, Volume 21, Issue 4, pp 1094–1101 | Cite as

Elevated mercury exposure and neurochemical alterations in little brown bats (Myotis lucifugus) from a site with historical mercury contamination

  • Dong-Ha Nam
  • David Yates
  • Pedro Ardapple
  • David C. Evers
  • John Schmerfeld
  • Niladri BasuEmail author


Despite evidence of persistent methylmercury (MeHg) contamination in the South River (Virginia, USA) ecosystem, there is little information concerning MeHg-associated neurological impacts in resident wildlife. Here we determined mercury (Hg) concentrations in tissues of insectivorous little brown bats (Myotis lucifugus) collected from a reference site and a MeHg-contaminated site in the South River ecosystem. We also explored whether neurochemical biomarkers (monoamine oxidase, MAO; acetylcholinesterase, ChE; muscarinic acetylcholine receptor, mAChR; N-methyl-d-aspartate receptor, NMDAR) previously shown to be altered by MeHg in other wildlife were associated with brain Hg levels in these bats. Concentrations of Hg (total and MeHg) in tissues were significantly higher (10–40 fold difference) in South River bats when compared to reference sites. Mean tissue mercury levels (71.9 ppm dw in liver, 7.14 ppm dw in brain, 132 ppm fw in fur) in the South River bats exceed (sub)-clinical thresholds in mammals. When compared to the South River bats, animals from the reference site showed a greater ability to demethylate MeHg in brain (33.1% of total Hg was MeHg vs. 65.5%) and liver (8.9% of total Hg was MeHg vs. 50.8%) thus suggesting differences in their ability to detoxify and eliminate Hg. In terms of Hg-associated neurochemical biomarker responses, interesting biphasic responses were observed with an inflection point between 1 and 5 ppm dw in the brain. In the reference bats Hg-associated decreases in MAO (r = −0.61; p < 0.05) and ChE (r = −0.79; p < 0.01) were found in a manner expected but these were not found in the bats from the contaminated site. Owing to high Hg exposures, differences in Hg metabolism, and the importance of the aforementioned neurochemicals in multiple facets of animal health, altered or perhaps even a lack of expected neurochemical responses in Hg-contaminated bats raise questions about the ecological and physiological impacts of Hg on the bat population as well as the broader ecosystem in the South River.


Methyl mercury South River Ecotoxicology Neurochemical biomarkers Wildlife 



This study was funded by the University of Michigan School of Public Health and Biodiversity Research Institute (BRI). We thank Rick Reynolds from the Virginia Department of Game and Inland Fisheries (VDGIF) for providing project advice. Also, special thanks to Larry, Josh, and the crew at the Augusta Forestry Center for their generosity in allowing use of their facility and field equipment. We offer a special thanks to Dan Cristol from the College of William and Mary and U.S. Fish and Wildlife Service biologists Casey Huck, Bita Zahedi, Tim Divoll, provided dedicated field assistance.


  1. Adams DH, Sonne C, Basu N, Dietz R, Nam DH, Leifsson PS, Jensen AL (2010) Mercury contamination in spotted seatrout, Cynoscion nebulosus: an assessment of liver, kidney, blood, and nervous system health. Sci Total Environ 408:5808–5816CrossRefGoogle Scholar
  2. Allinson G, Mispagel C, Kajiwara N, Anan Y, Hashimoto J, Laurenson L, Allinson M, Tanabe S (2006) Organochlorine and trace metal residues in adult southern bent-wing bat (Miniopterus schreibersii bassanii) in southeastern Australia. Chemosphere 64(9):1464–1471CrossRefGoogle Scholar
  3. Animal Care and Use Committee (1998) Guidelines for the capture, handling, and care of mammals as approved by the American Society of Mammalogists. J Mammal 79:1416–1431CrossRefGoogle Scholar
  4. Aschner M, Aschner JL (1990) Mercury neurotoxicity: mechanisms of blood-brain barrier transport. Neurosci Biobehav Rev 14(2):169–176CrossRefGoogle Scholar
  5. Basu N, Scheuhammer AM, Grochowina N, Klenavic K, Evans D, O’Brien M, Chan HM (2005) Effects of mercury on neurochemical receptors in wild river otters (Lontra canadensis). Environ Sci Technol 39(10):3585–3591CrossRefGoogle Scholar
  6. Basu N, Scheuhammer AM, Rouvinen-Watt K, Grochowina N, Klenavic K, Evans RD, Chan HM (2006) Methylmercury impairs components of the cholinergic system in captive mink (Mustela vison). Toxicol Sci 91:202–209CrossRefGoogle Scholar
  7. Basu N, Scheuhammer AM, Evans RD, O’Brien M, Chan HM (2007a) Cholinesterase and monoamine oxidase activity in relation to mercury levels in the cerebral cortex of wild river otters. Hum Exp Toxicol 26(3):213–220CrossRefGoogle Scholar
  8. Basu N, Scheuhammer AM, Rouvinen-Watt K, Grochowina N, Evans RD, O’Brien M, Chan HM (2007b) Decreased N-methyl-d-aspartic acid (NMDA) receptor levels are associated with mercury exposure in wild and captive mink. Neurotoxicology 28(3):587–593CrossRefGoogle Scholar
  9. Basu N, Scheuhammer AM, Bursian S, Rouvinen-Watt K, Elliott J, Chan HM (2007c) Mink as a sentinel in environmental health. Environ Res 103:130–144CrossRefGoogle Scholar
  10. Basu N, Scheuhammer AM, Rouvinen-Watt K, Evans RD, Grochowina N, Chan LH (2008) The effects of mercury on muscarinic cholinergic receptor subtypes (M1 and M2) in captive mink. Neurotoxicology 29(2):328–334CrossRefGoogle Scholar
  11. Basu N, Scheuhammer AM, Sonne C, Letcher RJ, Born EW, Dietz R (2009) Is dietary mercury of neurotoxicological concern to wild polar bears (Ursus maritimus)? Environ Toxicol Chem 28(1):133–140CrossRefGoogle Scholar
  12. Bergeron CM, Bodinof CM, Unrine JM, Hopkins WA (2010a) Mercury accumulation along a contamination gradient and nondestructive indices of bioaccumulation in amphibians. Environ Toxicol Chem 29(4):980–988CrossRefGoogle Scholar
  13. Bergeron CM, Bodinof CM, Unrine JM, Hopkins WA (2010b) Bioaccumulation and maternal transfer of mercury and selenium in amphibians. Environ Toxicol Chem 29(4):989–997CrossRefGoogle Scholar
  14. Bonuccelli U, Piccini P, Del Dotto P, Pacifici GM, Corsini GU, Muratorio A (1990) Platelet monoamine oxidase B activity in parkinsonian patients. J Neurol Neurosurg Psychiatry 53(10):854–855CrossRefGoogle Scholar
  15. Burton GV, Alley RJ, Rasmussen GL, Orton P, Cox V, Jones P, Graff D (1977) Mercury and behavior in wild mouse populations. Environ Res 14(1):30–34CrossRefGoogle Scholar
  16. Calabrese EJ, Baldwin LA (2003) Inorganics and hormesis. Crit Rev Toxicol 33(3–4):215–304CrossRefGoogle Scholar
  17. Carter LJ (1977) Chemical plants leave unexpected legacy for two Virginia Rivers. Science 198(4321):1015–1020CrossRefGoogle Scholar
  18. Castoldi AF, Coccini T, Ceccatelli S, Manzo L (2001) Neurotoxicity and molecular effects of methylmercury. Brain Res Bull 55(2):197–203CrossRefGoogle Scholar
  19. Clarkson TW, Magos L (2006) The toxicology of mercury and its chemical compounds. Crit Rev Toxicol 36(8):609–662CrossRefGoogle Scholar
  20. Cristol DA, Brasso RL, Condon AM, Fovargue RE, Friedman SL, Hallinger KK, Monroe AP, White AE (2008) The movement of aquatic mercury through terrestrial food webs. Science 320(5874):335CrossRefGoogle Scholar
  21. Cumbie PM (1975) Mercury levels in Georgia otter, mink and freshwater fish. Bull Environ Contam Toxicol 14(2):193–196CrossRefGoogle Scholar
  22. Dietz R, Born EW, Riget F, Sonne C, Aubail A, Drimmie R, Basu N (2011) Temporal trends and future predictions of mercury concentrations in Northwest Greenland polar bear (Ursus maritimus) hair. Environ Sci Technol 45(4):1458–1465CrossRefGoogle Scholar
  23. Ekino S, Susa M, Ninomiya T, Imamura K, Kitamura T (2007) Minamata disease revisited: an update on the acute and chronic manifestations of methyl mercury poisoning. J Neurol Sci 262(1–2):131–144CrossRefGoogle Scholar
  24. Eto K (2000) Minamata disease. Neuropathology 20(Suppl):S14–S19CrossRefGoogle Scholar
  25. Gerell R, Lundberg KG (1993) Decline of a bat pipistrellus pipistrellus population in an industrialized area in south sweden. Biol Consev 65:153–157CrossRefGoogle Scholar
  26. Hickey MB, Fenton MB (1996) Behavioral and thermoregulatory responses of female hoary bats, lasiurus cinereus (chiroptera: Vespertilionidae), to variations in prey availability. Ecoscience 3:414–422Google Scholar
  27. Hickey MB, Fenton MB, MacDonald KC, Soulliere C (2001) Trace elements in the fur of bats (Chiroptera: Vespertilionidae) from Ontario and Quebec, Canada. Bull Environ Contam Toxicol 66(6):699–706CrossRefGoogle Scholar
  28. Khan MA, Wang F (2009) Mercury-selenium compounds and their toxicological significance: toward a molecular understanding of the mercury-selenium antagonism. Environ Toxicol Chem 28(8):1567–1577CrossRefGoogle Scholar
  29. Kinghorn A, Solomon P, Chan HM (2007) Temporal and spatial trends of mercury in fish collected in the English-Wabigoon river system in Ontario, Canada. Sci Total Environ 372(2–3):615–623Google Scholar
  30. Kumar S (1998) Biphasic effect of aluminium on cholinergic enzyme of rat brain. Neurosci Lett 248(2):121–123CrossRefGoogle Scholar
  31. Meldrum BS (2000) Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J Nutr 130(4S Suppl):1007S–1015SGoogle Scholar
  32. Mergler D, Anderson HA, Chan LH, Mahaffey KR, Murray M, Sakamoto M, Stern AH (2007) Methylmercury exposure and health effects in humans: a worldwide concern. Ambio 36(1):3–11CrossRefGoogle Scholar
  33. Meteyer CU, Valent M, Kashmer J, Buckles EL, Lorch JM, Blehert DS, Lollar A, Berndt D, Wheeler E, White CL, Ballmann AE (2011) Recovery of little brown bats (Myotis lucifugus) from natural infection with geomyces destructants, white-nose syndrome. J Wildl Dis 47(3):618–626Google Scholar
  34. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: from structure to function. Physiol Rev 78(1):189–225Google Scholar
  35. Miura T, Koyama T, Nakamura I (1978) Mercury content in museum and recent specimens of chiroptera in Japan. Bull Environ Contam Toxicol 20(5):696–701CrossRefGoogle Scholar
  36. Nam DH, Basu N (2011) Rapid methods to detect organic mercury and total selenium in biological samples. Chem Cent J 5(1):3CrossRefGoogle Scholar
  37. Nam DH, Adams DH, Flewelling LJ, Basu N (2010) Neurochemical alterations in lemon shark (Negaprion brevirostris) brains in association with brevetoxin exposure. Aquat Toxicol 99(3):351–359CrossRefGoogle Scholar
  38. Nam DH, Adams DH, Reyier EA, Basu N (2011) Mercury and selenium levels in lemon sharks (Negaprion brevirostris) in relation to a harmful red tide event. Environ Monit Assess 176(1–4):549–559CrossRefGoogle Scholar
  39. Powell GV (1983) Industrial effluents as a source of mercury contamination in terrestrial riparian vertebrates. Environ Pollut A 5:51–57CrossRefGoogle Scholar
  40. Pybur MJ, Hobron DP, Onderka DK (1986) Mass mortality of bats due to probable blue-green algal toxicity. J Wildl Dis 22(3):449–450Google Scholar
  41. Rutkiewicz J, Nam DH, Cooley T, Neumann K, Padilla IB, Route W, Strom S, Basu N (2011) Mercury exposure and neurochemical biomarkers in bald eagles across several Great Lakes States. Ecotoxicology 20(7):1669–1676CrossRefGoogle Scholar
  42. Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36(1):12–18CrossRefGoogle Scholar
  43. Scheuhammer AM, Basu N, Burgess NM, Elliott JE, Campbell GD, Wayland M, Champoux L, Rodrigue J (2008) Relationships among mercury, selenium, and neurochemical parameters in common loons (Gavia immer) and bald eagles (Haliaeetus leucocephalus). Ecotoxicology 17(2):93–101CrossRefGoogle Scholar
  44. Sleeman JM, Cristol DA, White AE, Evers DC, Gerhold RW, Keel MK (2010) Mercury poisoning in a free-living northern river otter (Lontra canadensis). J Wildl Dis 46(3):1035–1039Google Scholar
  45. Stevens RT, Ashwood TL, Sleeman JM (1997) Mercury in hair of muskrats (Ondatra zibethicus) and mink (Mustela vison) from the U. S. Department of Energy Oak Ridge Reservation. Bull Environ Contam Toxicol 58(5):720–725CrossRefGoogle Scholar
  46. Tokuomi H (1968) Minamata disease. Naika 21(5):864–870Google Scholar
  47. Tomlinson G, Mutus B, McLennan I (1981) Activation and inactivation of acetylcholinesterase by metal ions. Can J Biochem 59(9):728–735CrossRefGoogle Scholar
  48. Wada H, Cristol DA, McNabb FM, Hopkins WA (2009) Suppressed adrenocortical responses and thyroid hormone levels in birds near a mercury-contaminated river. Environ Sci Technol 43(15):6031–6038CrossRefGoogle Scholar
  49. Wada H, Yates DE, Evers DC, Taylor RJ, Hopkins WA (2010) Tissue mercury concentrations and adrenocortical responses of female big brown bats (Eptesicus fuscus) near a contaminated river. Ecotoxicology 19(7):1277–1284CrossRefGoogle Scholar
  50. Weinstock M, Gorodetsky E, Poltyrev T, Gross A, Sagi Y, Youdim M (2003) A novel cholinesterase and brain-selective monoamine oxidase inhibitor for the treatment of dementia comorbid with depression and Parkinson’s disease. Prog Neuropsychopharmacol Biol Psychiatry 27(4):555–561CrossRefGoogle Scholar
  51. Wess J (2004) Muscarinic acetylcholine receptor knockout mice: novel phenotypes and clinical implications. Annu Rev Pharmacol Toxicol 44:423–450CrossRefGoogle Scholar
  52. Wobeser G, Nielsen NO, Schiefer B (1976) Mercury and Mink. II. Experimental methyl mercury intoxication. Can J Comp Med 40(1):34–45Google Scholar
  53. Wolfe MF, Schwarzbach S, Sulaiman RA (1998) Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146–160CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Dong-Ha Nam
    • 1
  • David Yates
    • 2
  • Pedro Ardapple
    • 2
  • David C. Evers
    • 2
  • John Schmerfeld
    • 3
  • Niladri Basu
    • 1
    Email author
  1. 1.Department of Environmental Health SciencesUniversity of Michigan School of Public HealthAnn ArborUSA
  2. 2.Biodiversity Research InstituteGorhamUSA
  3. 3.U.S. Fish and Wildlife ServiceAlbuquerqueUSA

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