Journal of Ornithology

, Volume 156, Issue 4, pp 1095–1103 | Cite as

The frequency distribution of lead concentration in feathers, blood, bone, kidney and liver of golden eagles Aquila chrysaetos: insights into the modes of uptake

  • Lukas JenniEmail author
  • Milena M. Madry
  • Thomas Kraemer
  • Jacqueline Kupper
  • Hanspeter Naegeli
  • Hannes Jenny
  • David Jenny
Original Article


Several cases of acute lead poisoning of golden eagles Aquila chrysaetos have been documented in the Alps. The question, however, remains how often golden eagles take up lead (once, chronically or episodically) and whether this uptake is in fatal or sublethal amounts. We approached this question by examining the level and frequency distribution of lead concentration in different tissues and in three segments of flight feathers in 41 golden eagles found dead, injured or moribund in the Swiss Alps. The frequency distribution of lead concentration in the blood, liver, kidney, wing coverts and shaft of flight feathers were all right-skewed. The highest values in blood, kidney and liver reached levels typical for acute fatal poisoning. In contrast, the frequency distribution of lead in bones was more symmetrical, but 71 % had bone lead concentrations >10 µg/g, which are considered elevated, and 29 % >20 µg/g, values often observed in cases of lethal poisoning. In 22 % of individuals, only one segment of a flight feather had a high lead concentration, while the other two segments had a low concentration. These findings indicate an episodic intake of lead of various amounts that may be immediately fatal (generating high blood levels) or sublethal. The patterns of lead in flight feathers and in bone suggest a repeated sublethal lead intake by the same individual. Such an episodic lead uptake seems only possible through ingestion of lead particles from carcasses or offal left behind by hunters. This also constitutes a risk to other scavengers, notably to the bearded vulture Gypaetus barbatus for which several high bone lead values have been found.


Golden eagle Lead poisoning Lead ammunition Lead in feather 


Die Häufigkeitsverteilung von Bleikonzentrationen in Federn, Blut, Knochen, Niere und Leber von Steinadlern Aquila chrysaetos : Einblicke in die Art und Weise der Aufnahme

Mehrere Fälle von akuter Bleivergiftung von Steinadlern Aquila chrysaetos sind aus den Alpen bekannt. Die Frage ist, wie oft Steinadler Blei aufnehmen (einmal, chronisch oder episodisch) und ob dies in letalen oder subletalen Dosen geschieht. Wir untersuchten die Konzentrationen von Blei und ihre Häufigkeitsverteilungen in verschiedenen Geweben und in drei Abschnitten von Flugfedern von 41 Steinadlern, die tot, verletzt oder sterbend in den Schweizer Alpen gefunden wurden. Die Häufigkeitsverteilungen der Bleikonzentrationen in Blut, Leber, Niere, Flügeldeckfedern und dem Kiel von Flugfedern waren alle rechtsschief. Die höchsten Werte in Blut, Leber und Niere erreichten Werte, die typisch für letale Vergiftungen sind. Die Häufigkeitsverteilung der Bleikonzentrationen in Knochen hingegen war eher symmetrisch, wobei 71 % der Individuen Konzentrationen >10 µg/g, die als erhöht gelten, und 29 % Werte >20 µg/g zeigten, wie sie häufig bei letalen Vergiftungen auftreten. Bei 22 % der Individuen zeigte nur einer von drei Kielabschnitten einer Flugfeder erhöhte Bleiwerte, während die anderen beiden Abschnitte niedrige Werte aufwiesen. Diese Befunde legen nahe, dass die Aufnahme von Blei episodisch und in unterschiedlicher, unmittelbar tödlicher oder subletaler Menge erfolgt. Das Muster von Blei in Flugfedern und Knochen zeigt, dass die mehrmalige Aufnahme einer subletalen Menge Blei durch dasselbe Individuum wohl öfter vorkommt. Solch eine episodische Bleiaufnahme findet sehr wahrscheinlich über die Aufnahme von Bleipartikeln in Kadavern oder im Aufbruch von gejagten Tieren statt. Dies ist auch ein Risiko für andere Aasfresser, insbesondere für den Bartgeier Gypaetus barbatus, bei welchem mehrere sehr hohe Bleiwerte in Knochen gefunden wurden.



We thank the authorities of the cantonal Fish and Game Departments and the many gamekeepers who helped collect dead and moribund golden eagles. Werner Degonda performed the autopsies in Chur. Veterinarians of the Universities of Berne and Zurich provided additional samples and data, particularly Janne Schöning, Roman Meier, Ulrike Cyrus, Richard Hoop and Jessica Gull. Injured or moribund birds were maintained in bird care stations by Christoph Meier, Erich Widmer, Vreni Mattmann and Andi Lischke. Lorenzo Vinciguerra, Ueli Schneppat and René Heim of the Natural History Museums of St. Gallen, Grisons and Luzern prepared tissue and bone samples of some golden eagles. Enrico Bassi from the Stelvio National Park and Daniel Hegglin, Stiftung Pro Bartgeier, provided data from bones of bearded vultures. Hans Schmid helped to coordinate the project. We thank David Kistler (Swiss Federal Institute of Aquatic Science and Technology) for access to the Microwave Digestion System and Fabian von Kaenel for his help with the ICP-MS measurements.


  1. Avery D, Watson RT (2009) Regulation of lead-based ammunition around the world. 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 161–168Google Scholar
  2. Bassi E, Ferloni M (2012) L’esposizione dei rapaci al piombo: il caso della provincia di Sondrio. In: Andreotti A and Borghesi F (eds): Il piombo nelle munizioni da caccia: problematiche e possibili soluzioni. Rapporti ISPRA, 158/2012, pp 53–54Google Scholar
  3. Bassi E, Ferloni M, Bianchi A (2013) L’intossicazione da piombo nei grandi rapaci necrofagi. In: Info Gipeto n. 30, Parco Naturale Alpi Marittime e Parco Nazionale dello Stelvio, Valdieri 2013. p 31Google Scholar
  4. Bassi E, Ferloni M, Gugiatti A, Pedrotti L, Di Giancamillo M, Grilli G (in press) Il rischio di saturnismo negli uccelli necrofagi in relazione alle attuali modalità di caccia degli ungulati. Atti XVI Convegno Italiano di Ornitologia. In: Tinarelli R, Andreotti A, Baccetti N, Melega L, Roscelli F, Serra L, Zenatello M (Eds.), Atti XVI Convegno Italiano di OrnitologiaGoogle Scholar
  5. Bezzel E, Fünfstück HJ (1995) Alpine Steinadler Aquila chrysaetos durch Bleivergiftung gefährdet? J Ornithol 136:294–296CrossRefGoogle Scholar
  6. Bloom PH, Clark WS (2001) Molt and sequence of plumages of golden eagles and a technique for in-hand ageing. North Am Bird Bander 26:97–116Google Scholar
  7. Burger J, Gochfeld M (2000a) Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health Part B 3:59–78CrossRefGoogle Scholar
  8. Burger J, Gochfeld M (2000b) Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. Sci Total Environ 257:37–52CrossRefPubMedGoogle Scholar
  9. Cardiel IE, Taggart MA, Mateo R (2011) Using Pb-Al ratios to discriminate between internal and external deposition of Pb in feathers. Ecotoxicol Environ Saf 74:911–917CrossRefPubMedGoogle Scholar
  10. Cerradelo S, Munoz E, To-Figueras J, Mateo R, Guitart R (1992) Intoxicacion por ingestion de perdigones de plomo en dos aguilas reales. Doñana Acta Vertebrata 19:122–127Google Scholar
  11. Clark AJ, Scheuhammer AM (2003) Lead poisoning in upland-foraging birds of prey in Canada. Ecotoxicology 12:23–30CrossRefPubMedGoogle Scholar
  12. Craig TH, Connelly JW, Craig EH, Parker TL (1990) Lead concentrations in golden and bald eagles. Wilson Bull 102:130–133Google Scholar
  13. Cramp S (1980) Handbook of the Birds of Europe, the Middle East and North Africa, vol 2. Oxford University Press, OxfordGoogle Scholar
  14. Dauwe T, Bervoets L, Pinxten R, Blust R, Eens M (2003) Variation of heavy metals within and among feathers of birds of prey: effects of molt and external contamination. Environ Pollut 124:429–436CrossRefPubMedGoogle Scholar
  15. Dmowski K (1999) Birds as bioindicators of heavy metal pollution: review and examples concerning European species. Acta Ornithol 34:1–25Google Scholar
  16. Ellenberg H, Dietrich J, Stoeppler M, Nürnberg HW (1985) Environmental monitoring of heavy metals with birds as pollution integratuing biomonitors: introduction, definitions and practical examples for Goshawk (Accipiter gentilis). In: Lekkas T (ed) Heavy metals in the environment. CEP Consultants Ltd., Athens, pp 724–726Google Scholar
  17. Ethier ALM, Braune BM, Scheuhammer AM, Bond DE (2007) Comparison of lead residues among avian bones. Environ Pollut 145:915–919CrossRefPubMedGoogle Scholar
  18. Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131:421–432CrossRefGoogle Scholar
  19. Franson JC, Pain DJ (2011) Lead in birds. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota. CRC Press, Boca Raton, pp 563–593CrossRefGoogle Scholar
  20. Franson JC, Sileo L, Pattee OH, Moore JF (1983) Effects of chronic dietary lead in American kestrels (Falco sparverius). J Wildl Dis 19:110–113CrossRefPubMedGoogle Scholar
  21. Fry M, Sorenson K, Grantham J, Burnett J, Brandt J, Koenig M (2009) Lead intoxication kinetics in condors from California. 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, p 266Google Scholar
  22. Gangoso L, Alvarez-Lloret P, Rodriguez-Navarro AB, Mateo R, Hiraldo F, Donázar JA (2009) Long-term effects of lead poisoning on bone mineralization in vlutures exposed to ammunition sources. Environ Pollut 157:569–574CrossRefPubMedGoogle Scholar
  23. Garcia-Fernandez AJ, Motas-Guzman M, Navas I, Maria-Mojica P, Luna A, Sanchez-Garcia JA (1997) Environmental exposure and distribution of lead in four species of raptors in southeastern Spain. Arch Environ Contam Toxicol 33:76–82CrossRefPubMedGoogle Scholar
  24. Hahn E, Hahn K, Stoeppler M (1989) Schwermetalle in Federn von Habichten (Accipiter gentilis) aus unterschiedlich belasteten Gebieten. J Ornithol 130:303–309CrossRefGoogle Scholar
  25. Haig SM, D’Elia J, Eagles-Smith C, Fait 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
  26. Haller H (1996) Der Steinadler in Graubünden. Langfristige Untersuchungen zur Populationsökologie von Aquila chrysaetos im Zentrum der Alpen. Ornithol Beob 93. Beiheft 9:1–168Google Scholar
  27. Harmata AR, Restani M (2013) Lead, mercury, selenium, and other trace elements in tissues of golden eagles from southwestern Montana, USA. J Wildl Dis 49:114–124CrossRefPubMedGoogle Scholar
  28. Helander B, Axelsson J, Borg H, Holm K, Bignert A (2009) Ingestion of lead ammunition and lead concentrations in white-tailed sea eagles (Haliaeetus albicilla) in Sweden. Sci Total Environ 407:5555–5563CrossRefPubMedGoogle Scholar
  29. Hoffman DJ, Pattee OH, Wiemeyer SN, Mulhern B (1981) Effects of lead shot ingestion on d-aminolevulinic acid dehydratase activity, hemaglobin concentration and serum chemistry in bald eagles. J Wildl Dis 17:423–431CrossRefPubMedGoogle Scholar
  30. Hunt G, Burnham W, Parish CN, Burnham KK, Mutch B, Oaks JL (2009) Bullet fragments in deer remains: implications for lead exposure in scavengers. 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 254–258Google Scholar
  31. Kendall RJ, Lacher TE, Bunck C, Daniel B, Driver C, Grue CE, Leighton F, Stansley W (1996) An ecological risk assessment of lead shot exposure in non-waterfowl avian species: upland game birds and raptors. Environl Toxicol Chem 151:1–20Google Scholar
  32. 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 20:1831–1837CrossRefPubMedGoogle Scholar
  33. Kenntner N, Crettenand 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
  34. Kramer JL, Redig PT (1997) Sixteen years of lead poisoning in eagles, 1980–1995: an epizootiologic view. J Raptor Res 31:327–332Google Scholar
  35. Krone O, Kenntner N, Trinogga A, Nadjafzadeh N, 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 A, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, pp 289–301Google Scholar
  36. 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 10:034003CrossRefGoogle Scholar
  37. Mateo R, Taggart MA, Meharg AA (2003) Lead and arsenic in bones of birds of prey from Spain. Environ Poll 126:107–114CrossRefGoogle Scholar
  38. Meretsky VJ, Snyder NFR, Beissinger SR, Clendenen DA, Wiley JW (2000) Demography of the California condor: implications for reestablishment. Cons Biol 14:957–967CrossRefGoogle Scholar
  39. Nriagu JO (1989) A global assessment of natural sources of atmospheric trace metals. Nature 338:47–49CrossRefGoogle Scholar
  40. Pain DJ, Sears J, Newton I (1995) Lead concentrations in birds of prey in Britain. Environ Poll 87:173–180CrossRefGoogle Scholar
  41. Pain DJ, Meharg AA, Ferrer M, Taggart MA, Penteriani V (2005) Lead concentrations in bones and feathers of the globally threatened Spanish imperial eagle. Biol Cons 121:603–610CrossRefGoogle Scholar
  42. 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
  43. Pattee OH, Wiemeyer SN, Mulhern B, Sileo L, Carpenter JW (1981) Experimental lead shot poisoning in bald eagles. J Wildl Manage 45:806–810CrossRefGoogle Scholar
  44. Pattee OH, Carpenter JW, Fritts SH, Rattner BA, Wiemeyer SN, Royle JA, Smith MR (2006) Lead poisoning in captive Andean condoirs (Vultur gryphus). J Wildl Dis 42:772–779CrossRefPubMedGoogle Scholar
  45. Rattner BA, Franson JC, Sheffield SR, Goddard CI, Leonard NJ, Stang D, Wingate PJ (2008) Impacts of lead ammunition and fishing tackle on natural resources. The Wildlife Society, Bethesda, MarylandGoogle Scholar
  46. Redig PT, Arent LR (2008) Raptor toxicology. Vet Clin North Am Exot Anim Pract 11:261–282CrossRefPubMedGoogle Scholar
  47. 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 21:72–77CrossRefPubMedGoogle Scholar
  48. Rodriguez-Ramos Fernandez J, Höfle U, Mateo R, Nicolas de Francisco O, Abbott R, Acevedo P, Blanco JM (2011) Assessment of lead exposure in Spanish imperial eagle (Aquila adalberti) from spent ammunition in central Spain. Ecotoxicology 20:670–681CrossRefPubMedGoogle Scholar
  49. Sanderson GC, Bellrose FC (1986) A review of the problem of lead poisoning in waterfowl. Illinois Natural History Survey Special Publication 4Google Scholar
  50. Schaub M, Zink R, Beissmann H, Sarrazin F, Arlettaz R (2009) When to end releases in reintroduction programmes: demographic rates and population viability analysis of beared vultures in the Alps. J Appl Ecol 46:92–100CrossRefGoogle Scholar
  51. Scheifler R, Coeurdassier M, Morilhat C, Bernard N, Faivre B, Flicoteaux P, Giraudoux P, Noël M, Piotte P, Rieffel D, de Vaufleury A, Badot PM (2006) Lead concentrations in feathers and blood of common blackbirds (Turdus merula) and in earthworms inhabiting unpollutes and moderately polluted urban ares. Sci Total Environ 371:197–205CrossRefPubMedGoogle Scholar
  52. Scheuhammer AM, Norris SL (1996) The ecotoxicology of lead shot and lead fishing weights. Ecotoxicology 5:279–295CrossRefPubMedGoogle Scholar
  53. Scheuhammer AM, Perrault JA, Routhier E, Braune BM, Campbell GD (1998) Elevated lead concentrations in edible portions of game birds harvested with lead shot. Environ Pollut 102:251–257CrossRefGoogle Scholar
  54. Sokal RR, Rohlf FJ (1995) Biometry. W.H. Freeman & Co, New YorkGoogle Scholar
  55. Stansley W, Murphy LA (2011) Liver lead concentrations in raptors in New Jersey, USA, 2008–2010. Bull Environ Contam Toxicol 87:171–174CrossRefPubMedGoogle Scholar
  56. Trinogga A, Fritscg 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 443:226–232CrossRefPubMedGoogle Scholar
  57. USFWS (1986) Use of lead shot for hunting migratory birds in the United States. Final supplement environmental impact statement. Washington, DC, Department of the Interior. Government Printing Office, Fish and Wildlife ServiceGoogle Scholar
  58. Wayland M, Neugebauer E, Bollinger T (1999) Concentrations of lead in liver, kidney, and bone of bald and golden eagles. Arch Environ Contam Toxicol 37:267–272CrossRefPubMedGoogle Scholar
  59. Zechner L, Steineck T, Tataruch F (2005) Bleivergiftung bei einem Steinadler (Aquila chrysaetos) in der Steiermark. Egretta 47:157–158Google Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2015

Authors and Affiliations

  • Lukas Jenni
    • 1
    Email author
  • Milena M. Madry
    • 2
  • Thomas Kraemer
    • 2
  • Jacqueline Kupper
    • 3
  • Hanspeter Naegeli
    • 3
  • Hannes Jenny
    • 4
  • David Jenny
    • 1
  1. 1.Swiss Ornithological InstituteSempachSwitzerland
  2. 2.Department of Forensic Pharmacology and Toxicology, Zurich Institute of Forensic MedicineUniversity of ZurichZurichSwitzerland
  3. 3.Institute of Veterinary Pharmacology and ToxicologyUniversity of Zürich-VetsuisseZurichSwitzerland
  4. 4.Fish and Game Department of the Canton of GrisonsChurSwitzerland

Personalised recommendations