Birds of Prey pp 251-272 | Cite as

Lead Poisoning in Birds of Prey

  • Oliver KroneEmail author


Naturally lead (plumbum, Pb) is embedded in the earth’s crust at a concentration of 0.016 g Pb/kg soil, making it a relatively rare metal. From there it is released into the environment by geochemical weathering, igneous processes and radioactive decay (Pattee and Pain 2003). Lead is probably the first metal used by mankind. It was known as opacifier and colourant for glazes and glasses since the fifth millennium B.C. But lead pigment has also been used in cosmetics as long ago as 4000 B.C. due to its softness and low melting point (327.5 °C); it is easily mined and moulded. Formed to coins and figures, lead played an important role in trading more than 4500 years ago in ancient Egypt. As a component of many metallic ores, lead was also considered as a by-product of mining precious metals such as silver. Cooking utensils have been made of lead, and lead piping was the mainstay of the water distribution system in the Roman Empire (Nriagu 1983). Since the Romans did not know sugar, they produced sapa, a syrup made of sweet fruits boiled in lead vessels. Sapa containing lead was used to sweeten drinks and meals. Lead poisoning from all these sources must have been a common disease in ancient Rome. Symptoms included colic, stillbirths, deformities and cases of brain damage. Although controversial (Scarborough 1984), high lead concentrations diagnosed in archaeological Roman bones arguably contributed to the fall of the Roman Empire (Gilfillan 1965). Described in antiquity, lead poisoning was no more mentioned in the literature until the Middle Ages, where it was then mentioned sporadically. Due to the increased use of lead in pottery, piping, shipbuilding, window making, arms industry, pigments and later book printing, lead poisoning reached epidemic dimensions during the period of industrialisation (Hernberg 2000). For millennia the main route of lead exposure was primarily via occupation, but the introduction of leaded paint for residential use in the nineteenth century significantly increased lead accumulation in children (Bellinger 2004). Symptoms in children from lead paint recognised in Australia contributed largely to the understanding of childhood lead poisoning (Henretig 2006). European governments started to ban lead-based paints in the early 1900s, culminating in a ban by the League of Nations in 1922 (Gilbert and Weiss 2006).



I am grateful to I. Rottenberger from the German Institute for Experimentation and Testing of Hunting and Sporting Firearms (DEVA) for providing the cuts through the different bullet types and to R. Cromie from Wildfowl & Wetlands Trust (WWT), UK, for proofreading the manuscript.


  1. Aliyev V, Bozalan M, Guvendik G, Soeylemezoglu T (2011) The potential health risk assessment of lead levels in children’s toys. Toxicol Lett 205(Suppl 1):S255–S255CrossRefGoogle Scholar
  2. Arnemo JM, Andersen O, Stokke S, Thomas VG, Krone O, Pain DJ, Mateo R (2016) Health and environmental risks from lead-based ammunition: science versus socio-politics. EcoHealth 13(4):618–622PubMedPubMedCentralCrossRefGoogle Scholar
  3. Atchison WD (2003) Effects of toxic environmental contaminants on voltage-gated calcium channel function: from past to present. J Bioenerg Biomembr 35:507–532PubMedCrossRefPubMedCentralGoogle Scholar
  4. Austin W, Day K, Gatto A, Humphrey J, Parish C, Rodgers J, Sieg R, Smith B, Sullivan K, Young J (2012) A review of the third five years of the California condor reintroduction program in the Southwest (2007–2011). USFWS, SacramentoGoogle Scholar
  5. Bedrosian B, Craighead D, Crandall R (2012) Lead exposure in bald eagles from big game hunting, the continental implications and successful mitigation efforts. PlosOne 7(12):e51978CrossRefGoogle Scholar
  6. Bellinger DC (2004) Lead. Pediatrics 113(4 Suppl):1016–1022PubMedPubMedCentralGoogle Scholar
  7. Bellrose FC (1959) Lead poisoning as a mortality factor in waterfowl populations. Ill Nat Hist Surv Bull 27:235–288Google Scholar
  8. Berny P, Vilagines L, Cugnasse JM, Mastain O, Chollet JY, Joncour G, Razin M (2015) Vigilance poison: Illegale poisoning and lead intoxication are the main factors affecting avian scavenger survival in the Pyrenees (France). Ecotoxicol Environ Saf 118:71–82PubMedCrossRefPubMedCentralGoogle Scholar
  9. Beyer WN, Spann JW, Sileo L, Franson JC (1988) Lead poisoning in six captive avian species. Arch Environ Contam Toxicol 17:121–130PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bezzel E, Fünfstück HJ (1995) Alpine Steinadler Aquila chrysaetos durch Bleivergiftungen gefährdet? J Ornithol 136:294–296CrossRefGoogle Scholar
  11. Bounas A, Ganoti M, Giannakaki E, Akrivos A, Vavylis D, Zorilla I, Saravia V (2016) First confirmed case of lead poisoning in the endangered Egyptian vulture (Neophron percnopterus) in the Balkans. Vulture News 70:22–29CrossRefGoogle Scholar
  12. Bouton CM, Frelin LP, Forde CE, Arnold Godwin H, Pevsner J (2001) J Neurochem 76:1724–1735PubMedCrossRefPubMedCentralGoogle Scholar
  13. Busse F, Omidi L, Timper K, Leichtle A, Windgassen M, Kluge E, Stumvoll M (2008) Lead poisoning due to adulterated marijuana. N Engl J Med 358:1641–1642PubMedCrossRefPubMedCentralGoogle Scholar
  14. Cade TJ (2007) Exposure of California condors to lead from spent ammunition. J Wildl Man 71(7):2125–2133CrossRefGoogle Scholar
  15. Carpenter JW, Pattee OH, Fritts SH, Rattner BA, Wiemeyer SN, Royle JA, Smith MA (2003) Experimental lead poisoning in turkey vultures (Cathartes aura). J Wildl Dis 39:96–104PubMedCrossRefPubMedCentralGoogle Scholar
  16. Chao SH, Bu CH, Cheung WY (1990) Activation of troponin C by Cd2+ and Pb2+. Arch Toxicol 64:490–496PubMedCrossRefPubMedCentralGoogle Scholar
  17. 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 40:6143–6150PubMedCrossRefPubMedCentralGoogle Scholar
  18. Clark AJ, Scheuhammer AM (2003) Lead poisoning in upland-foraging birds of prey in Canada. Ecotoxicology 12:23–30PubMedCrossRefPubMedCentralGoogle Scholar
  19. Conrad ME, Barton JC (1978) Factors effecting absorption and excretion of lead in the rat. Gastroenterology 74:731–740PubMedPubMedCentralGoogle Scholar
  20. Craighead D, Bedrosian B (2007) Blood lead levels of common ravens with access to big-game offal. J Wildl Man 72:240–245CrossRefGoogle Scholar
  21. Cromie R, Newth J, Reeves J, O’Brien M, Beckmann K, Brown M (2015) The sociological and political aspects of reducing lead poisoning from ammunition in the UK: why the transition to non-toxic ammunition is so difficult. In: Delahay RJ, Spray CJ (eds) Proceedings of the Oxford Lead Symposium. Lead ammunition: understanding and minimising the risk to human and environmental health. Edward Grey Institute, The University of Oxford, pp 104–124Google Scholar
  22. 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
  23. De Francisco ON, Feeney D, Armién WA, Redig PT (2016) Correlation of brain magnetic resonance imaging of spontaneously lead poisoned bald eagles (Haliaeetus leucocephalus) with histological lesions: a pilot study. Res Vet Sci 105:236–242PubMedCrossRefPubMedCentralGoogle Scholar
  24. DeMichele SJ (1984) Nutrition of lead. Comp Biochem Physiol 78:401–408CrossRefGoogle Scholar
  25. Denbow DM (2000) Gastrointestinal anatomy and physiology. In: Whittow GC (ed) Sturkie’s avian physiology, 5th edn. Academic Press, San Diego, pp 299–325CrossRefGoogle Scholar
  26. Ethier ALM, Braune BM, Scheuhammer AM, Bond DE (2007) Comparison of lead residues among avian bones. Environ Pollut 145:915–919PubMedCrossRefPubMedCentralGoogle Scholar
  27. European Union (2003) Directive 2002/96/EC of the European Parliament and of the council of 27 January 2003 on waste electrical and electronic equipment (WEEE). Off J Eur Union L37:24–39 Accessed 06 July 2017Google Scholar
  28. European Union (2013) Commission directive 2013/28/EU of 17 may 2013 amending annex II to directive 2000/53/EC of the European Parliament and of the council on end-of-life vehicles. Off J Eur Union L135:14–18. Accessed 06 July 2017Google Scholar
  29. Finkelstein ME, George D, Scherbinski S, Gwiazda R, Johnson M, Burnett J, Brandt J, Lawrey S, Pessier AP, Clark M, Wynne J, Grantham J, Smith DR (2010) Feather lead concentrations and 207Pb/206Pb ratios reveal lead exposure history of California condors (Gymnogyps californianus). Environ Sci Technol 44:2639–2647PubMedCrossRefPubMedCentralGoogle Scholar
  30. Finley MT, Dieter MP (1978) Influence of laying on lead accumulation in bone of mallard ducks. J Toxicol Environ Health 4:123–129PubMedCrossRefGoogle Scholar
  31. Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131:421–432CrossRefGoogle Scholar
  32. Franson JC (1996) Interpretation of tissue lead residues in birds other than waterfowl. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife, interpreting tissue concentrations, SETAC Spec Publ Series. Lewis Publishers, CRC Press, Boca Raton, pp 265–279Google Scholar
  33. Franson JC, Pain DJ (2011) Lead in birds. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota: interpreting tissue concentrations, 2nd edn. CRC Press, Boca Raton, pp 563–593CrossRefGoogle Scholar
  34. Franson JC, Sileo L, Pattee OH, Moore JF (1983) Effects of chronic dietary lead in American kestrels (Falco sparverius). J Wildl Dis 19:110–113PubMedCrossRefGoogle Scholar
  35. Franson JC, Michael G, Perry MC, Moore JF (1986) Blood protoporphyrin for detecting lead exposure in canvasbacks. In: Feierabend JS, Russel AB (eds) Lead poisoning in wild waterfowl. A workshop. Proceedings of the symposium held 3–4 March 1984, Wichita, Kansas, Cooperative Lead Poisoning Control Information Program, National Wildlife Federation, Washington, pp 32–37Google Scholar
  36. Friend M (1987) Lead poisoning. In: Friend M (ed) Field guide to wildlife diseases, vol 1. US Department of the Interior, Fish and Wildlife Service, Washington DC, pp 175–189Google Scholar
  37. Friend M, Franson JC (1999) Field manual of wildlife diseases. General field procedures and diseases of birds. USGS, Biological Resource Division, Madison, p 426Google Scholar
  38. Fullmer CS, Edelstein S, Wasserman RH (1985) Lead-binding properties of intestinal calcium-binding proteins. J Biol Chem 260:6816–6819PubMedGoogle Scholar
  39. Gangoso L, Alvarez-Lloret P, Rodriguez-Navarro AAB, Mateo R, Hiraldo F, Donazar JA (2009) Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environ Pollut 157:569–574PubMedCrossRefGoogle Scholar
  40. Garcia-Fernandez AJ, Martinez-Lopez E, Romero D, Maria-Mojica P, Godino A, Jimenez P (2005) High levels of lead blood in griffon vultures (Gyps fulvus) from Cazorla Natural Park (Southern Spain). Environ Toxicol 20:459–463PubMedCrossRefPubMedCentralGoogle Scholar
  41. Gilbert SG, Weiss B (2006) A rationale for lowering the blood lead action level from 10 to 2 mg/dL. Neurotoxicology 27:693–701PubMedPubMedCentralCrossRefGoogle Scholar
  42. Gilfillan SC (1965) Lead poisoning and the fall of Rome. J Occup Med 7:53–60PubMedPubMedCentralGoogle Scholar
  43. 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 407:5555–5563PubMedCrossRefPubMedCentralGoogle Scholar
  44. Henny C, 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
  45. Henretig FM (2006) Lead. In: Nelson LS, Lewin NA, Howland MA, Hoffmann RS, Goldfrank LR, Flomenbaum NE (eds) Goldfrank’s toxicologic emergencies, 9th edn. McGraw-Hill Medical, New York, pp 1266–1283Google Scholar
  46. Hernandez M, Margalida A (2008) Pesiticide abuse in Europe: effects on the cinereous vulture (Aegypius monachus) population in Spain. Ecotoxicology 17:264–272PubMedCrossRefGoogle Scholar
  47. Hernandez M, Margalida A (2009) Assessing the risk of lead exposure for the conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) population. Environ Res 109:837–842PubMedCrossRefGoogle Scholar
  48. Hernberg S (2000) Lead poisoning in a historical perspective. Am J Ind Med 38(3):244–254PubMedCrossRefGoogle Scholar
  49. Hoffman DJ, Pattee OH, Wiemeyer SN, Mulhern B (1981) Effects of lead shot ingestion on δ-aminolevulinic acid dehydratase activity, hemaglobin concentration and serum chemistry in bald eagles. J Wildl Dis 17:423–431PubMedCrossRefGoogle Scholar
  50. Hoffman DJ, Franson JC, Pattee OH, Bunck CM, Murray HC (1985) Biochemical and haematological effects of lead ingestion in nestling American kestrels (Falco sparverius). Comp Biochem Physiol 80:431–439Google Scholar
  51. Hutton M, Goodman GT (1980) Metal contamination of feral pigeons Columba livia from the London area: part 1—tissue accumulation of lead, cadmium and zinc. Environ Pollut A 22:207–217CrossRefGoogle Scholar
  52. Irschik I, Bauer F, Sager M, Paulsen P (2013) Copper residues in meat from wild artiodactyls hunted with two types of rifle bullets manufactured from copper. Eur J Wildl Res 59:129–136CrossRefGoogle Scholar
  53. Ishihara N, Matsushiro T (1986) Biliary and urinary excretion of metals in humans. Arch Environ Health 41:324–330PubMedCrossRefPubMedCentralGoogle Scholar
  54. Ishihara N, Koizumi M, Yoshida A (1987) Metal concentrations in human pancreatic juice. Arch Environ Health 42:356–360PubMedCrossRefPubMedCentralGoogle Scholar
  55. Iwata H, Watanabe M, Kim EY, Gotoh R, Yasunaga G, Tanabe S, Masuda Y, Fujita S (2000) Contamination by chlorinated hydrocarbons and lead in Stellar’s sea eagle and white-tailed sea eagle from Hokkaido, Japan. In: Ueta M, McGrady MJ (eds) First symposium on Stellar’s and White-Tailed Sea eagles in East Asia. Wild Bird Society of Japan, Tokyo, pp 91–106Google Scholar
  56. Janssen DL, Oosterhuis JE, Allen JL, Anderson MP, Kelts DG, Wiemeyer SN (1986) Lead poisoning in free-ranging California condors. J Am Vet Med Assoc 189:1115–1117PubMedPubMedCentralGoogle Scholar
  57. Jenni L, Madry MM, Kraemer T, Kupper J, Naegeli H, Jenny H, Jenny D (2015) The frequency distribution of lead concentration in feathers, blood, bone, kidney and liver of golden eagles Aquila chrysaetos: insights into the modes of uptake. J Ornithol 156:1095–1103CrossRefGoogle Scholar
  58. Kanstrup N (2006) Non-toxic shot – Danish experience. In: Boere CG, Galbraith CA, Stroud DA (eds) Waterbirds around the world. The Stationery Office, Edinburgh, p 861Google Scholar
  59. Karstad L (1971) Angiopathy and cardiopathy in wild waterfowl from ingestion of lead shot. Conn Med 35:355–360PubMedPubMedCentralGoogle Scholar
  60. Kelly TR, Grantham J, George D, Welch A, Brandt J, Burnet LJ, Sorenson KJ, Johnson M, Poppenga R, Moen D, Rasico J, Rivers JW, Battistone C, Johnson CK (2014) Spatiotemporal patterns and risk factors for lead exposure in endangered California condors during 15 years of reintroduction. Conserv Biol 28:1721–1730PubMedCrossRefPubMedCentralGoogle Scholar
  61. Kendall RJ, Scanlon PF (1983) Histologic and ultrastructural lesions of mourning doves (Zenaida macroura) poisoned by lead shot. Poult Sci 62:952–956PubMedCrossRefPubMedCentralGoogle Scholar
  62. 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 –2000. Environ Toxicol Chem 20:1831–1837PubMedCrossRefPubMedCentralGoogle Scholar
  63. Kenntner N, Krone O, Altenkamp R, Tataruch F (2003) Environmental contaminants in liver and kidney of free-ranging northern goshawks in three regions of Germany. Arch Environ Contam Toxicol 45(1):128–135PubMedCrossRefPubMedCentralGoogle Scholar
  64. Kenntner N, Oehme G, Heidecke D, Tataruch F (2004) Retrospektive Untersuchung zur Bleiintoxikation und Exposition mit potenziell toxischen Schwermetallen von Seeadlern Haliaeetus albicilla in Deutschland. Vogelwelt 125:63–75Google Scholar
  65. Kenntner N, Cretten Y, Fünfstück HJ, Janovsky M, Tataruch F (2007) Lead poisoning and heavy metal exposure of golden eagles (Aquila chrysaetos) from the European alps. J Ornithol 148:173–177CrossRefGoogle Scholar
  66. Kim EY, Goto R, Iwata H, Masuda Y, Tanabe S, Fujita S (1999) Preliminary survey of lead poisoning of Steller’s sea eagle (Haliaeetus pelagicus) and white-tailed sea eagle (Haliaeetus albicilla) in Hokkaido, Japan. Environ Toxicol Chem 18:448–451Google Scholar
  67. Kinard J (2004) Pistols: an illustrated history of their impact. ABC-CLIO, USAGoogle Scholar
  68. Kirberger M, Yang JJ (2008) Structural differences between Pb2+- and Ca2+-binding sites in proteins: implications with respect to toxicity. J Inorg Biochem 102:1901–1909PubMedPubMedCentralCrossRefGoogle Scholar
  69. Knott J, Green R, Pain DJ (2009a) Lead poisoning in Red Kites Milvus milvus. In: David F (coord) Status, monitoring and trends, Statuts, suivis et tendances, Red Kite International symposium – October, 17th et 18th 2009 – Colloque international Milan royal, 17–18 October, 2009, Montbéliard, France, pp 106–108Google Scholar
  70. Knott J, Gilbert J, Green RE, Hoccom DG (2009b) Comparison of the lethality of lead and copper bullets in deer control operations to reduce incidental lead poisoning: field trials in England and Scotland. Conserv Evid 6:71–78Google Scholar
  71. Kramer JL, Redig PT (1997) Sixteen years of lead poisoning in eagles, 1980 – 1995: an epizootiologic view. J Raptor Res 32:327–332Google Scholar
  72. Krone O, Wille F, Kenntner N, Boertmann D, Tataruch F (2004) Mortality factors, environmental contaminants, and parasites of White-Tailed Sea eagles from Greenland. Avian Dis 48:417–424PubMedCrossRefPubMedCentralGoogle Scholar
  73. Krone O, Stjernberg T, Kenntner N, Tataruch F, Koivusaari J, Nuuja I (2006) Mortality, helminth burden and contaminant residues in white-tailed sea eagles from Finland. Ambio 35:98–104PubMedCrossRefPubMedCentralGoogle Scholar
  74. Krone O, Kenntner N, Tataruch F (2009a) Gefährdungsursachen des Seeadlers (Haliaeetus albicilla L. 1758). Denisia 27: 139–146Google Scholar
  75. Krone O, Kenntner N, Trinogga A, Nadjafzadeh N, Scholz F, Sulawa J, Totschek K, Schuck-Wersig P, Zieschank R (2009b) Lead poisoning in white-tailed sea eagles: causes and approaches to solutions in Germany. In: Watson RT, Fuller M, Pokras A, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, pp 289–301Google Scholar
  76. Krone O, Berger A, Schulte R (2009c) Recording movement and activity pattern of a White-Tailed Sea eagle (Haliaeetus albicilla) by a GPS datalogger. J Ornithol 150:273–280CrossRefGoogle Scholar
  77. Labonde J (1991) Avian toxicology. Vet Clinic North Am Small Anim Pract 21:1329–1342CrossRefGoogle Scholar
  78. 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 to scavrenger: lead concentrations in feathers of wild Andean condors. Biol Conserv 144:1464–1471CrossRefGoogle Scholar
  79. Li Y, Moon K, Wong CP (2005) Electronics without lead. Science 308:1419–1420PubMedCrossRefPubMedCentralGoogle Scholar
  80. Lumeij JT (1985) Clinicopathologic aspects of lead poisoning in birds: a review. Review papers. Vet Q 7:133–138PubMedCrossRefPubMedCentralGoogle Scholar
  81. Madry MM, Kraemer T, Kupper J, Naegeli H, Jenny H, Jenni L, Jenny D (2015) Excessive lead burden among golden eagles in the Swiss alps. Environ Res Lett 10(3). CrossRefGoogle Scholar
  82. Markovac J, Goldstein GW (1988) Picomolar concentrations of lead stimulate brain protein kinase C. Nature 334:71–73PubMedCrossRefPubMedCentralGoogle Scholar
  83. Martin PA, Campbell D, Hughes K, McDaniel T (2008) Lead in the tissues of terrestrial raptors in southern Ontario, Canada, 1995–2001. Sci Total Environ 391:96–103PubMedCrossRefPubMedCentralGoogle Scholar
  84. Martinez-Haro M, Taggart MA, Green AJ, Mateo R (2009) Avian digestive tract simulation to study the effect of grit geochemistry and food on Pb shot bioaccessibility. Environ Sci Technol 43:9480–9486PubMedCrossRefPubMedCentralGoogle Scholar
  85. Mateo R (2009) Lead poisoning in wild birds in Europe and the regulations adopted by different countries. 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, pp 71–98Google Scholar
  86. Mateo R, Molina R, Grifols J, Guitar R (1997) Lead poisoning in free ranging griffon vulture (Gyps fulvus). Vet Rec 140:47–48PubMedCrossRefPubMedCentralGoogle Scholar
  87. Mateo R, Cadenas R, Manez M, Guitar R (2001) Lead shot ingestion in two raptor species from Donana, Spain. Ecotoxicol Environ Saf 48:6–10PubMedCrossRefPubMedCentralGoogle Scholar
  88. Mateo R, Vallverdu-Coll N, Lopez-Antia A, Taggart MA, Martínez-Haro M, Guitart R, Ortiz-Santaliestra ME (2014) Reducing Pb poisoning in birds and Pb exposure in game meat consumers: the dual benefit of effective Pb shot regulation. Environ Int 63:163–168PubMedCrossRefPubMedCentralGoogle Scholar
  89. Meyer CB, Meyer JS, Francisco AB, Holder J, Verdonck F (2016) Can ingestion of lead shot and poisons change population trends of three European birds: grey partridge, common buzzard, and red kite? PLoS One 11(1):e0147189. Accessed 06 July 2017CrossRefPubMedPubMedCentralGoogle Scholar
  90. Mudge G (1983) The incidence and significance of ingested lead pellet poisoning in British waterfowl. Biol Conserv 27:333–372CrossRefGoogle Scholar
  91. Müller K, Altenkamp R, Brunnberg L (2007) Morbidity of free-ranging White-Tailed Sea eagles (Haliaeetus albicilla) in Germany. J Avian Med Surg 21:265–274PubMedCrossRefPubMedCentralGoogle Scholar
  92. Nadjafzadeh M, Hofer H, Krone O (2013) The link between feeding ecology and lead poisoning in white-tailed eagles. J Wildl Manag 77:48–57CrossRefGoogle Scholar
  93. Nadjafzadeh M, Hofer H, Krone O (2015) Lead exposure and food processing in white-tailed eagles and other scavengers: an experimental approach to simulate lead uptake at shot mammalian carcasses. Eur J Wildl Res 61:763–774CrossRefGoogle Scholar
  94. Nam DH, Lee DP (2009) Abnormal lead exposure in globally threatened cinereous vultures (Aegypius monachus) wintering in South Korea. Ecotoxicology 18:225–229PubMedCrossRefPubMedCentralGoogle Scholar
  95. Nriagu JO (1983) Lead & lead poisoning in antiquity. Wiley-Interscience Publication, New YorkGoogle Scholar
  96. Onalaja AO, Claudio L (2000) Genetic susceptibility to lead poisoning. Environ Health Perspect 108:23–28PubMedPubMedCentralCrossRefGoogle Scholar
  97. Pain DJ (1992) Lead poisoning in waterfowl: a review. In: Pain DJ (ed) Lead poisoning in waterfowl. Proceedings of the international waterfowl and wetlands research bureau workshop, Brussels, Belgium. I. WR.B. Special Publication 16. UK, p 7–13Google Scholar
  98. Pain DJ (1996) Lead in waterfowl. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife – interpreting tissue concentrations. A Special Publication of SETAC, CRC Press, South Carolina, pp 251–264Google Scholar
  99. Pain DJ, Meharg AA, Ferrer M, Taggart M, Penteriani V (2005) Lead concentrations in bone and feathers of the globally threatened Spanish imperial eagle. Biol Conserv 121:603–610CrossRefGoogle Scholar
  100. Pain DJ, Carter I, Sainsbury A, Shore R, Eden P, Taggart M, Konstantinos S, Walker L, Meharg A, Raab A (2007) Lead contamination and associated disease in captive and reintroduced red kites Milvus milvus in England. Sci Total Environ 376:116–127PubMedCrossRefPubMedCentralGoogle Scholar
  101. Pain DJ, 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, pp 99–118Google Scholar
  102. Pattee OH, Pain DJ (2003) Lead in the environment. In: Hoffman DJ, Rattner BA, Burton GA Jr, Cairns J Jr (eds) Handbook of ecotoxicology, 2nd edn. Lewis, Boca Raton, pp 373–408Google Scholar
  103. Pattee OH, Wiemeyer SN, Mulhern BM, Sileo L, Carpenter JW (1981) Experimental lead-shot poisoning in bald eagles. J Wildl Manag 45:806–810CrossRefGoogle Scholar
  104. 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 42:772–779PubMedCrossRefPubMedCentralGoogle Scholar
  105. Paulsen P, Sager M, Bauer F, Schumann-Irschik I (2015) Pilot study on metal contents in meat portions from wild game killed by “lead-free” rifle bullets. J Food Saf Food Qual 66:128–131Google Scholar
  106. Pikula J, Hajkova P, Bandouchova H, Bednarova I, Adam V, Beklova M, Kral J, Ondracek K, Osickova J, Pohanka M, Sedlackova J, Skochova H, Sobotka J, Treml F, Kizek R (2013) Lead toxicosis of captive vultures: case description and responses to chelation therapy. BMC Vet Res 9:11PubMedPubMedCentralCrossRefGoogle Scholar
  107. Pounds JG, Long GJ, Rosen JF (1991) Cellular and molecular toxicity of lead in bone. Environ Health Perspect 91:17–32PubMedPubMedCentralCrossRefGoogle Scholar
  108. Rattner BA, Fleming WJ, Bunck CM (1989) Comparative toxicity of lead shot in black ducks (Anas rubripes) and mallards (Anas platyrhnchos). J Wildlife Dis 25:175–183CrossRefGoogle Scholar
  109. Redig PT, Stowe CM, Barnes DM, Arent TD (1980) Lead toxicosis in raptors. J Am Vet Med Assoc 177:941–943PubMedPubMedCentralGoogle Scholar
  110. Reiser MH, Temple SA (1981) Effects of chronic lead ingestion on birds of prey. In: Cooper JE, Greenwood AG (eds) Recent advances in the study of raptor diseases. Chiron Publications, Keighley, pp 21–25Google Scholar
  111. Repper R, Drasch G, Grimm F, Kösters J (1986) Die Auswirkungen implantierter Schrotkugeln auf einige Parameter bei Tauben. Deutsche Veterinärmedizinische Gesellschaft e.V., Tagung der Fachgruppe Geflügelkrankheiten in Verbindung mit dem Institut für Geflügelkrankheiten der Ludwig-Maximilians-Universität München, 5: 34–48Google Scholar
  112. Rodriguez-Ramos Fernandez J, 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 20:670–681PubMedCrossRefPubMedCentralGoogle Scholar
  113. Rossi E (2008) Low level environmental lead exposure – a continuing challenge. Clin Biochem Rev/Aust Assoc Clin Biochem 29(2):63–70Google Scholar
  114. Ruby MV, Davis A, Kempton JH, Drexler JW, Bergstrom PD (1992) Lead bioavailability: dissolution kinetics under simulated gastric conditions. Environ Sci Technol 26:1242–1248CrossRefGoogle Scholar
  115. Saito K, Kurosawa N, Shimura R (2000) Lead poisoning in endangered sea-eagles in eastern Hokkaido through ingestion of shot sika deer. In: Lumeij JT, Remple DR, Redig PT, Lierz M, Cooper JE (eds) Raptor biomedicine III. Zoological Education Network, Florida, pp 163–166Google Scholar
  116. Scarborough J (1984) The myth of lead poisoning among the romans: an essays review. J Hist Med Allied Sci 39(4):469–475PubMedCrossRefPubMedCentralGoogle Scholar
  117. Scheuhammer AM (1987) The chronic toxicity of Aluminium, cadmium, mercury and lead in birds: a review. Environ Pollut 46:263–295PubMedCrossRefPubMedCentralGoogle Scholar
  118. Scheuhammer AM, Templeton DM (1998) Use of stable isotope ratios to distinguish sources of lead exposure in wild birds. Ecotoxicology 7:37–42CrossRefGoogle Scholar
  119. Schock MR, Hyland RN, Welch MM (2008) Occurrence of contaminant accumulation in lead pipe scales from domestic drinking water distribution systems. Environ Sci Technol 42(12):4285–4291PubMedCrossRefPubMedCentralGoogle Scholar
  120. Sileo L, Jones RN, Hatch RC (1973) The effect of ingested lead shot on the electrocardiogram of Canada geese. Avian Dis 17:308–313PubMedCrossRefPubMedCentralGoogle Scholar
  121. Stauber E, Finch N, Talcott PA, Gay JM (2010) Lead poisoning of bald (Haliaeetus leucocephalus) and golden (Aquila chrysaetos) eagles in the US inland pacific northwest region – an 18-year retrospective study: 1981-2008. J Avian Med Surg 24:279–287PubMedCrossRefPubMedCentralGoogle Scholar
  122. 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, 1972–1973. US Fish and Wildl Serv Spec Sci Rep Wildl 223:1–12Google Scholar
  123. Strom SM, Langenberg JA, Businga NK, Batten JK (2009) Lead exposure in Wisconsin birds. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of spent lead ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, Idaho, pp 194–201Google Scholar
  124. Thomas VG (2013) Lead-free rifle ammunition: product availability, price, effectiveness, and role in global wildlife conservation. Ambio 42:737–745PubMedPubMedCentralCrossRefGoogle Scholar
  125. Thomas VG, Kanstrup N, Gremse C (2015) Key questions and responses regarding the transition to use of lead-free ammunition. In: Delahay RJ, Spray CJ (eds) Proceedings of the Oxford lead symposium. Lead ammunition: understanding and minimising the risk to human and environmental health. Edward Grey Institute, The University of Oxford, Oxford, pp 125–134Google Scholar
  126. Thompson LJ (2012) Chapter 31. Lead. In: Gupta RC (ed) Veterinary toxicology. Basic and clinical principles, 2nd edn. Elsevier, Amsterdam, pp 438–441Google Scholar
  127. Trinogga A, Fritsch G, Hofer H, Krone O (2013) Are lead-free hunting rifle bullets as effective at killing wildlife as conventional lead bullets? A comparison based on wound size and morphology. Sci Total Environ 443:226–232PubMedCrossRefPubMedCentralGoogle Scholar
  128. Wayland M, Bollinger T (1999) Lead exposure and poisoning in bald eagles and golden eagles in the Canadian prairie provinces. Environ Pollut 104:341–350CrossRefGoogle Scholar
  129. Wiemeyer GM, Perez MA, Bianchini LT, Sampietro L, Bravo GF, Jacome NL, Astore V, Lambertucci SA (2017) Repeated conservation threats across the Americas: high levels of blood and bone lead in the Andean condor widen the problem to a continental scale. Environ Pollut 220:672–679PubMedCrossRefPubMedCentralGoogle Scholar
  130. World Health Organization (1989) Lead—environmental aspects. Environmental Health Criteria, No. 85. Geneva, Switzerland. Accessed 06 July 2017
  131. World Health Organization (2011) Lead in drinking-water. Background document for development of WHO Guidelines for Drinking-water Quality. Geneva, Switzerland. Accessed 06 July 2017
  132. Zechner L, Steineck T, Tataruch F (2005) Bleivergiftungen bei einem Steinadler (Aquila chrysaetos) in der Steiermark. Egretta 47: 157–158Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Wildlife DiseasesLeibniz Institute for Zoo and Wildlife ResearchBerlinGermany

Personalised recommendations