, Volume 23, Issue 9, pp 1722–1731 | Cite as

Lead and eagles: demographic and pathological characteristics of poisoning, and exposure levels associated with other causes of mortality

  • J. Christian FransonEmail author
  • Robin E. Russell


We conducted a retrospective analysis to evaluate demographic and pathologic characteristics in 484 bald eagles (Haliaeetus leucocephalus) and 68 golden eagles (Aquila chrysaetos) diagnosed with lead poisoning at the U.S. Geological Survey National Wildlife Health Center. As part of our analysis, we compared characteristics of lead poisoned eagles with those that died of other causes. Odds of lead poisoning were greater for bald eagles versus golden eagles, females versus males, adults versus juveniles, and eagles from the Mississippi and Central flyways versus the Atlantic and Pacific flyways. In addition to spatial, species, and demographic associations, we detected a distinct temporal trend in the collection date of lead poisoned bald eagle carcasses. These carcasses were found at greater frequency in late autumn and winter than spring and summer. Lesions in lead poisoned birds included emaciation, evidence of bile stasis, myocardial degeneration and necrosis, and renal tubular nephrosis and necrosis. Ingested lead ammunition or fragments were found in 14.2 % of bald eagles and 11.8 % of golden eagles. The overall mean liver lead concentration (wet weight basis) for eagles diagnosed with lead poisoning was 28.9 ± 0.69 SE mg/kg in bald eagles and 19.4 ± 1.84 SE mg/kg in golden eagles. In eagles diagnosed with collision trauma, electrocution, poisoning (other than lead), emaciation, infectious disease, trapping death, other, and undetermined causes, average liver lead concentrations were low (<1 mg/kg) and did not differ among causes of mortality. Thus, based on our data, we found no evidence that lead exposure of eagles predisposed them to other causes of mortality.


Bald eagle Golden eagle Lead exposure Lead poisoning Mortality Pathology 



We thank the field biologists who submitted eagle carcasses, members of the field team at the NWHC for consulting with field personnel, the many pathologists who conducted necropsies, and staff of the NWHC laboratories who provided diagnostic support, including lead analysis. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 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
  2. Bellrose FC (1959) Lead poisoning as a mortality factor in waterfowl populations. Ill Nat Hist Surv Bull 27:235–288Google Scholar
  3. Beyer WN, Spann JW, Sileo L, Franson JC (1988) Lead poisoning in six captive avian species. Arch Environ Contain Toxicol 17:121–130CrossRefGoogle Scholar
  4. Buehler DA (2000) Bald eagle (Haliaeetus leucocephalus). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca. doi: 10.2173/bna.506. Accessed 9 May 2014
  5. Burger J (1995) A risk assessment for lead in birds. J Toxicol Environ Health 45:369–396CrossRefGoogle Scholar
  6. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  7. 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
  8. 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
  9. Department of the Interior (DOI) (2007) Endangered and threatened wildlife and plants: removing the bald eagle in the lower 48 states from the list of endangered and threatened wildlife. Fed Reg 72:37346–37372Google Scholar
  10. Duke GE, Evanson OA, Jegers A (1976) Meal to pellet intervals in 14 species of captive raptors. Comp Biochem Physiol 53A:1–6CrossRefGoogle Scholar
  11. Eisler R (2000) Handbook of chemical risk assessment: health hazards to humans, plants, and animals, vol 1. Metals. Lewis Publishers, Boca RatonCrossRefGoogle Scholar
  12. Fournier MA, Hines JE (1994) Effects of starvation on muscle and organ mass of king eiders Somateria spectabilis and the ecological and management implications. Wildfowl 45:188–197Google Scholar
  13. Frank A (1986) Lead fragments in tissues from wild birds: a cause of misleading analytical results. Sci Total Environ 54:275–281CrossRefGoogle Scholar
  14. 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
  15. Franson JC, Smith MR (1999) Poisoning of wild birds from exposure to anticholinesterase compounds and lead: diagnostic methods and selected cases. Seminars Avian Exotic Pet Med 8:3–11CrossRefGoogle Scholar
  16. Franson JC, Thomas NJ, Smith MR, Robbins AH, Newman S, McCartin PC (1996) A retrospective study of postmortem findings in red-tailed hawks. J Raptor Res 30:7–14Google Scholar
  17. Friend M, Franson JC, Anderson WL (2009) Biological and societal dimensions of lead poisoning in birds in the USA. 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 34–60Google Scholar
  18. Garcelon DK (1990) Observations of aggressive interactions by bald eagles of known age and sex. Condor 92:532–534CrossRefGoogle Scholar
  19. Griffin CR, Baskett TS, Sparrowe RD (1980) Bald eagles and the management program at Swan Lake National Wildlife Refuge. Trans N Am Wildl Nat Resour Conf 45:252–262Google Scholar
  20. Grinnell B (1894) Lead poisoning. For Stream 42:117–118Google Scholar
  21. Halley DJ, Gjershaug JO (1998) Inter- and intra-specific dominance relationships and feeding behaviour of golden eagles Aquila chrysaetos and sea eagles Haliaeetus albicilla at carcasses. IBIS 140:295–301CrossRefGoogle Scholar
  22. Haseltine SD, Heinz GH, Reichel WL, Moore JF (1981) Organochlorine and metal residues in eggs of waterfowl nesting on islands in Lake Michigan off Door County, Wisconsin, 1977–78. Pesticides Monit J 15:90–97Google Scholar
  23. 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
  24. Hosmer DW, Lemeshow S (2000) Applied logistic regression, 2nd edn. Wiley, New YorkCrossRefGoogle Scholar
  25. Hough E (1894) Lead-poisoned ducks. For Stream 42:117Google Scholar
  26. 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
  27. Hunter B, Wobeser G (1980) Encephalopathy and peripheral neuropathy in lead-poisoned mallard ducks. Avian Dis 24:169–178CrossRefGoogle Scholar
  28. Jacobson E, Carpenter JW, Novilla M (1977) Suspected lead toxicosis in a bald eagle. JAVMA 171:952–954Google Scholar
  29. Kaiser TE, Reichel WL, Locke LN, Cromartie E, Krynitsky AJ, Lamont TG, Mulhern BM, Prouty RM, Stafford CJ, Swineford DM (1980) Organochlorine pesticide, PCB, and PBB residues and necropsy data for bald eagles from 29 states: 1975–77. Pestic Monit J 13:145–149Google Scholar
  30. 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
  31. 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
  32. Kéry M (2010) Introduction to winbugs for ecologists. Academic Press, BurlingtonGoogle Scholar
  33. Kochert MN, Steenhof K (2002) Golden eagles in the U.S. and Canada: status, trends, and conservation challenges. J Raptor Res 36:32–40Google Scholar
  34. Kochert MN, Steenhof K, Mcintyre CL, Craig EH (2002) Golden eagle (Aquila chrysaetos). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca. doi: 10.2173/bna.684. Accessed 9 May 2014
  35. Kramer JL, Redig PT (1997) Sixteen years of lead poisoning in eagles, 1980–95: an epizootiologic view. J Raptor Res 31:327–332Google Scholar
  36. Lasko TA, Bhagwat JG, Zou KH, Ohno-Machado L (2005) The use of receiver operating characteristic curves in biomedical informatics. J Biomed Inform 38:404–415CrossRefGoogle Scholar
  37. Locke LN, Thomas NJ (1996) Lead poisoning of waterfowl and raptors. In: Fairbrother A, Locke LN, Hoff GL (eds) Noninfectious diseases of wildlife, 2nd edn. Iowa State University Press, Ames, pp 108–117Google Scholar
  38. Locke LN, Bagley GE, Frickie DN, Young LT (1969) Lead poisoning and aspergillosis in an Andean condor. JAVMA 155:1052–1056Google Scholar
  39. MacDonald JW, Randall CJ, Ross HM, Moon GM, Ruthven AD (1983) Lead poisoning in captive birds of prey. Vet Rec 113(3):65–66Google Scholar
  40. Mulhern BM, Reichel WL, Locke LN, Lamont TG, Belisle A, Cromartie E, Bagley GF, Prouty RM (1970) Organochlorine residues and autopsy data from bald eagles 1966-68. Pestic Monit J 4:141–144Google Scholar
  41. 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
  42. Nelson TA, Mitchell C, Abbott C (1989) Lead-shot ingestion by bald eagles in western Arkansas. Southwest Nat 34:245–249CrossRefGoogle Scholar
  43. Neumann K (2009) Bald eagle lead poisoning in winter. 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 210–218Google Scholar
  44. O’Halloran J, Myers AA, Duggan PF (1989) Some sub-lethal effects of lead on mute swan Cygnus olor. J Zool Lond 218:627–632CrossRefGoogle Scholar
  45. 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 WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, pp 99–118Google Scholar
  46. Pain DJ, Sears J, Newton I (1995) Lead concentrations in birds of prey in Britain. Environ Pollut 87:173–180Google Scholar
  47. Pattee OH, Hennes SK (1983) Bald eagles and waterfowl: the lead shot connection. Trans N Am Wildl Nat Resour Conf 48:230–237Google Scholar
  48. 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
  49. Reichel WL, Schmeling SK, Cromartie E, Kaiser TE, Krynitsky AJ, Lamont TG, Mulhern BM, Prouty RM, Stafford CJ, Swineford DM (1984) Pesticide, PCB, and lead residues and necropsy data for bald eagles from 32 states: 1978-81. Environ Monit Assess 4:395–403CrossRefGoogle Scholar
  50. 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
  51. 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 20:670–681CrossRefGoogle Scholar
  52. Route WT, Key RL, Russell RE, Lindstrom AB, Strynar MJ (2014) Spatial and temporal patterns in concentrations of perfluorinated compounds in bald eagle nestlings in the upper midwestern United States. Environ Sci Technol. doi: 10.1021/es501055d Google Scholar
  53. Russell RE, Franson JC (2014) Causes of mortality in eagles submitted to the National Wildlife Health Center 1975–2013. Wildl Soc Bull. doi: 10.1002/wsb.469
  54. Sabine N, Klimstra WD (1985) Ecology of bald eagles wintering in southern Illinois. Trans Ill Acad Sci 78:13–24Google Scholar
  55. Saito K (2009) Lead poisoning of Steller’s sea-eagle (Haliaeetus pelagicus) and white-tailed eagle (Haliaeetus albicilla) caused by the ingestion of lead bullets and slugs, in Hokkaido, Japan. 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 302–309Google Scholar
  56. Smith JP, Farmer CJ, Hoffman SW, Kaltenecker GS, Woodruff KZ, Sherrington PF (2008) Trends in autumn counts of migratory raptors in western North America. In: Bildstein KL, Smith JP, Ruelas Inzunza E, Veit RR (eds) State of North America’s Birds of Prey. Series in Ornithology 3. Nuttall Ornithological Club, Cambridge and American Ornithologists’ Union, Washington DC, pp. 217–251Google Scholar
  57. 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: 1991–2008. J Avian Med Surg 24:279–287CrossRefGoogle Scholar
  58. Sturtz S, Ligges U, Gelman A (2005) R2WinBUGS: a package for running WinBUGS from R. J Stat Softw 12:1–16Google Scholar
  59. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Accessed 27 June 2014
  60. 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
  61. Warner SE, Britton EE, Becker DN, Coffey MJ (2014) Bald eagle lead exposure in the upper Midwest. J Fish Wildl Manag 5:e1944-687X. doi: 10.3996/032013-JFWM-029 Google Scholar
  62. 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
  63. Wayland M, Wilson LK, Elliott JE, Miller MJR, Bollinger T, McAdie M, Langelier K, Keating J, Froese JMW (2003) Mortality, morbidity, and lead poisoning of eagles in western Canada, 1986–98. J Raptor Res 37:8–18Google Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2014

Authors and Affiliations

  1. 1.U.S. Geological SurveyNational Wildlife Health CenterMadisonUSA

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