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Examining the Effects of Chronic Selenium Exposure on Traditionally Used Stress Parameters in Juvenile American Alligators (Alligator mississippiensis)

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Abstract

Environmental contaminants, such as the trace element selenium (Se), are a continuing concern to species worldwide due to their potential pathophysiological effects, including their influence on the stress response mediated through glucocorticoids (GCs; stress hormones). Environmental concentrations of Se are increasing due to anthropogenic activities, including the incomplete combustion of coal and subsequent disposal of coal combustion wastes. However, most studies examining how Se affects GCs have been focused on lower trophic organisms. The objectives of this study were to investigate the effects of long-term Se exposure on traditionally used stress parameters and to identify which of these parameters best indicate Se accumulation in liver and kidney of the American alligator (Alligator mississippiensis), a top trophic carnivore found in the southeastern United States and known to inhabit Se-containing areas. Alligators were divided into three dietary treatments and fed prey spiked with 1000 or 2000 ppm of selenomethionine (SeMet) or deionized water (control treatment) for 7 weeks. Following the 7-week treatment protocol, blood and tissue samples were obtained to measure plasma corticosterone (CORT; the main crocodilian GC), tail scute CORT, the ratio of peripheral blood heterophils (H) to lymphocytes (L) as H/L ratio, and body condition. To evaluate which parameter best indicated Se accumulation in the liver and kidney, principal component and discriminant analyses were performed. The only parameter significantly correlated with liver and kidney Se concentrations was scute CORT. Our results suggest that measurement of CORT in tail scutes compared with plasma CORT, H/L ratios, and body condition is the best indicator of Se-exposure and accumulation in crocodilians.

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References

  • Baxter-Gilbert JH, Riley JL, Mastromonaco GF, Litzgus JD, Lesbarreres D (2014) A novel technique to measure chronic levels of corticosterone in turtles living around a major roadway. Conserv Physiol 2:cou036. https://doi.org/10.1093/conphys/cou036

    Article  CAS  Google Scholar 

  • Beck ML, Hopkins WA, Hallagan JJ, Jackson BP, Hawley DM (2014) Exposure to residual concentrations of elements from a remediated coal fly ash spill does not adversely influence stress and immune responses of nestling tree swallows. Conserv Physiol 2:cou018. https://doi.org/10.1093/conphys/cou018

    Article  CAS  Google Scholar 

  • Cyr NE, Romero LM (2007) Chronic stress in free-living European starlings reduces corticosterone concentrations and reproductive success. Gen Comp Endocrinol 151:82–89. https://doi.org/10.1016/j.ygcen.2006.12.003

    Article  CAS  Google Scholar 

  • Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772

    Article  Google Scholar 

  • Fairhurst GD, Marchant TA, Soos C, Machin KL, Clark RG (2013) Experimental relationships between levels of corticosterone in plasma and feathers in a free-living bird. J Exp Biol Exp Biol 216:4071–4081. https://doi.org/10.1242/jeb.091280

    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, 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. https://doi.org/10.1016/j.ygcen.2015.01.023

    Article  CAS  Google Scholar 

  • Finger JW Jr, Williams RJ, Hamilton MT, Elsey RM, Oppenheimer VA, Holladay SD, Gogal RM Jr (2015b) Influence of collection time on hematologic and immune markers in the American alligator (Alligator mississippiensis). J Immunoass Immunochem 36:496–509. https://doi.org/10.1080/15321819.2014.1001030

    Article  CAS  Google Scholar 

  • Finger JW Jr, Hamilton MT, Metts BS, Glenn TC, Tuberville TD (2016) 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. https://doi.org/10.1007/s00244-016-0301-9

    Article  CAS  Google Scholar 

  • Finger JW Jr, Hamilton MT, Glenn TC, Tuberville TD (2017) Dietary selenomethionine administration in the American alligator (Alligator mississippiensis): hepatic and renal Se accumulation and its effects on growth and body condition. Arch Environ Contam Toxicol 72:439–448

    Article  CAS  Google Scholar 

  • Finger JW Jr, Hamilton MT, Kelley MD, Zhang Y, Kavazis AN, Glenn TC, Tuberville TD (2018) Dietary selenomethionine administration and its effects on the American alligator (Alligator mississippiensis): oxidative status and corticosterone levels. Arch Environ Contam Toxicol 75:37–44. https://doi.org/10.1007/s00244-018-0530-1

    Article  CAS  Google Scholar 

  • Goessling JM, Kennedy H, Mendonça MT, Wilson AE, Grindstaff J (2015) A meta-analysis of plasma corticosterone and heterophil: lymphocyte ratios—is there conservation of physiological stress responses over time? Funct Ecol 29:1189–1196. https://doi.org/10.1111/1365-2435.12442

    Article  Google Scholar 

  • Guillette LJ, Crain DA, Rooney AA, Woodward AR (1997) Effect of acute stress on plasma concentrations of sex and stress hormones in juvenile alligators living in control and contaminated lakes. J Herpetol 31:347–353

    Article  Google Scholar 

  • Hamilton MT, Finger JW Jr, Winzeler ME, Tuberville TD (2016) Evaluating the effect of sample type on American alligator (Alligator mississippiensis) analyte values in a point-of-care blood analyser. Conserv Physiol 4:cov065. https://doi.org/10.1093/conphys/cov065

    Article  CAS  Google Scholar 

  • Hamilton MT, Finger JW Jr, Elsey RM, Mastromonaco GF, Tuberville TD (2018) Corticosterone in American alligator (Alligator mississippiensis) tail scutes: evaluating the feasibility of using unconventional samples for investigating environmental stressors. Gen Comp Endocrinol 268:7–13. https://doi.org/10.1016/j.ygcen.2018.07.008

    Article  CAS  Google Scholar 

  • Haskins DL, Hamilton MT, Stacy NI, Finger JW Jr, Tuberville TD (2017a) Effects of selenium exposure on the hematology, innate immunity, and metabolic rate of yellow-bellied sliders (Trachemys scripta scripta). Ecotoxicol 26:1134–1146

    Article  CAS  Google Scholar 

  • Haskins DL, Hamilton MT, Jones AL, Finger JW Jr, Bringolf RB, Tuberville TD (2017b) Accumulation of coal combustion residues and their immunological effects in the yellow-bellied slider (Trachemys scripta scripta). Environ Pollut 224:810–819

    Article  CAS  Google Scholar 

  • Hopkins WA, Mendonca 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, Congdon JD (1999) Responsiveness of the hypothalamo-pituitary-interrenal axis in an amphibian (Bufo terrestris) exposed to coal combustion wastes. Comp Biochem Physiol 122:191–196

    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). Ecotoxical Environ Saf 58:285–293. https://doi.org/10.1016/s0147-6513(03)00076-9

    Article  CAS  Google Scholar 

  • Hopkins WA, Staub BP, Baionno JA, Jackson BP, Talent LG (2005) Transfer of selenium from prey to predators in a simulated terrestrial food chain. Environ Pollut 134:447–456. https://doi.org/10.1016/j.envpol.2004.09.010

    Article  CAS  Google Scholar 

  • Janz DM, De Forest D, Brooks M, Chapman P, Gilron G, Hoff D, Hopkins W, McIntyre DO, Mebane C, Palace V, Skorupa J, Wayland M (2010) Selenium toxicity to aquatic organisms. In: Chapman PM et al (eds) Ecological assessment of selenium in the aquatic environment. Society of Environmental Toxicology and Chemistry, Pensacola, FL, pp 139–230

    Google Scholar 

  • Kohrle J, Jakob F, Contempre B, Dumont JE (2005) Selenium, the thyroid, and the endocrine system. Endocr Rev 26:944–984. https://doi.org/10.1210/er.2001-0034

    Article  CAS  Google Scholar 

  • Lance VA, Elsey RM (1999) Plasma catecholamines and plasma corticosterone following restraint stress in juvenile alligators. J Exp Zool 283:559–565

    Article  CAS  Google Scholar 

  • Lance VA, Lauren D (1984) Circadian variation in plasma corticosterone in the American alligator, Alligator mississippiensis, and the effects of ACTH injections. Gen Comp Endocrinol 54:1–7

    Article  CAS  Google Scholar 

  • Lattin CR, Romero LM (2014) Chronic exposure to a low dose of ingested petroleum disrupts corticosterone receptor signalling in a tissue-specific manner in the house sparrow (Passer domesticus). Conserv Physiol 2:cou058. https://doi.org/10.1093/conphys/cou058

    Article  CAS  Google Scholar 

  • Lattin CR, Ngai HM, Romero LM (2014) Evaluating the stress response as a bioindicator of sub-lethal effects of crude oil exposure in wild house sparrows (Passer domesticus). PLoS ONE 9:e102106. https://doi.org/10.1371/journal.pone.0102106

    Article  CAS  Google Scholar 

  • Lemly AD (2004) Aquatic selenium pollution is a global environmental safety issue. Ecotox Environ Safe 59:44–56

    Article  CAS  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 

  • Miller LL, Wang F, Palace VP, Hontela A (2007) Effects of acute and subchronic exposures to waterborne selenite on the physiological stress response and oxidative stress indicators in juvenile rainbow trout. Aquat Toxicol 83:263–271. https://doi.org/10.1016/j.aquatox.2007.05.001

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Moleón MS, Parachú Marcó MV, Pietrobon EO, Jahn GA, Beldomenico PM, Siroski PA (2017) Corticosterone levels and immunological indices in stressed juvenile broad-snouted caimans. J Zool. https://doi.org/10.1111/jzo.12513

    Article  Google Scholar 

  • Morici LA, Elsey RM, Lance VA (1997) Effects of long-term corticosterone implants on growth and immune function in juvenile alligators, Alligator mississippiensis. J Exp Zool 279:156–162

    Article  CAS  Google Scholar 

  • Müller C, Jenni-Eiermann S, Jenni L (2011) Heterophils/Lymphocytes-ratio and circulating corticosterone do not indicate the same stress imposed on Eurasian kestrel nestlings. Funct Ecol 25:566–576. https://doi.org/10.1111/j.1365-2435.2010.01816.x

    Article  Google Scholar 

  • Nilsen FM et al (2017) Trace element biodistribution in the American alligator (Alligator mississippiensis). Chemosphere 181:343–351. https://doi.org/10.1016/j.chemosphere.2017.04.102

    Article  CAS  Google Scholar 

  • Patterson S, Zee J, Wiseman S, Hecker M (2017) Effects of chronic exposure to dietary selenomethionine on the physiological stress response in juvenile white sturgeon (Acipenser transmontanus). Aquat Toxicol 186:77–86. https://doi.org/10.1016/j.aquatox.2017.02.003

    Article  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 Bioch and Physiol Part A: Mol Integr Physio 140:73–79

    Article  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 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89. https://doi.org/10.1210/edrv.21.1.0389

    Article  CAS  Google Scholar 

  • Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166:869–887. https://doi.org/10.1007/s00442-011-1943-y

    Article  Google Scholar 

  • Shilton C, Brown GP, Chambers L, Benedict S, Davis S, Aumann S, Isberg SR (2014) Pathology of runting in farmed saltwater crocodiles (Crocodylus porosus) in Australia. Vet Pathol 51:1022–1034. https://doi.org/10.1177/0300985813516642

    Article  CAS  Google Scholar 

  • Tuberville TD, Scott DE, Metts BS, Finger JW Jr, Hamilton MT (2016) Hepatic and renal trace element concentrations in American alligators (Alligator mississippiensis) following chronic dietary exposure to coal fly ash contaminated prey. Environ Pollut 214:680–689. https://doi.org/10.1016/j.envpol.2016.04.003

    Article  CAS  Google Scholar 

  • Turton JA, Ladds PW, Manolis C, Webb GJW (1997) Relationship of blood corticosterone, immunoglobulin and haematological values in young crocodiles (Crocodylus porosus) to water temperature, clutch of origin and body weight. Aust Vet J 75:114–119

    Article  CAS  Google Scholar 

  • Wada H, Hahn TP, Breuner CW (2007) Development of stress reactivity in white-crowned sparrow nestlings: total corticosterone response increases with age, while free corticosterone response remains low. Gen Comp Endocrinol 150:405–413. https://doi.org/10.1016/j.ygcen.2006.10.002

    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. https://doi.org/10.1006/enrs.2002.4384

    Article  CAS  Google Scholar 

  • Wiseman S, Thomas JK, McPhee L, Hursky O, Raine JC, Pietrock M, Giesy JP, Hecker M, Janz DM (2011) Attenuation of the cortisol response to stress in female rainbow trout chronically exposed to dietary selenomethionine. Aquat Toxicol 105:643–651. https://doi.org/10.1016/j.aquatox.2011.09.002

    Article  CAS  Google Scholar 

  • Zee J, Patterson S, Wiseman S, Hecker M (2016) Is hepatic oxidative stress a main driver of dietary selenium toxicity in white sturgeon (Acipenser transmontanus)? Ecotoxicol Environ Saf 133:334–340. https://doi.org/10.1016/j.ecoenv.2016.07.004

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Ruth Elsey and her staff at RWR for providing alligators used in this study. Sharon L. Finger helped in transporting alligators from LA to SC. They thank members of the Tuberville lab, in particular Nick Bossebroek and Bess Harris, for assisting with the feeding, blood sampling, and dissections of alligators. Megan E. Winzeler was instrumental in keeping track of data on blood sampling days. Support was provided in part by Award Numbers DE-FC09-07SR22506 and DE-EM0004391 from Department of Energy to the University of Georgia Research Foundation and a Grant from the Area Closures Project to TDT. Additional support was provided by the IUCN Crocodilian Specialist Group Student Research Assistance Scheme to MTH. All experimental procedures were approved by the University of Georgia’s Institutional Animal Care and Use Committee.

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Authors and Affiliations

  1. Department of Biological Sciences, Auburn University, Auburn, AL, 36849, USA

    John W. Finger Jr. & Meghan D. Kelley

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

    John W. Finger Jr. & Travis C. Glenn

  3. Savannah River Ecology Laboratory, University of Georgia, PO Drawer E, Aiken, SC, 29802, USA

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

  4. Department of Comparative, Diagnostic, and Population Medicine, College of Veterinary Medicine, University of Florida, Gainesville, FL, 32610, USA

    Nicole I. Stacy

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  1. John W. Finger Jr.
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Correspondence to John W. Finger Jr..

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Finger, J.W., Hamilton, M.T., Kelley, M.D. et al. Examining the Effects of Chronic Selenium Exposure on Traditionally Used Stress Parameters in Juvenile American Alligators (Alligator mississippiensis). Arch Environ Contam Toxicol 77, 14–21 (2019). https://doi.org/10.1007/s00244-019-00626-9

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