Mercury bioaccumulation in Southern Appalachian birds, assessed through feather concentrations

Ecotoxicology

Volumn 23, Issue 2, 2014, Pages 304-316

  Keller, Rebecca Hylton ^a   Xie, Lingtian ^b,c   Buchwalter, David B ^c   Franzreb, Kathleen E ^d   Simons, Theodore R ^c  

^a Appalachian Mountains Joint Venture   (United States)

^b INSTITUTE OF APPLIED ECOLOGY   (China)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Appalachian Mountains; Mercury; Nitrogen 15 stable isotope; Songbirds; Terrestrial; Trophic position

Indexed keywords

MERCURY; NITROGEN; STABLE ISOTOPE;

BIOACCUMULATION; FEATHER; MERCURY (ELEMENT); SONGBIRD; STABLE ISOTOPE; TROPHIC LEVEL;

ADULT; ANIMAL TISSUE; ARTICLE; ATMOSPHERIC DEPOSITION; BIOACCUMULATION; BIRD; CHEMICAL ANALYSIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ECOTOXICITY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; ENVIRONMENTAL MONITORING; FEMALE; FORAGING BEHAVIOR; GEOGRAPHIC DISTRIBUTION; MERCURIALISM; NONHUMAN; PREDICTION; PRIORITY JOURNAL; SEASONAL VARIATION; WATER ANALYSIS;

APPALACHIANS;

ANIMALIA; AVES;

ANIMALS; BIRDS; ENVIRONMENTAL MONITORING; ENVIRONMENTAL POLLUTANTS; FEATHERS; FEMALE; LINEAR MODELS; MALE; MERCURY;

EID: 84896704695     PISSN: 09639292     EISSN: 15733017     Source Type: Journal    
DOI: 10.1007/s10646-013-1174-6     Document Type: Article

References (84)

1. Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second International Symposium on Information Theory. Akademiai Kiado, Budapest, pp 267-281
2. Alsop FJ Jr (1991) Birds of the smokies. Great Smoky Mountains Association, Gatlinburg
3. Atwell L, Hobson KA, Welch HE (1998) Biomagnification and bioaccumulation of mercury in an arctic marine food web: insights from stable nitrogen isotope analysis. Can J Fish Aquat Sci 55:1114-1121
4. Bates D, Maechler M, Bolker B, Walker S (2013) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.0-5. http://CRAN.R-project.org/ package=lme4. Accessed 15 Oct 2013
5. Bearhop S, Ruxton GD, Furness RW (2000) The dynamics of mercury in the blood and feathers of great skuas. Environ Toxicol Chem 19:1638-1643
6. Bergeron CM, Bodinof CM, Unrine JM, Hopkins WA (2010) Mercury accumulation along a contamination gradient and nondestructive indices of bioaccumulation in amphibians. Environ Toxicol Chem 29:980-988
7. Bond AL, Diamond AW (2009) Mercury concentrations in seabird tissues from Machias Seal Island, New Brunswick, Canada. Sci Total Environ 407:4340-4347
8. Brasso RL, Cristol DA (2008) Effects of mercury exposure on the reproductive success of tree swallows (Tachycinea bicolor). Ecotoxicology 17:133-141
9. Burger J (1993) Metals in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 1993:203-311
10. Burgess NM, Hobson KA (2006) Bioaccumulation of mercury in yellow perch (Perca flavescens) and common loons (Gavia immer) in relation to lake chemistry in Atlantic Canada. Hydrobiologia 567:275-282
11. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer-Verlag, New York
12. Chen CY, Stemberger RS, Kamman NC, Mayes BM, Folt CL (2005) Patterns of Hg bioaccumulation and transfer in aquatic food webs across multi-lake studies in the northeast U.S. Ecotoxicology 14:135-147
13. Condon AM, Cristol DA (2009) Feather growth influences blood mercury levels of young songbirds. Environ Toxicol Chem 28:395-401
14. Crewther WG, Fraser RD, Lennox FG, Lindley H (1965) The chemistry of keratins. In: Anifinsen CB, Anson ML, Edsoll JT, Richards FM (eds) Advances in protein chemistry. Academic Press, New York, pp 191-303
15. 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 329:335
16. De Graaf RM, Tilghman NG, Anderson SH (1985) Foraging guilds of North American Birds. Environ Manag 9:493-536
17. Dietz R, Riget F, Born EW, Sonne C, Grandjean P, Kirkegaard M, Olsen MT, Asmund G, Renoni A, Baagøe H, Andreasen C (2006) Trends in mercury in hair of Greenlandic polar bears (Ursus maritimus) during 1892-2001. Environ Sci Technol 40:1120-1125
18. Driscoll CT, Han Y, Chen CY, Evers DC, Fallon Lambert K, Holsen TM, Kamman NC, Munson RK (2007) Mercury contamination in forest and freshwater ecosystems in the Northeastern United States. BioSci 57:17-28
19. Eagles-Smith C, Ackerman JT (2009) Rapid changes in small fish mercury concnetrations in estuarine wetlands: implications for wildlife risk and monitoring programs. Environ Sci Technol 43:8658-8664
20. Eisler R (2006) Mercury hazards to living organisms. Taylor and Francis Publishers, London
21. Evers DC, Clair TA (2005) Mercury in North-eastern North America: a synthesis of existing databases. Ecotoxicology 14:7-13
22. Evers DC, Burgess NM, Champoux L, Hoskins B, Major A, Goodale WM, Taylor RJ, Poppenga R, Daigle T (2005) Patterns and interpretation of mercury exposure in freshwater avian communities in northeastern North America. Ecotoxicology 14:193-221
23. Evers DC, Savoy LJ, DeSorbo CR, Yates DE, Haso W, Taylor KM, Siegel LS, Cooley HH Jr, Bank MS, Major A, Muey K, Mower B, Vogel HS, Schoch N, Pokras M, Goodale MW, Fair J (2008) Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17:69-81
24. Frederick PC, Jayasena N (2012) Altered pairing behavior and reproductive success in white ibises exposed to environmentally relevant concentrations of methylmercury. Proc R Soc Lond Ser B 278:1851-1857
25. Frederick PC, Hylton B, Heath JA, Spalding MG (2004) A historical record of mercury contamination in Southern Florida (USA) as inferred from avian feather tissue. Environ Toxicol Chem 23:1474-1478
26. Frederick PC, Campbell A, Jayasena N, Borkhataria R (2011) Survival of White Ibises (Eudocimus albus) in response to chronic experimental methylmercury exposure. Ecotoxicology 20:358-364
27. Gilmour CC, Henry EA, Mitchell R (1992) Sulfate stimulation and mercury methylation in freshwater sediments. Environ Sci Technol 26:2281-2287
28. Griegal DR (2002) Inputs and outputs of mercury from terrestrial watersheds: a review. Environ Rev 10:1-39
29. Guigueno MF, Elliott KH, Levac J, Wayland M, Elliott JE (2012) Differential exposure of alpine ospreys to mercury: melting glaciers, hydrology or deposition patterns? Environ Int 40:24-32
30. Hall BD, St Louis VL (2004) Methylmercury and total mercury in plant litter decomposing in upland forests and flooded landscapes. Environ Sci Technol 38:5010-5021
31. Hallinger KK, Cornell KL, Brasso RL, Cristol DA (2011) Mercury exposure and survival in free-living tree swallows (Tachycineta bicolor). Ecotoxicology 20:39-46
32. Harmon SM, King JK, Gladden JB, Chandler GT, Newman LA (2005) Mercury body burdens in Gambusia holbrooki and Erimyzon sucetta in a wetland mesocosm amended with sulfate. Chemosphere 59:227-233
33. Hawley DM, Hallinger KK, Cristol DA (2009) Compromised immune competence in free-living tree swallows exposed to mercury. Ecotoxicology 18:499-503
34. Hobson KA, Bairlein F (2003) Isotopic fractionation and turnover in captive Garden Warblers (Sylvia borin): implications for delineating dietary and migratory associations in wild passerines. Can J Zool 81:1630-1635
35. Inger R, Bearhop S (2008) Applications of stable isotope analysis to avian ecology. Ibis 150:447-461
36. Jackson AK, Evers DC, Etterson MA, Condon AM, Folsom SB, Detweiler J, Schmerfeld J, Cristol DA (2011) Mercury exposure affects the reproductive success of a free-living terrestrial songbird, the Carolina Wren (Thryothorus ludovicianus). Auk 128:759-769
37. Jardine TD, Kidd KA, Rasmussen JB (2012) Aquatic and terrestrial organic matter in the diet of stream consumers: implication for mercury bioaccumulation. Ecol Appl 22:843-855
38. Keeler GJ, Landis MS, Norris GS, Christianson EM, Dvonch JT (2006) Source of mercury wet deposition in Eastern Ohio, USA. Environ Sci Technol 40:5874-5881
39. Kim KH, Hansom PJ, Barnett MO, Lindberg SE (1997) Biogeochemistry of mercury in the air-soil-plant system. In: Sigel A, Sigel H (eds) Metal ions in biological systems, vol 34., Mercury and its Effects on Environment and BiologyMarcel Dekker, New York, pp 185-212
40. Krabbenhoft DP, Babiarz C (1992) The role of groundwater transport in aquatic mercury cycling. Water Resour Res 28:3119-3128
41. Lane OP, Evers DC (2007) Methylmercury availability in New England estuaries as indicated by Saltmarsh Sharp-tailed Sparrow, 2004-2006. BioDiversity Research Institute. BRI Report 2007-14
42. Lasorsa BK, Gill GA, Horvat M (2012) Analytical methods for measuring mercury in water, sediment and biota. In: Bank MS (ed) Mercury in the environment: pattern and process. University of California Press, Berkeley, pp 24-54
43. Lawson ST (1999) Cloud water chemistry and mercury deposition in a high elevation spruce-fir forest. M.S. Thesis, University of Vermont
44. McLaughlin SB, Wimmer R (1999) Tansley Review No. 104 calcium physiology and terrestrial ecosystem processes. Ann Bot 83:373-417
45. Miller EK, VanArsdale A, Keeler JG, Chalmers A, Poissant L, Kamman N, Brulotte R (2005) Estimation and mapping of wet and dry mercury deposition across northeastern North America. Ecotoxicology 14:5-70
46. Morrissey CA, Bendell-Young LI, Elliott JE (2004) Linking contaminant profiles to the diet and breeding location of American dippers using stable isotopes. J Appl Ecol 41:502-512
47. Morrissey CA, Bendell-Young LI, Elliott JE (2005) Assessing trace-metal exposure to American dippers in mountain streams of southwestern British Columbia, Canada. Environ Toxicol Chem 24:836-845
48. Morrissey CA, Elliott JE, Ormerod SJ (2010) Diet shifts during egg laying: implications for measuring contaminants in bird eggs. Environ Poll 158:447-454
49. National Atmospheric Deposition Program (2007) NADP Program Office (NRSP-3), Illinois State Water Survey, 2204 Griffith Dr., Champaign, IL 61820. http://nadp.sws.uiuc.edu/MDN/maps.aspx. Accessed 15 Oct 2013
50. National Park Service Air Resources Division (2002) Air quality in the national parks, 2nd edn. Department of the Interior, Lakewood
51. Nodvin SC, Miegroet H, Lindberg SE, Nicholas NS, Johnson DW (1995) Acidic deposition, ecosystem processes, and nitrogen saturation in a high elevation Southern Appalachian watershed. Water Air Soil Pollut 85:1647-1652
52. Osborne CE, Evers DE, Duron M, Schoch N, Yates D, Buck D, Lane OP, Franklin J (2011) Mercury contamination within terrestrial ecosystems in New England and Mid-Atlantic states: profiles of soil, invertebrates, songbirds, and bats. BioDiversity Research Institute. BRI report 2011-09
53. Paritte JM, Kelly JF (2009) Effect of cleaning regime on stable-isotope ratios of feathers in Japanese quail (Coturnix japonica). Auk 126:165-174
54. Parker AJ (1982) The topographic relative moisture index: an approach to soil-moisture assessment in mountain terrain. Phys Geogr 3:160-168
55. Pearson SF, Levey DJ, Greenberg CH, Martínez del Rio C (2003) Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135:516-523
56. Poole A (eds) (2005) The birds of North America online; Cornell Laboratory of Ornithology, Ithaca, NY, http://bna.bords.cornell.edu/BNA/. Accessed 15 Oct 2013
57. Post DM (2002) Using stable isotope methods to estimate trophic position: models, methods, and assumptions. Ecology 83:703-718
58. Post DM, Pace ML, Hairston NG Jr (2000) Ecosystem size determines food-chain length in lakes. Nature 405:1047-1049
59. Pyle P (1997) Identification guide to North American birds, Part 1. Slate Creek Press, Bolinas
60. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 15 Oct 2013
61. Rimmer CC, McFarland KP, Evers DC, Miller EK, Aubry Y, Busby D, Taylor RJ (2005) Mercury concentrations in Bicknell's Thrush and other insectivorous passerines in montane forests of Northeastern North America. Ecotoxicology 14:223-240
62. Rimmer CC, Miller EK, McFarland KP, Taylor RJ, Faccio SD (2010) Mercury bioaccumulation and trophic transfer in the terrestrial food web of a montane forest. Ecotoxicology 19:697-709
63. Robinson SA, Lajeunesse MJ, Forbes MR (2012) Sex difference in mercury contamination of birds: testing multiple hypotheses with meta-analysis. Environ Sci Technol 46:7094-7101
64. Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2009) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36:12-19
65. Scheuhammer AM, Basu N, Evers DC, Heinz GH, Sandheinrich MB (2012) Ecotoxicology of mercury in fish and wildlife: recent advances. In: Bank MS (ed) Mercury in the Environment: Pattern and Process. University of California Press, Berkeley, pp 223-238
66. Seewagen CL (2010) Threats of environmental mercury to birds: knowledge gaps and priorities for future research. Bird Conserv 20:112-123
67. Seewagen CL (2013) Blood mercury levels and the stopover refueling performance of a long-distance migratory songbird. Can J Zool 91:41-45
68. Shortle WC, Smith KT (1988) Aluminum-induced calcium deficiency syndrome in declining red spruce. Science 240:1017-1018
69. Shriver WG, Evers DC, Hodgman TP, Macculloch BJ, Taylor RJ (2006) Mercury in sharp-tailed Sparrows breeding in coastal wetlands. Environ Bioindic 1:129-135
70. Townsend JM, Rimmer CC, Driscoll CT, McFarland KP, Iñigo-Elias (2013) Mercury concentrations in tropical resident and migrant songbirds on Hispaniola. Ecotoxicology 22:86-93
71. Valente RJ, Shea C, Humes KL, Tanner RL (2007) Atmospheric mercury in the Great Smoky Mountains compared to regional and global levels. Atmos Environ 41:1861-1873
72. Vander Zanden MJ, Rasmussen JB (1996) A trophic position model of pelagic food webs: impact on contaminant bioaccumulation in lake trout. Ecol Monogr 66:451-477
73. 15N and the trophic position of aquatic consumers. Ecology 80:1395-1404
74. Vitz AC, Rodewald AD (2012) Using stable isotopes to investigate the dietary trophic level of fledgling songbirds. J Field Ornithol 83:73-84
75. 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 43:6031-6038
76. Warner SE, Shriver WG, Olsen BJ, Greenberg RG, Taylor RJ (2012) Mercury in wing and tail feathers of hatch-year and adult tidal marsh sparrows. Arch Environ Contam Toxicol 63:586-593
77. Weathers KC, Lovett GM, Likens GE (1995) Cloud deposition to a spruce forest edge. Atmos Environ 29:665-672
78. Weathers KC, Lovett GM, Likens GE, Lathrop R (2000) The effect of landscape features on deposition to Hunter Mountain, Catskill Mountains, New York. Ecol Appl 10:528-540
79. Weathers KC, Simkin SM, Lovett GM, Lindberg SE (2006) Empirical modeling of atmospheric deposition in mountainous landscapes. Ecol Appl 16:1590-1607
80. White RD, Patterson KD, Weaklery A, Ulrey CJ, Drake J (2003) Vegetation classification of Great Smoky Mountains National Park. Report submitted to BRD-NPS Vegetation Mapping Program, Nature Serve, Durham, NC
81. Xun L, Campbell NER, Rudd JWM (1987) Measurement of specific rates of net methylmercury production in the water column and surface sediments of acidified and circumneutral lakes. Can J Fish Aquat Sci 44:750-757
82. Yates DE, Mayack DT, Munney K, Evers DC, Major M, Kaur T, Taylor RJ (2005) Mercury levels in mink (Mustela vison) and river otter (Lontra Canadensis) from northeastern North America. Ecotoxicology 14:263-274
83. Zuur AF, Ieno EN, Meesters EHWG (2009) A beginner's guide to R. Springer, New York
84. Zuur AF, Ieno EN, Walker NF, Saveliev AA, Smith GM (2013) Mixed effects models with extensions in ecology with R. Springer, NY