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A Review and Assessment of Spent Lead Ammunition and Its Exposure and Effects to Scavenging Birds in the United States

  • Nancy H. Golden
  • Sarah E. Warner
  • Michael J. Coffey
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 237)

Abstract

There are multiple sources of lead in the environment. However, scientific evidence points to spent lead ammunition as the most frequent cause of lead exposure and poisoning in scavenging birds in the United States. Despite the ban on its use for waterfowl hunting, lead ammunition is still widely used for other hunting and shooting activities. Therefore, it can remain on the landscape in carcasses not retrieved and in discarded offal piles. Carcasses and gut piles can be attractive food sources to scavenging birds that can ingest bullet fragments or shot while feeding. Scavenging birds may be particularly vulnerable to exposure and effects of lead due to their foraging strategies and food preferences, physiological processes that facilitate the absorption of lead, and demographic traits. Numerous lines of evidence support ammunition as the source of exposure in the majority of lead poisoned scavenging birds and include the recovery of ingested lead fragments or shot from exposed birds, observations of birds feeding on contaminated carcasses, isotopic signatures of lead in tissue that match that found in ammunition, patterns of mortality coincident with hunting seasons, and the lack of abundant evidence for other lead sources. Lead can be replaced in ammunition by alternative metals that are currently available and present limited environmental threats.

Keywords

Lead Ammunition Bird Poisoning metals 

Notes

Acknowledgements

We thank Drs. John Elliott, Grainger Hunt, Philip Smith, Noel Snyder, Scott Wright, and three anonymous reviewers for thoughtful and constructive reviews of draft versions of this document; Steven Choy, U.S. Fish and Wildlife Service, for editorial and technical support; and Dr. Chris Franson, USGS National Wildlife Health Center, for providing technical expertise.

Disclaimer The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

References

  1. Álvarez-Lloret P, Rodríguez-Navarro AB, Romanek CS, Ferrandis P, Martínez-Haro M, Mateo R (2014) Effects of lead shot ingestion on bone mineralization in a population of red-legged partridge (Alectoris rufa). Sci Total Environ 466–467:34–39CrossRefGoogle Scholar
  2. Anderson WL, Havera SP, Zercher BW (2000) Ingestion of lead and nontoxic shotgun pellets by ducks in the Mississippi flyway. J Wildl Manage 64:848–857CrossRefGoogle Scholar
  3. Arizona Game and Fish Department (2012) Survey, harvest and hunt data for big and small game. http://www.azgfd.gov/regs/HuntArizona2012.pdf. Accessed 15 May 2014
  4. Bagley GE, Locke LN, Nightingale GT (1967) Lead poisoning in Canada geese in Delaware. Am Assoc Avian Pathol 11:601–608Google Scholar
  5. Bannon DI, Parsons PJ, Centeno JA, Lal S, Xu H, Rosencrance AB, Dennis WE, Johnson MS (2011) Lead and copper in pigeons (Columbia livia) exposed to a small arms–range soil. Arch Environ Contam Toxicol 60:351–360CrossRefGoogle Scholar
  6. Barbosa F Jr, Tanus-Santos JE, Gerlach RF, Parsons PJ (2005) A critical review of biomarkers used for monitoring human exposure to lead: advantages, limitations, and future needs. Environ Health Perspect 113:1669–1674CrossRefGoogle Scholar
  7. Barrett MW, Karstad LH (1971) A fluorescent erythrocyte test for lead poisoning in waterfowl. J Wildl Manage 35:109–119CrossRefGoogle Scholar
  8. Bedrosian B, Craighead D (2009) Blood lead levels of bald and golden eagles sampled during and after hunting seasons in the Greater Yellowstone Ecosystem Extended abstract. In: Watson RT, Fuller M, Pokras M, Hunt G (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID, pp 219–220, https://www.peregrinefund.org/subsites/conference-lead/PDF/0209%20Bedrosian.pdf Google Scholar
  9. Bedrosian B, Craighead D, Crandall R (2012) Lead exposure in bald eagles from big game hunting, the continental implications and successful mitigation efforts. PLoS One 7, e51978CrossRefGoogle Scholar
  10. Behmke S, Fallon J, Duerr AE, Lehner A, Buchweitz J, Katzner T (2015) Chronic lead exposure is epidemic in obligate scavenger populations in eastern North America. Environ Int 79:51–55CrossRefGoogle Scholar
  11. Bellrose FC (1951) Effects of ingested lead shot upon waterfowl populations. North Am Wildl Conf Trans 16:125–133Google Scholar
  12. Bellrose FC (1959) Lead poisoning as a mortality factor in waterfowl populations. Nat Hist Surv Bull 27:235–288Google Scholar
  13. Bellrose FC (1965) Wasted waterfowl. Final report. Exhibit F. Mississippi Flyway Council Planning Committee, Mississippi, p 72Google Scholar
  14. Berglund ǺMM, Ingvarsson PK, Danielsson H, Nyholm NEI (2010) Lead exposure and biological effects in pied flycatchers (Ficedula hypoleuca) before and after the closure of a lead mine in northern Sweden. Environ Pollut 158:1368–1375CrossRefGoogle Scholar
  15. Beyer WN (1988) Lead poisoning in six captive avian species. Arch Environ Contam Toxicol 17:121–130CrossRefGoogle Scholar
  16. Beyer WN, Franson JC, Locke LN, Stroud RK, Sileo L (1998) Retrospective study of the diagnostic criteria in a lead-poisoning survey of waterfowl. Arch Environ Contam Toxicol 35:506–512CrossRefGoogle Scholar
  17. Beyer WN, Franson JC, French JB, May T, Rattner BA, Shearn-Bochsler VI, Warner SE, Weber J, Mosby M (2013) Toxic exposure of songbirds to lead in the Southeast Missouri Lead Mining District. Arch Environ Contam Toxicol 65:598–610. doi: 10.1007/s00244-013-9923-3 CrossRefGoogle Scholar
  18. Bloom PH, Scott JM, Pattee OH, Smith MR (1989) Lead contamination of golden eagles (Aquila chrysaetos) within the range of the California condor (Gymnogyps californianus). Proceedings of the 3rd world conference on birds of prey and owls, Eliat, Israel. In: Meyburgh BU, Chancellor RD (eds) Raptors in the modern world, pp 481–482. http://www.raptors-international.org/book/raptors_in_the_modern_world/Bloom_Scott_1989_481-482.pdf
  19. Blus LJ, Henny CJ, Hoffman DJ, Grove RA (1991) Lead toxicosis in tundra swans near a mining and smelting complex in northern Idaho. Arch Environ Contam Toxicol 21:549–555CrossRefGoogle Scholar
  20. Boarman W, Heinrich B (1999) Common raven (Corvus corax), the birds of North America online, Poole A (ed) Cornell Lab of Ornithology, Ithaca. http://bna.birds.cornell.edu/bna/species/476. Accessed 15 May 2014
  21. Bollhöfer B, Rosman KJR (2001) Isotopic source signatures for atmospheric lead: the northern hemisphere. Geochim Cosmochim Act 65:1727–1740CrossRefGoogle Scholar
  22. Bressler JP, Goldstein GW (1991) Mechanisms of lead neurotoxicity. Biochem Pharmacol 41:479–484CrossRefGoogle Scholar
  23. Buckley NJ (1999) Black vulture (Coragyps atratus), the birds of North America online, Poole A (ed) Cornell Lab of Ornithology, Ithaca. http://bna.birds.cornell.edu/bna/species/411. Accessed 15 May 2014
  24. Buehler DA (2000) Bald eagle (Haliaeetus leucocephalus), the birds of North America online, Poole A (ed) Cornell Lab of Ornithology, Ithaca. http://bna.birds.cornell.edu/bna/species/506. Accessed 15 May 2014
  25. Buerger TT, Mirarchi RE, Lisano ME (1986) Effects of lead shot ingestion on captive mourning dove survivability and reproduction. J Wildl Manage 50:1–8CrossRefGoogle Scholar
  26. Burger J (1994) Heavy metals in avian eggshells: another excretion method. J Toxicol Environ Health 41:207–220CrossRefGoogle Scholar
  27. Burger J, Gochfeld M (1990) Tissue levels of lead in experimentally exposed herring gull (Larus argentatus) chicks. J Toxicol Environ Health 29:219–233CrossRefGoogle Scholar
  28. Burger J, Gochfeld M (2000) Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health B 3:59–78CrossRefGoogle Scholar
  29. Burger J, Lavery MH, Gochfeld M (1994) Temporal changes in lead levels in common tern feathers in New York and relationship of field levels to adverse effects in the laboratory. Environ Toxicol Chem 13:581–586CrossRefGoogle Scholar
  30. Burger J, Gochfeld M, Jeitner C, Snigaroff D, Snigaroff R, Stamm T, Volz C (2008) Assessment of metals in down feathers of female common eiders and their eggs from the Aleutians: Arsenic, cadmium, chromium, lead, manganese, mercury, and selenium. Environ Monit 143:247–256CrossRefGoogle Scholar
  31. California Department of Fish and Game (2011) Report of the 2010/11 game take hunter survey. 143:247–256. https://www.dfg.ca.gov/Wildl/hunting/uplandgame/reports/surveys.html
  32. Carpenter JW, Pattee OH, Fritts SH, Rattner BA, Wiemeyer SN, Royle JA, Smith MR (2003) Experimental lead poisoning in turkey vultures (Cathartes aura). J Wildl Dis 39:96–104CrossRefGoogle Scholar
  33. Centers for Disease Control and Prevention (CDC) (2012) CDC Response to Advisory Committee on Childhood Lead Poisoning Prevention Recommendations in “Low Level Lead Exposure Harms Children: A Renewed Call of Primary Prevention” June 7, 2012, http://www.cdc.gov/nceh/lead/acclpp/cdc_response_lead_exposure_recs.pdf
  34. Chupp NR, Dalke PD (1964) Waterfowl mortality in the Coeur D’alene river valley, Idaho. J Wildl Manage 28:692–702CrossRefGoogle Scholar
  35. Church ME, Gwiazda R, Risebrough RW, Sorenson K, Chamberlain CP, Farry S, Heinrich W, Rideout BA, Smith DR (2006) Ammunition is the principal source of lead accumulated by California condors re-introduced to the wild. Environ Sci Technol 40:6143–6150CrossRefGoogle Scholar
  36. Clausen B, Wolstrup C (1978) Copper load in mute swans (Cygnus olor) found in Denmark. Norisk Vet Med 30:260–266Google Scholar
  37. Cogan CB, D’Elia J, Convery K, Brandt J, Bulgerin T (2012) Analysis of California condor (Gymnogyps californianus) activity using satellite telemetry data. Open Ornithol J 5:82–93CrossRefGoogle Scholar
  38. Cornatzer WE, Fogarty EF, Cornatzer EW (2009) Qualitative and quantitative detection of lead bullet fragments in random venison packages donated to the Community Action Food Centers of North Dakota, 2007. In: Watson RT, Fuller M, Pokras M, Hunt G (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID, pp 154–156, https://www.peregrinefund.org/subsites/conference-lead/PDF/0111%20Cornatzer.pdf Google Scholar
  39. Craighead D, Bedrosian B (2008) Blood lead levels of common ravens with access to big-game offal. J Wildl Manage 72:240–245CrossRefGoogle Scholar
  40. Craighead D, Bedrosian B (2009) A relationship between blood lead levels of common ravens and the hunting season in the southern Yellowstone Ecosystem. In: Watson RT, Fuller M, Pokras M, Hunt G (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID, pp 1–4, https://www.peregrinefund.org/subsites/conference-lead/PDF/0206%20Craighead.pdf Google Scholar
  41. Cruz-Martinez L, Redig PT, Deen J (2012) Lead from spent ammunition: a source of exposure and poisoning in bald eagles. Hum Wildl Interact 6:94–104Google Scholar
  42. Custer TW, Franson JC, Pattee OH (1984) Tissue lead distribution and hematologic effects in American kestrels (Falco sparverius L.) fed biologically incorporated lead. J Wildl Dis 20:39–42CrossRefGoogle Scholar
  43. Dauwe T, Bervoets L, Blust R, Pinxten R, Eens M (1999) Are eggshells and egg contents of great and blue tits suitable as indicators of heavy metal pollution. Bel J Zool 129:439–447Google Scholar
  44. Dauwe T, Bervoets L, Blust R, Eens M (2002) Tissue levels of lead in experimentally exposed zebra finches (Taeniopygia guttata) with particular attention on the use of feathers as biomonitors. Arch Environ Contam Toxicol 42:88–92CrossRefGoogle Scholar
  45. Dauwe T, Jenssens E, Bervoets L, Blust R, Eens M (2005) Heavy metal concentrations in female laying great tits (Parus major) and their clutches. Arch Environ Contam Toxicol 49:249–256CrossRefGoogle Scholar
  46. DeMent SH, Chisolm JJ Jr, Eckhaus MA, Strandberg JD (1987) Toxic lead exposure in the urban rock dove. J Wildl Dis 23:273–278CrossRefGoogle Scholar
  47. Dobrowolska A, Melosik M (2008) Bullet-derived lead in tissues of the wild boar (Sus scrofa) and red deer (Cervus elaphus). Eur J Wildl Res 54:231–235CrossRefGoogle Scholar
  48. Domenech R, Langer H (2009) Blood-lead levels of fall migrant golden eagles in west-central Montana. In: Watson RT, Fuller M, Pokras M, Hunt G (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID, pp 221–222, https://www.peregrinefund.org/subsites/conference-lead/PDF/0210%20Domenech.pdf Google Scholar
  49. Douglas-Stroebel E, Hoffman DJ, Brewer GL, Sileo L (2004) Effects of lead-contaminated sediment and nutrition on mallard duckling brain growth and biochemistry. Chem Environ Pollut 131:215–222CrossRefGoogle Scholar
  50. Duke GE (1997) Gastrointestinal physiology and nutrition in wild birds. Proc Nutr Soc 56:1049–1056CrossRefGoogle Scholar
  51. Duke GE, Jegers AA, Loff G, Evanson OA (1975) Gastric digestion in some raptors. Comp Biochem Physiol 50A:649–656CrossRefGoogle Scholar
  52. Duke GE, Evanson OA, Jegers A (1976) Meal to pellet intervals in 14 species of captive raptors. Comp Biochem Physiol 53A:1–6CrossRefGoogle Scholar
  53. Dusek GL, Mackie RJ, Herriges JD, Compton BB (1989) Population ecology of white-tailed deer along the lower Yellowstone River. Wildlife monographs ISSN:00840173. Wildl Soc Bull 104:1–68Google Scholar
  54. Edens FW, Benton E, Bursian SJ, Morgan GW (1976) Effect of dietary lead on reproductive performance in Japanese quail, Coturnix coturnix japonica. Toxicol Appl Pharmacol 38:307–314CrossRefGoogle Scholar
  55. Eisler R (2000) Lead. In: Eisler R (ed) Handbook of chemical risk assessment: health hazards to humans, plants, and animals, Vol 1 – metals. Lewis Publishers, Boca Raton, FL, pp 201–311CrossRefGoogle Scholar
  56. Elliott JE, Langelier KM, Scheuhammer AM, Sinclair PH, Whitehead PE (1992) Incidence of lead poisoning and lead shot in waterfowl gizzards from British Columbia, 1988–91. Can Wildl Serv Prog Notes 200:12Google Scholar
  57. Elliott JE, Birmingham AL, Wilson LK, McAdie M, Trudeau S, Mineau P (2008) Fonofos poisons raptors and waterfowl several months after granular application. Environ Toxicol Chem 27:452–460CrossRefGoogle Scholar
  58. Ewins PJ, Andress RA (1995) The diet of bald eagles, Haliaeetus leucocephalus, wintering in the Lower Great Lakes Basin, 1987–1995. Can Field Nat 109:418–425Google Scholar
  59. Farner DS (1960) Digestion and the digestive system. In: Marshall AJ (ed) Biological and comparative physiology of birds. Academic, New York, NY, pp 411–468CrossRefGoogle Scholar
  60. Fernandez JRR, Höfle U, Mateo R, de Francisco ON, Abbott R, Acevedo P, Blanco JM (2011) Assessment of lead exposure in Spanish imperial eagle (Aquila adalberti) from spent ammunition in central Spain. Ecotoxicology 20:670–681CrossRefGoogle Scholar
  61. Finkelstein ME, Gwiazda RH, Smith DR (2003) Lead poisoning of seabirds: environmental risks from leaded paint at a decommissioned military base. Environ Sci Technol 37:3256–3260CrossRefGoogle Scholar
  62. Finkelstein ME, George D, Scherbinski S, Gwiazda R, Johnson M, Burnett J, Brandt J, Lawrey S, Pessier AP, Clark M (2010) Feather lead concentrations and 207Pb/206Pb ratios reveal lead exposure history of California condors (Gymnogyps californianus). Environ Sci Technol 44:2639–2647CrossRefGoogle Scholar
  63. Finkelstein ME, Doak DF, George D, Burnett J, Brandt J, Church M, Grantham J, Smith DR (2012) From the cover: lead poisoning and the deceptive recovery of the critically endangered California condor. Proc Natl Acad Sci U S A 109:11449–11454CrossRefGoogle Scholar
  64. Finley MT, Dieter MP (1978) Erythrocyte δ-aminolevulinic acid dehydratase activity in mallard ducks: duration of inhibition after lead shot dosage. J Wildl Manage 42:621–625CrossRefGoogle Scholar
  65. Finley MT, Dieter MP, Locke LN (1976) δ-Aminolevulinic acid dehydratase: inhibition in ducks dosed with lead shot. Environ Res 12:243–249CrossRefGoogle Scholar
  66. Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131:421–432CrossRefGoogle Scholar
  67. Franson JC, Hereford SG (1994) Lead poisoning in a Mississippi sandhill crane. Wilson Bull 106:766–768Google Scholar
  68. Franson JC, Pain D (2011) Lead in birds. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota, interpreting tissue concentrations, 2nd edn. Taylor & Francis Group LLC, Boca Raton, FL, pp 563–593CrossRefGoogle Scholar
  69. Franson JC, Russell RE (2014) Lead and eagles: demographic and pathological characteristics of poisoning, and exposure levels associated with other causes of mortality. Ecotoxicology 23:1722–1731CrossRefGoogle Scholar
  70. Franson JC, Sileo L, Pattee OH, Moore JF (1983) Effects of chronic dietary lead in American kestrels (Falco sparverius). J Wildl Dis 19:110–113CrossRefGoogle Scholar
  71. Franson JC, Haramis G, Perry MC, Moore JF (1986) Blood protoporphyrin for detecting lead exposure in canvasbacks. Final report. Lead poisoning in wild waterfowl – a workshop, National Wildlife Federation, Washington, DC, pp 32–37Google Scholar
  72. Franson JC, Hohman WL, Moore JL, Smith MR (1996) The efficacy of protoporphyrin as a predictive biomarker for lead exposure in canvasback ducks: effect of sample storage time. Environ Monit Assess 43:181–188CrossRefGoogle Scholar
  73. Franson JC, Hollmén T, Poppenga RH, Hario M, Kilpi M (2000) Metals and trace elements in tissues of common eiders (Somateria mollissima) from the Finnish Archipelago. Ornis Fennica 77:57–63Google Scholar
  74. Franson JC, Lahner LL, Meteyer CU, Rattner BA (2012) Copper pellets simulating oral exposure to copper ammunition: absence of toxicity in American kestrels (Falco sparverius). Arch Environ Contam Toxicol 62:145–153CrossRefGoogle Scholar
  75. Fry M, Sorenson K, Grantham J, Burnett J, Brandt J, Koenig M (2009) Lead intoxication kinetics in condors from California. Abstract. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID, doi:10.4080/ilsa.2009.0301Google Scholar
  76. Gangoso L, Álvarez-Lloret P, Rodríguez-Navarro AAB, Mateo R, Hiraldo F, Donázar JA (2009) Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environ Pollut 157:569–574CrossRefGoogle Scholar
  77. Gasparik J, Venglarcik J, Slamecka J, Kropil R, Smehyl P, Kopecky J (2012) Distribution of lead in selected organs and its effect on reproduction parameters of pheasants (Phasianus colchicus) after an experimental per oral administration. J Environ Sci Health A 49:1267–1271CrossRefGoogle Scholar
  78. Gerrard JM, Gerrard RN, Bortolotti GR, Dzus EH (1992) A 24-year study of bald eagles on Besnard Lake, Saskatchewan. J Raptor Res 26:159–166Google Scholar
  79. Goede AA, De Bruin M (1986) The use of bird feathers for indicating heavy metal pollution. Environ Monit Assess 7:249–256CrossRefGoogle Scholar
  80. Goede AA, de Voogt P (1985) Lead and cadmium in waders from the Dutch Wadden Sea. Environ Pollut Ser A Ecol Biol 37:311–322CrossRefGoogle Scholar
  81. Golden NH, Rattner BA (2003) Ranking terrestrial vertebrate species for utility in biomonitoring and vulnerability to environmental contaminants. Rev Environ Contam Toxicol 176:67–136Google Scholar
  82. Golden NH, Rattner BA, Cohen JB, Hoffman DJ, Ottinger MA (2003) Lead accumulation in feathers of nestling black-crowned night-herons (Nycticorax nycticorax) experimentally treated in the field. Environ Toxicol Chem 22:1517–1524CrossRefGoogle Scholar
  83. Gómez-Ramírez P, Martínez-López E, María-Mojica P, León-Ortega M, García-Fernández AJ (2010) Blood lead levels and δ-ALAD inhibition in nestlings of Eurasian eagle owl (Bubo bubo) to assess lead exposure associated to an abandoned mining area. Ecotoxicology 20:131–138CrossRefGoogle Scholar
  84. Goyer RA, Clarkson TW (2001) Toxic effects of metals. In: Klaassen CD (ed) Casarett and Doull’s toxicology: the basic science of poisons. McGraw-Hill, New York, NY, pp 811–868Google Scholar
  85. Grand JB, Franson JC, Flint PL, Petersen MR (2002) Concentrations of trace elements in eggs and blood of spectacled and common eiders on the Yukon-Kuskokwim Delta, Alaska, USA. Environ Toxicol Chem 21:1673–1678Google Scholar
  86. Grasman KA, Scanlon PF (1995) Effects of acute lead ingestion and diet on antibody and T-cell-mediated immunity in Japanese quail. Arch Environ Contam Toxicol 28:161–167Google Scholar
  87. Green RE, Newton I, Shultz S, Cunningham AA, Gilbert M, Pain DJ, Prakash V (2004) Diclofenac poisoning as a cause of vulture population declines across the Indian subcontinent. J Appl Ecol 41:793–800CrossRefGoogle Scholar
  88. Griffin CR, Baskett TS, Sparrowe RD (1980) Bald eagles and the management program at Swan Lake National Wildlife Refuge. Trans 45th N Am Wildl Nat Resour Conf 45:253–262Google Scholar
  89. Grinnell GB (1894) Lead-poisoning. Forest Stream 42:117–118Google Scholar
  90. Grue CE, Hoffman DJ, Beyer WN, Franson LP (1986) Lead concentrations and reproductive success in European starlings (Sturnus vulgaris) nesting within highway roadside verges. Environ Pollut Ser A Ecol Biol 42:157–182CrossRefGoogle Scholar
  91. Grund MD, Cornicelli L, Carlson LT, Butler EA (2010) Bullet fragmentation and lead deposition in white-tailed deer and domestic sheep. Hum Wildl Interact 4:257–265Google Scholar
  92. Hahn E, Hahn K, Stoeppler M (1993) Bird feathers as bioindicators in areas of the German Environmental Specimen Bank—bioaccumulation of mercury in food chains and exogenous deposition of atmospheric pollution with lead and cadmium. Sci Total Environ 140:259–270CrossRefGoogle Scholar
  93. Haig SM, D’Elia J, Eagles-Smith C, Fair JM, Gervais J, Herring G, Rivers JW, Schulz JH (2014) The persistent problem of lead poisoning in birds from ammunition and fishing tackle. Condor 116:408–428CrossRefGoogle Scholar
  94. Hansen JA, Audet D, Spears BL, Healy KA, Brazzle RE, Hoffman DJ, Dailey A, Beyer WN (2011) Lead exposure and poisoning of songbirds using the Coeur d’Alene River Basin, Idaho, USA. Integr Environ Assess Manag 7:587–595CrossRefGoogle Scholar
  95. Harmata AR (2011) Environmental contaminants in tissues of bald eagles sampled in southwestern Montana, 2006–2008. J Raptor Res 45:119–135CrossRefGoogle Scholar
  96. Harmata AR, Restani M (2013) Lead, mercury, selenium, and other trace elements in tissues of golden eagles from southwestern Montana, USA. J Wildl Dis 49:114–124CrossRefGoogle Scholar
  97. Harper RG, Scott D, Dunstan TC (1988) Nonfish prey of wintering bald eagles in Illinois. Wilson Bull 100:688–690Google Scholar
  98. Harris MC, Sleeman JM (2007) Morbidity and mortality of bald eagles (Haliaeetus leucocephalus) and peregrine falcons (Falco peregrinus) admitted to the Wildlife Center of Virginia, 1993–2003. J Zoo Wildl Med 38:62–66CrossRefGoogle Scholar
  99. Helander B, Axelsson J, Borg H, Holm K, Bignert A (2009) Ingestion of lead from ammunition and lead concentrations in white-tailed sea eagles (Haliaeetus albicilla) in Sweden. Sci Total Environ 407:5555–5563CrossRefGoogle Scholar
  100. Henderson BM, Winterfield RW (1975) Acute copper toxicosis in the Canada goose. Avian Dis 19:385–387CrossRefGoogle Scholar
  101. Henny CJ, Blus LJ, Hoffman DJ, Grove RA, Hatfield JS (1991) Lead accumulation and osprey production near a mining site on the Coeur d’Alene river, Idaho. Arch Environ Contam Toxicol 21:415–424CrossRefGoogle Scholar
  102. Henny CJ, Blus LJ, Hoffman DJ, Grove RA (1994) Lead in hawks, falcons and owls downstream from a mining site on the Coeur d’Alene river, Idaho. Environ Monit Assess 29:267–288Google Scholar
  103. Hoffman DJ, Pattee OH, Wiemeyer SN, Mulhern B (1981) Effects of lead shot ingestion on δ-aminolevulinic acid dehydratase activity, hemoglobin concentrations, and serum chemistry in bald eagles. J Wildl Dis 17:423–431CrossRefGoogle Scholar
  104. Hoffman DJ, Franson JC, Pattee OH, Bunck CM, Anderson A (1985) Survival, growth, and accumulation of ingested lead in nestling American kestrels (Falco sparverius). Arch Environ Contam Toxicol 14:89–94CrossRefGoogle Scholar
  105. Hollmén T, Franson JC, Poppenga RH, Hario M, Kilpi M (1998) Lead poisoning and trace elements in common eiders (Somateria mollissima) from Finland. Wildl Biol 4:193–203Google Scholar
  106. Hough E (1894) Lead-poisoned ducks. Forest Stream 42:117–118Google Scholar
  107. Hunt WG (2012) Implications of sublethal lead exposure in avian scavengers. J Raptor Res 46:389–393CrossRefGoogle Scholar
  108. Hunt WG, Burnham W, Parish CN, Burnham KK, Mutch B, Oaks JL (2006) Bullet fragments in deer remains: Implications for lead exposure in avian scavengers. Wildl Soc Bull 34:167–170CrossRefGoogle Scholar
  109. Hunt WG, Parish CN, Farry SC, Lord TG, Sieg R (2007) Movements of introduced California condors in Arizona in relations to lead exposure. In: Mee A, Hall L (eds) California condors in the 21st Century. Series in Ornithology No. 2, Nuttall Ornithological Club and the American Ornithologists’ Union, pp 79–96Google Scholar
  110. Hunt WG, Watson RT, Oaks JL, Parish CN, Burnham KK, Tucker RL, Belthoff JR, Hart G (2009) Lead bullet fragments in venison from rifle-killed deer: potential for human dietary exposure. PLoS One 4, e5330. doi: 10.1371/J.pone.0005330 CrossRefGoogle Scholar
  111. Iqbal S, Blumenthal W, Kennedy C, Yip FY, Pickard S, Flanders WD, Loringer K, Kruger K, Caldwell KL, Jean Brown M (2009) Hunting with lead: association between blood lead levels and wild game consumption. Environ Res 109:952–959CrossRefGoogle Scholar
  112. Irby HD, Locke LN, Bagley GE (1967) Relative toxicity of lead and selected substitute shot types to game farm mallards. J Wildl Manage 31:253–257CrossRefGoogle Scholar
  113. Jackson AJ, Ruxton GD, Houston DC (2008) The effect of social facilitation on foraging success in vultures: a modeling study. Biol Lett 4:311–313CrossRefGoogle Scholar
  114. Jacobson E, Carpenter JW, Novilla M (1977) Suspected lead toxicosis in a bald eagle. J Am Vet Med Assoc 171:952–954Google Scholar
  115. Johnson CK, Kelly TR, Rideout BA (2013) Lead in ammunition: a persistent threat to health and conservation. Ecohealth 10:455–464CrossRefGoogle Scholar
  116. Jordan JS, Bellrose FC (1951) Lead poisoning in wild waterfowl. Illinois National History Survey, Biological notes no. 26, Urbana, IL. https://www.ideals.illinois.edu/handle/2142/17294
  117. Kelly TR, Johnson CK (2011) Lead exposure in free-flying turkey vultures is associated with big game hunting in California. PLoS One 6, e15350CrossRefGoogle Scholar
  118. Kelly A, Kelly S (2005) Are mute swans with elevated blood lead levels more likely to collide with overhead power lines? Waterbirds 28:331–334CrossRefGoogle Scholar
  119. Kelly ME, Fitzgerald SD, Aulerich RJ, Balander RJ, Powell DC, Stickle RL, Stevens W, Cray C, Tempelman RJ, Bursian SJ (1998) Acute effects of lead, steel, tungsten, iron, and tungsten-polymer shot administered to game farm mallards. J Wildl Dis 34:673–687CrossRefGoogle Scholar
  120. Kelly TR, Bloom PH, Torres SG, Hernandez YZ, Poppenga RH, Boyce WM, Johnson CK (2011) Impact of the California lead ammunition ban on reducing lead exposure in golden eagles and turkey vultures. PLoS One 6, e17656CrossRefGoogle Scholar
  121. Kelly TR, Poppenga RH, Woods LA, Hernandez YZ, Boyce WM, Samaniego FJ, Torres SG, Johnson CK (2014a) Causes of mortality and unintentional poisoning in predatory and scavenging birds in California. Vet Rec 2014:e000028. P 1–9Google Scholar
  122. Kelly TR, Grantham J, George D, Welch A, Brandt J, Burnett LJ, Sorenson KJ, Johnson MW, Poppenga R, Moen D, Rasico J, Rivers JW, Battistone C, Johnson CE (2014b) Spatiotemporal patterns and risk factors for lead exposure in endangered California condors during 15 years of reintroduction. Conserv Biol 28:1721–1730Google Scholar
  123. Kendall RJ, Scanlon PF (1981) Effects of chronic lead ingestion on the reproductive characteristics of ringed turtle doves Streptopelia risoria and on tissue lead concentrations of adults and their progeny. Environ Pollut Ser A Ecol Biol 26:203–213CrossRefGoogle Scholar
  124. Kennedy S, Crisler JP, Smith E, Bush M (1977) Lead poisoning in sandhill cranes. J Am Vet Med Assoc 171:955–958Google Scholar
  125. Kenntner N, Tataruch F, Krone O (2001) Heavy metals in soft tissue of white-tailed eagles found dead or moribund in Germany and Austria from 1993 to 2000. Environ Toxicol Chem 20:1831–1837CrossRefGoogle Scholar
  126. Kirk DA, Mossman MJ (1998) Turkey vulture (Cathartes aura), the birds of North America Online, Poole A (ed) Cornell Lab of Ornithology, Ithaca. http://bna.birds.cornell.edu/bna/species/339. Accessed 15 May 2014
  127. Knopper LD, Mineau P, Scheuhammer AM, Bond DE, McKinnon DT (2006) Carcasses of shot Richardson’s ground squirrels may pose lead hazards to scavenging hawks. J Wildl Manage 70:295–299CrossRefGoogle Scholar
  128. Knott J, Gilbert J, Hoccom DG, Green RE (2010) Implications for wildlife and humans of dietary exposure to lead from fragments of lead rifle bullets in deer shot in the UK. Sci Total Environ 409:95–99CrossRefGoogle Scholar
  129. Kobayashi Y, Shimada A, Umemura T, Nagai T (1992) An outbreak of copper poisoning in mute swans (Cygnus olor). Jpn Vet Med Sci 54:229–233CrossRefGoogle Scholar
  130. Kochert MN, Steenhof K, Mcintyre CL, Craig EH (2002) Golden Eagle (Aquila chrysaetos), the birds of North America online, Poole A (ed) Cornell Lab of Ornithology, Ithaca. http://bna.birds.cornell.edu/bna/species/684. Accessed 15 May 2014
  131. Komosa A, Kitowski I (2008) Elevated lead concentration in skeletons of diurnal birds of prey Falconioformes and owls Strigiformes from eastern Poland—ecological approach and review. Ecol Chem Eng S 15:349–358Google Scholar
  132. Koranda J, Moore K, Stuart M, Conrado C (1979) Dietary effects of lead uptake and trace element distribution in mallard ducks dosed with lean shot. Lawrence Livermore Laboratory Report, Livermore CA 39 pp.Google Scholar
  133. Kramer JL, Redig PT (1997) Sixteen years of lead poisoning in eagles, 1980–95: an epizootiologic view. J Raptor Res 31:327–332Google Scholar
  134. Krementz DG, Ankney CD (1995) Changes in total body calcium and diet of breeding house sparrows. J Avian Biol 26:162–167CrossRefGoogle Scholar
  135. Krone O, Kenntner N, Trinogga A, Nadjafzadeh M, Scholz F, Sulawa J, Totschek K, Schuck-wersig P, Zieschank R (2009) Lead poisoning in white-tailed sea eagles: causes and approaches to solutions in Germany. In: Watson RT, Fuller M, Pokras M, Hunt G (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID, pp 1–13, https://www.peregrinefund.org/subsites/conference-lead/PDF/0207%20Krone.pdf Google Scholar
  136. Lambertucci SA, Donázar JA, Huertas AD, Jiménez B, Sáez M, Sanchez-Zapata JA, Hiraldo F (2011) Widening the problem of lead poisoning to a South-American top scavenger: lead concentrations in feathers of wild Andean condors. Biol Conserv 144:1464–1471CrossRefGoogle Scholar
  137. Lang AL, Andress RA, Martin PA (2001) Prey remains in bald eagle (Haliaeetus leucocephalus) pellets from a winter roost in the Upper St. Lawrence River, 1996–1997. Wildl Med 24:21–26Google Scholar
  138. Langelier KM, Andress CE, Grey TK, Wooldridge C, Lewis R, Marchetti R (1991) Lead poisoning in bald eagles in British Columbia. Can Vet J 32:108Google Scholar
  139. Langner HW, Domenach R, Slabe VA, Sullivan SP (2015) Lead and mercury in fall migrant golden eagles from western North America. Arch Environ Contam Toxicol 69:54–61CrossRefGoogle Scholar
  140. Leonzio C, Massi A (1989) Metal biomontoring in bird eggs: a critical experiment. Bull Environ Contam Toxicol 43:401–406CrossRefGoogle Scholar
  141. Locke LN, Bagley GE (1967) Lead poisoning in a sample of Maryland mourning doves. J Wildl Manage 31:515–518CrossRefGoogle Scholar
  142. Locke LN, Thomas NJ (1996) Lead poisoning of waterfowl and raptors. In: Fairbrother A, Locke LN, Huff GL (eds) Noninfectious disease of wildlife, 2nd edn. Iowa State University Press, Ames, IA, pp 108–117Google Scholar
  143. Locke LN, Bagley GE, Irby HD (1966) Acid-fast intranuclear inclusion bodies in the kidneys of mallards fed lead shot. Bull Wildl Dis Assoc 2:127–132CrossRefGoogle Scholar
  144. Locke LN, Irby HD, Bagley GE (1967) Histopathology of mallards dosed with lead and selected substitute shot. J Wildl Dis 3:143–147CrossRefGoogle Scholar
  145. Mateo R, Cadenas R, Manez M, Guitart R (2001) Lead shot ingestion in two raptor species from Doñana, Spain. Ecotoxicol Environ Saf 48:6–10CrossRefGoogle Scholar
  146. Mazliah J, Barron S, Bental E, Reznik I (1989) The effects of chronic lead intoxication in mature chickens. Avian Dis 33:566–570CrossRefGoogle Scholar
  147. McBride TJ, Smith JP, Gross HP, Hopper MJ (2004) Blood-lead and ALAD activity levels of cooper’s hawks (Accipiter cooperii) migrating through the southern Rocky Mountains. J Raptor Res 38:118–124Google Scholar
  148. Mee A, Rideout BA, Hamber JA, Todd JN, Austin G, Clark M, Wallace MP (2007) Junk ingestion and nestling mortality in a reintroduced population of California condors, Gymnogyps californianus. Bird Conserv Int 17:119–130CrossRefGoogle Scholar
  149. Merendino MT, Lobpries DS, Neaville JE, Ortego JD, Johnson WP (2013) Regional differences and long-term trends in lead exposure in mottled ducks. Wildl Soc Bull 33:1002–1008CrossRefGoogle Scholar
  150. Meretsky VJ, Snyder NFR (1992) Range use and movements of California Condors. Condor 94:313–335CrossRefGoogle Scholar
  151. Mierzykowski SE, Todd CS, Pokras MA, Oliveira RD (2013) Lead and mercury levels in livers of bald eagles recovered in New England. Final report. U.S. Fish and Wildlife Service, U.S. Department of Interior, Special Project Report FY13‐MEFO‐2‐EC. http://www.fws.gov/northeast/mainecontaminants/pdf/PbHg_BAEA_LiversNewEngland2013.pdf
  152. Miller MJ, Restani M, Harmata AR, Bortolotti GR, Wayland ME (1998) A comparison of blood lead levels in bald eagles from two regions on the great plains of North America. J Wildl Dis 34:704–714CrossRefGoogle Scholar
  153. Miller MJR, Wayland ME, Dzus EH, Bortolotti GR (2000) Availability and ingestion of lead shotshell pellets by migrant bald eagles in Saskatchewan. J Raptor Res 34:167–174Google Scholar
  154. Miller MJR, Wayland ME, Bortolotti GR (2001a) Exposure of migrant bald eagles to lead in prairie Canada. Environ Pollut 112:153–162CrossRefGoogle Scholar
  155. Miller MJ, Wayland ME, Bortolotti GR (2001b) Hemograms for and nutritional condition of migrant bald eagles tested for exposure to lead. J Wildl Dis 37:481–488CrossRefGoogle Scholar
  156. Millsap BA (1986) Status of wintering bald eagles in the conterminous 48 states. Wildl Soc Bull 14:433–440Google Scholar
  157. Molnar JJ (1983) Copper storage in the liver of the wildlife mute swan (Cygnus olor). Its possible relation to pollution. Arch Pathol 107:629–632Google Scholar
  158. Mora MA (2003) Heavy metals and metalloids in egg contents and eggshells of passerine birds from Arizona. Environ Pollut 125:393–400CrossRefGoogle Scholar
  159. Morgan GW, Edens FW, Thaxton P, Parkhurst CR (1975) Toxicity of dietary lead in Japanese quail. Poul Sci 54:1636–1642CrossRefGoogle Scholar
  160. Morrison JL, Dwyer JF (2012) Crested Caracara (Caracara cheriway), the birds of North America online, Poole A (ed) Cornell Lab of Ornithology, Ithaca. http://bna.birds.cornell.edu/bna/species/249. Accessed 15 May 2014
  161. Moulton DW, Frentress CD, Stutzenbaker CD, Lobpries DS, Brownlee WC (1988) Ingestion of shotgun pellets by waterfowl in Texas. In: Weller M (ed) Waterfowl in winter. University of Minnesota Press, Minneapolis, MN, pp 597–607Google Scholar
  162. Nadjafzadeh M, Hofer H, Krone O (2013) The link between feeding ecology and lead poisoning in white‐tailed eagles. J Wildl Manage 77:48–57CrossRefGoogle Scholar
  163. Nain S, Smits JEG (2011) Subchronic lead exposure, immunotoxicology and increased disease resistance in Japanese quail (Corturnix coturnix japonica). Ecotoxicol Environ Saf 74:787–792CrossRefGoogle Scholar
  164. Nam DH, Lee DP (2009) Abnormal lead exposure in globally threatened Cinereous vultures (Aegypius monachus) wintering in South Korea. Ecotoxicology 18:225–229CrossRefGoogle Scholar
  165. Nam DH, Rutkiewicz J, Basu N (2011) Multiple metals exposure and neurotoxic risk in bald eagles (Haliaeetus leucocephalus) from two Great Lakes states. Environ Monit Assess 95:13–22CrossRefGoogle Scholar
  166. Nelson TA, Mitchell C, Abbott C (1989) Lead-shot ingestion by bald eagles in western Arkansas. Southwest Nat 34:245–249CrossRefGoogle Scholar
  167. Neumann K (2009) Bald eagle lead poisoning in winter. In: Watson RT, Fuller M, Pokras M, Hunt G (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID, pp 210–218, http://www.huntingwithnonlead.org/PDFs_Main/Bald%20Eagle%20Lead%20Poisoning%20in%20Winter.pdf Google Scholar
  168. Nixon CM, Hansen LP, Brewer PA, Chelsvig JE, Esker TL, Etter D, Sullivan JB, Koerkenmeier RG, Mankin PC (2001) Survival of white-tailed deer in intensively farmed areas of Illinois. Can J Zool 79:581–588CrossRefGoogle Scholar
  169. Norheim G, Borch-Iohnsen B (1990) Chemical and morphological studies of liver from eider (Somateria mollissima) in Svalbard with special reference to the distribution of copper. J Comp Pathol 102:457–466CrossRefGoogle Scholar
  170. O’Halloran J, Myers AA, Duggan PF (1989) Some sub-lethal effects of lead on mute swan Cygnus olor. J Zool 218:627–632CrossRefGoogle Scholar
  171. Ochiai K, Jin K, Itakura C, Goryo M, Yamashita K, Mizuno N, Fujinaga T, Tsuzuki T (1992) Pathological study of lead poisoning in whooper swans (Cygnus cygnus) in Japan. Avian Dis 36:313–323CrossRefGoogle Scholar
  172. Onalaja AO, Claudio L (2000) Genetic susceptibility to lead poisoning. Environ Health Perspect 108:23–28CrossRefGoogle Scholar
  173. Pagel JE, Sharpe PB, Garcelon DK, Little AE, Taylor SK, Faulkner KR, Gorbics CS (2012) Exposure of bald eagles to lead on the northern Channel Islands, California. J Raptor Res 46:168–176CrossRefGoogle Scholar
  174. Pain DJ, Rattner BA (1988) Mortality and hematology associated with the ingestion of one number four lead shot in black ducks, Anas rubripes. Bull Environ Contam Toxicol 40:159–164CrossRefGoogle Scholar
  175. Pain D, Fisher IJ, Thomas VG (2009) A global update of lead poisoning in terrestrial birds from ammunition sources. In: Watson RT, Fuller M, Pokras M, Hunt G (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID, pp 99–118, https://www.peregrinefund.org/subsites/conference-lead/PDF/0108%20Pain.pdf Google Scholar
  176. Parish CN, Hunt WG, Feltes E, Seig R, Orr K (2009) Lead exposure among reintroduced population of California condors in northern Arizona and southern Utah. In: Watson RT, Fuller M, Pokras M, Hunt G (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID, pp 259–264, https://www.peregrinefund.org/subsites/conference-lead/PDF/0217%20Parish.pdf Google Scholar
  177. Pattee OH, Hennes SK (1983) Bald eagles and waterfowl: the lead shot connection. Trans 48th N Am Wildl Nat Resour Conf 48:230–237Google Scholar
  178. Pattee OH, Wiemeyer SN, Mulhern BM, Sileo L, Carpenter JW (1981) Experimental lead-shot poisoning in bald eagles. J Wildl Manage 45:806–810CrossRefGoogle Scholar
  179. Pattee OH, Carpenter JW, Fritts SH, Rattner BA, Wiemeyer SN, Royle JA, Smith MR (2006) Lead poisoning in captive Andean condors (Vultur gryphus). J Wildl Dis 42:772–779CrossRefGoogle Scholar
  180. Pauli JN, Buskirk SW (2007) Recreational shooting of prairie dogs: a portal for lead entering wildlife food chains. J Wildl Manage 71:103–108CrossRefGoogle Scholar
  181. Peraza MA, Ayala-Fierro F, Barber DS, Caserez E, Rael LT (1998) Effects of micronutrients on metal toxicity. Environ Health Perspect 106(Suppl 1):203–216CrossRefGoogle Scholar
  182. Peterson CA, Lee SL, Elliott JE (2001) Scavenging of waterfowl carcasses by birds in agricultural fields of British Columbia. J Field Ornithol 72:150–159CrossRefGoogle Scholar
  183. Prosser P, Nattrass C, Prosser C (2008) Rate of removal of bird carcasses in arable farmland by predators and scavengers. Ecotoxicol Environ Saf 71:601–608CrossRefGoogle Scholar
  184. Quarterman J (1986) Lead. In: Mertz W (ed) Trace elements in human and animal nutrition, vol 2, 5th edn. Academic, New York, NY, pp 281–317CrossRefGoogle Scholar
  185. Quortrup ER, Shillinger JE (1941) 3,000 Wild bird autopsies on western lake areas. J Am Vet Med Assoc 99:382–387Google Scholar
  186. Rabinowitz MB, Hall GS (2002) Isotopic characterization of six major brands of white basic lead carbonate paint pigments. Bull Environ Contam Toxicol 69:617–623CrossRefGoogle Scholar
  187. Rattner BA, Morehouse KA (1994) Ecological tiered testing protocol proposed for registration of shot used to hunt waterfowl. Proceedings of the fifteenth annual meeting of the society of environmental toxicology and chemistry. Abstract 90Google Scholar
  188. Rattner BA, Franson JC, Sheffield SR, Goddard CI, Leonard NJ, Stang D, Wingate PJ (2008) Sources and implications of lead ammunition and fishing tackle on natural resources. Wildlife society technical review 08-01. The Wildlife Society, Bethesda, MD, p 62Google Scholar
  189. Redig PT, Lawler EM, Schwartz S, Dunnette JL, Stephenson B, Duke GE (1991) Effects of chronic exposure to sublethal concentrations of lead acetate on heme synthesis and immune function in red-tailed hawks. Arch Environ Contam Toxicol 21:72–77CrossRefGoogle Scholar
  190. Rideout BA, Stalis I, Papendick R, Pesser A, Puschner B, Finkelstein ME, Smith DR, Johnson M, Mace M, Stroud R, Brandt J, Burnett J, Parish C, Petterson J, Witte C, Stringfield C, Orr K, Zuba J, Wallace M, Grantham J (2012) Patterns of mortality in free-ranging California condors (Gymnogyps californianus). J Wildl Dis 48:95–112CrossRefGoogle Scholar
  191. Ringelman JK, Miller MW, Andelt WF (1993) Effects of ingested tungsten-bismuth-tin shot on captive mallards. J Wildl Manage 57:725–732CrossRefGoogle Scholar
  192. Risebrough RW (2001) Absence of demonstrable toxicity to turkey vultures. Cathartes aura of copper and tungsten-tin-bismith-composite pellets. Final report. U.S. Fish and Wildlife Service, California Condor Recovery Program, Ventura, CAGoogle Scholar
  193. Rocke TE, Samuel MD (1991) Effects of lead shot ingestion on selected cells of the mallard immune system. J Wildl Dis 27:1–9CrossRefGoogle Scholar
  194. Roscoe DE, Nielsen SW, Lamola AA, Zuckerman D (1979) A simple quantitative test for erythrocytic protoporphyrin in lead-poisoned ducks. J Wildl Dis 15:127–136CrossRefGoogle Scholar
  195. Roscoe DE, Widjeskog L, Stansley W (1989) Lead poisoning of northern pintail ducks feeding in a tidal meadow contaminated with shot from a trap and skeet range. Bull Environ Contam Toxicol 42:226–233CrossRefGoogle Scholar
  196. Russell RE, Franson JC (2014) Causes of mortality in eagles submitted to the National Wildlife Health Center 1975–2013. Wildl Soc Bull 38:697–704CrossRefGoogle Scholar
  197. Samuel MD, Bowers EF (2000) Lead exposure in American black ducks after implementation of non-toxic shot. J Wildl Manage 64:947–953CrossRefGoogle Scholar
  198. Samuel MD, Bowers EF, Franson JC (1992) Lead exposure and recovery rates of black ducks banded in Tennessee. J Wildl Dis 28:555–561CrossRefGoogle Scholar
  199. Sanderson GC (1992) Lead poisoning mortality. In: Pain DJ (ed) Lead poisoning in waterfowl, proceedings of an IWRB workshop, Brussels, Belgium, 13–15 June, pp 14–18Google Scholar
  200. Sanderson GC, Bellrose FC (1986) Review of the problem of lead poisoning in waterfowl. Special publication. Natural History Survey, Champaign, ILGoogle Scholar
  201. Sanderson GC, Anderson WL, Foley GL, Skowron LM, Brawn JD, Seets JW (1997) Acute toxicity of ingested bismuth alloy shot in game-farm mallards. Ill Nat Hist Surv Bull 35:183–215Google Scholar
  202. Schempf PE (1997) Bald eagle longevity record from southeastern Alaska. J Field Ornithol 68:150–151Google Scholar
  203. Scheuhammer AM (1987) The chronic toxicity of aluminum, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295CrossRefGoogle Scholar
  204. Scheuhammer AM (1996) Influence of reduced dietary calcium on the accumulation and effects of lead, cadmium, and aluminum in birds. Environ Pollut 94:337–343CrossRefGoogle Scholar
  205. Scheuhammer AM, Norris SL (1996) The ecotoxicology of lead shot and lead fishing weights. Ecotoxicol 5:279-295Google Scholar
  206. Scheuhammer AM, Templeton DM (1998) Use of stable isotope ratios to distinguish sources of lead exposure in wild birds. Ecotoxicology 7:37–42CrossRefGoogle Scholar
  207. Scheuhammer AM, Thomas VG (2011) Eliminating lead from recreational shooting and angling: Relating wildlife science to environmental policy and regulation in North America. In: Elliott JE et al (eds) Wildlife ecotoxicology. Springer, New York, NY, pp 359–382CrossRefGoogle Scholar
  208. Scheuhammer AM, Money SL Kirk DA, Donaldson G (2003) Lead fishing sinkers and jigs in Canada: review of their use patterns and toxic impacts on wildlife. Can Wild Serv Occas Paper 108, Environment Canada, Ottawa, Canada 48 ppGoogle Scholar
  209. Schulz JH, Millspaugh JJ, Bermudez AJ, Gao X, Bonnot TW, Britt LG, Paine M (2006) Acute lead toxicosis in mourning doves. J Wildl Manage 70:413–421CrossRefGoogle Scholar
  210. Shillinger JE, Cottam CC (1937) The importance of lead poisoning in waterfowl. Division of Wildlife Resource, Bureau of Biological Survey. American Wildlife Institute. Transactions of the second North American wildlife conference, Jefferson, St. Louis, MIGoogle Scholar
  211. Sileo L, Fefer SI (1987) Paint chip poisoning of Laysan albatross at Midway Atoll. J Wildl Dis 23:432–437CrossRefGoogle Scholar
  212. Sileo LH, Creekmore DJ, Audet L (2001) Lead poisoning of waterfowl by contaminated sediment in the Coeur d’Alene River. Arch Environ Contam Toxicol 41:364–368CrossRefGoogle Scholar
  213. Simpson VR, Hunt AE, French MC (1979) Chronic lead poisoning in a heard of mute swans. Environ Pollut 18:187–202CrossRefGoogle Scholar
  214. Snyder NF, Schmitt NJ (2002) California Condor (Gymnogyps californianus), the birds of North America online, Poole A (ed) Cornell Lab of Ornithology, Ithaca. http://bna.birds.cornell.edu/bna/species/610. doi: 10.2173/bna.610#_blank. Accessed 3 Jun 2015
  215. Snyder NFR, Ramey RR, Sibley FC (1986) Nest site biology of the California condor. Condor 88:228–241CrossRefGoogle Scholar
  216. Snyder NFR, Johnson EV, Clenden DA (1987) Primary molt of California condors. Condor 89:468–485CrossRefGoogle Scholar
  217. Stansley W, Murphy LA (2011) Liver lead concentrations in raptors in New Jersey, USA, 2009–2010. Bull Environ Contam Toxicol 87:171–174CrossRefGoogle Scholar
  218. Stauber E, Finch N, Talcott PA, Gay JM (2010) Lead poisoning of bald (Haliaeetus leucocephalus) and golden (Aquila chrysaetos) eagles in the U.S. inland Pacific/Northwest – an 18 year retrospective study 1991–2008. J Avian Med Surg 24:279–287CrossRefGoogle Scholar
  219. Steenhof KL, Bond K, Bates K, Leppert LL (2002) Trends in midwinter counts of bald eagles in the contiguous United States, 1986–2000. Bird Popul 6:21–32Google Scholar
  220. Steenhof KL, Bond K, Dunn LL (2008) The midwinter bald eagle survey results and analysis 1986–2005. Final report. U.S. Geological Survey, National Biological Information Infrastructure, and Northwest Alliance for Computational Science and Engineering. http://ocid.nacse.org/nbii/eagles/
  221. Stendell RC, Smith RI, Burnham KP, Christensen RE (1979) Exposure of waterfowl to lead: a nationwide survey of residues in wing bones of seven species, 1972–73. Final report. U.S. Fish Wildlife Service special science report, wildlife no. 223, pp 1–12Google Scholar
  222. Stephens RM, Johnson AS, Plumb RE, Dickerson K, McKinstry MC, Anderson SH (2008) Risk assessment of lead poisoning in raptors caused by recreational shooting of prairie dogs. Intermt J Sci 13:116–123Google Scholar
  223. Stevenson AL, Scheuhammer AM, Chan HM (2005) Effects of nontoxic shot regulation on lead accumulation in ducks and American woodcock in Canada. Arch Environ Contam Toxicol 48:405–413CrossRefGoogle Scholar
  224. Stocek R (2000) Diet of wintering bald eagles, Haliaeetus leucocephalus, in New Brunswick. Can Field Nat 114:605–611Google Scholar
  225. Stormer FA, Kirkpatrick CM, Hoekstra TW (1979) Hunter inflicted wounding of white-tailed deer. Wildl Soc Bull 7:10–16Google Scholar
  226. Stout JH, Trust KA, Cochrane JF, Suydam RS, Quakenbush LT (2002) Environmental contaminants in four eider species from Alaska and arctic Russia. Environ Pollut 119:215–226CrossRefGoogle Scholar
  227. Strom SM, Langenberg JA, Businga NK, Batten JK (2009) Lead exposure in Wisconsin birds. In: Watson RT, Fuller M, Pokras M, Hunt G (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID, pp 194–201, http://dnr.wi.gov/topic/hunt/documents/pbbirds.pdf Google Scholar
  228. Thiboldeaux R (2008) The potential for ingestion exposure to lead fragments in venison in Wisconsin. Final report. Wisconsin Department of Health and Family Services, Madison, WI, pp 1–20Google Scholar
  229. Thomas VG, Guitart R (2013) Transition to non-toxic gunshot in Olympic shooting: Policy implications for IOC and UNEP in resolving and Environ problem. Ambio 42:746–754. doi: 10.1007/s13280-013-0393-7 CrossRefGoogle Scholar
  230. Tranel MA, Kimmel RO (2009) Impacts of lead ammunition on wildlife, the environment, and human health – a literature review and implications for Minnesota. The Peregrine Fund, Boise, ID, pp 318–337, https://www.peregrinefund.org/subsites/conference-lead/PDF/0307%20Tranel.pdf Google Scholar
  231. Trust KA, Miller MW, Ringelman JK, Orme IM (1990) Effects of ingested lead on antibody production in mallards (Anas platyrhynchos). J Wildl Dis 26:316–322CrossRefGoogle Scholar
  232. U.S. Environ Protection Agency (USEPA) (2005) Best management practices for lead at outdoor shooting ranges. EPA, Washington, DC. http://www.epa.gov/region2/waste/leadshot/
  233. U.S. Fish and Wildlife Service (USFWS) (1986) Final supplemental environmental impact statement. Use of lead shot for hunting migratory birds in the United States. U.S. Department of Interior Fish and Wildlife Service. FES 86–16:1–559Google Scholar
  234. U.S. Fish and Wildlife Service (USFWS) (1995) 50 CFR 20 migratory bird hunting. §20.21, page 10, What hunting methods are illegal? pp 1–36Google Scholar
  235. U.S. Fish and Wildlife Service (USFWS) (1996) California condor recovery plan, third revision. U.S. Fish and Wildlife Service (USFWS), Portland, OR, pp 1–62Google Scholar
  236. U.S. Fish and Wildlife Service (USFWS) (1997) Migratory bird hunting: revised test protocol for nontoxic approval procedures for shot and shot coating. Federal Register Vol. 62, No. 230 Monday December 1 1997. 50 CFR Part 20 RIN 1018-AB80. Final Rule. 63608-63610. Washington, DCGoogle Scholar
  237. U.S. Fish and Wildlife Service (USFWS) (1999) Subpart M – criteria and schedule for implementing nontoxic shot zones for the 1987–1988 and subsequent waterfowl hunting seasons. RST 50 CFR 7, 23, 1999, p 32 §20.143. Final Rule. U.S. Fish and Wildlife Service, Washington, DC, pp 31–36Google Scholar
  238. U.S. Fish and Wildlife Service (USFWS) (2006) Deer hunting in the United States: demographics and trends. Addendum to the 2006 National Survey of Fishing, Hunting, and Wildlife Associated Recreation. Report 2006–2010. http://digitalmedia.fws.gov/cdm/ref/collection/document/id/207
  239. U.S. Fish and Wildlife Service (USFWS) (2012) A review of the third five years of the California condor reintroduction program in the southwest (2007–2011). Final report. U.S. Fish and Wildlife Service, Pacific Southwest Office (Region 8), Sacramento, CAGoogle Scholar
  240. U.S. Fish and Wildlife Service (USFWS) (2013a) Non-toxic shot regulations for hunting waterfowl and coots in the U.S. http://www.fws.gov/migratorybirds/currentbirdissues/nontoxic.htm
  241. U.S. Fish and Wildlife Service (USFWS) (2013b) Migratory bird hunting; revisions of language for approval of nontoxic shot for use in waterfowl hunting. Federal Register/Vol. 78, No. 42/Monday, March 4, 2013. 50 CFR Part 20 [Docket No. FWS-R9-MB-2011-0077; FF09M21200-134-FXMB1231099BPP0]. RIN 1018-AY59. Washington, DCGoogle Scholar
  242. U.S. Fish and Wildlife Service (USFWS) (2013c) California condor (Gymnogyps californianus) 5-year review: summary and evaluation. Final report. US Fish and Wildlife Service Pacific Southwest Region, Sacramento, CAGoogle Scholar
  243. Veit HP, Kendall RJ, Scanlon PF (1983) The effect of lead shot ingestion on the testes of adult ringed turtle doves (Streptopelia risoria). Avian Dis 27:442–452CrossRefGoogle Scholar
  244. Verbeek NA, Caffrey C (2002) American crow (Corvus brachyrhynchos), the birds of North America online, Poole A (ed) Cornell Lab of Ornithology, Ithaca. http://bna.birds.cornell.edu/bna/species/647. Accessed 15 May 2014
  245. Vyas NB (1999) Factors influencing estimation of pesticide-related wildlife mortality. Toxicol Ind Health 15:186–191CrossRefGoogle Scholar
  246. Vyas NB, Spann JW, Heinz GH, Beyer WN, Jaquette JA, Mengel-Koch JM (2000) Lead poisoning of passerines at a trap and skeet range. Environ Pollut 107:159–166CrossRefGoogle Scholar
  247. Walters JR, Derrickson SR, Fry DM, Haig SM, John M, Wunderle JM (2008) Status of the California condor and efforts to achieve its recovery. Final report. Prepared by the AOU Committee on Conservation, California Condor Blue Ribbon Panel, A Joint Initiative of The American Ornithologists’ Union and Audubon California. https://wiki.umn.edu/pub/ESPM3241W/S11TopicSummaryTeamSeventeen/AOUreport.pdf
  248. Warner SE, Britton EE, Becker DN, Coffey MJ (2014) Bald eagles lead exposure in the upper Midwest. J Fish Wildl Manag 5:208–216CrossRefGoogle Scholar
  249. Watson JW, Davies RW (2015) Lead, mercury, and DDE in the blood of nesting golden eagles in the Columbia Basin Washington. J Raptor Res 49:217–221CrossRefGoogle Scholar
  250. Wayland M, Neugebauer E, Bollinger T (1999) Concentrations of lead in liver, kidney, and bone of bald and golden eagles. Arch Environ Contam Toxicol 37:267–272CrossRefGoogle Scholar
  251. Wayland M, Wilson LK, Elliott JE, Miller MJR, Bollinger T, McAdie M, Froese JMW (2003) Mortality, morbidity, and lead poisoning of eagles in western Canada, 1986–98. J Raptor Res 37:8–18Google Scholar
  252. Wetmore A (1919) Lead poisoning in waterfowl. Final report No. 793–19. United States Department of Agriculture Bull, Washington, DC, USAGoogle Scholar
  253. Weyers B, Gluck E, Stoeppler M (1988) Investigation of the significance of heavy metal contents of blackbird feathers. Sci Total Environ 77:61–67CrossRefGoogle Scholar
  254. Wiemeyer SN, Scott JM, Anderson MP, Bloom PH, Stafford CJ (1988) Environmental contaminants in California condors. J Wildl Manage 52:238–247CrossRefGoogle Scholar
  255. Wobeser GA (ed) (1997) Diseases of wild waterfowl, 2nd edn. Western College of Veterniary Medicine, University of Saskatchen, Saskatoon, Saskatchewan, Canada. Plenum, New York, NYGoogle Scholar
  256. Work TM, Smith MR (1996) Lead exposure in Laysan albatross adults and chicks in Hawaii: prevalence, risk factors, and biochemical effects. Arch Environ Contam Toxicol 31:115–119CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Nancy H. Golden
    • 1
  • Sarah E. Warner
    • 2
  • Michael J. Coffey
    • 3
  1. 1.U.S. Fish and Wildlife ServiceFalls ChurchUSA
  2. 2.U.S. Fish and Wildlife ServiceMadisonUSA
  3. 3.U.S. Fish and Wildlife ServiceCrab Orchard National Wildlife RefugeMarionUSA

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