JD, Sleeman JM (2002) Morbidity and mortality of reptiles admitted to the wildlife center of Virginia, 1991 to 2000. Journal of Wildlife Diseases 38:699–705

    Article  PubMed  Google Scholar 

  • Brown JD, Richards JM, Robertson R, Holladay S, Sleeman JM (2004) Pathology of aural abscesses in free living Eastern box turtles (Terrapene carolina carolina). Journal of Wildlife Diseases 40:704–712

    Article  PubMed  Google Scholar 

  • Budischak SA, Hester JM, Price SJ, Dorcas ME (2006) Natural history of Terrapene carolina (Box Turtles) in an urbanized landscape. Southeastern Naturalist 5:191–204.

    Article  Google Scholar 

  • Burnham KP, Anderson DR (1998) Model Selection and Inference: A Practical Information-Theoretic Approach, New York: Springer.

    Book  Google Scholar 

  • Campbell TW (2014) Clinical pathology. In: Current Therapy in Reptile Medicine and Surgery, Mader DR, Divers SJ (editors), St. Louis, Missouri: Saunders Elsevier, pp 70–92

    Chapter  Google Scholar 

  • Carson C, Lavender CJ, Handasyde KA, O’Brien CR, Hewitt N, Johnson PDR, Frye .JAM (2014) Potential wildlife sentinels for monitoring the endemic spread of human Buruli ulcer in South-East Australia. PLOS Neglected Tropical Diseases (DOI: 10.1371/journal.pntd.0002668

    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, Mazzaro L, Mazet J (2008) Health assessment of free-living alligator snapping turtles (Macrochelys temminckii) in Georgia and Florida. Journal of Wildlife Diseases 44:670–686.

    Article  CAS  PubMed  Google Scholar 

  • Chansue N, Sailasuta A, Tangtrongpiros J, Wangnaitham S, Assawawongkasem N (2011) Hematology and clinical chemistry of adult yellow-headed temple turtles (Hieremys annandalii) in Thailand. Veterinary Clinical Pathology 40:174–184.

    Article  PubMed  Google Scholar 

  • Childs JE, Krebs JW, Real LA, Gordon ER (2007) Animal-based national surveillance for zoonotic disease: quality, limitations, and implications of a model system for monitoring rabies. Preventative Veterinary Medicine 78:246–261

    Article  CAS  Google Scholar 

  • Christopher MM, Berry KH, Wallis IR, Nagy KA, Henen BT, Peterson CC (1999) Reference intervals and physiologic alterations in hematologic and biochemical values of free-ranging desert tortoises in the Mojave Desert. Journal of Wildlife Diseases 35:212–238.

    Article  CAS  PubMed  Google Scholar 

  • Chung CS, Cheng CH, Chin SC, Lee A, Chi C (2009) Morphologic and cytochemical characteristics of Asian yellow pond turtle (Ocadia sinensis) blood cells and their hematologic and plasma biochemical reference values. Journal of Zoo and Wildlife Medicine 40:76–85.

    Article  PubMed  Google Scholar 

  • Conrad PA, Miller MA, James ER, Mazet J, Dabritz H, Jessup DA, Gulland F, Grigg ME (2005) Transmission of Toxoplasma: Clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. International Journal for Parasitology 35:1155–1168

    Article  CAS  PubMed  Google Scholar 

  • Crawshaw GJ, Holz P (1996) Comparison of plasma biochemical values in blood and blood-lymph mixtures from red-eared sliders, Trachemys scripta elegans. Bulletin of the Association of Reptilian and Amphibian Veterinarians 6:7–9.

    Google Scholar 

  • Currylow, AF, MacGowan BJ, Williams RN (2012) Short-term management effects on a long-lived ectotherm. PLos One (DOI: 10.1371/journal.pone.0040473)

    PubMed  PubMed Central  Google Scholar 

  • Dantzler WH (1996) Comparative aspects of renal urate transport. Kidney International 49:1549–1551.

    Article  CAS  PubMed  Google Scholar 

  • De Voe R, Geissler K, Elmore S, Rotstein D, Lewbart G, Guy J (2004) Ranavirus-associated morbidity and mortality in a group of captive Eastern box turtles (Terrapene carolina carolina). Journal of Zoo and Wildlife Medicine 35:534–543

    Article  PubMed  Google Scholar 

  • Dickinson VM, Jarchow JL, Trueblood MH (2002) Hematology and plasma biochemistry reference range values for free-ranging desert tortoises in Arizona. Journal of Wildlife Diseases 38:143–53.

    Article  CAS  PubMed  Google Scholar 

  • Donaldson BM, Echternacht AC (2005) Aquatic habitat use relative to home range and seasonal movement of Eastern box turtles (Terrapene carolina carolina: Emydidae) in Eastern Tennessee. Journal of Herpetology 39:278–284.

    Article  Google Scholar 

  • Douros DL, Gaines KF, Novak JM (2015) Atrazine and glyphosate dynamics in a lotic ecosystem: the common snapping turtle as a sentinel species. Environmental Montoring and Assessment 187:114.

    Article  Google Scholar 

  • Duguy R (1970) Numbers of blood cells and their variations. In: Biology of the Reptilia, Gans C, Parsons TC (editors), vol 3, New York: Academic Press

  • Dyer JL, Yager P, Orciari L, Greenberg L, Walalce R, Hanlon CA, Blanton JD (2014) Rabies surveillance in the United States during 2013. Journal of the American Veterinary Medical Association 245:1111–1123.

    Article  PubMed  Google Scholar 

  • Fox GA (2001) Wildlife as sentinels of human health effects in the Great Lakes-St. Lawrence Basin. Enviornmental Health Perspectives 109:853–861.

    Google Scholar 

  • Golden NH, Rattner BA (2003) Ranking terrestrial vertebrate species for utility in biomonitoring and vulnerability to environmental contaminants. Review of Environmental Contamination and Toxicology 176:67–136.

    Google Scholar 

  • Gottdenker NL, Jacobson ER (1995) Effect of venipuncture sites on hematologic and clinical biochemical values in desert tortoises (Gopherus agassizii). American Journal of Veterinary Research 56:19–21.

    CAS  PubMed  Google Scholar 

  • Guilette LJ, Crain DA, Rooney AA,, Pickford DB (1995) Organization versus activation: the role of endocrine-disrupting contaminants (EDCs) during embryonic development in wildlife. Environmental Health Perspectives 103(S7):157–164

    Article  Google Scholar 

  • Hamer SA, Lehrer E, Magle SB (2012) Wild birds as sentinels for multiple zoonotic pathogens along an urban to rural gradient in greater Chicago, Illinois. Zoonoses Public Health 59:355–364

    Article  CAS  PubMed  Google Scholar 

  • Hester JM, Price SJ, Dorcas ME (2008) Effects of relocation on movements and home ranges of Eastern box turtles. Journal of Wildlife Management 72:772–777.

    Article  Google Scholar 

  • Jacobson ER, Berry KH, Stacy B, Huzella LM, Kalasinsky VF, Fleetwod ML, Mense MG (2009) Oxalosis in wild desert tortoises, Gopherus agassizii. Journal of Wildlife Diseases 45:982–988.

    Article  CAS  PubMed  Google Scholar 

  • Jandegian CM, Deem SL, Bhandari RK, Holliday CM, Nicks D, Rosenfeld CS, Selcer KW, Tillitt DE, Vom Saal FS, Velez-Rivera V, Yang Y, Holliday DK (2015) Developmental exposure to bisphenol A (BPA) alters sexual differentiation in painted turtles (Chrysemys picta). General Comparative Endocrinology 15:77–85.

    Article  Google Scholar 

  • Johnson AJ, Pessier AP, Wellehan JFX, Childress A, Norton TM, Stedman NL, Bloom DC, Belzer W, Titus VR, Wagner R, Brooks JW, Spratt J, Jacobson ER (2008) Ranavirus infection of free-living and captive box turtles and tortoises in the United States. Journal of Wildlife Diseases 44:851–863

    Article  CAS  PubMed  Google Scholar 

  • Johnstone CP, Lill A, Reina RD (2012) Does habitat fragmentation cause stress in the agile antechinus? A haematological approach. Journal of Comparative Physiology B 182:139–155.

    Article  Google Scholar 

  • Keller JM, Kucklick JR, Stamper MA, Harms CA, McClellan-Green PD (2004) Associations between organochlorine contaminant concentrations and clinical health parameters in loggerhead sea turtles from North Carolina, USA. Environmental Health Perspectives 112:1074–1079.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimble SJA, Williams RN (2012) Temporal variance in hematologic and plasma biochemical reference intervals for free-living Eastern box turtles (Terrapene carolina carolina). Journal of Wildlife Diseases 48:799–802

    Article  CAS  PubMed  Google Scholar 

  • Kirk CM, Amstrup S, Swor R, Holcomb D, O’Hara TM (2010) Hematology of southern Beaufort Sea polar bears (2005-2007): biomarker for an Arctic system health sentinel. EcoHealth 7:307–320.

    Article  PubMed  Google Scholar 

  • Knotkova Z, Dorrenstein GM, Jeki V, Janouskova J, Knotek Z (2008) Fasting and postprandial serum bile acid concentrations in 10 healthy female red-eared terrapins (Trachemys scripta elegans). Veterinary Record 163:510–514.

    Article  CAS  PubMed  Google Scholar 

  • Mans C, Braun J (2014) Update on common nutritional disorders of captive reptiles. Veterinary Clinics Exotic Animal Practice 17:369–395.

    Article  Google Scholar 

  • Mazet JK, Gardner IA, Jessup DA, Lowenstine LJ, Boyce WM (2000) Evaluation of changes in hematologic and clinical biochemical values after exposure to petroleum products in mink (Mustela vison) as a model for assessment of sea otters (Enhydra lutris). American Journal of Veterinary Research 61:1197–1203.

    Article  CAS  PubMed  Google Scholar 

  • Pittman HT, Bowerman WW, Grim LH, Grubb TG, Bridges WC (2011) Using nestling feathers to assess spatial and temporal concentrations of mercury in bald eagles at Voyageurs National Park, Minnesota, USA. Ecotoxicology 20:1626–1635

    Article  CAS  PubMed  Google Scholar 

  • Rie F, Ramos JG, Stoker C, Bussmann LE, Luque EH, Munoz-de-Toro M (2005) Reproductive endocrine disruption in a sentinel species (Chrysemys picta) on Cape Cod, Massachusetts. Archives of Environmental Contamination and Toxicology 48:217–224.

    Article  CAS  PubMed  Google Scholar 

  • Rose BMW, Allender MC (2011) Health assessment of wild Eastern box turtles (Terrapene carolina carolina) in east Tennessee. Journal of Herpetological Medicine and Surgery 21:107–112.

    Article  Google Scholar 

  • Schaeffer DJ, Herricks EE, Kerster HW (1988) Ecosystem health: I. Measuring ecosystem health. Environmental Management 12:445–455.

    Google Scholar 

  • Schrader G, Allender MC, Odoi A (2010) A retrospective study of diagnosis, treatment, and outcome of Eastern box turtles (Terrapene carolina carolina) presented to the University of Tennessee College of Veterinary Medicine wildlife clinic from 1995–2007. Journal of Wildlife Diseases 46:1079–1085

    Article  PubMed  Google Scholar 

  • Singleton CL, Norris AM, Sauther ML, Cuozzo FP, Youssouf Jacky IA (2015) Rig-tailed lemur (Lemur catta) health parameters across two habitats with varied level of human disturbance at the Beza Mahafaly special reserve, Madagascar. Folia Primatology 86:56–65.

    Article  Google Scholar 

  • Sleeman J (2008) Use of wildlife rehabilitation centers as monitors of ecosystem health. In: Zoo and Wild Animal Medicine, Current Therapy 6, Fowler ME, Miller RE (editors), St. Louis, Missouri: Saunders Elsevier, pp 97–104

  • Stacy NI, Alleman AR, Sayler KA (2011) Diagnostic hematology of reptiles. Clinical Laboratory Medicine 31:87–108.

    Article  Google Scholar 

  • Ulsh BA, Muhlmann-Diaz MC, Whicker FW, Hinton TG, Congdon JD, Bedford JS (2000) Chromosome translocations in turtles: a biomarker in a sentinel animal for ecological dosimetry. Radiation Research 153:752–759.

    Article  CAS  PubMed  Google Scholar 

  • Van Dijk PP (2011) Terrapene carolina. In: IUCN Red List of Threatened Species, Gland: World Conservation Union

  • Yang PY, Yu PH, Wu SH, Chie C-H (2014) Seasonal hematology and plasma biochemistry reference range values of the yellow-marginated box turtle (Cuora flavomarginata). Journal of Zoo and Wildlife Medicine 45:278–286.

    Article  PubMed  Google Scholar 

  • Yockney IJ, Nugent G, Latham MC, Perry M, Cross ML, Byrom AE (2013) Comparison of ranging behavior in a multi-species complex of free-living hosts of bovine tuberculosis in relation to their use as disease sentinels. Epidemiology and Infection 141:1407–1416.

    Article  CAS  PubMed  Google Scholar 

  • Zaias J, Norton TM, Fickel A, Spratt J, Altman NH, Cray C (2006) Biochemical and hematologic values for 18 clinically healthy radiated tortoises (Geochelone radiata) on St. Catherines Island, Georgia. Veterinary Clinical Pathology 35:321–325.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the many students of CRESO, University of Illinois College of Veterinary Medicine, and Prairie Research Institute. We are forever thankful to John Rucker and his Boykin spaniels.

Author information

Authors and Affiliations

  1. Wildlife Epidemiology Lab, Department of Comparative Biosciences, College of Veterinary Medicine, University of Illinois, 2001 S. Lincoln Ave., Urbana, IL, 61802, USA

    Terrell C. Lloyd, Matthew C. Allender & Grace Archer

  2. Illinois Natural History Survey, Prairie Research Institute, University of Illinois, 1816 S. Oak St., Champaign, IL, 61820, USA

    Christopher A. Phillips

  3. The Clinch River Environmental Studies Organization, Oak Ridge, TN, 37716, USA

    John Byrd

  4. Department of Microbiology, Immunology, and Pathology, College of Veterinary Medicine, Colorado State University, Fort Collins, CO, 80523, USA

    A. Russell Moore

Authors
  1. Terrell C. Lloyd
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew C. Allender
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Grace Archer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher A. Phillips
    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. A. Russell Moore
    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

Lloyd, T.C., Allender, M.C., Archer, G. et al. Modeling Hematologic and Biochemical Parameters with Spatiotemporal Analysis for the Free-Ranging Eastern Box Turtle (Terrapene carolina carolina) in Illinois and Tennessee, a Potential Biosentinel. EcoHealth 13, 467–479 (2016). https://doi.org/10.1007/s10393-016-1142-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-016-1142-8

Keywords

Search

Navigation