Lead in terrestrial game birds from Spain
We analysed exposure to Pb and its relationship with lead-based ammunition in seven species of terrestrial game birds—common woodpigeon (Columba palumbus), rock dove (Columba livia), stock dove (Columba oenas), European turtle-dove (Streptopelia turtur), red-legged partridge (Alectoris rufa), Barbary partridge (Alectoris barbara) and common quail (Coturnix coturnix)—from rural and urban areas in different parts of Spain (Valencia, Castilla-La Mancha, Castilla y León, Madrid, Islas Canarias and Navarra). A total of 530 liver samples were analysed, and the presence of Pb pellets was studied in the crop, gizzard and intestine; the state and appearance of these organs were also analysed. The number of specimens suspected to have ingested Pb shot was 28 (5.6%), and the geometric mean concentration of hepatic Pb was 0.054 μg g−1 (wet weight, ww). A low percentage of samples (4.8%) were above the abnormal exposure threshold (0.65 μg g−1 ww), and, in these specimens, renal Pb concentrations were determined. Common woodpigeons and rock doves from Madrid were found to have high concentrations of Pb in their livers, and, so, both species can be considered to be good bioindicators of Pb contamination in rural (common woodpigeons) and urban (rock doves) environments. Partridges bred for hunting may be more prone to ingesting pellets from the environment, a fact that should be taken into account in management decisions.
KeywordsAmmunition Game birds Lead Liver Spain Terrestrial habitats
This study was funded by the Spanish Sectoral Federation of Weapons and Ammunition (FSA). The authors would like to thank Miguel A. Sánchez Isarria for his help in collecting samples, to Valentín Urrutia and Inma Salvat for their help in processing the samples, to Alberto Ferrer (Departamento de Estadística e Investigación Operativa Aplicadas y Calidad, Universidad Politécnica de Valencia) for the statistical treatment of the data, and to the Department of Animal Surgery at the Veterinary Clinical Hospital of the University of Murcia for conducting the X-ray analyses of the samples.
- Ákoshegyi I (1997) Lead poisoning of pheasants caused by lead shots. Magy Allatorvosok Lapja 119(6):328–330Google Scholar
- Anger H (1971) Gamebird diseases. The Game Conservancy Trust Annual Review 2:51–53Google Scholar
- ATSDR (2014) Agency for Toxic Substances and Disease Registry, Division of Toxicology and Environmental Medicine Atlanta, GA 30333 (April 2014), Support document to the 2013 priority list of hazardous substances that will be the subject of toxicological profiles. http://www.atsdr.cdc.gov/SPL/resources/ATSDR_2013_SPL_Support_Document.pdf.
- Calvert HS (1876) Pheasants poisoned by swallowing shot. The Field 47:189Google Scholar
- Castrale JS (1989) Availability of spent lead shot in fields managed for mourning dove hunting. Wildl Soc Bull 17:184–189Google Scholar
- Clausen B, Wolstrup C (1979) Lead poisoning in game from Denmark. Dan Rev Game Biol 11:1–22Google Scholar
- Conti JA (1993) Diseases, parasites, and contaminants. In: Baskett TS, Sayer MW, Tomlinson RE and Mirarchi RE (eds) Ecology and management of the mourning dove. Wildlife Management Institute, Washington, D.C., USA, p: 205–224.Google Scholar
- Descalzo E, Mateo R (2018) La contaminación por munición de plomo en Europa: el plumbismo aviar y las implicaciones en la seguridad de la carne de caza. Instituto de Investigación en Recursos Cinegéticos (IREC), Ciudad Real, Spain. 82 pp.Google Scholar
- Dieter MP (1979) Blood delta-aminolevulinic acid dehydratase (ALAD) to monitor lead contamination in canvasback ducks (Aythya valisineria). In: Nielsen SWG, Migaki G, Scarpelli DG (eds) Animals as monitors of environmental pollutants. Washington, D.C., National Academy of Sciences, pp 177–191Google Scholar
- ECHA (2018) Annex XV Investigation Report. A review of the available information on lead in shot used in terrestrial environments, in ammunition and in fishing tackle. European Chemicals Agency. In: https://echa.europa.eu/-/echa-identifies-risks-to-terrestrial-environment-from-lead-ammunition.
- EFSA (2010) Panel on Contaminants in the Food Chain (CONTAM). Scientific opinion on lead in food. EFSA Journal 8(4), 1570, 151 pp.Google Scholar
- Fontoura A, Gonçalves D, Guyomarc'h JC, Saint-Jalme M (2000) La sexualité précoce des populations hivernantes de Cailles des blés. Cah d'Ethologie 20:21–34Google Scholar
- Geochemical Atlas of Spain (2019) Geological and Mining Institute of Spain, Government of Spain’s Ministry of Science, Innovation and Universities. http://info.igme.es/geoquimica/ (accessed May 15, 2019).
- Harrison R (2012) Lead pollution: causes and control. Springer Science & Business Media, Berlin, GermanyGoogle Scholar
- Holladay JP, Nisanian M, Williams S, Tuckfield RC, Kerr R, Jarrett T, Tannenbaum L, Holladay SD, Sharma A, Gogal RM Jr (2012) Dosing of adult pigeons with as little as one #9 lead pellet caused severe δ-ALAD depression, suggesting potential adverse effects in wild populations. Ecotoxicology 21(8):2331–2337. https://doi.org/10.1007/s10646-012-0989-x CrossRefGoogle Scholar
- Holland G (1882) Pheasant poisoned by swallowing shot. The Field 59:232Google Scholar
- Kerr R, Holladay S, Jarrett T, Selcer B, Meldrum B, Williams S, Tannenbaum L, Holladay J, Williams J, Gogal R (2010) Lead pellet retention time and associated toxicity in northern bobwhite quail (Colinus virginianus). Environ Toxicol Chem 29(12):2869–2874. https://doi.org/10.1002/etc.355 CrossRefGoogle Scholar
- Keymer IF (1958) A survey and review of the causes of mortality in British birds and the significance of wild birds as disseminators of disease. Vet Rec 70:713–720Google Scholar
- Mcconnell CA (1968) Experimental lead poisoning of bobwhite quail and mourning doves. Proc Ann Conf Southeastern Assoc Game Fish Comm 21:208–219Google Scholar
- Mirarchi RE, Baskett TS (1994) Mourning dove (Zenaida macroura). In: Poole A, Gill F (eds) The birds of North America, 117. The American Ornithologist’s Union, Washington, D.C., USAGoogle Scholar
- Mur P (2009) L'hivernage de la Caille des blés Coturnix coturnix en France. Alauda 77:103–114Google Scholar
- Pain DJ, Cromie R, Green RE (2015) Poisoning of birds and other wildlife from ammunition-derived lead in the UK. In: Delahay RJ and Spray CJ (eds.) Proceedings of the Oxford Lead Symposium Lead Ammunition: understanding and minimising the risks to human and environmental health, 58–83.Google Scholar
- Pain DJ, Cromie RL, Newth J, Brown MJ, Crutcher E, Hardman P, Hurst L, Mateo R, Meharg AA, Moran AC, Raab A, Taggart MA, Green RE (2010) Potential hazard to human health from exposure to fragments of lead bullets and shot in the tissues of game animals. PLoS One 5(4):e10315. https://doi.org/10.1371/journal.pone.0010315 CrossRefGoogle Scholar
- 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, Idaho, USA, pp 99–118Google Scholar
- Pattee OH, Pain DJ (2003) Lead in the environment. In: Hoffman DJ, Rattner BA, Burton GA Jr, Cairns J Jr (eds) Handbook of ecotoxicology, Second edn. CRC Press, Boca Raton, Florida, USA, pp 373–408Google Scholar
- Patrick L (2006) Lead toxicity, a review of the literature. Part 1: exposure, evaluation, and treatment. Altern Med Rev 11(1):2–22Google Scholar
- Pokras MA, Kneeland MR (2009) Understanding lead uptake and effects across species lines: a conservation medicine based approach. 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, Idaho, USA, pp 7–22Google Scholar
- Schulz JH, Millspaugh JJ, Washburn BE, Wester GR, Lanigan JT III, Franson JC (2002) Spentshot availability and ingestion on areas managed for mourning doves. Wildl Soc Bull 30:112–120Google Scholar
- Soler-Rodríguez F, Oropesa-Jiménez AL, García-Cambero JP, Pérez-López M (2004) Lead exposition by gunshot ingestion in red-legged Partridge (Alectoris rufa). Vet Hum Toxicol 46:133–134Google Scholar
- Steinnes E (2013) Lead. In: Alloway B (ed) Heavy metals in soils. Environmental pollution, vol 22. Springer, Dordrecht.Google Scholar
- Tokar EJ, Boyd WA, Freedman JH, Waalkes MP (2013) Toxic effects of metals. In: Klaassen CD (ed) Casarett and Doull’s toxicology: the basic science of poisons. McGraw-Hill, New York, pp 981–1030Google Scholar
- Tranel MA, Kimmel RO (2009) Impacts of lead ammunition on wildlife, the environment, and human health—a literature review and implications for Minnesota. 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, Idaho, USA, pp 318–337Google Scholar
- US EPA (2003) United States Environmental Protection Agency. National air quality and emissions trends report—2003 special studies edition. EPA/454/R-03/005. Research Triangle Park, North Carolina, p 277Google Scholar
- US EPA (2014) United States Environmental Protection Agency. List of priority pollutants. URL https://www.epa.gov/sites/production/files/2015-09/documents/priority-pollutant-list-epa.pdf.
- Walter H, Reese KP (2003) Fall diet of chukars (Alectoris chukar) in eastern Oregon and discovery of ingested lead pellets. West N Am Nat 63(3):402–405Google Scholar
- Watson M (2004) The effects of raptors on grey partridge populations. University of Oxford, DPhil ThesisGoogle Scholar
- Williams RJ, Holladay SD, Williams SM, Gogal RM Jr (2017) Environmental lead and wild birds: a review. Rev Environ Contam Toxicol 245:157–180Google Scholar