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Ecotoxicology

, Volume 20, Issue 4, pp 670–681 | Cite as

Assessment of lead exposure in Spanish imperial eagle (Aquila adalberti) from spent ammunition in central Spain

  • Julia Rodriguez-Ramos FernandezEmail author
  • Ursula Höfle
  • Rafael Mateo
  • Olga Nicolas de Francisco
  • Rachel Abbott
  • Pelayo Acevedo
  • Juan Manuel Blanco
Article

Abstract

The Spanish imperial eagle (Aquila adalberti) is found only in the Iberian Peninsula and is considered one of the most threatened birds of prey in Europe. Here we analyze lead concentrations in bones (n = 84), livers (n = 15), primary feathers (n = 69), secondary feathers (n = 71) and blood feathers (n = 14) of 85 individuals collected between 1997 and 2008 in central Spain. Three birds (3.6%) had bone lead concentration > 20 μg/g and all livers were within background lead concentration. Bone lead concentrations increased with the age of the birds and were correlated with lead concentration in rachis of secondary feathers. Spatial aggregation of elevated bone lead concentration was found in some areas of Montes de Toledo. Lead concentrations in feathers were positively associated with the density of large game animals in the area where birds were found dead or injured. Discontinuous lead exposure in eagles was evidenced by differences in lead concentration in longitudinal portions of the rachis of feathers.

Keywords

Aquila adalberti Lead Spanish imperial eagle Spent ammunition 

Notes

Acknowledgments

Lead analyses performed at IREC were funded by a grant of the Spanish Ministry of Science (CGL2007-62797). P. Acevedo is currently holding a Juan de la Cierva research contract awarded by the Ministerio de Ciencia e Innovación—Fondo Social Europeo and partially by the project CGL2009-11316—FEDER. Use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Comments provided by C. Bunck, J.C. Franson and C.J. Johnson were appreciated. We would like to thank to EL Organismo Autónomo de Espacios Naturales de Castilla-La Mancha and EL Centro de Estudios de Rapaces Ibéricas.

References

  1. Acevedo P, Ruiz-Fons F, Estrada R, Marquez AL, Miranda MA, Gortazar C, Lucientes JA (2010) Broad assessment of factors determining Culicoides imicola abundance: modelling the present and forecasting its future in climate change scenarios. PLoS ONE 5:e14236Google Scholar
  2. Burger J (1993) Metals in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 5:203–311Google Scholar
  3. Burger J, Gochfeld M, Jeitner C, Burke S, Volz CD, Snigaroff R, Snigaroff D, Shukla T, Shukla S (2009) Mercury and other metals in eggs and feathers of glaucous-winged gulls (Larus glaucescens) in the Aleutians. Environ Monit Assess 152:179–194CrossRefGoogle Scholar
  4. Cardiel I, Taggart MA, Mateo R (in press) Using Pb–Al ratios to discriminate between internal and external deposition of Pb in feathers. Ecotoxicol Environ Saf. doi: 10.1016/j.ecoenv.2010.12.015
  5. Castaño Lopez JP (2005) El Águila Imperial Ibérica en Castilla La Mancha. Status, Ecología y Conservación. Graphitis Impresores, MadridGoogle Scholar
  6. 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(19):6143–6150CrossRefGoogle Scholar
  7. Delibes-Mateos M, Redpath SE, Angulo E, Ferreras P, Villafuerte R (2007) Rabbits as a keystone species in southern Europe. Biol Conserv 137:149–156CrossRefGoogle Scholar
  8. Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131:421–432CrossRefGoogle Scholar
  9. Friend M (1989) Lead poisoning: the invisible disease. In: Service USDOTIFAW (ed) Waterfowl management handbook. WashingtonGoogle Scholar
  10. Fry M (2004) Analysis of lead in California condor feathers: determination of exposure and depuration during feather growth. The Resources Agency. Department of Fish and Game. Habitat Conservation Branch, SacramentoGoogle Scholar
  11. Gangoso L, Alvarez-Lloret P, Rodriguez-Navarro AA, Mateo R, Hiraldo F, Donazar JA (2009) Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environ Pollut 157:569–574CrossRefGoogle Scholar
  12. Guitart R, To-Figueras J, Mateo R, Bertolero A, Cerradelo S, Martinez-Vilalta A (1994) Lead poisoning in waterfowl from the Ebro delta, Spain: calculation of lead exposure thresholds for Mallards. Arch Environ Contam Toxicol 27:289–293CrossRefGoogle Scholar
  13. 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
  14. Hernández M (1995) Lead poisoning in a free ranging imperial eagle. Suppl J Wildl Dis 31(3):NewsletterGoogle Scholar
  15. Hernández M, Margalida A (2008) Pesticide abuse in Europe: effects on the Cinereous vulture (Aegypius monachus) population in Spain. Ecotoxicology 17:264–272CrossRefGoogle Scholar
  16. Hernández M, Margalida A (2009) Assessing the risk of lead exposure for the conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) population. Environ Res 109:837–842CrossRefGoogle Scholar
  17. Höfle U, Blanco JM, Crespo E, Naranjo V, Jiménez-Clavero MA, Sanchez A, de la Fuente J, Gortazar C (2008) West Nile virus in the endangered Spanish imperial eagle. Vet Microbiol 129:171–178CrossRefGoogle Scholar
  18. Hunt WG, Burhham W (2006) Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildl Soc B 34:167–170CrossRefGoogle Scholar
  19. Hunt G, Burnham W, Parish C, Burnham K, Mutch B, Oaks JL (2009a) 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. doi: 10.4080/ilsa.2009.0123 Google Scholar
  20. Hunt WG, Parish CN, Orr K, Aguilar RF (2009b) Lead poisoning and the reintroduction of the California condor in northern Arizona. J Avian Med Surg 23:145–150CrossRefGoogle Scholar
  21. 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
  22. 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 48:417–424CrossRefGoogle Scholar
  23. 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 WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise. doi: 10.4080/ilsa.2009.0207 Google Scholar
  24. Landrigan PJ, Todd AC (1994) Lead poisoning. West J Med 161:153–159Google Scholar
  25. Lucio A (1991) Ordenación y gestión en caza menor. In: Fuentes A, Sánchez I, Pajuelo L (eds) Manual de ordenación y gestión cinegética. IFEBA, Badajoz, pp 219–255Google Scholar
  26. Manly BFJ (1997) Randomization, bootstrap, and Monte Carlo methods in biology, 2nd edn. Chapman and Hall, London, p 399Google Scholar
  27. Martí R, Moral JC (2003) Atlas de las Aves Reproductoras de España. Dirección General de Conservación de la Naturaleza-Sociedad Española de Ornitología, MadridGoogle Scholar
  28. Martinez-Lopez E, Martinez JE, Maria-Mojica P, Penalver J, Pulido M, Calvo JF, Garcia-Fernandez AJ (2004) Lead in feathers and delta-aminolevulinic acid dehydratase activity in three raptor species from an unpolluted Mediterranean forest (southeastern Spain). Arch Environ Contam Toxicol 47:270–275CrossRefGoogle Scholar
  29. Mateo R (2009) Lead poisoning in wild birds in Europe and the regulations adopted by the 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. doi: 10.4080/ilsa.2009.0107 Google Scholar
  30. Mateo R (2010) Toxicology and wildlife conservation in Europe: the inadequacy of current EU regulations. Vet J 183:241–242CrossRefGoogle Scholar
  31. Mateo R, Molina R, Grifols J, Guitart R (1997) Lead poisoning in a free ranging griffon vulture (Gyps fulvus). Vet Rec 140:47–48CrossRefGoogle Scholar
  32. Mateo R, Estrada J, Paquet JY, Riera X, Dominguez L, Guitart R, Martinez-Vilalta A (1999) Lead shot ingestion by marsh harriers Circus aeruginosus from the Ebro delta, Spain. Environ Pollut 104:435–440CrossRefGoogle Scholar
  33. 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
  34. Mateo R, Taggart M, Meharg AA (2003) Lead and arsenic in bones of birds of prey from Spain. Environ Pollut 126:107–114CrossRefGoogle Scholar
  35. Mateo R, Green AJ, Lefranc H, Baos R, Figuerola J (2007) Lead poisoning in wild birds from southern Spain: a comparative study of wetland areas and species affected, and trends over time. Ecotoxicol Environ Saf 66:119–126CrossRefGoogle Scholar
  36. MMA. Ministerio de Medio Ambiente (2007) Inventario Nacional de Biodiversidad. Vertebrados. http://www.mma.es/portal/secciones/biodiversidad/inventarios/inb/atlas_aves_reproductoras/pdf/aguila_imperial_iberica.pdf. Accessed Jan 2010
  37. Muñoz PM, Boadella M, Arnal MC, de Miguel MJ, Revilla M, Martínez D, Vicente J, Acevedo P, Oleaga A, Ruiz-Fons R, Marin CM, Prieto JM, de la Fuente J, Barral M, Barberán M, Fernández de Luco D, Blasco JM, Gortazar C (2010) Spatial distribution and risk factors of Brucellosis in Iberian wild ungulates. BMC Infect Dis 10:46CrossRefGoogle Scholar
  38. Pain DJ (1996) Lead in waterfowl. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife: interpreting tissue concentrations. SETAC. Special publication series. CRC Lewis Publisher, Boca Raton, pp 251–264Google Scholar
  39. Pain DJ, Bavoux C, Burneleau G (1997) Seasonal blood lead concentrations in Marsh Harriers (Circus aeruginosus) from Charente-Maritime, France: relationship with hunting season. Biol Conserv 81:1–7CrossRefGoogle Scholar
  40. Pain DJ, Meharg AA, Ferrer M, Taggart M, Penteriani V (2005) Lead concentrations in bones and feathers of the globally threatened Spanish imperial eagle. Biol Conserv 121:603–610CrossRefGoogle Scholar
  41. 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. doi: 10.4080/ilsa.2009.0107 Google Scholar
  42. Perez-Lopez M, Hermoso de Mendoza M, Lopez Beceiro A, Soler Rodriguez F (2008) Heavy metal (Cd, Lead, Zn) and metalloid (As) content in raptor species from Galicia (NW Spain). Ecotoxicol Environ Saf 70:154–162CrossRefGoogle Scholar
  43. Rattner BA, Golden NH, Toschik PC, McGowan PC, Custer TW (2008) Concentrations of metals in blood and feathers of nestling ospreys (Pandion haliaetus) in Chesapeake and Delaware Bays. Arch Environ Contam Toxicol 54:114–122CrossRefGoogle Scholar
  44. Redig PT, Arent LR (2008) Raptor toxicology. Vet Clin N Am Exot Anim Pract 11:261–282CrossRefGoogle Scholar
  45. Redig PT, Smith DR, Cruz-Martinez L (2009) Potential sources of Lead exposure for Bald eagles: a retrospective study. 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. doi: 10.4080/ilsa.2009.0208 Google Scholar
  46. Ríos Saldaña CA (2010) Los planes técnicos de caza de Castilla-La Mancha y su aplicación en la gestión y conservación de las especies cinegéticas. Unpublished PhD Thesis, University of Castilla-La Mancha, p 283Google Scholar
  47. Rodriguez-Ramos J, Gutierrez V, Hofle U, Mateo R, Monsalve L, Crespo E, Blanco JM (2009) Lead in Griffon and Cinereous vultures in central Spain: correlation between clinical signs and blood lead levels. Extended 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. doi: 10.4080/ilsa.2009.0208
  48. Rosenberg MS (2001) PASSAGE. Pattern analysis, spatial statistics and geographic exegesis. Version 1.0. Department of Biology, Arizona State University, TempeGoogle Scholar
  49. Saggese MD, Quaglia A, Lambertucci SA, Bo MA, Sarasola JH, Pereyra-Lobos R, Maceda JJ (2009) Survey of lead toxicosis in free-ranging raptors from Argentina. 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. doi: 10.4080/ilsa.2009.0208 Google Scholar
  50. Scheuhammer AM, Norris SL (1996) The ecotoxicology of lead shot and lead fishing weights. Ecotoxicology 5:279–295CrossRefGoogle Scholar
  51. Strochlic DE, Romero LM (2007) The effects of chronic psychological and physical stress on feather replacement in European starlings (Sturnus vulgaris). Comp Biochem Physiol A Mol Integr Physiol 149:68–79CrossRefGoogle Scholar
  52. Vicente J, Hofle U, Garrido JM, Fernandez-de-Mera IG, Acevedo P, Juste R, Barral M, Gortazar C (2007) Risk factors associated with the prevalence of tuberculosis-like lesions in fenced wild boar and red deer in south central Spain. Vet Res 38:451–464CrossRefGoogle Scholar
  53. Wayland M, Bollinger T (1999) Lead exposure and poisoning in Bald eagles and Golden eagles in the Canadian prairie province. Environ Pollut 104:341–350CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Julia Rodriguez-Ramos Fernandez
    • 1
    • 6
    Email author
  • Ursula Höfle
    • 1
  • Rafael Mateo
    • 1
  • Olga Nicolas de Francisco
    • 2
  • Rachel Abbott
    • 3
  • Pelayo Acevedo
    • 4
  • Juan Manuel Blanco
    • 5
  1. 1.National Institute of Game Research—Instituto de Investigación en Recursos Cinegéticos, IREC (UCLM-CSIC-JCCM)Ciudad RealSpain
  2. 2.Centro de Recuperación de VallcalentLleidaSpain
  3. 3.U.S. Geological Survey, National Wildlife Health CenterMadisonUSA
  4. 4.Biogeography, Diversity and Conservation Research Team, Department of Animal Biology, Faculty of SciencesUniversity of MalagaMalagaSpain
  5. 5.Center for Studies on Iberian Raptors—Centro de Estudios de Rapaces IbéricasSevilleja de la JaraSpain
  6. 6.Department of Pathobiological Sciences, School of Veterinary MedicineUniversity of WisconsinMadisonUSA

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