Impacts of Sublethal Mercury Exposure on Birds: A Detailed Review

  • Margaret C. Whitney
  • Daniel A. CristolEmail author
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 244)


Mercury is a ubiquitous environmental contaminant known to accumulate in, and negatively affect, fish-eating and oceanic bird species, and recently demonstrated to impact some terrestrial songbirds to a comparable extent. It can bioaccumulate to concentrations of >1 μg/g in tissues of prey organisms such as fish and insects. At high enough concentrations, exposure to mercury is lethal to birds. However, environmental exposures are usually far below the lethal concentrations established by dosing studies.

The objective of this review is to better understand the effects of sublethal exposure to mercury in birds. We restricted our survey of the literature to studies with at least some exposures >5 μg/g. The majority of sublethal effects were subtle and some studies of similar endpoints reached different conclusions. Strong support exists in the literature for the conclusion that mercury exposure reduces reproductive output, compromises immune function, and causes avoidance of high-energy behaviors. For some endpoints, notably certain measures of reproductive success, endocrine and neurological function, and body condition, there is weak or contradictory evidence of adverse effects and further study is required. There was no evidence that environmentally relevant mercury exposure affects longevity, but several of the sublethal effects identified likely do result in fitness reductions that could adversely impact populations. Overall, 72% of field studies and 91% of laboratory studies found evidence of deleterious effects of mercury on some endpoint, and thus we can conclude that mercury is harmful to birds, and the many effects on reproduction indicate that bird population declines may already be resulting from environmental mercury pollution.


Avian Bald eagle Behavior Bird Common loon Dosing Ecotoxicology Effects Endocrine function Forster’s tern Hormones Immune function Longevity Mallard Metals Methylmercury Mercury Neurological function Reproduction Review Sublethal Survivorship Tree swallow White ibis Zebra finch 



This work was supported by National Science Foundation (IOS-1257590) as well as the American Ornithologists’ Union, Virginia Academy of Science, Williamsburg Bird Club, and College of William and Mary Graduate School. An early draft of this manuscript was sent to many active researchers in the field for their feedback, and we thank J. Ackerman, R. Brasso, B. Braune, A. Condon, T. and C. Custer, C. Henny, G. Heinz, A. Jackson, K. Kenow, J. Rutkiewicz, and C. Seewagen for their constructive comments.


  1. Ackerman JT, Eagles-Smith CA, Takekawa JY, Iverson SA (2008a) Survival of postfledging Forster’s terns in relation to mercury exposure in San Francisco Bay. Ecotoxicology 17:789–801. doi: 10.1007/s10646-008-0237-6CrossRefGoogle Scholar
  2. Ackerman JT, Takekawa JY, Eagles-Smith CA, Iverson SA (2008b) Mercury contamination and effects on survival of American avocet and black-necked stilt chicks in San Francisco Bay. Ecotoxicology 17:103–116. doi: 10.1007/s10646-007-0164-yCrossRefGoogle Scholar
  3. Ackerman JT, Overton CT, Casazza ML, Takekawa JY, Eagles-Smith CA, Keister RA, Herzog MP (2012) Does mercury contamination reduce body condition of endangered California clapper rails? Environ Pollut 162:439–448. doi: 10.1016/j.envpol.2011.12.004CrossRefGoogle Scholar
  4. Adams EM, Frederick PC (2008) Effects of methylmercury and spatial complexity on foraging behavior and foraging efficiency in juvenile white ibises (Eudocimus albus). Environ Toxicol Chem 27:1708–1712CrossRefGoogle Scholar
  5. Adams EM, Frederick PC, Larkin ILV, Guillette LJ Jr (2009) Sublethal effects of methylmercury on fecal metabolites of testosterone, estradiol, and corticosterone in captive juvenile white ibises (Eudocimus albus). Environ Toxicol Chem 28:982–989. doi: 10.1897/08-253.1CrossRefGoogle Scholar
  6. Albers PH, Koterba MT, Rossmann R, Link WA, French JB, Bennett RS, Bauer WC (2007) Effects of methylmercury on reproduction in American kestrels. Environ Toxicol Chem 26:1856–1866. doi: 10.1897/06-592R.1CrossRefGoogle Scholar
  7. Anteau MJ, Afton AD, Custer CM, Custer TW (2007) Relationships of cadmium, mercury, and selenium with nutrient reserves of female lesser scaup (Aythya affinis) during winter and spring migration. Environ Toxicol Chem 26:515–520CrossRefGoogle Scholar
  8. Anthony RG, Miles AK, Estes JA, Isaacs FB (1999) Productivity, diets, and environmental contaminants in nesting bald eagles from the Aleutian archipelago. Environ Toxicol Chem 18:2054–2062. doi: 10.1002/etc.5620180925CrossRefGoogle Scholar
  9. Barr JF, Canadian Wildlife Service (1986) Population dynamics of the common loon (Gavia immer) associated with mercury-contaminated waters in Northwestern Ontario. Environment Canada, Canadian Wildlife Service, Hull, QCGoogle Scholar
  10. Bennett RS, French JBJ, Rossmann R, Haebler R (2009) Dietary toxicity and tissue accumulation of methylmercury in American kestrels. Arch Environ Contam Toxicol 56:149–156. doi: 10.1007/s00244-008-9168-8CrossRefGoogle Scholar
  11. Bouland AJ, White AE, Lonabaugh KP, Varian-Ramos CW, Cristol DA (2012) Female-biased offspring sex ratios in birds at a mercury-contaminated river. J Avian Biol 43:244–251. doi: 10.1111/j.1600-048X.2012.05612.xCrossRefGoogle Scholar
  12. Bouton SN, Frederick PC, Spalding MG, McGill H (1999) Effects of chronic, low concentrations of dietary methylmercury on the behavior of juvenile great egrets. Environ Toxicol Chem 18:1934–1939CrossRefGoogle Scholar
  13. Bowerman WW IV, Evans ED, Giesy JP, Postupalsky S (1994) Using feathers to assess risk of mercury and selenium to bald eagle reproduction in the Great Lakes region. Arch Environ Contam Toxicol 27:294–298. doi: 10.1007/BF00213162CrossRefGoogle Scholar
  14. Brasso RL, Cristol DA (2008) Effects of mercury exposure on the reproductive success of tree swallows (Tachycineta bicolor). Ecotoxicology 17:133–141CrossRefGoogle Scholar
  15. Braune BM, Scheuhammer AM, Crump D, Jones S, Porter E, Bond D (2012) Toxicity of methylmercury injected into eggs of thick-billed murres and arctic terns. Ecotoxicology 21:2143–2152. doi: 10.1007/s10646-012-0967-3CrossRefGoogle Scholar
  16. Burgess NM, Meyer MW (2008) Methylmercury exposure associated with reduced productivity in common loons. Ecotoxicology 17:83–91. doi: 10.1007/s10646-007-0167-8CrossRefGoogle Scholar
  17. Bustamante P, Carravieri A, Goutte A, Barbraud C, Delord K, Chastel O, Weimerskirch H, Cherel Y (2016) High feather mercury concentrations in the wandering albatross are related to sex, breeding status and trophic ecology with no demographic consequences. Environ Res 144:1–10. doi: 10.1016/j.envres.2015.10.024CrossRefGoogle Scholar
  18. Carlson JR, Cristol D, Swaddle JP (2014) Dietary mercury exposure causes decreased escape takeoff flight performance and increased molt rate in European starlings (Sturnus vulgaris). Ecotoxicology 23:1464–1473. doi: 10.1007/s10646-014-1288-5CrossRefGoogle Scholar
  19. Caudill MT, Spear EL, Varian-Ramos CW, Cristol DA (2015) PHA-stimulated immune-responsiveness in mercury-dosed zebra finches does not match results from environmentally exposed songbirds. Bull Environ Contam Toxicol 94:407–411. doi: 10.1007/s00128-015-1472-1CrossRefGoogle Scholar
  20. Champoux L, Boily M, Fitzgerald G (2017) Thyroid hormones, retinol and clinical parameters in relation to mercury and organohalogen contaminants in great blue heron (Ardea herodias) nestlings from the St. Lawrence River, Québec, Canada. Arch Environ Contam Toxicol 72:200–214. doi: 10.1007/s00244-017-0364-2CrossRefGoogle Scholar
  21. Clarkson CE, Erwin RM, Riscassi A (2012) The use of novel biomarkers to determine dietary mercury accumulation in nestling waterbirds. Environ Toxicol Chem 31:1143–1148. doi: 10.1002/etc.1767CrossRefGoogle Scholar
  22. Costa RA, Eeva T, Eira C, Vaqueiro J, Medina P, Vingada JV (2014) Great tits breeding performance and mercury contamination from the paper and pulp industry in the west coast of Portugal. Chem Ecol 30:206–215. doi: 10.1080/02757540.2013.856891CrossRefGoogle Scholar
  23. Costantini D, Meillère A, Carravieri A, Lecomte V, Sorci G, Faivre B, Weimerskirch H, Bustamante P, Labadie P, Budzinski H, Chastel O (2014) Oxidative stress in relation to reproduction, contaminants, gender and age in a long-lived seabird. Oecologia 175:1107–1116. doi: 10.1007/s00442-014-2975-xCrossRefGoogle Scholar
  24. 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 320:335CrossRefGoogle Scholar
  25. Custer TW, Hines RK, Melancon MJ, Hoffman DJ, Wickliffe JK, Bickham JW, Martin JW, Henshel DS (1997) Contaminant concentrations and biomarker response in great blue heron eggs from 10 colonies on the upper Mississippi River, USA. Environ Toxicol Chem 16:260–271. doi: 10.1002/etc.5620160223CrossRefGoogle Scholar
  26. Custer TW, Custer CM, Hines RK, Sparks DW, Melancon MJ, Hoffman DJ, Bickham JW, Wickliffe JK (2000) Mixed-function oxygenases, oxidative stress, and chromosomal damage measured in lesser scaup wintering on the Indiana Harbor Canal. Arch Environ Contam Toxicol 38:522–529CrossRefGoogle Scholar
  27. Custer CM, Custer TW, Warburton D, Hoffman DJ, Bickham JW, Matson CW (2006) Trace element concentrations and bioindicator responses in tree swallows from northwestern Minnesota. Environ Monit Assess 118:247–266. doi: 10.1007/s10661-006-1499-1CrossRefGoogle Scholar
  28. Custer CM, Custer TW, Hill EF (2007) Mercury exposure and effects on cavity-nesting birds from the Carson River, Nevada. Arch Environ Contam Toxicol 52:129–136. doi: 10.1007/s00244-006-0103-6CrossRefGoogle Scholar
  29. Custer TW, Custer CA, Johnson KM, Hoffman DJ (2008) Mercury and other element exposure to tree swallows (Tachycineta bicolor) nesting on Lostwood National Wildlife Refuge, North Dakota. Environ Pollut 155:217–226. doi: 10.1016/j.envpol.2007.12.003CrossRefGoogle Scholar
  30. Custer TW, Custer CM, Thogmartin WE, Dummer PM, Rossmann R, Kenow KP, Meyer MW (2012) Mercury and other element exposure in tree swallows nesting at low pH and neutral pH lakes in northern Wisconsin USA. Environ Pollut 163:68–76. doi: 10.1016/j.envpol.2011.12.017CrossRefGoogle Scholar
  31. Elbert RA, Anderson DW (1998) Mercury levels, reproduction, and hematology in western grebes from three California Lakes, USA. Environ Toxicol Chem 17:210–213. doi: 10.1002/etc.5620170212CrossRefGoogle Scholar
  32. Evans HL, Garman RH, Laties VG (1982) Neurotoxicity of methylmercury in the pigeon. Neurotoxicology 3:21–36Google Scholar
  33. Evers DC, Taylor KM, Major A, Taylor RJ, Poppenga RH, Scheuhammer AM (2003) Common loon eggs as indicators of methylmercury availability in North America. Ecotoxicology 12:69–81. doi: 10.1023/A:1022593030009CrossRefGoogle Scholar
  34. Evers DC, Savoy LJ, DeSorbo CR et al (2008) Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17:69–81. doi: 10.1007/s10646-007-0168-7CrossRefGoogle Scholar
  35. Fallacara DM, Halbrook RS, French JB (2011a) Toxic effects of dietary methylmercury on immune function and hematology in American kestrels (Falco sparverius). Environ Toxicol Chem 30:1320–1327. doi: 10.1002/etc.494CrossRefGoogle Scholar
  36. Fallacara DM, Halbrook RS, French JB (2011b) Toxic effects of dietary methylmercury on immune system development in nestling American kestrels (Falco sparverius). Environ Toxicol Chem 30:1328–1337. doi: 10.1002/etc.519CrossRefGoogle Scholar
  37. Fimreite N, Karstad L (1971) Effects of dietary methyl mercury on red-tailed hawks. J Wildl Manage 35:293–300CrossRefGoogle Scholar
  38. Finkelstein ME, Grasman KA, Croll DA, Tershy BR, Keitt BS, Jarman WM, Smith DR (2007) Contaminant-associated alteration of immune function in black-footed albatross (Phoebastria nigripes), a North Pacific predator. Environ Sci Technol 26:1896–1903. doi: 10.1897/06-505R.1CrossRefGoogle Scholar
  39. Finley MT, Stendell RC (1978) Survival and reproductive success of black ducks fed methyl mercury. Environ Pollut 16:51–64. doi: 10.1016/0013-9327(78)90137-4CrossRefGoogle Scholar
  40. Fort J, Lacoue-Labarthe T, Nguyen HL, Boue A, Spitz J, Bustamante P (2015) Mercury in wintering seabirds, an aggravating factor to winter wrecks? Sci Total Environ 527:448–454. doi: 10.1016/j.scitotenv.2015.05.018CrossRefGoogle Scholar
  41. Franceschini MD, Lane OP, Evers DC, Reed JM, Hoskins B, Romero LM (2009) The corticosterone stress response and mercury contamination in free-living tree swallows, Tachycineta bicolor. Ecotoxicology 18:514–521. doi: 10.1007/s10646-009-0309-2CrossRefGoogle Scholar
  42. Franceschini MD, Evers DC, Kenow KP, Meyer MW, Pokras M, Romero LM (2017) Mercury correlates with altered corticosterone but not testosterone or estradiol concentrations in common loons. Ecotoxicol Environ Saf 142:348–354. doi: 10.1016/j.ecoenv.2017.04.030CrossRefGoogle Scholar
  43. Frederick P, Jayasena N (2010) Altered pairing behaviour and reproductive success in white ibises exposed to environmentally relevant concentrations of methylmercury. Proc Roy Soc B. doi:  10.1098/rspb.2010.2189CrossRefGoogle Scholar
  44. Frederick P, Campbell A, Jayasena N, Borkhataria R (2011) Survival of white ibises (Eudocimus albus) in response to chronic experimental methylmercury exposure. Ecotoxicology 20:358–364CrossRefGoogle Scholar
  45. Gerrard PM, St. Louis VL (2001) The effects of experimental reservoir creation on the bioaccumulation of methylmercury and reproductive success of tree swallows (Tachycineta bicolor). Environ Sci Technol 35:1329–1338. doi: 10.1021/es001537fCrossRefGoogle Scholar
  46. Gibson LA, Lavoie RA, Bissegger S, Campbell LM, Langlois VS (2014) A positive correlation between mercury and oxidative stress-related gene expression (GPX3 and GSTM3) is measured in female double-crested cormorant blood. Ecotoxicology 23:1004–1014. doi: 10.1007/s10646-014-1243-5CrossRefGoogle Scholar
  47. Gillet A-MTY, Seewagen CL (2014) Mercury exposure of a wetland songbird, Agelaius phoeniceus, in the New York metropolitan area and its effect on nestling growth rate. Environ Monit Assess 186:4029–4036. doi: 10.1007/s10661-014-3677-xCrossRefGoogle Scholar
  48. Goutte A, Barbraud C, Meillère A, Carravieri A, Bustamante P, Labadie P, Budzinski H, Delord K, Cherel Y, Weimerskirch H, Chastel O (2014a) Demographic consequences of heavy metals and persistent organic pollutants in a vulnerable long-lived bird, the wandering albatross. Proc R Soc B 281:20133313. doi: 10.1098/rspb.2013.3313CrossRefGoogle Scholar
  49. Goutte A, Bustamante P, Barbraud C, Delord K, Weimerskirch H, Chastel O (2014b) Demographic responses to mercury exposure in two closely related Antarctic top predators. Ecology 95:1075–1086. doi: 10.1890/13-1229.1CrossRefGoogle Scholar
  50. Hallinger KK, Cristol DA (2011) The role of weather in mediating the effect of mercury exposure on reproductive success in tree swallows. Ecotoxicology 20:1368–1377. doi: 10.1007/s10646-011-0694-1CrossRefGoogle Scholar
  51. Hallinger KK, Zabransky DJ, Kazmer KA, Cristol DA (2010) Birdsong differs between mercury-polluted and reference sites. Auk 127:156–161. doi: 10.1525/auk.2009.09058CrossRefGoogle Scholar
  52. Hallinger KK, Cornell KL, Brasso RL, Cristol DA (2011) Mercury exposure and survival in free-living tree swallows (Tachycineta bicolor). Ecotoxicology 20:39–46. doi: 10.1007/s10646-010-0554-4CrossRefGoogle Scholar
  53. Hamilton M, Scheuhammer A, Basu N (2011) Mercury, selenium and neurochemical biomarkers in different brain regions of migrating common loons from Lake Erie, Canada. Ecotoxicology 20:1677–1683. doi: 10.1007/s10646-011-0754-6CrossRefGoogle Scholar
  54. Hargreaves AL, Whiteside DP, Gilchrist G (2010) Concentrations of 17 elements, including mercury, and their relationship to fitness measures in arctic shorebirds and their eggs. Sci Total Environ 408:3153–3161. doi: 10.1016/j.scitotenv.2010.03.027CrossRefGoogle Scholar
  55. Hawley DM, Hallinger KK, Cristol DA (2009) Compromised immune competence in free-living tree swallows exposed to mercury. Ecotoxicology 18:499–503CrossRefGoogle Scholar
  56. Heath JA, Frederick PC (2005) Relationships among mercury concentrations, hormones, and nesting effort of white ibises (Eudocimus albus) in the Florida Everglades. Auk 255–267. doi:  10.1642/0004-8038(2005)122[0255:RAMCHA]2.0.CO;2CrossRefGoogle Scholar
  57. Heinz G (1974) Effects of low dietary levels of methyl mercury on mallard reproduction. Bull Environ Contam Toxicol 11:386–392. doi: 10.1007/BF01684947CrossRefGoogle Scholar
  58. Heinz G (1975) Effects of methylmercury on approach and avoidance-behavior of mallard ducklings. Bull Environ Contam Toxicol 13:554–564CrossRefGoogle Scholar
  59. Heinz GH (1976a) Methylmercury: second-year feeding effects on mallard reproduction and duckling behavior. J Wildl Manag 40:82–90. doi: 10.2307/3800158CrossRefGoogle Scholar
  60. Heinz GH (1976b) Methylmercury: second-generation reproductive and behavioral effects on mallard ducks. J Wildl Manag 40:710–715. doi: 10.2307/3800567CrossRefGoogle Scholar
  61. Heinz GH (1979) Methylmercury: reproductive and behavioral effects on three generations of mallard ducks. J Wildl Manag 43:394–401. doi: 10.2307/3800348CrossRefGoogle Scholar
  62. Heinz G (1980) Eggshell thickness in mallards fed methylmercury. Bull Environ Contam Toxicol 25:498–502CrossRefGoogle Scholar
  63. Heinz GH, Locke LN (1976) Brain lesions in mallard ducklings from parents fed methylmercury. Avian Dis 20:9–17CrossRefGoogle Scholar
  64. Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR, Kondrad SL, Erwin CA (2009) Species differences in the sensitivity of avian embryos to methylmercury. Arch Environ Contam Toxicol 56:129–138. doi: 10.1007/s00244-008-9160-3CrossRefGoogle Scholar
  65. Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR (2010a) Enhanced reproduction in mallards fed a low level of methylmercury: an apparent case of hormesis. Environ Toxicol Chem 29:650–653. doi: 10.1002/etc.64CrossRefGoogle Scholar
  66. Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR (2010b) Reproduction in mallards exposed to dietary concentrations of methylmercury. Ecotoxicology 19:977–982. doi: 10.1007/s10646-010-0479-yCrossRefGoogle Scholar
  67. Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR, Kondrad SL, Erwin CA (2011) Teratogenic effects of injected methylmercury on avian embryos. Environ Toxicol Chem 30:1593–1598. doi: 10.1002/etc.530CrossRefGoogle Scholar
  68. Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR, Kondrad SL, Erwin CA (2012a) Hormesis associated with a low dose of methylmercury injected into mallard eggs. Arch Environ Contam Toxicol 62:141–144. doi: 10.1007/s00244-011-9680-0CrossRefGoogle Scholar
  69. Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR (2012b) A comparison of the teratogenicity of methylmercury and selenomethionine injected into bird eggs. Arch Environ Contam Toxicol 62:519–528. doi: 10.1007/s00244-011-9717-4CrossRefGoogle Scholar
  70. Helander B, Olsson M, Reutergårdh L (1982) Residue levels of organochlorine and mercury compounds in unhatched eggs and the relationships to breeding success in white-tailed sea eagles Haliaeetus albicilla in Sweden. Ecography 5:349–366. doi: 10.1111/j.1600-0587.1982.tb01049.xCrossRefGoogle Scholar
  71. Henny CJ, Hill EF, Hoffman DJ, Spalding MG, Grove RA (2002) Nineteenth century mercury: hazard to wading birds and cormorants of the Carson River, Nevada. Ecotoxicology 11:213–231CrossRefGoogle Scholar
  72. Henny CJ, Kaiser JL, Packard HA, Grove RA, Taft MR (2005) Assessing mercury exposure and effects to American dippers in headwater streams near mining sites. Ecotoxicology 14:709–725. doi: 10.1007/s10646-005-0023-7CrossRefGoogle Scholar
  73. Henny CJ, Hill EF, Grove RA, Chelgren ND, Haggerty PK (2017) Mercury and drought along the lower Carson River, Nevada: IV. Snowy egret post-fledging dispersal, timing of migration and survival, 2002-2004. Ecotoxicol Environ Saf 135:358–367. doi: 10.1016/j.ecoenv.2016.10.002CrossRefGoogle Scholar
  74. Henry KA, Cristol DA, Varian-Ramos CW, Bradley EL (2014) Oxidative stress in songbirds exposed to dietary methylmercury. Ecotoxicology 1–7. doi:  10.1007/s10646-014-1400-xCrossRefGoogle Scholar
  75. Herring G, Gawlik DE, Rumbold DG (2009) Feather mercury concentrations and physiological condition of great egret and white ibis nestlings in the Florida Everglades. Sci Total Environ 407:2641–2649. doi: 10.1016/j.scitotenv.2008.12.043CrossRefGoogle Scholar
  76. Herring G, Ackerman JT, Eagles-Smith CA (2010) Embryo malposition as a potential mechanism for mercury-induced hatching failure in bird eggs. Environ Toxicol Chem 29:1788–1794. doi: 10.1002/etc.208CrossRefGoogle Scholar
  77. Herring G, Ackerman JT, Herzog MP (2012) Mercury exposure may suppress baseline corticosterone levels in juvenile birds. Environ Sci Technol 46:6339–6346. doi: 10.1021/es300668cCrossRefGoogle Scholar
  78. Herring G, Eagles-Smith CA, Gawlik DE, Beerens JM, Ackerman JT (2014) Physiological condition of juvenile wading birds in relation to multiple landscape stressors in the Florida Everglades: effects of hydrology, prey availability, and mercury bioaccumulation. PLoS One 9:e106447. doi: 10.1371/journal.pone.0106447CrossRefGoogle Scholar
  79. Herring G, Eagles-Smith CA, Ackerman JT (2017) Mercury exposure may influence fluctuating asymmetry in waterbirds. Environ Toxicol Chem 36:1599–1605. doi: 10.1002/etc.3688CrossRefGoogle Scholar
  80. Hill EF, Soares JH (1984) Subchronic mercury exposure in coturnix and a method of hazard evaluation. Environ Toxicol Chem 3:489–502. doi: 10.1002/etc.5620030311CrossRefGoogle Scholar
  81. Hill EF, Henny CJ, Grove RA (2008) Mercury and drought along the lower Carson River, Nevada: II. Snowy egret and black-crowned night-heron reproduction on Lahontan Reservoir, 1997-2006. Ecotoxicology 17:117–131. doi: 10.1007/s10646-007-0180-yCrossRefGoogle Scholar
  82. Hoffman D, Moore J (1979) Teratogenic effects of external egg applications of methyl mercury in the mallard, Anas platyrhynchos. Teratology 20:453–461. doi: 10.1002/tera.1420200315CrossRefGoogle Scholar
  83. Hoffman DJ, Ohlendorf HM, Marn CM, Pendleton GWP (1998) Association of mercury and selenium with altered glutathione metabolism and oxidative stress in diving ducks from the San Francisco Bay region, USA. Environ Toxicol Chem 17:167–172. doi: 10.1002/etc.5620170205CrossRefGoogle Scholar
  84. Hoffman DJ, Spalding MG, Frederick PC (2005) Subchronic effects of methylmercury on plasma and organ biochemistries in great egret nestlings. Environ Toxicol Chem 24:3078–3084CrossRefGoogle Scholar
  85. Hoffman DJ, Henny CJ, Hill EF, Grove RA, Kaiser JL, Stebbins KR (2009) Mercury and drought along the lower Carson River, Nevada: III. Effects on blood and organ biochemistry and histopathology of snowy egrets and black-crowned night-herons on Lahontan reservoir, 2002-2006. J Toxicol Environ Health Part A 72:1223–1241. doi: 10.1080/15287390903129218CrossRefGoogle Scholar
  86. Hoffman DJ, Eagles-Smith CA, Ackerman JT, Adelsbach TL, Stebbins KR (2011) Oxidative stress response of Forster’s terns (Sterna forsteri) and Caspian terns (Hydroprogne caspia) to mercury and selenium bioaccumulation in liver, kidney, and brain. Environ Toxicol Chem 30:920–929. doi: 10.1002/etc.459CrossRefGoogle Scholar
  87. 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. doi: 10.1525/auk.2011.11106CrossRefGoogle Scholar
  88. Jayasena N, Frederick PC, Larkin ILV (2011) Endocrine disruption in white ibises (Eudocimus albus) caused by exposure to environmentally relevant levels of methylmercury. Aquat Toxicol 105:321–327CrossRefGoogle Scholar
  89. Jenko K, Karouna-Renier NK, Hoffman DJ (2012) Gene expression, glutathione status, and indicators of hepatic oxidative stress in laughing gull (Larus atricilla) hatchlings exposed to methylmercury. Environ Toxicol Chem 31:2588–2596. doi: 10.1002/etc.1985CrossRefGoogle Scholar
  90. Ji X, Hu W, Cheng J, Yuan T, Xu F, Qu L, Wang W (2006) Oxidative stress on domestic ducks (Shaoxing duck) chronically exposed in a mercury-selenium coexisting mining area in China. Ecotoxicol Environ Saf 64:171–177. doi: 10.1016/j.ecoenv.2005.03.009CrossRefGoogle Scholar
  91. Kalisińska E, Budis H, Podlasińska J, Łanocha N, Kavetska KM (2010) Body condition and mercury concentration in apparently healthy goosander (Mergus merganser) wintering in the Odra estuary, Poland. Ecotoxicology 19:1382–1399. doi: 10.1007/s10646-010-0524-xCrossRefGoogle Scholar
  92. Kenow KP, Gutreuter S, Hines RK, Meyer MW, Fournier F, Karasov WH (2003) Effects of methyl mercury exposure on the growth of juvenile common loons. Ecotoxicology 12:171–181. doi: 10.1023/A:1022598525891CrossRefGoogle Scholar
  93. Kenow KP, Grasman KA, Hines RK, Meyer MW, Gendron-Fitzpatrick A, Spalding MG, Gray BR (2007) Effects of methylmercury exposure on the immune function of juvenile common loons (Gavia immer). Environ Toxicol Chem 26:1460–1469CrossRefGoogle Scholar
  94. Kenow KP, Hoffman DJ, Hines RK, Meyer MW, Bickham JW, Matson CW, Stebbins KR, Montagna P, Elfessi A (2008) Effects of methylmercury exposure on glutathione metabolism, oxidative stress, and chromosomal damage in captive-reared common loon (Gavia immer) chicks. Environ Pollut 156:732–738. doi: 10.1016/j.envpol.2008.06.009CrossRefGoogle Scholar
  95. Kenow KP, Hines RK, Meyer MW, Suarez SA, Gray BR (2010) Effects of methylmercury exposure on the behavior of captive-reared common loon (Gavia immer) chicks. Ecotoxicology 19:933–944. doi: 10.1007/s10646-010-0475-2CrossRefGoogle Scholar
  96. Kenow KP, Meyer MW, Rossmann R, Gendron-Fitzpatrick A, Gray BR (2011) Effects of injected methylmercury on the hatching of common loon (Gavia immer) eggs. Ecotoxicology 20:1684–1693. doi: 10.1007/s10646-011-0743-9CrossRefGoogle Scholar
  97. King K, Custer T, Quinn J (1991) Effects of mercury, selenium, and organochlorine contaminants on reproduction of Forster terns and black skimmers nesting in a contaminated Texas bay. Arch Environ Contam Toxicol 20:32–40CrossRefGoogle Scholar
  98. Klimstra JD, Yee JL, Heinz GH, Hoffman DJ, Stebbins KR (2012) Interactions between methylmercury and selenomethionine injected into mallard eggs. Environ Toxicol Chem 31:579–584. doi: 10.1002/etc.1708CrossRefGoogle Scholar
  99. Kobiela ME, Cristol DA, Swaddle JP (2015) Risk-taking behaviours in zebra finches affected by mercury exposure. Anim Behav 103:153–160. doi: 10.1016/j.anbehav.2015.02.024CrossRefGoogle Scholar
  100. Laties VG, Evans HL (1980) Methylmercury-induced changes in operant discrimination by the pigeon. J Pharmacol Exp Ther 214:620–628Google Scholar
  101. Lewis CA, Cristol DA, Swaddle JP, Varian-Ramos CW, Zwollo P (2013) Decreased immune response in zebra finches exposed to sublethal doses of mercury. Arch Environ Contam Toxicol 64:327–336. doi: 10.1007/s00244-012-9830-zCrossRefGoogle Scholar
  102. Loerzel SM, Samuelson DA, Szabo N (1999) Ocular effects of methylmercury in juvenile double-crested cormorants (Phalacrocorax auritus). Invest Ophthalmol Vis Sci 40:S445Google Scholar
  103. Longcore JR, Dineli R, Haines TA (2007) Mercury and growth of tree swallows at Acadia National Park, and at Orono, Maine, USA. Environ Monit Assess 126:117–127. doi: 10.1007/s10661-006-9325-3CrossRefGoogle Scholar
  104. Lundholm C (1995) Effects of methyl mercury at different dose regimes on eggshell formation and some biochemical characteristics of the eggshell gland mucosa of the domestic fowl. Comp Biochem Physiol C-Pharmacol Toxicol Endocrinol 110:23–28. doi: 10.1016/0742-8413(94)00081-KCrossRefGoogle Scholar
  105. Maddux SL, Cristol DA, Varian-Ramos CW, Bradley EL (2014) The effect of mercury on baseline corticosterone in a breeding songbird. Bull Environ Contam Toxicol. doi:  10.1007/s00128-014-1440-1CrossRefGoogle Scholar
  106. McCullagh EA, Cristol DC, Phillips JB (2015) Plumage color and reproductive output of eastern bluebirds (Sialia sialis) nesting near a mercury-contaminated river. J Environ Sci Health A 50:1020–1028. doi: 10.1080/10934529.2015.1038168CrossRefGoogle Scholar
  107. McKay JL, Maher CR (2012) Relationship between blood mercury levels and components of male song in Nelson’s sparrows (Ammodramus nelsoni). Ecotoxicology 21:2391–2397. doi: 10.1007/s10646-012-0994-0CrossRefGoogle Scholar
  108. Merrill EH, Hartigan JJ, Meyer MW (2005) Does prey biomass or mercury exposure affect loon chick survival in Wisconsin? J Wildl Manag 69:57–67. doi: 10.2193/0022-541X(2005)069<0057:DPBOME>2.0.CO;2CrossRefGoogle Scholar
  109. Meyer MW, Evers DC, Hartigan JJ, Rasmussen PS (1998) Patterns of common loon (Gavia immer) mercury exposure, reproduction, and survival in Wisconsin, USA. Environ Toxicol Chem 17:184–190. doi: 10.1897/1551-5028(1998)017<0184:POCLGI>2.3.CO;2CrossRefGoogle Scholar
  110. Mitro MG, Evers DC, Meyer MW, Piper WH (2008) Common loon survival rates and mercury in New England and Wisconsin. J Wildl Manag 72:665–673. doi: 10.2193/2006-551CrossRefGoogle Scholar
  111. Moore CS, Cristol DA, Maddux SL, Varian-Ramos CW, Bradley EL (2014) Lifelong exposure to methylmercury disrupts stress-induced corticosterone response in zebra finches (Taeniopygia guttata). Environ Toxicol Chem 33:1072–1076. doi: 10.1002/etc.2521CrossRefGoogle Scholar
  112. Nicholson JK, Osborn D (1984) Kidney lesions in juvenile starlings Sturnus vulgaris fed on a mercury-contaminated synthetic diet. Environ Pollut Series A Ecol Biol 33:195–206. doi: 10.1016/0143-1471(84)90010-2CrossRefGoogle Scholar
  113. Nocera JJ, Taylor PD (1998) In situ behavioral response of common loons associated with elevated mercury (Hg) exposure. Ecol Soc 2:10. Scholar
  114. Olivero-Verbel J, Agudelo-Frias D, Caballero-Gallardo K (2013) Morphometric parameters and total mercury in eggs of snowy egret (Egretta thula) from Cartagena Bay and Totumo Marsh, north of Colombia. Mar Pollut Bull 69:105–109. doi: 10.1016/j.marpolbul.2013.01.013CrossRefGoogle Scholar
  115. Olsen B, Evers D, DeSorbo C (2000) Effect of methylated mercury on the diving frequency of the common loon. J Ecol Res 2:67–72Google Scholar
  116. Pass DA, Little PB, Karstad LH (1975) The pathology of subacute and chronic methyl mercury poisoning of the Mallard duck (Anas platyrhynchos). J Comp Pathol 85:7–21. doi: 10.1016/0021-9975(75)90079-1CrossRefGoogle Scholar
  117. Pollentier CD, Kenow KP, Meyer MW (2007) Common loon (Gavia immer) eggshell thickness and egg volume vary with acidity of nest lake in northern Wisconsin. Waterbirds 30:367–374. doi: 10.1675/1524-4695(2007)030[0367:CLGIET]2.0.CO;2CrossRefGoogle Scholar
  118. Pollet IL, Leonard ML, O’Driscoll NJ, Burgess NM, Shutler D (2017) Relationships between blood mercury levels, reproduction, and return rate in a small seabird. Ecotoxicology 26:97–103. doi: 10.1007/s10646-016-1745-4CrossRefGoogle Scholar
  119. Pollock B, Machin KL (2009) Corticosterone in relation to tissue cadmium, mercury and selenium concentrations and social status of male lesser scaup (Aythya affinis). Ecotoxicology 18:5–14. doi: 10.1007/s10646-008-0250-9CrossRefGoogle Scholar
  120. Provencher JF, Forbes MR, Hennin HL, Love OP, Braune BM, Mallory ML, Gilchrist HG (2016) Implications of mercury and lead concentrations on breeding physiology and phenology in an Arctic bird. Environ Pollut 218:1014–1022. doi: 10.1016/j.envpol.2016.08.052CrossRefGoogle Scholar
  121. Provencher JF, Forbes MR, Mallory ML, Wilson S, Gilchrist HG (2017) Anti-parasite treatment, but not mercury burdens, influence nesting propensity dependent on arrival time or body condition in a marine bird. Sci Total Environ 575:849–857. doi: 10.1016/j.scitotenv.2016.09.130CrossRefGoogle Scholar
  122. Rowse LM, Rodewald AD, Sullivan SMP (2014) Pathways and consequences of contaminant flux to Acadian flycatchers (Empidonax virescens) in urbanizing landscapes of Ohio, USA. Sci Total Environ 485:461–467. doi: 10.1016/j.scitotenv.2014.03.095CrossRefGoogle Scholar
  123. Rutkiewicz J, Scheuhammer A, Crump D, Jagla M, Basu N (2010) Investigation of spatial trends and neurochemical impacts of mercury in herring gulls across the Laurentian Great Lakes. Environ Pollut 158:2733–2737. doi: 10.1016/j.envpol.2010.04.018CrossRefGoogle Scholar
  124. Rutkiewicz J, Nam D-H, Cooley T, Neumann K, Padilla IB, Route W, Strom S, Basu N (2011) Mercury exposure and neurochemical impacts in bald eagles across several Great Lakes states. Ecotoxicology 20:1669–1676. doi: 10.1007/s10646-011-0730-1CrossRefGoogle Scholar
  125. Rutkiewicz J, Bradley M, Mittal K, Basu N (2013) Methylmercury egg injections: part 2—pathology, neurochemistry, and behavior in the avian embryo and hatchling. Ecotox Environ Safety 93:77–86. doi: 10.1016/j.ecoenv.2013.04.007CrossRefGoogle Scholar
  126. Scheuhammer A (1988) Chronic dietary toxicity of methylmercury in the zebra finch, Poephila guttata. Bull Environ Contam Toxicol 40:123–130CrossRefGoogle Scholar
  127. 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 17:93–101. doi: 10.1007/s10646-007-0170-0CrossRefGoogle Scholar
  128. Schoch N, Glennon MJ, Evers DC, Duron M, Jackson AK, Driscoll CT, Ozard JW, Sauer AK (2014) The impact of mercury exposure on the common loon (Gavia immer) population in the Adirondack Park, New York, USA. Waterbirds 37:133–146CrossRefGoogle Scholar
  129. Scoville SA, Lane OP (2013) Cerebellar abnormalities typical of methylmercury poisoning in a fledged saltmarsh sparrow, Ammodramus caudacutus. Bull Environ Contam Toxicol 90:616–620. doi: 10.1007/s00128-013-0974-yCrossRefGoogle Scholar
  130. Seewagen CL (2013) Blood mercury levels and the stopover refueling performance of a long-distance migratory songbird. Can J Zool 91:41–45. doi: 10.1139/cjz-2012-0199CrossRefGoogle Scholar
  131. Sepúlveda MS, Williams GE Jr, Frederick PC, Spalding MG (1999) Effects of mercury on health and first-year survival of free-ranging great egrets (Ardea albus) from southern Florida. Arch Environ Contam Toxicol 37:369–376CrossRefGoogle Scholar
  132. Snelgrove-Hobson SM, Rao PV, Bhatnagar MK (1988) Ultrastructural alterations in the kidneys of Pekin ducks fed methylmercury. Can J Vet Res 52:89–98Google Scholar
  133. Spalding MG, Bjork RD, Powell GVN, Sundlof SF (1994) Mercury and cause of death in great white herons. J Wildl Manag 58:735–739. doi: 10.2307/3809688CrossRefGoogle Scholar
  134. Spalding MG, Frederick PC, McGill HC, Bouton SN, Richey LJ, Schumacher IM, Blackmore CG, Harrison J (2000a) Histologic, neurologic, and immunologic effects of methylmercury in captive great egrets. J Wildl Dis 36:423–435. doi: 10.7589/0090-3558-36.3.423CrossRefGoogle Scholar
  135. Spalding MG, Frederick PC, McGill HC, Bouton SN, McDowell LR (2000b) Methylmercury accumulation in tissues and its effects on growth and appetite in captive great egrets. J Wildl Dis 36:411–422CrossRefGoogle Scholar
  136. Stern GA, Macdonald RW, Outridge PM, Wilson S, Chetelat J, Cole A, Hintelmann H, Loseto LL, Steffen A, Wang F, Zdanowicz C (2012) How does climate change influence arctic mercury? Sci Total Environ 414:22–42. doi: 10.1016/j.scitotenv.2011.10.039CrossRefGoogle Scholar
  137. Sunderland EM, Krabbenhoft DP, Moreau JW, Strode SA, Landing WM (2009) Mercury sources, distribution, and bioavailability in the North Pacific Ocean: Insights from data and models. Global Biogeochm Cycles 23:GB2010Google Scholar
  138. Swaddle JP, Diehl TR, Taylor CE, Fanaee AS, Benson JL, Huckstep NR, Cristol DA (2017) Exposure to dietary mercury alters cognition and behavior of zebra finches. Curr Zool 63:213–219. doi: 10.1093/cz/zox007CrossRefGoogle Scholar
  139. Tartu S, Goutte A, Bustamante P, Angelier F, Moe B, Clément-Chastel C, Bech C, Gabrielsen GW, Bustnes JO, Chastel O (2013) To breed or not to breed: endocrine response to mercury contamination by an Arctic seabird. Biol Lett 9:20130317. doi: 10.1098/rsbl.2013.0317CrossRefGoogle Scholar
  140. Tartu S, Bustamante P, Goutte A, Cherel Y, Weimerskirch H, Bustnes JO, Chastel O (2014) Age-related mercury contamination and relationship with luteinizing hormone in a long-lived Antarctic bird. PLoS One 9:e103642. doi: 10.1371/journal.pone.0103642CrossRefGoogle Scholar
  141. Tartu S, Angelier F, Wingfield JC, Bustamante P, Labadie P, Budzinski H, Weimerskirch H, Bustnes JO, Chastel O (2015) Corticosterone, prolactin and egg neglect behavior in relation to mercury and legacy POPs in a long-lived Antarctic bird. Sci Total Environ 505:180–188. doi: 10.1016/j.scitotenv.2014.10.008CrossRefGoogle Scholar
  142. Taylor CE, Cristol DA (2015) Tissue mercury concentrations and survival of tree swallow embryos, nestlings and young adult females on a contaminated site. Bull Environ Contam Toxicol 95:459–464. doi: 10.1007/s00128-015-1643-0CrossRefGoogle Scholar
  143. Thompson DR, Hamer KC, Furness RW (1991) Mercury accumulation in great skuas Catharacta skua of known age and sex, and its effects upon breeding and survival. J Appl Ecol 28:672–684. doi: 10.2307/2404575CrossRefGoogle Scholar
  144. Varian-Ramos CW, Swaddle JP, Cristol DA (2014) Mercury reduces avian reproductive success and imposes selection: an experimental study with adult- or lifetime-exposure in zebra finch. PLoS One 9:e95674. doi: 10.1371/journal.pone.0095674CrossRefGoogle Scholar
  145. 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. doi: 10.1021/es803707fCrossRefGoogle Scholar
  146. 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. doi: 10.1006/enrs.2002.4384CrossRefGoogle Scholar
  147. Wayland M, Drake KL, Alisauskas RT, Kellett DK, Traylor J, Swoboda C, Mehl K (2008) Survival rates and blood metal concentrations in two species of free-ranging North American sea ducks. Environ Toxicol Chem 27:698–704. doi: 10.1897/07-321CrossRefGoogle Scholar
  148. Weech SA, Scheuhammer AM, Elliott JE (2006) Mercury exposure and reproduction in fish-eating birds breeding in the Pinchi Lake region, British Columbia, Canada. Environ Toxicol Chem 25:1433–1440CrossRefGoogle Scholar
  149. White AE, Cristol DA (2014) Plumage coloration in belted kingfishers (Megaceryle alcyon) at a mercury-contaminated river. Waterbirds 37:144–152. doi: 10.1675/063.037.0203CrossRefGoogle Scholar
  150. Wiemeyer SN, Lamont TG, Bunck CM, Sindelar CR, Gramlich FJ, Fraser JD, Byrd MA (1984) Organochlorine pesticide, polychlorobiphenyl, and mercury residues in bald eagle eggs—1969–79—and their relationships to shell thinning and reproduction. Arch Environ Contam Toxicol 13:529–549. doi: 10.1007/BF01056332CrossRefGoogle Scholar
  151. Wolf SE, Swaddle JP, Cristol DA, Buchser WJ (2017) Methylmercury exposure reduces the auditory brainstem response of zebra finches (Taeniopygia guttata). J Assoc Res Otolaryngol. doi: 10.1007/s10162-017-0619-7CrossRefGoogle Scholar
  152. Yu MS, Eng ML, Williams TD, Basu N, Elliott JE (2016) Acute embryotoxic effects but no long-term reproductive effects of in ovo methylmercury exposure in zebra finches (Taeniopygia guttata). Environ Toxicol Chem 35:1534–1540. doi: 10.1002/etc.3307CrossRefGoogle Scholar
  153. Yu MS, Eng ML, Williams TD, Guigueno MF, Elliott JE (2017) Assessment of neuroanatomical and behavioural effects of in ovo methylmercury exposure in zebra finches (Taeniopygia guttata). Neurotoxicology 59:33–39. doi: 10.1016/j.neuro.2017.01.001CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Biology, Institute for Integrative Bird Behavior StudiesThe College of William and MaryWilliamsburgUSA

Personalised recommendations