Advertisement

The threat of global mercury pollution to bird migration: potential mechanisms and current evidence

  • Chad L. SeewagenEmail author
Article

Abstract

Mercury is a global pollutant that has been widely shown to adversely affect reproduction and other endpoints related to fitness and health in birds, but almost nothing is known about its effects on migration relative to other life cycle processes. Here I consider the physiological and histological effects that mercury is known to have on non-migrating birds and non-avian vertebrates to identify potential mechanisms by which mercury might hinder migration performance. I posit that the broad ability of mercury to inactivate enzymes and compromise the function of other proteins is a single mechanism by which mercury has strong potential to disrupt many of the physiological processes that make long-distance migration possible. In just this way alone, there is reason to expect mercury to interfere with navigation, flight endurance, oxidative balance, and stopover refueling. Navigation and flight could be further affected by neurotoxic effects of mercury on the brain regions that process geomagnetic information from the visual system and control biomechanics, respectively. Interference with photochemical reactions in the retina and decreases in scotopic vision sensitivity caused by mercury also have the potential to disrupt visual-based magnetic navigation. Finally, migration performance and possibly survival might be limited by the immunosuppressive effects of mercury on birds at a time when exposure to novel pathogens and parasites is great. I conclude that mercury pollution is likely to be further challenging what is already often the most difficult and perilous phase of a migratory bird’s annual cycle, potentially contributing to global declines in migratory bird populations.

Keywords

Methylmercury Migratory Navigation Long-distance flight Stopover Oxidative stress Immunocompetence 

Notes

Acknowledgements

Daniel A. Cristol, Alexander R. Gerson, Yanju Ma, Christopher G. Guglielmo, and three anonymous reviewers provided helpful ideas and comments on previous versions of the manuscript. I also thank Daniel Cristol for the invitation and encouragement to write this article for the Special Issue. Financial support for the preparation of the manuscript was provided by the Great Hollow Nature Preserve & Ecological Research Center.

Compliance with ethical standards

Conflict of interest

The author declares that he has no conflict of interest.

References

  1. Ali SF, LeBel CP, Bondy SC (1992) Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity. Neurotoxicol 13:637–648Google Scholar
  2. Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science 331:296–302CrossRefGoogle Scholar
  3. Bingman VP, Cheng K (2005) Mechanisms of animal global navigation: Comparative perspectives and enduring challenges. Ethol Ecol Evol 17:295–318CrossRefGoogle Scholar
  4. Borg K, Erne K, Hanko E, Wanntorp H (1970) Experimental secondary methyl mercury poisoning in the goshawk (Accipiter g. gentilis L.). Environ Pollut 1:91–104CrossRefGoogle Scholar
  5. 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
  6. Bowlin MS, Cochran WW, Wikelski MC (2005) Biotelemetry of new world thrushes during migration: physiology, energetics and orientation in the wild. Integr Comp Biol 45:295–304CrossRefGoogle Scholar
  7. Bridger MA, Thaxton JP (1983) Humoral immunity in the chicken as affected by mercury. Arch Environ Contam Toxicol 12:45–49CrossRefGoogle Scholar
  8. Buehler DM, Tieleman BI, Piersma T (2010) Indices of immune function are lower in Red Knots (Calidris canutus) recovering protein than in those storing fat during stopover in Delaware Bay. Auk 127:394–401CrossRefGoogle Scholar
  9. Burbacher TM, Grant KS, Mayfield DB, Gilbert SG, Rice DC (2005) Prenatal methylmercury exposure affects spatial vision in adult monkeys. Toxicol Appl Pharmacol 208:21–28CrossRefGoogle Scholar
  10. Cambier S, Benard G, Mesmer-Dudons N, Gonzalez P, Rossignol R, Brethes D, Bourdineaud JP (2009) At environmental doses, dietary methylmercury inhibits mitochondrial energy metabolism in skeletal muscles of the zebra fish (Danio rerio). Int J Biochem Cell Biol 41:791–799CrossRefGoogle Scholar
  11. Canto-Pereira LH, Lago M, Costa MF, Rodrigues AR, Saito CA, Silveira LCL, Ventura DF (2005) Visual impairment on dentists related to occupational mercury exposure. Environ Toxicol Pharmacol 19:517–522CrossRefGoogle Scholar
  12. 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 23:1464–1473CrossRefGoogle Scholar
  13. Carta P, Flore C, Alinovi R, Ibba A, Tocco MG, Aru G, Carta R, Girei E, Mutti A, Lucchini R, Randaccio FS (2003) Sub-clinical neurobehavioral abnormalities associated with low level of mercury exposure through fish consumption. Neurotoxicol 24:617–623CrossRefGoogle Scholar
  14. 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 94:407–411CrossRefGoogle Scholar
  15. 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 72:200–214CrossRefGoogle Scholar
  16. Chen YW, Huang CF, Tsai KS, Yang RS, Yen CC, Yang C, Lin-Shiau SY, Liu SH (2006) Methylmercury induces pancreatic β-cell apoptosis and dysfunction. Chem Res Toxicol 19:1080–1085CrossRefGoogle Scholar
  17. Chen YW, Yang CY, Huang CF, Hung DZ, Leung YM, Liu SH (2009) Heavy metals, islet function and diabetes development. Islets 1:169–176CrossRefGoogle Scholar
  18. Chen YW, Huang CF, Yang CY, Yen CC, Tsai KS, Liu SH (2010) Inorganic mercury causes pancreatic β-cell death via the oxidative stress-induced apoptotic and necrotic pathways. Toxicol Appl Pharmacol 243:323–331CrossRefGoogle Scholar
  19. Chernetsov NS (2016) Orientation and navigation of migrating birds. Biol Bull 43:788–803CrossRefGoogle Scholar
  20. Clarkson CE, Erwin RM, Riscassi A (2012) The use of novel biomarkers to determine dietary mercury accumulation in nestling waterbirds. Environ ToxicolChem 31:1143–1148CrossRefGoogle Scholar
  21. Cnotka J, Möhle M, Rehkämper G (2008) Navigational experience affects hippocampus size in homing pigeons. Brain Behav Evol 72:233–238CrossRefGoogle Scholar
  22. Cooper-Mullin C, McWilliams SR (2016) The role of the antioxidant system during intense endurance exercise: lessons from migrating birds. J Exp Biol 219:3684–3695CrossRefGoogle Scholar
  23. Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251CrossRefGoogle Scholar
  24. Cristol DA, Reynolds EB, Leclerc JE, Donner AH, Farabaugh CS, Ziegenfus CW (2003) Migratory dark-eyed juncos, (Junco hyemalis), have better spatial memory and denser hippocampal neurons than nonmigratory conspecifics. Anim Behav 66:317–328CrossRefGoogle Scholar
  25. 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 118:247–266CrossRefGoogle Scholar
  26. Custer TW, Custer CM, Johnson KM, Hoffman D (2008) Mercury and other element exposure to tree swallows (Tachycineta bicolor) nesting on Lostwood National Wildlife Refuge, North Dakota. Environ Pollut 155:217–226CrossRefGoogle Scholar
  27. DeLuca WV, Woodworth BK, Rimmer CC, Marra PP, Taylor PD, McFarland KP, Mackenzie SA, Norris DR (2015) Transoceanic migration by a 12-g songbird. Biol Lett 11:20141045CrossRefGoogle Scholar
  28. Driscoll CT, Mason RP, Chan HM, Jacob DJ, Pirrone N (2013) Mercury as a global pollutant: sources, pathways, and effects. Environ Sci Technol 47:4967–4983CrossRefGoogle Scholar
  29. Driscoll CT, Han YJ, Chen CY, Evers DC, Lambert KF, Holsen TM, Kamman NC, Munson RK (2007) Mercury contamination in forest and freshwater ecosystems in the northeastern United States. BioScience 57:17–28CrossRefGoogle Scholar
  30. Dyer CA (2007) Heavy metals as endocrine-disrupting chemicals. In: Gore AC (ed) Endorcrine disrupting chemicals: from basic research to clinical practice. Humana Press, New Jersey, p 111–133CrossRefGoogle Scholar
  31. Egeler O, Williams TD, Guglielmo CG (2000) Modulation of lipogenic enzymes, fatty acid synthase and Δ 9-desaturase, in relation to migration in the western sandpiper (Calidris mauri). J Comp Physiol B 170:169–174CrossRefGoogle Scholar
  32. Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Top Med Chem 1:529–539CrossRefGoogle Scholar
  33. Evans HL, Garman RH. 1980. Scotopic vision as an indicator of neurotoxicity. In: Merigan WH, Weiss B (Eds) Neurotoxicity of the visual system. Raven Press, New York. pp 135–147Google Scholar
  34. Evans HL, Garman RH, Laties VG (1982) Neurotoxicity of methylmercury in the pigeon. Neurotoxicology 3:21–36Google Scholar
  35. Evers DC, Savoy LJ, DeSorbo CR, Yates DE, Hanson W, Taylor KM, Siegel LS, Cooley Jr JH, Bank MS, Major A, Munney K (2008) Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17:69–81CrossRefGoogle Scholar
  36. Feige JN, Gelman L, Michalik L, Desvergne B, Wahli W (2006) From molecular action to physiological outputs: peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions. Prog Lipid Res 45:120–159CrossRefGoogle Scholar
  37. Figuerola J, Green AJ (2000) Haematozoan parasites and migratory behaviour in waterfowl. Evol Ecol 14:143–153CrossRefGoogle Scholar
  38. Fox DA (2015) Retinal and visual system: occupational and environmental toxicology. In: Lotti M, Bleeker ML (eds) Occupational neurology. Elselvier B.V., Amsterdam, p 325–340CrossRefGoogle Scholar
  39. Fox DA, Sillman AJ (1979) Heavy metals affect rod, but not cone, photoreceptors. Science 206:78–80CrossRefGoogle Scholar
  40. Fujimura M, Usuki F, Sawada M, Takashima A (2009) Methylmercury induces neuropathological changes with tau hyperphosphorylation mainly through the activation of the c-jun-N-terminal kinase pathway in the cerebral cortex, but not in the hippocampus of the mouse brain. Neurotoxicology 30:1000–1007CrossRefGoogle Scholar
  41. Gonzalez P, Dominique Y, Massabuau JC, Boudou A, Bourdineaud JP (2005) Comparative effects of dietary methylmercury on gene expression in liver, skeletal muscle, and brain of the zebrafish (Danio rerio). Environ Sci Technol 39:3972–3980CrossRefGoogle Scholar
  42. Goodridge AG, Ball EG (1967) The effect of prolactin on lipogenesis in the pigeon in vitro studies. Biochemistry 6:2335–2343CrossRefGoogle Scholar
  43. Griminger P (1986) Lipid metabolism. In: Sturkie PD (ed) Avian physiology, 4th edn. Springer Verlag, New York, NY, p 345–358CrossRefGoogle Scholar
  44. Guglielmo CG (2010) Move that fatty acid: fuel selection and transport in migratory birds and bats. Integr Comp Biol 50:336–345CrossRefGoogle Scholar
  45. Gupta PK, Sastry KV (1981) Effect of mercuric chloride on enzyme activities in the digestive system and chemical composition of liver and muscles of the catfish, (Heteropneustes fossilis). Ecotoxicol Environ Saf 5:389–400CrossRefGoogle Scholar
  46. Hambly C, Harper EJ, Speakman JR (2004) The energetic cost of variations in wing span and wing asymmetry in the zebra finch (Taeniopygia guttate). J Exp Biol 207:3977–3984CrossRefGoogle Scholar
  47. 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 20:1677–1683CrossRefGoogle Scholar
  48. Hasselquist D, Lindström Å, Jenni-Eiermann S, Koolhaas A, Piersma T (2007) Long flights do not influence immune responses of a long-distance migrant bird: a wind-tunnel experiment. J Exp Biol 210:1123–1131CrossRefGoogle Scholar
  49. Hawley DM, Hallinger KK, Cristol DA (2009) Compromised immune competence in free-living tree swallows exposed to mercury. Ecotoxicology 18:499–503CrossRefGoogle Scholar
  50. Hawryshyn CW, Mackay WC, Nilsson TH (1982) Methyl mercury induced visual deficits in rainbow trout. Can J Zool 60:3127–3133CrossRefGoogle Scholar
  51. Healy SD, Gwinner E, Krebs JR (1996) Hippocampal volume in migratory and non-migratory warblers: effects of age and experience. Behav Brain Res 81:61–68CrossRefGoogle Scholar
  52. Heinz GH, Locke LN (1976) Brain lesions in mallard ducklings from parents fed methylmercury. Avian Dis 20:9–17CrossRefGoogle Scholar
  53. 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
  54. Henry KA, Cristol DA, Varian-Ramos CW, Bradley EL (2015) Oxidative stress in songbirds exposed to dietary methylmercury. Ecotoxicology 24:520–526CrossRefGoogle Scholar
  55. Herring G, Eagles‐Smith CA, Ackerman JT (2017) Mercury exposure may influence fluctuating asymmetry in waterbirds. Environ Toxicol Chem 36:1599–1605CrossRefGoogle Scholar
  56. Heyers D, Manns M, Luksch H, Güntürkün O, Mouritsen H (2007) A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS One 2:e937CrossRefGoogle Scholar
  57. 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 A 72:1223–1241CrossRefGoogle Scholar
  58. 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
  59. Hoffman DJ, Heinz GH (1998) Effects of mercury and selenium on glutathione metabolism and oxidative stress in mallard ducks. Environ Toxicol Chem 17:161–166CrossRefGoogle Scholar
  60. Holland RA, Thorup K, Gagliardo A, Bisson IA, Knecht E, Mizrahi D, Wikelski M (2009) Testing the role of sensory systems in the migratory heading of a songbird. J Exp Biol 212:4065–4071CrossRefGoogle Scholar
  61. Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521–528CrossRefGoogle Scholar
  62. Jenni-Eiermann S, Jenni L (1992) High plasma triglyceride levels in small birds during migratory flight: A new pathway for fuel supply during endurance locomotion at very high mass-specific metabolic rates? Physiol Zool 65:112–123CrossRefGoogle Scholar
  63. Karasov WH, Martinez del Rio C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. Princeton, New JerseyGoogle Scholar
  64. Karasov WH, Pinshow B (1998) Changes in lean mass and in organs of nutrient assimilation in a long-distance passerine migrant at a springtime stopover site. Physiol Zool 71:435–438CrossRefGoogle Scholar
  65. Kawakami T, Hanao N, Nishiyama K, Kadota Y, Inoue M, Sato M, Suzuki S (2012) Differential effects of cobalt and mercury on lipid metabolism in the white adipose tissue of high-fat diet-induced obesity mice. Toxicol Appl Pharmacol 258:32–42CrossRefGoogle Scholar
  66. 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
  67. Kirby JS, Stattersfield AJ, Butchart SH, Evans MI, Grimmett RF, Jones VR, O’Sullivan J, Tucker GM, Newton I (2008) Key conservation issues for migratory land and waterbird species on the world’s major flyways. Bird Conser Int 18:S49–S73CrossRefGoogle Scholar
  68. Klaassen RH, Hake M, Strandberg R, Koks BJ, Trierweiler C, Exo KM, Bairlein F, Alerstam T (2014) When and where does mortality occur in migratory birds? Direct evidence from long-term satellite tracking of raptors. J Anim Ecol 83:176–84CrossRefGoogle Scholar
  69. Klaassen M, Hoye BJ, Nolet BA, Buttemer WA (2012) Ecophysiology of avian migration in the face of current global hazards. Philos Trans R Soc Lond B Biol Sci 367:1719–1732CrossRefGoogle Scholar
  70. Klaper R, Carter BJ, Richter CA, Drevnick PE, Sandheinrich MB, Tillitt D (2008) Use of a 15k gene microarray to determine gene expression changes in response to acute and chronic methylmercury exposure in the fathead minnow (Pimephales promelas). J Fish Biol 72:2207–2280CrossRefGoogle Scholar
  71. Krause JS, Németh Z, Pérez JH, Chmura HE, Ramenofsky M, Wingfield JC (2016) Annual hematocrit profiles in two subspecies of white-crowned sparrow: a migrant and a resident comparison. Physiol Biochem Zool 89:51–60CrossRefGoogle Scholar
  72. Landler L, Painter MS, Coe BH, Youmans PW, Hopkins WA, Phillips JB (2017) High levels of maternally transferred mercury disrupt magnetic responses of snapping turtle hatchlings (Chelydra serpentina). Environ Pollut 228:19–25CrossRefGoogle Scholar
  73. Landys-Ciannelli MM, Jukema J, Piersma T (2002) Blood parameter changes during stopover in a long‐distance migratory shorebird, the bar‐tailed godwit (Limosa lapponica taymyrensis). J Avian Biol 33:451–455CrossRefGoogle Scholar
  74. 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 64:327–336CrossRefGoogle Scholar
  75. Lindstrom A, Alerstam T (1992) Optimal fat loads in migrating birds: a test of the time-minimization hypothesis. Am Nat 140:477–491CrossRefGoogle Scholar
  76. Ma Y, Perez CR, Branfireun BA, Guglielmo CG (2018a) Dietary exposure to methylmercuryaffects flight endurance in a migratory songbird. Environ Pollut 234:894–901CrossRefGoogle Scholar
  77. Ma Y, Branfireun BA, Hobson KA, Guglielmo CG (2018b) Evidence of negative seasonal carry-over effects of breeding ground mercury exposure on survival of migratory songbirds. J Avian Biol.  https://doi.org/10.1111/jav.01656 CrossRefGoogle Scholar
  78. Marasco V, Costantini D (2016) Signaling in a polluted world: oxidative stress as an overlooked mechanism linking contaminants to animal communication. Front Ecol Evol 4:95CrossRefGoogle Scholar
  79. Maués LAL, Macchi BM, Crespo-López ME, Nasciutti LE, Picanço-Diniz DLW, Antunes-Rodrigues J, do Nascimento JLM (2015) Methylmercury inhibits prolactin release in a cell line of pituitary origin. Braz J Med Biol Res 48:691–696CrossRefGoogle Scholar
  80. McFarlan JT, Bonen A, Guglielmo CG (2009) Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J Exp Biol 212:2934–2940CrossRefGoogle Scholar
  81. McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393CrossRefGoogle Scholar
  82. McWilliams SR, Karasov WH (2014) Spare capacity and phenotypic flexibility in the digestive system of a migratory bird: defining the limits of animal design. Proc R Soc B 281:20140308CrossRefGoogle Scholar
  83. Mehlman DW, Mabey SE, Ewert DN, Duncan C, Abel B, Cimprich D, Sutter RD, Woodrey M (2005) Conserving stopover sites for forest-dwelling migratory landbirds. Auk 122:1281–1290CrossRefGoogle Scholar
  84. Mela M, Grötzner SR, Legeay A, Mesmer-Dudons N, Massabuau JC, Ventura DF, de Oliveira Ribeiro CA (2012) Morphological evidence of neurotoxicity in retina after methylmercury exposure. Neurotoxicology 33:407–415CrossRefGoogle Scholar
  85. Møller AP, Erritzøe J (1998) Host immune defence and migration in birds. Evol Ecol 12:945–953CrossRefGoogle Scholar
  86. Morris SR, Holmes DW, Richmond ME (1996) A ten-year study of the stopover patterns of migratory passerines during fall migration on Appledore Island, Maine. Condor 98:395–409CrossRefGoogle Scholar
  87. Morton ML (2002) The mountain white-crowned sparrow: migration and reproduction at high altitude. Stud Avian Biol 24Google Scholar
  88. Mouritsen H, Hore PJ (2012) The magnetic retina: Light-dependent and trigeminal magnetoreception in migratory birds. Curr Opin Neurobiol 22:343–352CrossRefGoogle Scholar
  89. Mouritsen H, Feenders G, Liedvogel M, Wada K, Jarvis ED (2005) Night-vision brain area in migratory songbirds. Proc Natl Acad Sci USA 102:8339–8344CrossRefGoogle Scholar
  90. Mouritsen H, Janssen-Bienhold U, Liedvogel M, Feenders G, Stalleicken J, Dirks P, Weiler R (2004) Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc Natl Acad Sci USA 101:14294–14299CrossRefGoogle Scholar
  91. Moye JK, Perez CR, Pritsos CA (2016) Effects of parental and direct methylmercury exposure on flight activity in young homing pigeons (Columba livia). Environ Pollut 5:23–30CrossRefGoogle Scholar
  92. Nebel S, Bauchinger U, Buehler DM, Langlois LA, Boyles M, Gerson AR, Price ER, McWilliams SR, Guglielmo CG (2012) Constitutive immune function in European starlings, (Sturnus vulgaris), is decreased immediately after an endurance flight in a wind tunnel. J Exp Biol 215:272–278CrossRefGoogle Scholar
  93. Newton I (2006) Can conditions experienced during migration limit the population levels of birds? J Ornithol 147:146–166CrossRefGoogle Scholar
  94. Norris RD, Marra PP (2007) Seasonal interactions, habitat quality, and population dynamics in migratory birds. Condor 109:535–47CrossRefGoogle Scholar
  95. Norris K, Evans MR (2000) Ecological immunology: Life history trade-offs and immune defense in birds. Behav Ecol 11:19–26CrossRefGoogle Scholar
  96. North American Bird Conservation Initiative (NABCI) (2016) The state of North America’s birds 2016. Environment and Climate Change Ottawa, CanadaGoogle Scholar
  97. Owen JC, Moore FR (2006) Seasonal differences in immunological condition of three species of thrushes. Condor 108:389–398CrossRefGoogle Scholar
  98. Owen JC, Moore FR (2008) Relationship between energetic condition and indicators of immune function in thrushes during spring migration. Can J Zool 86:638–647CrossRefGoogle Scholar
  99. Pereira R, Guilherme S, Brandão F, Raimundo J, Santos MA, Pacheco M, Pereira P (2016) Insights into neurosensory toxicity of mercury in fish eyes stemming from tissue burdens, oxidative stress and synaptic transmission profiles. Mar Environ Res 113:70–79CrossRefGoogle Scholar
  100. Pierce BJ, McWilliams SR, Place AR, Huguenin MA (2004) Diet preferences for specific fatty acids and their effect on composition of fat reserves in migratory Red-eyed Vireos (Vireo olivaceous). Comp Biochem Physiol A Mol Integr Physiol 138:503–514CrossRefGoogle Scholar
  101. 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 18:5–14CrossRefGoogle Scholar
  102. Pravosudov VV, Kitaysky AS, Omanska A (2006) The relationship between migratory behaviour, memory and the hippocampus: an intraspecific comparison. Proc R Soc Lond B Biol Sci 273:2641–2649CrossRefGoogle Scholar
  103. Ramenofsky M (2011) Hormones in migration and reproductive cycles of birds. In: Norris DO, Lopez KH (eds) Hormones and reproduction of vertebrates. Academic Press, Amsterdam, p 205–236Google Scholar
  104. Ramenofsky M, Savard R, Greenwood MRC (1999) Seasonal and diel transitions in physiology and behavior in the migratory dark-eyed junco. Comp Biochem Physiol A Mol Integr Physiol 122:385–397CrossRefGoogle Scholar
  105. Rice KM, Walker Jr EM, Wu M, Gillette C, Blough ER (2014) Environmental mercury and its toxic effects. J Prev Med Public Health 47:74–83CrossRefGoogle Scholar
  106. Richter CA, Martyniuk CJ, Annis ML, Brumbaugh WG, Chasar LC, Denslow ND, Tillitt DE (2014) Methylmercury-induced changes in gene transcription associated with neuroendocrine disruption in largemouth bass (Micropterus salmoides). Gen Comp Endocrinol 203:215–224CrossRefGoogle Scholar
  107. 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 19:697–709CrossRefGoogle Scholar
  108. 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 14:223–240CrossRefGoogle Scholar
  109. Risely A, Klaassen M, Hoye B (2018) Migratory animals feel the cost of getting sick: a meta-analysis across species. J Anim Ecol 87:301–314CrossRefGoogle Scholar
  110. Ritz T, Adem S, Schulten K (2000) A model for photoreceptor-based magnetoreception in birds. Biophys J 78:707–718CrossRefGoogle Scholar
  111. Sarafian T, Verity MA (1991) Oxidative mechanisms underlying methyl mercury neurotoxicity. Int J Dev Neurosci 9:147–153CrossRefGoogle Scholar
  112. Sastry KV, Gupta PK (1980) Changes in the activities of some digestive enzymes of (Channa punctatus), exposed chronically to mercuric chloride. J Environ Sci Health B 15:109–119CrossRefGoogle Scholar
  113. Sastry KV, Rao DR (1984) Effect of mercuric chloride on some biochemical and physiological parameters of the freshwater murrel, Channa punctatus. Environ Res 34:343–350CrossRefGoogle Scholar
  114. Schaub M, Jenni L, Bairlein F (2008) Fuel stores, fuel accumulation, and the decision to depart from a migration stopover site. Behav Ecol 19:657–666CrossRefGoogle Scholar
  115. Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36:12–19CrossRefGoogle Scholar
  116. Schumacher L, Abbott LC (2017) Effects of methyl mercury exposure on pancreatic beta cell development and function. J Appl Toxicol 37:4–12CrossRefGoogle Scholar
  117. Scoville SA, Lane OP (2013) Cerebellar abnormalities typical of methylmercury poisoning in a fledged saltmarsh sparrow (Ammodramus caudacutus). Bull Environ Contam Toxicol 90:616–620CrossRefGoogle Scholar
  118. Seewagen CL, Cristol DA, Gerson AR (2016) Mobilization of mercury from lean tissues during simulated migratory fasting in a model songbird. Sci Rep 6:25762Google Scholar
  119. Seewagen CL (2013) Blood mercury levels and the stopover refueling performance of a long-distance migratory songbird. Can J Zool 91:41–45CrossRefGoogle Scholar
  120. Seewagen CL, Guglielmo CG (2011) Quantitative magnetic resonance analysis and a morphometric predictive model reveal lean body mass changes in migrating Nearctic–Neotropical passerines. J Comp Physiol B 181:413–421CrossRefGoogle Scholar
  121. Seewagen CL (2010) Threats of environmental mercury to birds: knowledge gaps and priorities for future research. Bird Conserv Int 20:112–123CrossRefGoogle Scholar
  122. Selin NE (2009) Global biogeochemical cycling of mercury: a review. Annu Rev Environ Resour 34:43–63CrossRefGoogle Scholar
  123. Sepúlveda MS, Williams Jr GE, 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
  124. Sharma JM (1991) Overview of the avian immune system. Vet Immunol Immunopathol 30:13–17CrossRefGoogle Scholar
  125. Sherry DF, Hoshooley JS (2007) Neurobiology of spatial behavior. In: Otter KA (ed) Ecology and behavior of chickadees and tits: an integrated approach. Oxford University Press, Oxford, p 9–23CrossRefGoogle Scholar
  126. Shimizu T, Bowers AN, Budzynski CA, Kahn MC, Bingman VP (2004) What does a pigeon (Columba livia) brain look like during homing? selective examination of ZENK expression. Behav Neurosci 118:845–851CrossRefGoogle Scholar
  127. Sillett T Scott, Holmes RT (2002) Variation in survivorship of a migratory songbird throughout its annual cycle J Anim Ecol 71:296–308CrossRefGoogle Scholar
  128. Skrip MM, McWilliams SR (2016) Oxidative balance in birds: an atoms to organisms to ecology primer for ornithologists. J Field Ornithol 87:1–20CrossRefGoogle Scholar
  129. Soldin OP, O’Mara DM, Aschner M (2008) Thyroid hormones and methylmercury toxicity. Biol Trace Elem Res 126:1CrossRefGoogle Scholar
  130. Solov’yov IA, Mouritsen H, Schulten K (2010) Acuity of a cryptochrome and vision-based magnetoreception system in birds. Biophys J 99:40–49CrossRefGoogle Scholar
  131. Spalding MG, Frederick PC, McGill HC, Bouton SN, Richey L, Schumacher IM, Blackmore GM, Harrison J (2000a) Histologic, neurologic, and immunologic effects of methylmercury in captive great egrets J Wildl Dis 36:423–435CrossRefGoogle Scholar
  132. 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
  133. Stapput K, Thalau P, Wiltschko R, Wiltschko W (2008) Orientation of birds in total darkness. Curr Biol 18:602–606CrossRefGoogle Scholar
  134. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336CrossRefGoogle Scholar
  135. Strasser R, Bingman VP, Ioalé P, Casini G, Bagnoli P (1998) The homing pigeon hippocampus and the development of landmark navigation. Dev Psychobiol 33:305–315CrossRefGoogle Scholar
  136. 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 63:213–219CrossRefGoogle Scholar
  137. Tan SW, Meiller JC, Mahaffey KR (2009) The endocrine effects of mercury in humans and wildlife. ‎Crit Rev Toxicol 39:228–269CrossRefGoogle Scholar
  138. 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 505:180–188CrossRefGoogle Scholar
  139. Tessier-Lavigne M, Mobbs P, Attwell D (1985) Lead and mercury toxicity and the rod light response. Invest Ophthalmol Vis Sci 26:1117–1123Google Scholar
  140. Thaxton P, Parkhurst CR (1973) Toxicity of mercury to young chickens 3: changes in immunological responsiveness. Poult Sci 52:761–764CrossRefGoogle Scholar
  141. Thomas AL (1993) The aerodynamic costs of asymmetry in the wings and tail of birds: asymmetric birds can’t fly round tight corners. Proc R Soc Lond B Biol Sci 254:181–189CrossRefGoogle Scholar
  142. Tinkov AA, Ajsuvakova OP, Skalnaya MG, Popova EV, Sinitskii AI, Nemereshina ON, Gatiatulina ER, Nikonorov AA, Skalny AV (2015) Mercury and metabolic syndrome: a review of experimental and clinical observations. Biometals 28:231–254CrossRefGoogle Scholar
  143. Van Gils JA, Munster VJ, Radersma R, Liefhebber D, Fouchier RA, Klaassen M (2007) Hampered foraging and migratory performance in swans infected with low-pathogenic avian influenza A virus. PloS One 2:e184CrossRefGoogle Scholar
  144. Ventura DF, Simoes AL, Tomaz S, Costa MF, Lago M, Costa MTV, Rodrigues AR, Saito C, Silveira LCL (2005) Colour vision and contrast sensitivity losses of mercury intoxicated industry workers in Brazil. ‎Environ Toxicol Pharmacol 19:523–529CrossRefGoogle Scholar
  145. Wada H, Cristol DA, McNabb FA, Hopkins WA (2009) Suppressed adrenocortical responses and thyroid hormone levels in birds near a mercury-contaminated river. ‎Environ Sci Technol 43:6031–6038CrossRefGoogle Scholar
  146. Warfvinge K, Bruun A (1996) Mercury accumulation in the squirrel monkey eye after mercury vapour exposure. Toxicology 107:189–200CrossRefGoogle Scholar
  147. Weber JM (2011) Metabolic fuels: regulating fluxes to select mix. J Exp Biol 214:286–294CrossRefGoogle Scholar
  148. Wingfield JC, Breuner CW, Jacobs J (1997) Corticosterone and behavioral responses to unpredictable events. In: Harvey S, Etches RJ (eds.) Perspectives in avian endocrinology. Journal of Endocrinology Press, Bristol, pp 267–278Google Scholar
  149. Wittenberg BA, Wittenberg JB (1989) Transport of oxygen in muscle. Annu Rev Physiol 51:857–878CrossRefGoogle Scholar
  150. Whitney MC, Cristol DA (2017) Impacts of sublethal mercury exposure on birds: a detailed review. Rev Environ Contam Toxicol 244:113–163Google Scholar
  151. Wolfe MF, Schwarzbach S, Sulaiman RA (1998) Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146–160CrossRefGoogle Scholar
  152. Yadetie F, Karlsen OA, Lanzén A, Berg K, Olsvik P, Hogstrand C, Goksøyr A (2013) Global transcriptome analysis of Atlantic cod (Gadus morhua) liver after in vivo methylmercury exposure suggests effects on energy metabolism pathways. Aquat Toxicol 126:314–325CrossRefGoogle Scholar
  153. Ynalvez R, Gutierrez J, Gonzalez-Cantu H (2016) Mini-review: toxicity of mercury as a consequence of enzyme alteration. BioMetals 29:781–788CrossRefGoogle Scholar
  154. Zapka M, Heyers D, Hein CM, Engels S, Schneider NL, Hans J, Weiler S, Dryer D, Kishkinev D, Wild JM, Mouritsen H (2009) Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461:1274–1277CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Great Hollow Nature Preserve & Ecological Research CenterNew FairfieldUSA

Personalised recommendations