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Ecotoxicology

, Volume 19, Issue 7, pp 1277–1284 | Cite as

Tissue mercury concentrations and adrenocortical responses of female big brown bats (Eptesicus fuscus) near a contaminated river

  • Haruka Wada
  • David E. Yates
  • David C. Evers
  • Robert J. Taylor
  • William A. HopkinsEmail author
Article

Abstract

Much of the research on mercury (Hg) in wild vertebrates has focused on piscivores and other animals at high trophic levels. However, recent studies indicated that insectivorous terrestrial vertebrates may also be at risk. In the present study, we examined blood and fur Hg concentrations as well as the adrenocortical responses of insectivorous big brown bats (Eptesicus fuscus) near the Hg-contaminated South River, VA and a nearby reference area. Baseline glucocorticoids and adrenocortical responses to handling have been widely used to assess the influence of environmental stressors because plasma glucocorticoids rise in response to various physical, psychological, and physiological challenges. Female bats captured at the contaminated site had 2.6 times higher blood and fur Hg concentrations than those captured at the reference site (blood: 0.11 vs. 0.04 μg/g wet weight; fur: 28.0 vs. 10.9 μg/g fresh weight). Fur Hg concentrations at the contaminated site were higher than most wild omnivorous and carnivorous mammals reported in the literature. Although fur and blood Hg concentrations were tightly correlated, fur Hg concentrations averaged 260 times higher than concentrations in blood. This suggests that fur may be an important depuration route for bats, just as it is in other mammals. Despite the high Hg concentrations in bat tissue, we did not observe any site difference in adrenocortical responses. Our results suggest that the bats at the contaminated site were exposed to Hg concentrations below those causing adverse effects on their adrenal axis.

Keywords

Mercury Cortisol Fur:blood ratio Insectivore Eptesicus fuscus 

Notes

Acknowledgements

We thank Calvin Jordan and Jessenta Reynes for providing their barns, the South River Science Team for technical support, Virginia Department of Environmental Quality for sponsoring the South River Science Team, Tim Divoll and Danielle Temple from BioDiversity Research Institute, Gorham, Maine for their help in the field, and Sarah Budischak and Guillaume Salze for reviewing the manuscript. We also thank Dan Cristol from the College of William and Mary, U.S. Fish and Wildlife Service biologists John Schmerfeld and Sumalee Hoskin for their support, and DuPont for funding this study. Research was completed with oversight from the South River Science Team which is a collaboration of state and federal agencies, academic institutions, and environmental interests.

References

  1. Ackerman JT, Takekawa JY, Eagles-Smith CA, Iverso SA (2008) Mercury contamination and effects on survival of American avocet and black-necked stilt chicks in san francisco bay. Ecotoxicology 17:103–116CrossRefGoogle Scholar
  2. Arnett EB, Brown WK, Erickson WP et al (2008) Patterns of bat fatalities at wind energy facilities in North America. J Wildl Manag 72:61–78CrossRefGoogle Scholar
  3. Basu N, Scheuhammer AM, Rouvinen-Watt K et al (2006) Methylmercury impairs components of the cholinergic system in captive mink (mustela vison). Toxicol Sci 91:202–209CrossRefGoogle Scholar
  4. Baxter CV, Fausch KD, Saunders WC (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol 50:201–220CrossRefGoogle Scholar
  5. Bergeron CM, Husak JF, Unrine JM, Romanek CS, Hopkins WA (2007) Influence of feeding ecology on blood mercury concentrations in four species of turtles. Environ. Toxicol. Chem 26:1733–1741CrossRefGoogle Scholar
  6. 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 29:980–988CrossRefGoogle Scholar
  7. Bergeron CM, Bodinof CM, Unrine JM, Hopkins WA (2010b) Bioaccumulation and maternal transfer of mercury and selenium in amphibians. Environ. Toxicol. Chem 29:989–997CrossRefGoogle Scholar
  8. Bleau H, Daniel C, Chevalier G, van Tra H, Hontela A (1996) Effects of acute exposure to mercury chloride and methylmercury on plasma cortisol, t3, t4, glucose and liver glycogen in rainbow trout (oncorhynchus mykiss). Aquat Toxicol 34:221–235CrossRefGoogle Scholar
  9. Blehert DS, Hicks AC, Behr M et al (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323:227CrossRefGoogle Scholar
  10. Brookens TJ, Harvey JT, O’Hara TM (2007) Trace element concentrations in the pacific harbor seal (phoca vitulina richardii) in central and northern California. Sci. Total Environ 372:676–692CrossRefGoogle Scholar
  11. Budtz-Jorgensen E, Grandjean P, Jorgensen PJ, Weihe P, Keiding N (2004) Association between mercury concentrations in blood and hair in methylmercury-exposed subjects at different ages. Environ. Res 95:385–393CrossRefGoogle Scholar
  12. Burton GV, Alley RJ, Rasmussen GL et al (1977) Mercury and behavior in wild mouse populations. Environ. Res 14:30–34CrossRefGoogle Scholar
  13. Cardona-Marek T, Knott KK, Meyer BE, O’Hara TM (2009) Mercury concentrations in southern Beaufort Sea polar bears: variation based on stable isotopes of carbon and nitrogen. Environ. Toxicol. Chem 28:1416–1424CrossRefGoogle Scholar
  14. Carter LJ (1977) Chemical plants leave unexpected legacy for two Virginia rivers. Science 198:1015–1020CrossRefGoogle Scholar
  15. Cernichiari E, Toribara TY, Liang L, Marsh DO, Berlin MW, Myers GJ, Cox C, Shamlaye CF, Choisy O, Davidson P, Clarkson TW (1995) The biological monitoring of mercury in the seychelles study. Neurotoxicology 16(4):613–627Google Scholar
  16. Cernichiari E, Myers GJ, Ballatori N et al (2007) The biological monitoring of prenatal exposure to methylmercury. Neurotoxicology 28:1015–1022CrossRefGoogle Scholar
  17. Clark DR, Shore RF (2001) Chiroptera. In: Shore RF, Rattner BA (eds) Ecotoxicology of wild mammals. Wiley, London, pp 159–214Google Scholar
  18. Cristol DA, Brasso RL, Condon AM et al (2008) The movement of aquatic mercury through terrestrial food webs. Science 320:335CrossRefGoogle Scholar
  19. Cumbie RM, Jenkins JH (1975) Mercury accumulation in native animals of the southeast. Proc Annu Conf Southeast Assoc Game Fish Commun 28:639–648Google Scholar
  20. Eisler R (2006) Mercury hazards to living organisms. Taylor and Francis Publishers, LondonCrossRefGoogle Scholar
  21. Evers DC, Burgess NM, Champoux L et al (2005) Patterns and interpretation of mercury exposure in freshwater avian communities in northeastern North America. Ecotoxicology 14:193–221CrossRefGoogle Scholar
  22. Franceschini MD, Lane OP, Evers DC et al (2009) The corticosterone stress response and mercury contamination in free-living tree swallows, tachycineta bicolor. Ecotoxicology 18:514–521CrossRefGoogle Scholar
  23. Friedmann AS, Watzin MC, Brinck-Johnsen T, Leiter JC (1996) Low levels of dietary methylmercury inhibit growth and gonadal development in juvenile walleye (Stizostedion vitreum). Aquat Toxicol 35:265–278CrossRefGoogle Scholar
  24. Hickey MBC, Fenton MB (1996) Behavioural and thermoregulatory responses of female hoary bats, lasiurus cinereus (chiroptera: Vespertilionidae), to variations in prey availability. Ecoscience 3:414–422Google Scholar
  25. Hickey MBC, 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 66:699–706CrossRefGoogle Scholar
  26. 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 108:237–246CrossRefGoogle Scholar
  27. Kenow KP, Meyer MW, Hines RK, Karasov WH (2007) Distribution and accumulation of mercury in tissues of captive-reared common loon (gavia immer) chicks. Environ. Toxicol. Chem 26:1047–1055CrossRefGoogle Scholar
  28. Kirubagaran R, Joy KP (1991) Changes in adrenocortical-pituitary activity in the catfish, clarias batrachus (l.), after mercury treatment. Ecotoxicol. Environ. Saf 22:36–44CrossRefGoogle Scholar
  29. Kunz TH, Fenton MB (2003) Bat ecology. The University of Chicago Press, ChicagoGoogle Scholar
  30. Kurta A (1999) Big brown bats, Eptesicus fuscus. In: Wilson DE, Ruff S (eds) The Smithsonian book of North American mammals. Smithsonian Institution Press, Washington, London, pp 115–117Google Scholar
  31. Linzey DW (1998) Big brown bat Eptesicus fuscus (beauvois). The mammals of Virginia. The McDonald & Woodward Publishing Company, Blacksburg, pp 77–80Google Scholar
  32. Miura T, Koyama T, Nakamura I (1978) Mercury content in museum and recent specimens of chiroptera in japan. Bull. Environ. Contam. Toxicol 20:696–701CrossRefGoogle Scholar
  33. Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc. Natl. Acad. Sci. USA 98:166–170CrossRefGoogle Scholar
  34. Newman J, Zillioux E, Rich E, Liang L, Newman C (2004) Historical and other patterns of monomethyl and inorganic mercury in the Florida panther (Puma concolor coryi). Arch. Environ. Contam. Toxicol 48:75–80CrossRefGoogle Scholar
  35. Phillips GL (1966) Ecology of the big brown bat (chiroptera: Vespertilionidae) in northeastern Kansas. Am. Midl. Nat 75:168–198CrossRefGoogle Scholar
  36. Porcella DB, Zillioux EJ, Grieb TM, Newman JR, West GB (2004) Retrospective study of mercury in raccoons (Procyon lotor) in south Florida. Ecotoxicology 13:207–221CrossRefGoogle Scholar
  37. Reeder DM, Kosteczko NS, Kunz TH, Widmaier EP (2004) Changes in baseline and stress-induced glucocorticoid levels during the active period in free-ranging male and female little brown myotis, Myotis lucifugus (chiroptera: Vespertilionidae). Gen. Comp. Endocrinol 136:260–269CrossRefGoogle Scholar
  38. Rimmer CC, McFarland KP, Evers DC et al (2005) Mercury concentrations in bicknell’s thrush and other insectivorous passerines in montane forests of northeastern North America. Ecotoxicology 14:223–240CrossRefGoogle Scholar
  39. Roelke M, Schultz D, Facemire C, Sundlof S, Royals H (1991) Mercury contamination in florida panthers. A report of the Florida Panther Technical Subcommittee to the Florida Panther Interagency Committee. Tallahassee, FLGoogle Scholar
  40. Romero LM, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc. Natl. Acad. Sci. USA 98:7366–7370CrossRefGoogle Scholar
  41. Ronald K, Tessaro SV, Uthe JF, Freeman HC, Frank R (1977) Methylmercury poisoning in the harp seal (Pagophilus groenlandicus). Sci. Total Environ 8:1–11CrossRefGoogle 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 36:12–18CrossRefGoogle Scholar
  43. Spalding MG, Frederick PC, McGill HC et al (2000) Histologic, neurologic, and immunologic effects of methylmercury in captive great egrets. J Wildl Dis 36:423–435Google Scholar
  44. Stevens RT, Ashwood TL, Sleeman JM (1997) Mercury in hair of muskrats (ondatra zibethicus) and mink (mustela vison) from the us department of energy oak ridge reservation. Bull. Environ. Contam. Toxicol 58:720–725CrossRefGoogle Scholar
  45. Sundberg J, Jönsson S, Karlsson MO, Hallén IP, Oskarsson A (1998) Kinetics of methylmercury and inorganic mercury in lactating and nonlactating mice. Toxicol. Appl. Pharmacol 151:319–329CrossRefGoogle Scholar
  46. Suzuki T (1979) Dose-effect and dose-response relationships of mercury and its derivatives. In: Nriagu JO (ed) The biogeochemistry of mercury in the environment. Elsevier/North Holland Biomedical Press, Amsterdam, pp 399–431Google Scholar
  47. Takizawa Y (1979) Epidemiology of mercury poisoning. In: Nriagu JO (ed) The biogeochemistry of mercury in the environment. Elsevier/North Holland Biomedical Press, Amsterdam, pp 325–365Google Scholar
  48. USEPA (1997) Characterization of human health and wildlife risks from mercury exposure in the united states. Mercury Study Report to Congress, vol 7. U.S. Environmental Protection Agency, Washington, DCGoogle Scholar
  49. USEPA (1998) Mercury in solids and solutions by thermal decomposition, amalgamation, and atomic absorption spectrophotometry. USEP Agency, SW-846 Method 7473Google Scholar
  50. 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 150:405–413CrossRefGoogle Scholar
  51. Wada H, Cristol DA, McNabb FMA, Hopkins WA (2009) Suppressed adrenocortical responses and thyroid hormone levels in birds near a mercury-contaminated river. Environ. Sci. Technol 43:6031–6038CrossRefGoogle Scholar
  52. Walker BG, Boersma PD, Wingfield JC (2005) Field endocrinology and conservation biology. Integr Comp Biol 45:12–18CrossRefGoogle Scholar
  53. Walters DM, Fritz KM, Otter RR (2008) The dark side of subsidies: adult stream insects export organic contaminants to riparian predators. Ecol. Appl 18:1835–1841CrossRefGoogle Scholar
  54. Wingfield JC (1994) Modulation of the adrenocortical response to stress in birds. In: Davey KG, Peter RE, Tobe SS (eds) Perspectives in comparative endocrinology. National Research Council of Canada, Ottawa, pp 520–528Google Scholar
  55. Wobeser G, Nielsen NO, Schiefer B (1976) Mercury and mink. II. Experimental methyl mercury intoxication. Can J Comp Med 40:34–45Google Scholar
  56. Wolfe MF, Atkeson T, Bowerman W, Burger K, Evers DC, Murray MW, Zillioux E (2007) Wildlife indicators. In: Harris R, Krabbenhoft DP, Mason R, Murray MW, Reash R, Saltman T (eds) Ecosystem response to mercury contamination: indicators of change. CRC Press, SETAC, Webster, pp 123–189Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Haruka Wada
    • 1
  • David E. Yates
    • 2
  • David C. Evers
    • 2
  • Robert J. Taylor
    • 3
  • William A. Hopkins
    • 1
    Email author
  1. 1.Department of Fisheries and Wildlife SciencesVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  2. 2.BioDiversity Research InstituteGorhamUSA
  3. 3.Trace Element Research LabTexas A&M UniversityCollege StationUSA

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