Skip to main content
SpringerLink
Log in

Chronic Ingestion of Coal Fly-Ash Contaminated Prey and Its Effects on Health and Immune Parameters in Juvenile American Alligators (Alligator mississippiensis)

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Coal-burning power plants supply approximately 37 % of the electricity in the United States. However, incomplete combustion produces ash wastes enriched with toxic trace elements that have historically been disposed of in aquatic basins. Organisms inhabiting such habitats may accumulate these trace elements; however, studies investigating the effects on biota have been primarily restricted to shorter-lived, lower-trophic organisms. The American alligator (Alligator mississippiensis), a long-lived, top-trophic carnivore, has been observed inhabiting these basins, yet the health or immune effects of chronic exposure and possible accumulation remains unknown. In this study, we investigated how chronic dietary ingestion of prey contaminated with coal combustion wastes (CCWs) for 25 months, and subsequent accumulation of trace elements present in CCWs, affected juvenile alligator immune function and health. Alligators were assigned to one of four dietary-treatment groups including controls and those fed prey contaminated with CCWs for one, two, or three times a week. However, no effect of Dietary Treatment (p > 0.05) was observed on any immune parameter or hematological or plasma analyte we tested. Our results suggest that neither exposure to nor accumulation of low doses of CCWs had a negative effect on certain aspects of the immune and hematological system. However, future studies are required to elucidate this further.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abbas AK, Lichtman AH, Pillai S (2010) Cellular and molecular immunology. Elsevier, Philadelphia

    Google Scholar 

  • Allsteadt J, Lang JW (1995) Sexual dimorphism in the genital morphology of young American alligators, Alligator mississippiensis. Herpetologica 51:314–325

    Google Scholar 

  • Beck ML, Hopkins WA, Hawley DM (2014) Relationships among plumage coloration, blood selenium concentrations and immune responses of adult and nestling tree swallows. J Exp Biol 218:3415–3424

    Article  Google Scholar 

  • Brown GP, Shilton CM, Shine R (2011) Measuring amphibian immunocompetence: validation of the phytohemagglutinin skin-swelling assay in the cane toad, Bufo marinus. Method Ecol Evol 2:341–348

    Article  Google Scholar 

  • Burger J, Gocheild M, Rooney AA, Orlando EF, Woodward AR, Guillette LJ Jr (2000) Metals and metalloids in tissues of American alligators in three Florida lakes. Arch Environ Contam Toxicol 38:501–508

    Article  CAS  Google Scholar 

  • Campbell KR (2003) Ecotoxicology of crocodilians. Appl Herpetol 1:45–163

    Article  Google Scholar 

  • Campbell JW, Waters MN, Tarter A, Jackson J (2010) Heavy metal and selenium concentrations in liver tissue from wild American alligator (Alligator mississippiensis) livers near Charleston, South Carolina. J Wildl Dis 46:1234–1241

    Article  CAS  Google Scholar 

  • Cherry DS, Rodgers JH Jr, Cairns J Jr, Dickson KL, Guthrie RK (1976) Responses of mosquitofish (Gambusia affinis) to ash effluent and thermal stress. Trans Am Fish Soc 105:686–694

    Article  Google Scholar 

  • Conroy CJ, Papenfuss T, Parker J, Hahn NE (2009) Use of tricaine methanesulfonate (MS222) for euthanasia of reptiles. J Am Assoc Lab Sci 48:28–32

    CAS  Google Scholar 

  • Dangleben NL, Skibola CF, Smith MT (2013) Arsenic immunotoxicity: a review. Environ Health 12:73

    Article  Google Scholar 

  • Delany MF (1990) Late summer diet of juvenile American alligators. J Herpetol 24:418–421

    Article  Google Scholar 

  • Delany MF, Abercrombie CL (1986) Alligator food habits in Northcentral Florida. J Wildl Manag 50:348–353

    Article  Google Scholar 

  • Demas GE, Zysling DA, Beechler BR, Muehlenbein MP, French SS (2011) Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. J Anim Ecol 80:710–730

    Article  Google Scholar 

  • Fairbrother A, Fowles J (1990) Subchronic effects of sodium selenite and selenomethionine on several immune functions in mallards. Arch Environ Contam Toxicol 19:836–844

    Article  CAS  Google Scholar 

  • Fairbrother A, Fix M, O’Hara T, Ribic CA (1994) Impairment of growth and immune function of avocet chicks from sites with elevated selenium, arsenic, and boron. J Wildl Dis 30:222–233

    Article  CAS  Google Scholar 

  • Finger JW Jr, Gogal RM Jr (2013) Endocrine-disrupting chemical exposure and the American alligator: a review of the potential role of environmental estrogens on the immune system of a top trophic carnivore. Arch Environ Contam Toxicol 65:704–714

    Article  CAS  Google Scholar 

  • Finger JW Jr, Isberg SR (2012) A review of innate immune functions in crocodilians. CAB Rev 7:1–11

    Article  Google Scholar 

  • Finger JW Jr, Adams AL, Thomson PC, Shilton CM, Brown GP, Moran C, Glenn TC et al (2013) Using phytohaemagglutinin to determine immune responsiveness in saltwater crocodiles (Crocodylus porosus). Aust J Zool 61:301–311

    Article  Google Scholar 

  • Finger JW Jr, Thomson PC, Adams AL, Benedict S, Moran C, Isberg SR (2015a) Reference levels for corticosterone and immune function in farmed saltwater crocodiles (Crocodylus porosus) hatchlings using current Code of Practice guidelines. Gen Comp Endocrinol 212:63–72

    Article  CAS  Google Scholar 

  • Finger JW Jr, Williams RJ, Hamilton MT, Elsey RM, Oppenheimer VA, Holladay SD et al (2015b) Influence of collection time on hematologic and immune markers in the American alligator (Alligator mississippiensis). J Immunoass Immunochem 36:496–509

    Article  CAS  Google Scholar 

  • Franklin CE, Davis BM, Peucker SKJ, Stephenson H, Mayer R, Whittier J et al (2003) Comparison of stress induced by manual restraint and immobilisation in the estuarine crocodile, Crocodylus porosus. J Exp Zool 298:86–92

    Article  Google Scholar 

  • Glassman AB, Holbrook TW, Bennett CE (1979) Correlation of leech infestation and eosinophilia in alligators. J Parasitol 65:323–324

    Article  CAS  Google Scholar 

  • Guillette LJ, Woodward AR, Crain DA, Masson GR, Palmer BD, Cox C et al (1997) The reproductive cycle of the female American alligator (Alligator mississippiensis). Gen Comp Endocrinol 108:87–101

    Article  CAS  Google Scholar 

  • Haley P, Perry R, Ennulat D, Frame S, Johnson C, Lapointe JM et al (2005) STP position paper: best practice guideline for the routine pathology evaluation of the immune system. Toxicol Pathol 33:404–407

    Article  CAS  Google Scholar 

  • Hamilton MT, Finger JW Jr, Winzeler ME, Tuberville TD (2016a) Evaluating the effect of sample type on American alligator (Alligator mississippiensis) analyte values in a point-of-care analyser. Conserv Physiol 4:1–7

    Article  Google Scholar 

  • Hamilton MT, Kupar CA, Kelley MD, Finger JW Jr, Tuberville TD (2016b) Blood and plasma biochemistry reference intervals for wild juvenile American alligators (Alligator mississippiensis). J Wildl Dis 52:631–635

    Article  Google Scholar 

  • Hoffman PR (2007) Mechanisms by which selenium influences immune responses. Arch Immunol Ther Exp 55:289–297

    Article  Google Scholar 

  • Hopkins WA, Mendcona MT, Congdon JD (1997) Increased circulating levels of testosterone and corticosterone in southern toads, Bufo terrestris, exposed to coal combustion waste. Gen Comp Endocrinol 108:237–246

    Article  CAS  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 

  • 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 18:1258–1263

    Article  CAS  Google Scholar 

  • 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 21:906–913

    Article  CAS  Google Scholar 

  • Hopkins WA, Staub BP, Baionno JA, Jackson BP, Roe JH, Ford NB (2004) Trophic and maternal transfer of selenium in brown house snakes (Lamprophis fuliginosus). Ecotox Environ Safe 58:285–293

    Article  CAS  Google Scholar 

  • Hughes MR, Smits JE, Elliot JE, Bennett DC (2000) Morphological and pathological effects of cadmium ingestion on pekin ducks expose to saline. J Toxicol Environ Heatlh A 61:591–608

    Article  CAS  Google Scholar 

  • Isberg SR, Thomson PC, Nicholas FW, Barker SC, Moran C (2005) Quantitative analysis of production traits in saltwater crocodiles (Crocodylus porosus): II. Age at slaughter. J Anim Breed Genet 122:370–377

    Article  CAS  Google Scholar 

  • Lance V, Elsey RM (1999) Hormonal and metabolic responses of juvenile alligators to cold shock. J Exp Zool 283:566–572

    Article  CAS  Google Scholar 

  • Lance V, Joanen T, McNease L (1983) Selenium vitamin E and trace elements in the plasma of wild and farm-reared alligators during the reproductive cycle. Can J Zool 61:1744–1751

    Article  CAS  Google Scholar 

  • Lang JW, Andrews HV (1994) Temperature-dependent sex determination in crocodilians. J Exp Zool 270:28–44

    Article  Google Scholar 

  • Lemly AD, Skorupa JP (2012) Wildlife and the coal waste policy debate: proposed rules for coal waste disposal ignore lessons from 45 years of wildlife poisoning. Environ Sci Technol 46:8595–8600

    Article  CAS  Google Scholar 

  • Lovely CJ, Pittman JM, Leslie AJ (2012) Normal haematology and blood biochemistry of wild Nile crocodiles (Crocodylus niloticus) in the Okavango Delta, Botswana. J S Afr Vet Assoc 78:137–144

    Google Scholar 

  • Milnes MR, Guillette LJ Jr (2008) Alligator tales: new lessons about environmental contaminants from a sentinel species. Bioscience 58:1027–1036

    Article  Google Scholar 

  • Morgan BP, Gasque P (1997) Extrahepatic complement biosynthesis: where, when and why? Clin Exp Immunol 107:1–7

    Article  CAS  Google Scholar 

  • National Research Council (2006) Managing coal combustion residues in mines. National Academies Press, Washington, DC

    Google Scholar 

  • Qin X, Gao B (2006) The complement system in liver diseases. Cell Mol Immunol 3:333–340

    CAS  Google Scholar 

  • Roe JH, Hopkins WA, Baionno JA, Staub BP, Rowe CL, Jackson BP (2004) Maternal transfer of selenium in Alligator mississippiensis nesting downstream from a coal-burning power plant. Environ Toxicol Chem 23:1969–1972

    Article  CAS  Google Scholar 

  • Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Physiol A 140:73–79

    Article  Google Scholar 

  • Rooney AA, Bermudez DS, Guillete LJ Jr (2003) Altered histology of the thymus and spleen in contaminant-exposed juvenile American alligators. J Morphol 256:349–359

    Article  Google Scholar 

  • Rowe C, Kinney O, Fiori A, Congdon J (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 

  • Rowe CL, Hopkins WA, Zehnder C, Congdon JD (2001) Metabolic costs incurred by crayfish (Procambarus acutus) in a trace element-polluted habitat: further evidence of similar responses among diverse taxonomic groups. Comp Biochem Physiol C 129:275–283

    CAS  Google Scholar 

  • Rowe CL, Hopkins WA, Congdon JD (2002) Ecotoxicological implications of aquatic disposal of coal combustion residues in the United States: a review. Environ Monit Assess 80:207–276

    Article  CAS  Google Scholar 

  • Savabieasfahani M, Lochmiller RL, Sinclair JA (1998) Sensitivity of wild cotton rats (Sigmodon hispidus) to the immunotoxic effects of low-level arsenic exposure. Arch Environ Contam Toxicol 34:289–296

    Article  CAS  Google Scholar 

  • Sellers RS, Morton D, Michael B, Roome N, Johnson JK, Yano BL et al (2007) Society of Toxicologic Pathology position paper: organ weight recommendations for toxicology studies. Toxicol Pathol 35:751–755

    Article  Google Scholar 

  • Sykes JM, Klaphake E (2008) Reptile hematology. Vet Clin Exotic Anim Practice 11:481–500

    Article  Google Scholar 

  • Thrall MA, Weiser G, Allison RW, Campbell TW (eds) (2012) Veterinary hematology and clinical chemistry, 2nd edn. Wiley-Blackwell, Ames

    Google Scholar 

  • Tuberville TD, Scott DE, Metts BS, Finger JW, Hamilton MT (2016) Hepatic and renal trace element concentrations in American alligators (Alligator mississipiensis) following chronic dietary exposure to fly ash contaminated prey. Environ Pollut 214:680–689

    Article  CAS  Google Scholar 

  • United States Energy Information Administration (2014) Electric power monthly, April 2016. United States Department of Energy, Energy Information Administration, Washington, DC. http://www.eia.gov/electricity/monthly/pdf/epm.pdf

  • Warner JK, Combrink X, Myburgh JG, Downs CT (2016) Blood lead concentrations in free-ranging Nile crocodiles (Crocodylus niloticus) from South Africa. Ecotoxicology 25:950–958

    Article  CAS  Google Scholar 

  • Wayland M, Gilchrist HG, Marchant T, Keating J, Smits JE (2002) Immune function, stress response, and body condition in Arctic-breeding common eiders in relation to cadmium, mercury, and selenium concentrations. Environ Res 90:47–60

    Article  CAS  Google Scholar 

  • Webb GJW, Messel H (1978) Morphometric analysis of Crocodylus porosus from the north coast of Arnhem Land, Northern Australia. Aust J Zool 26:1–27

    Article  Google Scholar 

  • Woodward AR, White JH, Linda SB (1995) Maximum size of the alligator (Alligator mississippiensis). J Herpetol 4:507–513

    Article  Google Scholar 

  • Zayas MA, Rodriguez HA, Galoppo GH, Stoker C, Durando M, Luque EH et al (2011) Hematology and blood biochemistry of young healthy broad-snouted caimans (Caiman latirostris). J Herpetol 45:516–524

    Article  Google Scholar 

Download references

Acknowledgments

Support was provided in part by Award Number DE-FC09-07SR22506 from Department of Energy to the University of Georgia Research Foundation. All experimental protocols were approved by the Institutional Animal Care and Use Committee at the University of Georgia (Approval No. A2010 11-561-Y3-A3). J. W. F. was funded by the Interdisciplinary Toxicology Program and the Department of Environmental Health Science at the University of Georgia. MTH and all sample analysis was funded by a grant from the Area Closures Project to T. D. T. We thank David E. Scott and Stacey L. Lance for their assistance with project design and dissections. Brett DeGregorio was instrumental in setting up the experimental tanks; Caitlin Kupar assisted with the collection of prey, and Matthew Atkinson helped conduct PHA assays on alligators. We would also like to thank John Seaman at SREL for guidance on tissue digestions and data interpretation. Thanks must also be extended to Suresh Benedict at Berrimah Veterinary Laboratories in Berrimah, NT, Australia, for advisement on BKAs and to Peter C. Thomson at the University of Sydney for statistical insight.

Author information

Author notes

  1. John W. Finger Jr.

    Present address: Department of Biological Sciences, Auburn University, Auburn, AL, 36849, USA

  2. Brian S. Metts

    Present address: Grovetown Middle School, Grovetown, GA, 30813, USA

Authors and Affiliations

  1. Department of Environmental Health Science, University of Georgia, Athens, GA, 30602, USA

    John W. Finger Jr. & Travis C. Glenn

  2. Savannah River Ecology Laboratory, University of Georgia, Aiken, SC, 29802, USA

    John W. Finger Jr., Matthew T. Hamilton, Brian S. Metts & Tracey D. Tuberville

  3. Interdisciplinary Toxicology Program, University of Georgia, Athens, GA, 30602, USA

    John W. Finger Jr., Travis C. Glenn & Tracey D. Tuberville

  4. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA, 30602, USA

    Matthew T. Hamilton

Authors
  1. John W. Finger Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew T. Hamilton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brian S. Metts
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Travis C. Glenn
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tracey D. Tuberville
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John W. Finger Jr..

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Finger, J.W., Hamilton, M.T., Metts, B.S. et al. Chronic Ingestion of Coal Fly-Ash Contaminated Prey and Its Effects on Health and Immune Parameters in Juvenile American Alligators (Alligator mississippiensis). Arch Environ Contam Toxicol 71, 347–358 (2016). https://doi.org/10.1007/s00244-016-0301-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-016-0301-9

Keywords

Search

Navigation