Abstract
Cadmium, lead, mercury, selenium, iron, zinc and arsenic levels were measured in blood samples from 59 free-ranging white stork nestlings from colonies located in three different environmental conditions in Western Spain. The reference colony was situated in “Llanos de Cáceres y Sierra de Fuentes”, an Area of Special Interest for Bird Protection. A second colony was located close to (4.9 km) an urban landfill and a third one was close to both an intensive agricultural area and an urban landfill (1.5 km). Blood samples were diluted and elemental analysis was performed using inductively coupled plasma mass spectrometer. In all cases, the essential metals zinc and iron were found at the highest mean concentrations followed by lead > selenium > mercury > arsenic > cadmium. Regarding toxic metals, the highest concentrations were found for lead (ranging from 23.27 to 146.4 µg/L) although in all cases the concentrations were lower than those considered to cause subclinical effects. The metals levels detected in the chick’s blood were not related to the previously reported levels in the soil next to the colonies, which may indicate that landfills are the main source of metals in white stork nestlings. The present data showed that metal levels in white stork chicks may be influenced by the use of landfills as feeding areas by the parents. However, more studies on the metal content in the feed of white stork and the influence of the distance to the landfill are necessary to establish the causality of these findings.
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Álvarez CR, Moreno MJ, Alonso LL, Gómara B, Bernardo FG, Martín-Doimeadios RR, González M (2013) Mercury, methylmercury, and selenium in blood of bird species from Doñana National Park (Southwestern Spain) after a mining accident. Environ Sci Pollut Res Int 20:5371–5372
Baos R, Blas J, Bortolotti GR, Marchant TA, Hiraldo F (2006a) Adrenocortical response to stress and thyroid hormone status in free-living nestling white storks (Ciconia ciconia) exposed to heavy metal and arsenic contamination. Environ Health Perspect 114:1497–1501
Baos R, Forero MG, Gómez G, Gónzalez MJ, Hiraldo F, Jiménez B, Jovani R, Tella JL (2006b) Relationships between T-cell mediated immnune response and Pb, Zn, Cu, Cd, and As concentration in blood of nestling white storks (Ciconia ciconia) and Black kites (Milvus migrans) from Doñana (Southwestern Spain) after the Aznalcóllar toxic spill. Environ Toxicol Chem 25:1153–1159
Baos R, Jovani R, Serrano D, Tella JL, Hiraldo F (2012) Developmental exposure to a toxic spill compromises long-term reproductive performance in a wild, long-lived bird: the white stork (Ciconia ciconia). PLoS One 7:e34716
Benito V, Devesa V, Muñoz O, Suñer MA, Montoro R, Baos R, Hiraldo F, Ferrer M, Fernández M, González MJ (1999) Trace elements in blood collected from birds feeding in the area around Doñana National Park affected by the toxic spill from the Aznalcóllar mine. Sci Total Environ 6:309–323
Binkowski LJ, Meissner W (2013) Levels of metals in blood samples from Mallards (Anas platyrhynchos) from urban areas in Poland. Environ Pollut 178:336–342
Blanco G (1996) Population dynamics and communal roosting of white storks foraging at a Spanish refuse dump. Colonial Waterbirds 19:273–276
Blanco G, Frias O, Jimenez B, Gomez G (2003) Factors influencing variability and potential uptake routes of heavy metals in black kites exposed to emissions from a solid-waste incinerator. Environ Toxicol Chem 22:2711–2718
Blázquez E, Aguirre J, Martínez-Haro M, Mateo R, Jiménez B (2006) The use of white stork (Ciconia ciconia) nestlings in a biomonitoring programme for organochlorines through the region of Madrid (Spain). Organohalogen Compd 68:2081–2085
Burger J, Gochfeld M (1997) Age differences in metals in the blood of Herring (Larus argentatus) and Franklin’s (Larus pipixcan) gulls. Arch Environ Contam Toxicol 33:436–440
Cabo P, Espín S, Martínez-López E, Roscales JL, Jiménez B, García-Fernández AJ (2012) Metales pesados en sangre de pollos de Cigüeña blanca (Ciconia ciconia) de Madrid y Aragón. Rev Toxicol 29:72
Chen D, Martin P, Burgess NM, Champoux L, Elliott JE, Forsyth DJ, Idrissi A, Letcher RJ (2013) European starlings (Sturnus vulgaris) suggest that landfills are an important source of bioaccumulative flame retardants to Canadian terrestrial ecosystems. Environ Sci Technol 47:12238–12247
Clarkson TW, Weiss B, Cox C (1983) Public health consequences of heavy metals in dump sites. Environ Health Perspect 48:113–127
Cramp S, Simmons KEL (1980) The birds of the Western Palearctic. Oxford University Press, Oxford
Dallinga JH, Schoenmakers S (1987) Regional decrease in the number of white storks (Ciconia ciconia) in relation to food resources. Colon Waterbird 10:167–177
Directive 1999/31/CE of the European Parliament and of the Council of 26 April 1999 on the landfill of waste. Official Journal of the European Union 182, 1–19
Directive 2009/147/EC of the European Parliament and of the Council of 30 November 2009 on the conservation of wild birds. Official Journal of the European Union 20, 7–25
Domínguez JA, Moreno FA, González F, Pita MA (2011) Informe ambiental de Extremadura 2011. Consejería de Agricultura, Desarrollo Rural, Medio Ambiente y Energía de la Junta de Extremadura. http://extremambiente.gobex.es/. Accessed 3 Oct 2013
Earle CDA, Rhue RD, Earle JFK (1999) Mercury in a municipal solid waste landfill. Waste Manag Res 17:305–312
Elliott J, Scheuhammer A, Leighton F, Pearce P (1992) Heavy metal and metallothionein concentrations in Atlantic Canadian seabirds. Arch Environ Contam Toxicol 22:63–73
Evers DC, Savoy LJ, DeSorbo CR, Yates DE, Hanson W, Taylor KM, Siegel LS, Cooley JH, Bank MS, Major A, Munney K, Mower BF, Vogel HS, Schoch N, Pokras M, Goodale MW, Fair J (2008) Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17:69–81
Falandysz J, Jakuczun B, Mizera T (1988) Metals and organochlorines in four female white-tailed eagles. Mar Pollut Bull 19:521–526
Forastiere F, Badaloni C, DeHoogh D, von Kraus MK, Martuzzi M, Mitis F, Palkovicova L, Porta D, Presiss P, Ranzi A, Perucci AA, Briggs D (2011) Health impact assessment of waste management facilities in three European countries. Environ Health 10:53
Franson JC, Pain DJ (2011) Lead in birds. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota: interpreting tissue concentrations. CRC Press Taylor & Francis Group, Boca Raton, pp 563–593
García-Fernández AJ, Sánchez-García JA, Gómez-Zapata M, Luna A (1996) Distribution of cadmium in blood and tissues of wild birds. Arch Environ Contam Toxicol 30:252–258
García-Fernández AJ, Romero D, Martinez-López E, Navas I, Pulido M, Maria-Mojica P (2005) Environmental lead exposure in the European kestrel (Falco tinnunculus) from southeastern Spain: the influence of leaded gasoline regulations. Bull Environ Contam Toxicol 74:314–319
Goutner V, Becker P, Liordos V, Tsachalidis E (2011) Mercury in white stork (Ciconia ciconia) chick feathers from northeastern mediterranean areas in relation to age, brood size, and hatching order. Arch Environ Contam Toxicol 61:327–336
Hargreaves J, Adl MS, Warman PR (2008) A review of the use of composted municipal solid waste in agriculture. Agric Ecosyst Environ 123:1–14
Hernández AJ, Adarve-Alcazar MJ, Pastor J (1998) Some impacts of urban waste landfills on Mediterranean soils. Land Degrad Develop 9:21–33
Hernández LM, Gómara G, Fernández M, Jiménez B, González MJ, Baos R, Hiraldo F, Ferrer M, Benito V, Suner MA, Devesa V, Munoz O, Montoro R (1999) Accumulation of heavy metals and As in wetland birds in the area around Doñana National Park affected by the Aznalcóllar toxic spill. Sci Total Environ 242:293–308
Johnson BL, DeRosa CT (1995) Chemical mixtures released from hazardous waste sites: implications for health risk assessment. Toxicology 105:145–156
Kahle S, Becker PH (1999) Bird blood as bioindicator for mercury in the environment. Chemosphere 39:2451–2457
Kamiński P, Kurhalyuk N, Kasprzak M, Jerzak L, Tkachenko H, Szady-Grad M, Klawe JJ, Koim B (2009) The impact of element–element interactions on antioxidant enzymatic activity in the blood of white stork (Ciconia ciconia) chicks. Arch Environ Contam Toxicol 56:325–337
Khan S, Cao Q, Zheng Y, Huang Y, Zhu Y (2008) Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ Pollut 152:686–692
Khan K, Lu Y, Khan H, Ishtiaq M, Khan S, Waqas M, Wei L, Wang T (2013) Heavy metals in agricultural soils and crops and their health risks in Swat District, northern Pakistan. Food Chem Toxicol 58:449–458
Kruszyk R, Ciach M (2010) White Storks, Ciconia ciconia, forage on rubbish dumps in Poland: a novel behaviour in population. Eur J Wildlife Res 56:83–87
López-Arias M, Grau-Corbí JM (2005) Metales pesados, materia orgánica y otros parámetros de la capa superficial de los suelos agrícolas y de pastos de la España Peninsular. Resultados provinciales y puntuales. INIA, Madrid, II
Massemin-Challet S, Gendner JP, Samtmann S, Pichegru L, Wulgue A, Le Maho Y (2006) The effect of migration strategy and food availability on white stork Ciconia ciconia breeding success. Ibis 148:503–508
Matejczyk M, Plaza GA, Nalęcz-Jawecki G, Ulfig K, Markowska-Szczupak A (2011) Estimation of the environmental risk posed by landfills using chemical, microbiological and ecotoxicological testing of leachates. Chemosphere 82:1017–1023
Medina F, Avilés JM, Sánchez A (1998) Diferencias intraespecíficas en el uso de un vertedero por parte de la Cigüeña Blanca (Ciconia ciconia) en el oeste de la Península Ibérica. Butlletí del Grup Català d’Anellament 15:9–14
Merian E (1991) Metals and their compounds in the environment: occurrence, analysis and biological relevance. Wiley, Weinheim
Nordberg GF, Kjellstrom T, Nordberg M (1985) Kinetics and metabolism. In: Freiberg L, Elinder GC, Kjellstrom T, Nordberg GF (eds) Cadmium and health: a toxicological and epidemiological appraisal. Exposure dose and metabolism. CRC Press, Boca Raton, pp 103–178
Norris DO (2000) Endocrine disruptors of the stress axis in natural populations: how can we tell? Amer Zool 40:393–401
Pagana KD, Pagana TJ (2010) Mosby’s manual of diagnostic and laboratory tests, 4th edn. Mosby, St. Louis
Peakall DB, Lovett RJ (1972) Mercury: its occurrence and effects in the ecosystem. Bioscience 22:20–25
Peris SJ (2003) Feeding in urban refuse dumps: ingestion of plastic objects by the white stork (Ciconia ciconia). Ardeola 50:81–84
Rushton L (2003) Health hazards and waste management. Br Med Bull 68:183–197
Sáez M, Aguirre JI, Jiménez B (2009) Organochlorines in plasma of nestlings and adults white stork (Ciconia ciconia) from Madrid, Spain. Organohalogen Compd 71:2915–2918
Samuel MD, Bowers EF, Franson JC (1992) Lead exposure and recovery rates of black ducks banded in Tennessee. J Wildl Dis 28:555–561
Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295
Smith SR (2009) A critical review of the bioavailability and impacts of heavy metals in municipal solid waste composts compared to sewage sludge. Environ Int 35:142–156
Smits JE, Bortolotti GR, Baos R, Blas J, Hiraldo F, Xie Q (2005) Skeletal pathology in white storks (Ciconia ciconia) associated with heavy metal contamination in southwestern Spain. Toxicol Pathol 33:441–448
Spahn SA, Sherry TW (1999) Cadmium and lead exposure associated with reduced growth rates, poorer fledging success of Little Blue Heron chicks (Egretta caerulea) in South Louisiana Wetlands. Arch Environ Contam Toxicol 37:377–384
Stewart F, Furness R, Monteiro L (1996) Relationships between heavy metal and metallothionein concentrations in Lesser Black-Backed Gulls, Larus fuscus, and Cory’s Shearwater, Calonectris diomedea. Arch Environ Contam Toxicol 30:299–305
Tkachenko H, Kurhaluk N (2012) Pollution-induced oxidative stress and biochemical parameter alterations in the blood of white stork nestlings Ciconia ciconia from regions with different degrees of contamination in Poland. J Environ Monit 14:3182–3191
Tortosa F, Caballero J, Reyes-López J (2002) Effect of rubbish dumps on breeding success in the white stork in southern Spain. Waterbirds 25:39–43
U.S. Department of the Interior (U.S. DI) (1998) Guidelines for interpretation of the biological effects of selected constituents in biota, water, and sediment. National Irrigation Water Quality Program Information Report No 3. USDI, Denver
Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, New Jersey
Acknowledgments
Irene de la Casa-Resino was supported by fellowship PRE09001 from Consejería de Empleo, Empresa e Innovación (Gobierno de Extremadura, Spain).
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de la Casa-Resino, I., Hernández-Moreno, D., Castellano, A. et al. Breeding near a landfill may influence blood metals (Cd, Pb, Hg, Fe, Zn) and metalloids (Se, As) in white stork (Ciconia ciconia) nestlings. Ecotoxicology 23, 1377–1386 (2014). https://doi.org/10.1007/s10646-014-1280-0
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DOI: https://doi.org/10.1007/s10646-014-1280-0