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Lead and cadmium in wild boar (Sus scrofa) in the Sierra Nevada Natural Space (southern Spain)

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Abstract

The aims of the present study were to investigate Pb and Cd levels in tissues of wild boar (Sus scrofa) from the Sierra Nevada Natural Space (SNNS) (southern Spain). Heavy metal concentrations in livers, kidneys and bones from 111 animals were determined by inductively coupled plasma optical emission spectrometry (ICP-OES). Bones and kidneys were the most Pb- and Cd-contaminated tissues, respectively; Cd concentrations were 5.6 times higher in kidneys than in livers. This is the first biomonitoring study of these pollutants in wild boar tissues in the SNNS, and findings indicate that this population is chronically exposed to these heavy metals. The detected Pb and Cd concentrations were lower than those found in many studies performed in Europe on the same species.

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References

  • Abadin H, Ashizawa A, Stevens YW, Llados F, Diamond G, Sage G, Citra M, Quinones A, Bosch SJ, Swarts SG (2007) Toxicological profile for lead. Agency for Toxic Substances and Disease Registry (US), Atlanta (GA)

  • Amici A, Danieli PP, Russo C, Primi R, Ronchi B (2012) Concentrations of some toxic and trace elements in wild boar (Sus scrofa) organs and tissues in different areas of the Province of Viterbo (Central Italy). Ital J Anim Sci 11(e65):354–362. doi:10.4081/ijas.2012.e65

    CAS  Google Scholar 

  • Bilandžić N, Sedak M, Vratarić D, Perić T, Šimić B (2009) Lead and cadmium in red deer and wild boar from different hunting grounds in Croatia. Sci Total Environ 407:4243–4247. doi:10.1016/j.scitotenv.2009.04.009

    Article  Google Scholar 

  • Bilandžić N, Sedak M, Đokić M, Šimić B (2010) Wild boar tissue levels of cadmium, lead and mercury in seven regions of continental Croatia. Bull Environ Contam Toxicol 84(6):738–743

  • Bilandžić N, Sedak M, Đokić M, Šimić B (2012) Heavy metal concentrations in tissues of wild boar of continental Croatia. IJEP 2:6–9

  • Bonet FJ, Pérez-Luque AJ, Moreno R, Zamora R (2010). Sierra Nevada Global Change Observatory. Structure and basic data. Environ Dep (Andalusian Reg. Gov). Granada 1–48.

  • Burger J, Fossi C, McClellan-Green P, Orlando EF (2007) Methodologies, bioindicators, and biomarkers for assessing gender-related differences in wildlife exposed to environmental chemicals. Environ Res 104:135–152. doi:10.1016/j.envres.2006.08.002

    Article  CAS  Google Scholar 

  • Commission decision of 19 July 2006 (2006/613/EC) adopting, pursuant to Council Directive 92/43/EEC, the list of sites of community importance for the Mediterranean biogeographical región. Official Journal of the European Union, L 259:1–104.

  • Commission Regulation (EC) N° 1881/2006 of 19 December 2006, setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union, L 364:5–24

  • Cook JA, Johnson MS (1996) Cadmium in small mammals. In: Beyer WN, Heinz GH, Redmond-Norwood A (eds) Environmental contaminants in wildlife. Interpreting tissue concentrations, 1996th edn. Lewis Publisher, Boca Raton, pp 377–388

    Google Scholar 

  • Cooke JA (2011) Cadmium in small mammals. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota. Interpreting tissue concentrations. CRC Press, Boca Raton, pp 627–642

    Chapter  Google Scholar 

  • Cortés-Gómez AA, Fuentes-Mascorro G, Romero D (2014) Metals and metalloids in whole blood and tissues of Olive Ridley turtles (Lepidochelys olivacea) from La Escobilla Beach (Oaxaca, Mexico). Mar Pollut Bull 89:367–75. doi:10.1016/j.marpolbul.2014.09.035

    Article  Google Scholar 

  • Council Directive 79/409/EEC of 2 April 1979 on the conservation of wild birds. CELEX-EUR Official Journal L 103:1–18

  • Cullen JT, Maldonado MT (2013) Biogeochemistry of cadmium and its release to the environment. Met Ions Life Sci 11:31–62. doi:10.1007/978-94-007-5179-8_2

    Article  CAS  Google Scholar 

  • Durkalec M, Szkoda J, Kołacz R, Opaliński S, Nawrocka A, Żmudzki J (2015) Bioaccumulation of lead, cadmium and mercury in roe deer and wild boars from areas with different levels of toxic metal pollution. Int J Environ Res 9:205–212

    CAS  Google Scholar 

  • Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Top Med Chem 1:529–539

    Article  CAS  Google Scholar 

  • Falandysz J, Szymczyk-Kobrzyńska K, Brzostowski A, Zalewski K, Zasadowski A (2005) Concentrations of heavy metals in the tissues of red deer (Cervus elaphus) from the region of Warmia and Mazury, Poland. Food Addit Contam 22:141–149. doi:10.1080/02652030500047273

    Article  CAS  Google Scholar 

  • Faroon O, Ashizawa A, Wright S, Tucker P, Jenkins K, Ingerman L, Rudisill C (2012) Toxicological profile for cadmium. Agency for Toxic Substances and Disease Registry (US), Atlanta (GA)

  • Gasparik J, Dobias M, Capcarova M, Smehyl P, Slamecka J, Bujko J (2012) Concentration of cadmium, mercury, zinc, copper and cobalt in the tissues of wild boar (Sus scrofa) hunted in the western Slovakia. J Environ Sci Heal A 47:1212–1216

  • Giambérini L, Cajaraville MP (2005) Lysosomal responses in the digestive gland of the freshwater mussel, Dreissena polymorpha, experimentally exposed to cadmium. Environ Res 98:210–214

    Article  Google Scholar 

  • Gisbert JA (2004) Intoxicación por otros metales. In: Villanueva Cañadas E, Gisbert Calabuig JA (eds) Medicina Legal y Toxicología. Elsevier Masson, Barcelona, pp 964–980

    Google Scholar 

  • Gómez-Ramírez P, Shore RF, van den Brink NW, van Hattum B, Bustnes JO, Duke G, Fritsch C, García-Fernández AJ, Helander BO, Jaspers V, Krone O, Martínez-López E, Mateo R, Movalli P, Sonne C (2014) An overview of existing raptor contaminant monitoring activities in Europe. Environ Int 67:12–21

    Article  Google Scholar 

  • Goyer RA (1996) Toxic effects of metals. In: Klaassen CD (ed.) Casarett and Doull’s toxicology: the basic science of poisons. McGraw-Hill, New York pp 691–736

  • Gust K, Fleeger J (2006) Exposure to cadmium-phenanthrene mixtures elicits complex toxic responses in the freshwater tubificid oligochaete, Ilyodrilus templetoni. Arch Environ Contam Toxicol 51:54–60. doi:10.1007/s00244-005-1075-7

    Article  CAS  Google Scholar 

  • Hermoso de Mendoza García M, Hernández Moreno D, Soler Rodríguez F, López Beceiro A, Fidalgo Alvarez LE, Pérez López M (2011) Sex- and age-dependent accumulation of heavy metals (Cd, Pb and Zn) in liver, kidney and muscle of roe deer (Capreolus capreolus) from NW Spain. J Env Sci Heal A Tox Hazard Subst Env Eng 46:109–116. doi:10.1080/10934529.2011.532422

    Article  Google Scholar 

  • Kakkar P, Jaffery FN (2005) Biological markers for metal toxicity. Environ Toxicol Pharmacol 19:335–349. doi:10.1016/j.etap.2004.09.003

    Article  CAS  Google Scholar 

  • Kenntner N, Krone O, Altenkamp R, Tataruch F (2003) Environmental contaminants in liver and kidney of free-ranging northern goshawks (Accipiter gentilis) from three regions of Germany. Arch Environ Contam Toxicol 45:128–135

    Article  CAS  Google Scholar 

  • Kottferová J, Koréneková B (1998) Distribution of Cd and Pb in the tissues and organs of free-living animals in the territory of Slovakia. Bull Environ Contam Toxicol 60:171–176. doi:10.1007/s001289900607

    Article  Google Scholar 

  • Kuiters AT (1996) Accumulation of cadmium and lead in red deer and wild boar at the Veluwe, the Netherlands. Vet Q 18(3):S134–S135. doi:10.1080/01652176.1996.9694715

    Article  CAS  Google Scholar 

  • Launer P, Kasten E, Graeser K, Hahnewald Th (1991) Schwermetalluntersuchungen bei Schwarzwild aus dem immissionsbelasteten Gebiet ‘Tharandter Wald’, Kreis Freital. Mh Vet Med 46:683–687

  • Ley 2/1989, de 18 de julio, por la que se aprueba el Inventario de Espacios Naturales Protegidos de Andalucía y se establecen medidas adicionales para su protección. BOE 201:27071–27129.

  • Ley 3/1999, de 11 de enero, por la que se crea el Parque Nacional de Sierra Nevada. BOE 11:1512–1525.

  • Ma WC (2011) Lead in mammals. In: Beyer W, Meador J (eds) Environmental contaminants in biota. Interpreting Tissue Concentrations, Boca Ratón, pp 595–608

    Chapter  Google Scholar 

  • Mandas L (2005) Problemi sanitari della fauna selvatica nelle oasi di protezione faunistica. In: Proc Reg Congr On Ambiente e sviluppo sostenibile: La nuova provincia del Medio Campidano - tutela e valorizzazione della fauna locale. Montevecchio (CA), Italy, pp 3–11

    Google Scholar 

  • Mankovská B (1990) Kumulácia t’azkých kovov v lesnej zveri. Záverecná správa, VÚLH Zvolen (Cited by J. Kottferová and B. Koréneková 1998).

  • Mao JS, Cao J, Graedel TE (2009) Losses to the environment from the multilevel cycle of anthropogenic lead. Environ Pollut 157:2670–2677. doi:10.1016/j.envpol.2009.05.003

    Article  CAS  Google Scholar 

  • Medvedev N (1999) Levels of heavy metals in Karelian wildlife, 1989–91. Environ Monit Assess 56:177–193. doi:10.1023/A:1005988511058

    Article  CAS  Google Scholar 

  • Michalska K, Zmudzki J (1992) Zawartosc metali w tkankach dzikow, saren i jeleni w regionie wielkopolskim. Medycyna Wet MDWTAG 48:145–192

  • Nawrot TS, Staessen JA, Roels HA, Munters E, Cuypers A, Richart T, Ruttens A, Smeets K, Clijsters H, Vangronsveld J (2010) Cadmium exposure in the population: from health risks to strategies of prevention. Biometals 23:769–782. doi:10.1007/s10534-010-9343-z

    Article  CAS  Google Scholar 

  • Nriagu JO (1989) A global assessment of natural sources of atmospheric trace metals. Nature 338:47–49. doi:10.1038/338047a0

    Article  CAS  Google Scholar 

  • Palero-Fernández FJ, Martín-Izard A (2005) Trace element contents in galena and sphalerite from ore deposits of the Alcudia Valley mineral field (Eastern Sierra Morena, Spain). J Geochemical Explor 86:1–25

    Article  Google Scholar 

  • Panek E, Zawodny Z (1993) Trace metals in the roadside mountain soils of Sierra Nevada, Spain. Environ Geochem Health 15:229–235

    Article  CAS  Google Scholar 

  • Patrick L (2006) Lead toxicity, a review of the literature. Part 1: exposure, evaluation, and treatment. Altern Med Rev 11:2–22

    Google Scholar 

  • Piskorová L, Vasilková Z, Krupicer I (2003) Heavy metal residues in tissues of wild boar (Sus scrofa) and red fox (Vulpes vulpes) in the Central Zeplim region of the Solvak Republic. Czch J Anim Sci 48:134–138

  • Pyatt FB, Pyatt AJ, Walker C, Sheen T, Grattan JP (2005) The heavy metal content of skeletons from an ancient metalliferous polluted area in southern Jordan with particular reference to bioaccumulation and human health. Ecotoxicol Environ Saf 60:295–300

    Article  CAS  Google Scholar 

  • Ráez-Bravo A, Granados JE, Cano-Manuel FJ, Soriguer RC, Fandos P, Pérez JM, Pavlov IY, Romero D (2015) Toxic and essential element concentrations in Iberian ibex (Capra pyrenaica) from the Sierra Nevada Natural Park (Spain): reference intervals in whole blood. Bull Environ Contam Toxicol 96:273–280. doi:10.1007/s00128-015-1711-5

    Article  Google Scholar 

  • Rani A, Kumar A, Lal A, Pant M (2014) Cellular mechanisms of cadmium-induced toxicity: a review. Int J Environ Health Res 24:378–399

    Article  CAS  Google Scholar 

  • Reglero MM, Taggart MA, Monsalve-González L, Mateo R (2009) Heavy metal exposure in large game from a lead mining area: effects on oxidative stress and fatty acid composition in liver. Environ Pollut 157:1388–1395. doi:10.1016/j.envpol.2008.11.036

    Article  CAS  Google Scholar 

  • Riget F, Dietz R, Vorkamp K, Johansen P, Muir D (2004) Levels and spatial and temporal trends of contaminants in Greenland biota: an updated review. Sci Total Environ 331:29–52

    Article  CAS  Google Scholar 

  • Rodríguez-Estival J, Martínez-Haro M, Monsalve-González L, Mateo R (2011a) Interactions between endogenous and dietary antioxidants against Pb-induced oxidative stress in wild ungulates from a Pb polluted mining area. Sci Total Environ 409:2725–2733. doi:10.1016/j.scitotenv.2011.04.010

    Article  Google Scholar 

  • Rodríguez-Estival J, Taggart MA, Mateo R (2011b) Alterations in vitamin A and E levels in liver and testis of wild ungulates from a lead mining area. Arch Environ Contam Toxicol 60:361–71. doi:10.1007/s00244-010-9597-z

    Article  Google Scholar 

  • Rodríguez-Estival J, Álvarez-Lloret P, Rodríguez-Navarro AB, Mateo R (2013a) Chronic effects of lead (Pb) on bone properties in red deer and wild boar: relationship with vitamins A and D3. Environ Pollut 174:142–149. doi:10.1016/j.envpol.2012.11.019

    Article  Google Scholar 

  • Rodríguez-Estival J, de la Lastra JM, Ortiz-Santaliestra ME, Vidal D, Mateo R (2013b) Expression of immunoregulatory genes and its relationship to lead exposure and lead-mediated oxidative stress in wild ungulates from an abandoned mining area. Environ Toxicol Chem 32:876–83. doi:10.1002/etc.2134

    Article  Google Scholar 

  • Roffe TJ, Work TM (2005) Wildlife health and disease investigations. In: Braun CE (ed) Techniques for wildlife investigations and management. The Wildlife Society, Bethesda, pp 197–212

    Google Scholar 

  • Rudy M (2009) The analysis of correlations between the age and the level of bioaccumulation of heavy metals in tissues and the chemical composition of sheep meat from the region in SE Poland. Food Chem Toxicol 47:1117–1122

    Article  CAS  Google Scholar 

  • Sánchez-Hernandez JC (2000) Trace element contamination in Antarctic ecosystems. Rev Environ Contam Toxicol 166:83–127

    Google Scholar 

  • Santiago D, Motas-Guzmán M, Reja A, María-Mojica P, Rodero B, García-Fernández AJ (1998) Lead and cadmium in red deer and wild boar from Sierra Morena Mountains (Andalusia, Spain). Bull Environ Contam Toxicol 61:730–737. doi:10.1007/s001289900822

    Article  CAS  Google Scholar 

  • Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295

    Article  CAS  Google Scholar 

  • Sevillano-Morales JS (2013) Metales Pesados en Especies Cinegéticas de Caza Mayor: estudio epidemiológico y riesgo alimentario. Córdoba, Servicio de Publicaciones de la Universidad de Córdoba

  • Skibniewski M, Skibniewska EM, Kośla T (2015) The content of selected metals in muscles of the red deer (Cervus elaphus) from Poland. Environ Sci Pollut Res Int 22:8425–8431. doi:10.1007/s11356-014-4007-0

    Article  CAS  Google Scholar 

  • Srebočan E, Crnić AP, Ekert-Kabalin AM, Lazarus M, Jurasović J, Tomljanović K, Andreić D, Perović IS, Čož-Rakovac R (2011) Cadmium, lead, and mercury concentrations in tissues of roe deer (Capreolus capreolus L.) and wild boar (Sus scrofa L.) from lowland Croatia. Czech J Food Sci 29:624–633

    Google Scholar 

  • Suttle NF (2010) Mineral nutrition of livestock. CAB International, Oxfordshire

    Book  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 981–1030

    Google Scholar 

  • Venäläinen ER, Anttila M, Peltonen K (2005) Heavy metals in tissue samples of Finnish moose, Alces alces. Bull Environ Contam Toxicol 74:526–536. doi:10.1007/s00128-005-0616-0

    Article  Google Scholar 

  • Wolkers H, Wensing T, Groot Bruinderink GW (1994) Heavy metal contamination in organs of red deer (Cervus elaphus) and wild boar (Sus scrofa) and the effect on some trace elements. Sci Total Environ 144:191–199. doi:10.1016/0048-9697(94)90438-3

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to the Dirección General de Medio Ambiente of the Junta de Andalucía for their flexibility in granting permits and to the managers of SNNS for their on-going support. The authors would also like to thank A. Sánchez, J. López, I. Puga, E. Martínez, M. Cárdenas, F. Casado, A. Rodríguez and the staff of Sierra Nevada National Park, who made the capture of the animals and the collection of samples possible. Thanks too are due to F. San Nicolás for the processing of the samples. The research activities were partially funded by the Junta de Andalucía, Plan Andaluz de Investigación (RNM-118 group).

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Authors and Affiliations

  1. Área de Toxicología, Facultad de Veterinaria. Campus Regional de Excelencia Internacional “Campus Mare Nostrum”, Universidad de Murcia, E-30071, Murcia, Spain

    Rocío Mulero & Diego Romero

  2. Parque Nacional y Parque Natural de Sierra Nevada. Ctra, Antigua de Sierra Nevada Km7, E-18071, Pinos Genil, Granada, Spain

    Javier Cano-Manuel & José E. Granados

  3. Agencia de Medio Ambiente y Agua, Consejería de Agricultura, Pesca y Alimentación. Gerencia de Granada, E-18013, Granada, Spain

    Javier Cano-Manuel & José E. Granados

  4. Servei d’Ecopatologia de Fauna Salvatge (SEFaS), Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona (UAB), Barcelona, Spain

    Arián Ráez-Bravo

  5. Dpto. Biología Animal, Biología Vegetal y Ecología, Universidad de Jaén, Campus las Lagunillas s/n, E-23071, Jaén, Spain

    Jesús M. Pérez & José Espinosa

  6. Estación Biológica de Doñana. CSIC, Avd. María Luisa s/n, E-41013, Sevilla, Spain

    Ramón Soriguer

  7. IREC. CSIC, Ronda de Toledo, 12, 13071, Ciudad Real, Spain

    Ramón Soriguer

  8. Agencia de Medio Ambiente y Agua, Consejería de Agricultura, Pesca y Alimentación. Servicios Centrales, E-41013, Sevilla, Spain

    Paulino Fandos

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  1. Rocío Mulero
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  2. Javier Cano-Manuel
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  3. Arián Ráez-Bravo
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  4. Jesús M. Pérez
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  5. José Espinosa
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  8. José E. Granados
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  9. Diego Romero
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Correspondence to Diego Romero.

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Mulero, R., Cano-Manuel, J., Ráez-Bravo, A. et al. Lead and cadmium in wild boar (Sus scrofa) in the Sierra Nevada Natural Space (southern Spain). Environ Sci Pollut Res 23, 16598–16608 (2016). https://doi.org/10.1007/s11356-016-6845-4

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