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.
Similar content being viewed by others
References
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:e14236
Burger J (1993) Metals in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 5:203–311
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 152:179–194
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
Castaño Lopez JP (2005) El Águila Imperial Ibérica en Castilla La Mancha. Status, Ecología y Conservación. Graphitis Impresores, Madrid
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):6143–6150
Delibes-Mateos M, Redpath SE, Angulo E, Ferreras P, Villafuerte R (2007) Rabbits as a keystone species in southern Europe. Biol Conserv 137:149–156
Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131:421–432
Friend M (1989) Lead poisoning: the invisible disease. In: Service USDOTIFAW (ed) Waterfowl management handbook. Washington
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, Sacramento
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 157:569–574
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 27:289–293
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 407:5555–5563
Hernández M (1995) Lead poisoning in a free ranging imperial eagle. Suppl J Wildl Dis 31(3):Newsletter
Hernández M, Margalida A (2008) Pesticide abuse in Europe: effects on the Cinereous vulture (Aegypius monachus) population in Spain. Ecotoxicology 17:264–272
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 109:837–842
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 129:171–178
Hunt WG, Burhham W (2006) Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildl Soc B 34:167–170
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
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 23:145–150
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 20:1831–1837
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 48:417–424
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
Landrigan PJ, Todd AC (1994) Lead poisoning. West J Med 161:153–159
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 219–255
Manly BFJ (1997) Randomization, bootstrap, and Monte Carlo methods in biology, 2nd edn. Chapman and Hall, London, p 399
Martí R, Moral JC (2003) Atlas de las Aves Reproductoras de España. Dirección General de Conservación de la Naturaleza-Sociedad Española de Ornitología, Madrid
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 47:270–275
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
Mateo R (2010) Toxicology and wildlife conservation in Europe: the inadequacy of current EU regulations. Vet J 183:241–242
Mateo R, Molina R, Grifols J, Guitart R (1997) Lead poisoning in a free ranging griffon vulture (Gyps fulvus). Vet Rec 140:47–48
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 104:435–440
Mateo R, Cadenas R, Manez M, Guitart R (2001) Lead shot ingestion in two raptor species from Doñana, Spain. Ecotoxicol Environ Saf 48:6–10
Mateo R, Taggart M, Meharg AA (2003) Lead and arsenic in bones of birds of prey from Spain. Environ Pollut 126:107–114
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 66:119–126
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
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 10:46
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 251–264
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 81:1–7
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 121:603–610
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
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 70:154–162
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 54:114–122
Redig PT, Arent LR (2008) Raptor toxicology. Vet Clin N Am Exot Anim Pract 11:261–282
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
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 283
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
Rosenberg MS (2001) PASSAGE. Pattern analysis, spatial statistics and geographic exegesis. Version 1.0. Department of Biology, Arizona State University, Tempe
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
Scheuhammer AM, Norris SL (1996) The ecotoxicology of lead shot and lead fishing weights. Ecotoxicology 5:279–295
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 149:68–79
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 38:451–464
Wayland M, Bollinger T (1999) Lead exposure and poisoning in Bald eagles and Golden eagles in the Canadian prairie province. Environ Pollut 104:341–350
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rodriguez-Ramos Fernandez, J., Höfle, U., Mateo, R. et al. Assessment of lead exposure in Spanish imperial eagle (Aquila adalberti) from spent ammunition in central Spain. Ecotoxicology 20, 670–681 (2011). https://doi.org/10.1007/s10646-011-0607-3
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-011-0607-3