Abstract
Selenium (Se) is an essential nutrient which in excess causes toxicity. The disposal of incompletely combusted coal, which often is rich in Se, into aquatic settling basins is increasing the risk of Se exposure worldwide. However, very few studies have looked at the physiological effects of Se exposure on long-lived, top trophic vertebrates, such as the American alligator (Alligator mississippiensis). During a 7-week period, alligators were fed one of three dietary treatments: mice injected with deionized water or mice injected with water containing 1000 or 2000 ppm selenomethionine (SeMet). One week after the last feeding alligators were bled within 3 min of capture for plasma corticosterone (CORT). A few days later, all alligators were euthanized and whole blood and tail tissue were harvested to measure oxidative damage, an antioxidant-associated transcription factor, and antioxidant enzymes [glutathione peroxidase-1 (GPX1), superoxide dismutase-1 (SOD1), and SOD2] by Western blotting. There was a dose-dependent increase in baseline CORT levels in alligators administered SeMet. Except for blood SOD2 levels, SeMet treatment had no effect (p > 0.05 for all) on oxidative status: oxidative damage, GPX1, SOD1, and muscle SOD2 levels were similar among treatments. Our results illustrate that high levels of Se may act as a stressor to crocodilians. Future studies should investigate further the physiological effects of Se accumulation in long-lived, top-trophic vertebrates.
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Brady C, Petrie SA, Schummer ML, Badzinski SS, Belzile N, Chen YW (2013) Effects of dietary selenium on the health and survival of captive wintering lesser scaup. Environ Pollut 175:8–15. https://doi.org/10.1016/j.envpol.2012.12.005
Brigelius-Flohe R, Maiorino M (2013) Glutathione peroxidases. Biochim Biophys Acta 1830:3289–3303. https://doi.org/10.1016/j.bbagen.2012.11.020
Burger J, Gochfeld M, Rooney AA, Orlando EF, Woodward AR, Guillette LJ (2000) Metals and metalloids in tissues of American alligators in three Florida lakes. Arch Environ Contam Toxicol 38:501–508. https://doi.org/10.1007/s002449910066
Cheng WH, Fu YX, Porres JM, Ross DA, Lei XG (1999) Selenium-dependent cellular glutathione peroxidase protects mice against a pro-oxidant-induced oxidation of NADPH, NADH, lipids, and protein. FASEB J 13:1467–1475
Elsey RM, Lance VA (1983) Effect of diet on blood selenium and glutathione peroxidase activity in the alligator. Comp Biochem Physiol 76B:831–837
Elsey RM, Joanen T, McNease L, Lance VA (1990a) Growth rate and plasma corticosterone levels in juvenile alligators maintained at different stocking densities. J Exp Zool 255:30–36
Elsey RM, Joanen T, McNease L, Lance VA (1990b) Stress and plasma corticosterone levels in the American alligator-relationships with stocking density and nesting success. Comp Biochem Physiol 95:55–63
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. https://doi.org/10.1007/s00244-013-9953-x
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
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 Immunoassay Immunochem 36:496–509. https://doi.org/10.1080/15321819.2014.1001030
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
Finger JW Jr, Botero J, Zhang Y, Still SE, Hoffman AJ, Kavazis AN, Cristol DA, Wada H (2017a) No effect of lifelong methylmercury exposure on oxidative status in zebra finches (Taeniopygia guttata): a demonstration of methylmercury-induced selection? Bull Environ Contam Toxicol 99:668–672. https://doi.org/10.1007/s00128-017-2202-7
Finger JW Jr, Hamilton MT, Glenn TC, Tuberville TD (2017b) 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. https://doi.org/10.1007/s00244-017-0370-4
Fukai T, Ushio-Fukai M (2011) Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 15:1583–1606. https://doi.org/10.1089/ars.2011.3999
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
Gunderson MP, Kools SAE, Milnes MR, Guillette LJ (2003) Effect of acute stress on plasma β-corticosterone, estradiol-17β and testosterone concentrations in juvenile American alligators collected from three sites within the Kissimmee-Everglades drainage basin in Florida (USA). Comp Biochem Physiol C: Toxicol Pharmacol 135:365–374. https://doi.org/10.1016/s1532-0456(03)00138-8
Hamilton MT (2016) Characterizing stress and immune parameters in the American alligator (Alligator mississippiensis). University of Georgia
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 blood analyser. Conserv Physiol 4:cov065. https://doi.org/10.1093/conphys/cov065
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. https://doi.org/10.7589/2015-10-275
Haskins DL, Hamilton MT, Jones AL, Finger JW Jr, Bringolf RB, Tuberville TD (2017a) Accumulation of coal combustion residues and their immunological effects in the yellow-bellied slider (Trachemys scripta scripta). Environ Pollut 224:810–819
Haskins DL, Hamilton MT, Stacy NI, Finger JW Jr, Tuberville TD (2017b) Effects of selenium exposure on the hematology, innate immunity, and metabolic rate of yellow-bellied sliders (Trachemys scripta scripta). Ecotoxicology 26:1134–1146
Haskins DL, Howerth EW, Tuberville TD (2017c) Experimentally induced selenosis in yellow-bellied slider turtles (Trachemys scripta scripta). Vet Pathol 55:473–477
Hill GE, Fu X, Balenger S, McGraw KJ, Giraudeau M, Hood WR (2013) Changes in concentrations of circulating heat-shock proteins in House Finches in response to different environmental stressors. J Field Ornithol 84:416–424. https://doi.org/10.1111/jofo.12040
Hoffman DJ, Heinz GH (1998) Effects of mercury and selenium on glutathione metabolism and oxidative stress in mallard ducks. Environ Toxicol Chem 17:161–166
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
Hopkins WA, Mendonca MT, Congdon JD (1999a) Responsiveness of the hypothalamo-pituitary-interrenal axis in an amphibian (Bufo terrestris) exposed to coal combustion wastes. Comp Biochem Physiol 122:191–196
Hopkins WA, Rowe CL, Congdon JD (1999b) 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
Hopkins WA, Roe JH, Snodgrass J, 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
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). Ecotoxicol Environ Saf 58:285–293. https://doi.org/10.1016/s0147-6513(03)00076-9
Hyatt HW, Kephart WC, Holland AM, Mumford P, Mobley CB, Lowery RP, Roberts MD, Wilson JM, Kavazis AN (2016) A ketogenic diet in rodents elicits improved mitochondrial adaptations in response to resistance exercise training compared to an isocaloric Western diet. Front Physiol 7:533. https://doi.org/10.3389/fphys.2016.00533
Janz DM et al (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. https://doi.org/10.1201/ebk1439826775-c6
Jing CL, Dong XF, Wang ZM, Liu S, Tong JM (2015) Comparative study of DL-selenomethionine vs sodium selenite and seleno-yeast on antioxidant activity and selenium status in laying hens. Poult Sci 94:965–975. https://doi.org/10.3382/ps/pev045
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
Lance VA, Elsey RM (1999) Plasma catecholamines and plasma corticosterone following restraint stress in juvenile alligators. J Exp Zool 283:559–565
Lance VA, Elsey RM, Butterstein G, Trosclair PL (2004) Rapid suppression of testosterone secretion after capture in male American alligators (Alligator mississippiensis). Gen Comp Endocrinol 135:217–222. https://doi.org/10.1016/j.ygcen.2003.09.013
Lemly AD (2004) Aquatic selenium pollution is a global environmental safety issue. Ecotox Environ Safe 59:44–56
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. https://doi.org/10.1021/es301467q
Ma Q (2013) Role of nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol 53:401–426. https://doi.org/10.1146/annurev-pharmtox-011112-140320
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
Miller LL, Rasmussen JB, Palace VP, Hontela A (2009) The physiological stress response and oxidative stress biomarkers in rainbow trout and brook trout from selenium-impacted streams in a coal mining region. J Appl Toxicol 29:681–688. https://doi.org/10.1002/jat.1458
Misra S, Hamilton C, Niyogi S (2012) Induction of oxidative stress by selenomethionine in isolated hepatocytes of rainbow trout (Oncorhynchus mykiss). Toxicol In Vitro 26:621–629. https://doi.org/10.1016/j.tiv.2012.02.001
Monteiro DA, Rantin FT, Kalinin AL (2009) The effects of selenium on oxidative stress biomarkers in the freshwater characid fish matrinxã, Brycon cephalus (Günther, 1869) exposed to organophosphate insecticide Folisuper 600 BR® (methyl parathion). Comp Biochem Physiol 149:40–49. https://doi.org/10.1016/j.cbpc.2008.06.012
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
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
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 129:275–283
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
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
Spallholz JE, Hoffman DJ (2002) Selenium toxicity: cause and effects in aquatic birds. Aquat Toxicol 57:27–37
Spallholz JE, Shriver BJ, Reid TW (2001) Dimethyldiselenide and methylseleninic acid generate superoxide in an in vitro chemiluminescence assay in the presence of glutathione: implications for the anticarcinogenic activity of L-selenomethionine and L-Se-methylselenocysteine. Nutr Cancer 40:34–41. https://doi.org/10.1207/S15327914NC401_8
Stewart MJ, Spallholz JE, Neldner KH, Pence BC (1999) Selenium compounds have disparate abilities to impose oxidative stress and induce apoptosis. Free Radic Biol Med 26:42–48
Thomas JK, Janz DM (2011) Dietary selenomethionine exposure in adult zebrafish alters swimming performance, energetics and the physiological stress response. Aquat Toxicol 102:79–86. https://doi.org/10.1016/j.aquatox.2010.12.020
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
Vidal D, Bay SM, Schlenk D (2005) Effects of dietary selenomethionine on larval rainbow trout (Oncorhynchus mykiss). Arch Environ Contam Toxicol 49:71–75. https://doi.org/10.1007/s00244-004-0160-7
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
Ware LL, Petrie SA, Bailey RC, Badzinski SS, Schummer ML, Chen YW, Belzile N (2012) Effects of elevated selenium on body condition, oxidative stress, and oragn health in greater scaup wintering in Lake Ontario. Wildl Soc Bull 36:506–511. https://doi.org/10.1002/wsb.158
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
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
Acknowledgements
The authors thank Dr. Ruth Elsey and her staff at Rockefeller Wildlife Refuge for providing alligators for this study. Sharon L. Finger helped in the transport of alligators from Louisiana to South Carolina. Dan Quinn, Nick Bossebroek, David Haskins, Bess Harris, Sam Dean, and Megan E. Winzeler were instrumental in assisting with the feeding, blood sampling, and dissections of alligators. We thank two anonymous reviewers whose comments helped to improve an earlier version of this manuscript. Support was provided in part by Award Number DE-FC09-07SR22506 from Department of Energy to the University of Georgia Research Foundation, by the Crocodile Specialists Group, and Savannah River Nuclear Solutions – Area Completions Project. All experimental procedures were approved by the University of Georgia’s Institutional Animal Care and Use Committee.
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Finger, J.W., Hamilton, M.T., Kelley, M.D. et al. Dietary Selenomethionine Administration and Its Effects on the American Alligator (Alligator mississippiensis): Oxidative Status and Corticosterone Levels. Arch Environ Contam Toxicol 75, 37–44 (2018). https://doi.org/10.1007/s00244-018-0530-1
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DOI: https://doi.org/10.1007/s00244-018-0530-1