Effects of heavy metals on biomarkers for oxidative stress in Griffon vulture (Gyps fulvus)

Environmental Research

Volumn 129, Issue , 2014, Pages 59-68

  Espín, Silvia ^a,c   Martínez López, Emma ^a   Jiménez, Pedro ^a   María Mojica, Pedro ^a,b   García Fernández, Antonio J ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b Santa Faz Wildlife Recovery Centre   (Spain)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

Biomarkers; Griffon vulture; Gyps fulvus; Metals; Oxidative stress

Indexed keywords

BIOLOGICAL MARKER; CADMIUM; CATALASE; COPPER; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; HEMOGLOBIN; LEAD; MERCURY; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; ZINC;

ANTIOXIDANT; BIOMARKER; CADMIUM; CONCENTRATION (COMPOSITION); COPPER; DNA; ENZYME ACTIVITY; FOOD SUPPLEMENTATION; INHIBITION; LEAD; LIPID; PROTEIN; RAPTOR; TOXICITY; WILD POPULATION; ZINC;

ANIMAL CELL; ANIMAL FOOD; ANIMAL HUNTING; ARTICLE; BLOOD SAMPLING; BULLET; CARCASS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; ERYTHROCYTE; FEEDING; FOOD INTAKE; GRIFFON VULTURE; HEAVY METAL BLOOD LEVEL; MEAT; NONHUMAN; OXIDATIVE STRESS; PORK; PRIORITY JOURNAL; VULTURE (BIRD);

COMUNIDAD VALENCIA; SPAIN;

BIOMARKERS; GRIFFON VULTURE; GYPS FULVUS; METALS; OXIDATIVE STRESS;

ANIMALS; ANTIOXIDANTS; BIOLOGICAL MARKERS; ENVIRONMENTAL MONITORING; ENVIRONMENTAL POLLUTANTS; FALCONIFORMES; METALS, HEAVY; OXIDATIVE STRESS; SPAIN;

EID: 84893178629     PISSN: 00139351     EISSN: 10960953     Source Type: Journal    
DOI: 10.1016/j.envres.2013.11.008     Document Type: Article

References (83)

1. Alonso-Álvarez C., Pérez-Rodríguez L., Mateo R., Chastel O., Viñuela J. The oxidation handicap hypothesis and the carotenoid allocation trade-off. J. Evol. Biol. 2008, 21:1789-1797.
2. Berglund A.M.M., Sturve J., Förlin L., Nyholm N.E.I. Oxidative stress in pied flycatcher (Ficedula hypoleuca) nestlings from metal contaminated environments in northern Sweden. Environ. Res. 2007, 105:330-339.
3. Bettger W.J., O'Dell B.L. A critical physiological role of zinc in the structure and function of biomembranes. Life Sci. 1981, 28:1425-1438.
4. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
5. Cardiel I.E., Taggart M.A., Mateo R. Using Pb-Al ratios to discriminate between internal and external deposition of Pb in feathers. Ecotoxicol. Environ. Saf 2011, 74:911-917.
6. Clairbone A. Catalase Activity. CRC Handbook of Methods in Oxygen Radical Research 1985, CRC Press, boca Raton, FL. R.A. Greenwald (Ed.).
7. Costantini D., Verhulst S. Does high antioxidant capacity indicate low oxidative stress?. Funct. Ecol. 2009, 23:506-509.
8. Custer C.M., Custer T.W., Warburton D., Hoffman D.J., Bickham J.W., Matson C.W. Trace element concentrations and bioindicator responses in tree swallows from northwestern Minnesota. Environ. Monit. Assess. 2006, 118:247-266.
9. Del Moral J.C. El Buitre Leonado en España. Población Reproductora en 2008 y Método de Censo 2009, SEO/BirdLife, Madrid.
10. Dobado-Berrios P.M., Tella J.L., Ceballos O., Donazar J.A. Effects of age and captivity on plasma chemistry values of the Egyptian vulture. Condor 1998, 100:719.
11. Donázar J.A. Los buitres ibéricos. Biología y Conservación 1993, J.M. Reyero Editores, Madrid.
12. Donázar J.A., Palacios C.J., Gangoso L., Ceballos O., González M.J., Hiraldo F. Conservation status and limiting factors in the endangered population of Egyptian vulture (Neophron percnopterus) in the Canary Islands. Biol. Conserv. 2002, 107:89-97.
13. Dowling D.K., Simmons L.W. Reactive oxygen species as universal constraints in life-history evolution. Proc. Biol. Sci. 2009, 276:1737-1745.
14. Elia A.C., Galarini R., Taticchi M.I., Dörr A.J.M., Mantilacci L. Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol. Environ. Saf. 2003, 55:162-167.
15. Ercal N., Gurer-Orhan H., Aykin-Burns N. Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr. Top. Med. Chem. 2001, 1:529-539.
16. Espín S. Biomonitoring of Persistent Environmental Pollutants Using Feathers and Assessment of Sublethal Effects Using Oxidative Stress Biomarkers in Wildbirds. Doctoral thesis 2013, University of Murcia.
17. Espín S., Martínez-López E., Gómez-Ramírez P., María-Mojica P., García-Fernández A.J. Razorbills (Alca torda) as bioindicators of mercury pollution in the southwestern Mediterranean. Mar. Pollut. Bull. 2012, 64(11):2461-2470.
18. EU Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off. J. Eur. Union 2006, 364:5-24.
19. Evers D.C., Lane O.P., Savoy L., Goodale W. Assessing the impacts of methylmercury on piscivoress using a wildlife criterion value based on the common loon, 1998-2003 (No. Report BRI 2004-2005). Maine Dept. Environ. Protection, BioDiversity Res. Inst., Falmouth, Maine 2004.
20. ExPASy Bioinformatics Resource Portal 2012, Swiss Institute of Bioinformatics. http://www.expasy.org.
21. Ferguson-Lees J., Christie D.A. Raptors: Birds of Prey of the World 2001, A and C Black Publications, Ltd., London, U.K.
22. Flora S.J.S., Mittal M., Mehta A. Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J. Med. Res. 2008, 128:501-523.
23. Franson J.C. Interpretation of tissue lead residues in birds other than waterfowl. Environmental Contaminants in Wildlife. Interpreting Tissue Concentrations 1996, CRC Lewis Publishers, Boca Raton, Florida.
24. Frederick P., Jayasena N. Altered pairing behaviour and reproductive success in white ibises exposed to environmentally relevant concentrations of methylmercury. Proc. R. Soc. B rspb 2010, 2010:2189.
25. Gangoso L., Álvarez-Lloret P., Rodríguez-Navarro A.A.B., Mateo R., Hiraldo F., Donázar J.A. Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environ. Pollut. 2009, 157:569-574.
26. García-Fernández A.J. Impregnación por Plomo y Cadmio en aves Silvestres de la Región de Murcia. Tesis Doctoral 1994, Universidad de Murcia.
27. García-Fernández, A.J., Jiménez, P., María-Mojica, P., Navas, I., Molina, I., Godino, A., 2008. Intoxicación por plomo en Buitres leonados (Gyps fulvus). Presented at the Actas del Seminario Mortalidad por intoxicación en aves necrófagas. Problemática y soluciones, Aínsa, Huesca, Spain.
28. García-Fernández A.J., Martínez-López E., Romero D., María-Mojica P., Godino A., Jiménez P. High levels of blood lead in griffon vultures (Gyps fulvus) from Cazorla Natural Park (Southern Spain). Environ. Toxicol. 2005, 20:459-463.
29. García-Fernández A.J., Navas I., Martínez-López E., María-Mojica P., Romero D., Godino A., Jiménez P., Gerique C. Niveles de zinc y cobre en aves silvestres procedentes de centros de recuperación ¿sirven para monitorizar contaminación ambiental?. Rev. Toxicol. 2005, 22:115.
30. García-Fernández A.J., Sánchez-García J.A., Jiménez-Montalban P., Luna A. Lead and cadmium in wild birds in Southeastern Spain. Environ. Toxicol. Chem. 1995, 14:2049-2058.
31. Gómez-Ramírez P., Martínez-López E., María-Mojica P., León-Ortega M., García-Fernández A.J. Blood lead levels and δ-ALAD inhibition in nestlings of Eurasian Eagle Owl (Bubo bubo) to assess lead exposure associated to an abandoned mining area. Ecotoxicology 2011, 20:131-138.
32. Griffith O.W. Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic. Biol. Med. 1999, 27:922-935.
33. Gurer H., Ozgünes H., Neal R., Spitz D.R., Ercal N. Antioxidant effects of N-acetylcysteine and succimer in red blood cells from lead-exposed rats. Toxicology 1998, 128:181-189.
34. Gurer H., Ercal N. Can antioxidants be beneficial in the treatment of lead poisoning?. Free Radic. Biol. Med. 2000, 29:927-945.
35. Habig W.H., Pabst M.J., Jakoby W.B. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 1974, 249:7130-7139.
36. Halliwell B., Gutteridge J. Free Radicals in Biology and Medicine 1999, Oxford University Press, USA. 3rd ed.
37. Halliwell B., Gutteridge J. Free Radicals in Biology and Medicine 2007, Oxford University Press, USA. 4th ed.
38. Hernández M., Margalida A. Assessing the risk of lead exposure for the conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) population. Environ. Res. 2009, 109:837-842.
39. Hernández-García A. In vitro Evaluation of Effects Induced by Lead, Cadmium and Their Binary Mixtures on Erythrocytes of Three Species of Wild Birds. Doctoral thesis 2010, University of Murcia.
40. Hoffman D.J., Eagles-Smith C.A., Ackerman J.T., Adelsbach T.L., Stebbins K.R. Oxidative stress response of Forster's terns (Sterna forsteri) and Caspian terns (Hydroprogne caspia) to mercury and selenium bioaccumulation in liver, kidney, and brain. Environ. Toxicol. Chem. 2011, 30:920-929.
41. Hoffman D.J., Heinz G.H., Sileo L., Audet D.J., Campbell J.K., LeCaptain L.J. Developmental toxicity of lead-contaminated sediment to mallard ducklings. Arch. Environ. Contam. Toxicol. 2000, 39:221-232.
42. Hoffman D.J., Heinz G.H., Sileo L., Audet D.J., Campbell J.K., LeCaptain L.J., Obrecht H.H. Developmental toxicity of lead-contaminated sediment in Canada geese (Branta canadensis). J. Toxicol. Environ. Health Part A 2000, 59:235-252.
43. Hoffman D.J., Henny C.J., Hill E.F., Grove R.A., Kaiser J.L., Stebbins K.R. Mercury and drought along the Lower Carson River, Nevada: III. Effects on blood and organ biochemistry and histopathology of snowy egrets and black-crowned night-herons on Lahontan Reservoir, 2002-2006. J. Toxicol. Environ. Health, Part A 2009, 72:1223-1241.
44. Hoffman D.J., Ohlendorf H.M., Marn C.M., Pendleton G.W.P. Association of mercury and selenium with altered glutathione metabolism and oxidative stress in diving ducks from the San Francisco bay region, USA. Environ. Toxicol. Chem. 1998, 17:167-172.
45. Hoffman D.J., Pattee O.H., Wiemeyer S.N., Mulhern B. Effects of lead shot ingestion on delta-aminolevulinic acid dehydratase activity, hemoglobin concentration, and serum chemistry in bald eagles. J. Wildl. Dis. 1981, 17:423-431.
46. Hoffman D.J., Spalding M.G., Frederick P.C. Subchronic effects of methylmercury on plasma and organ biochemistries in great egret nestlings. Environ. Toxicol. Chem. 2005, 24:3078-3084.
47. Hsu J.M. Lead toxicity as related to glutathione metabolism. J. Nutr. 1981, 111:26-33.
48. Huang Y.L., Cheng S.L., Lin T.H. Lipid peroxidation in rats administrated with mercuric chloride. Biol. Trace Elem. Res. 1996, 52:193-206.
49. Hunt W.G., Burnham W., Parish C.N., Burnham K.K., Mutch B., Oaks J.L. Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildlife Soc. Bull. 2006, 34:167-170.
50. Jemec A., Drobne D., Tisler T., Trebse P., Ros M., Sepcić K. The applicability of acetylcholinesterase and glutathione S-transferase in Daphnia magna toxicity test. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2007, 144:303-309.
51. Ji X., Hu W., Cheng J., Yuan T., Xu F., Qu L., Wang W. Oxidative stress on domestic ducks (Shaoxing duck) chronically exposed in a Mercury-Selenium coexisting mining area in China. Ecotoxicol. Environ. Saf. 2006, 64:171-177.
52. Josephy D. Molecular Toxicology 1997, Oxford University Press, New York.
53. Kamiński P., Kurhalyuk N., Jerzak L., Kasprzak M., Tkachenko H., Klawe J.J., Szady-Grad M., Koim B., Wiśniewska E. Ecophysiological determinations of antioxidant enzymes and lipoperoxidation in the blood of White Stork Ciconia ciconia from Poland. Environ. Res. 2009, 109:29-39.
54. Klaassen C.D., Bracken W.M., Dudley R.E., Goering P.L., Hazelton G.A., Hjelle J.J. Role of sulfhydryls in the hepatotoxicity of organic and metallic compounds. Fundam. Appl. Toxicol. 1985, 5:806-815.
55. Knopper L.D., Mineau P., Scheuhammer A.M., Bond D.E., McKinnon D.T. Carcasses of Shot Richardson's ground squirrels may pose lead hazards to scavenging hawks. J. Wildlife Manag. 2006, 70:295-299.
56. Koivula M.J., Eeva T. Metal-related oxidative stress in birds. Environ. Pollut. 2010, 158:2359-2370.
57. Koivula M.J., Kanerva M., Salminen J.-P., Nikinmaa M., Eeva T. Metal pollution indirectly increases oxidative stress in great tit (Parus major) nestlings. Environ. Res. 2011, 111:362-370.
58. Martínez-Haro M., Green A.J., Mateo R. Effects of lead exposure on oxidative stress biomarkers and plasma biochemistry in waterbirds in the field. Environ. Res. 2011, 111:530-538.
59. Martínez-López E., Martínez J.E., María-Mojica P., Peñalver J., Pulido M., Calvo J.F., García-Fernández A.J. Lead in feathers and delta-aminolevulinic acid dehydratase activity in three raptor species from an unpolluted Mediterranean forest (Southeastern Spain). Arch. Environ. Contam. Toxicol. 2004, 47:270-275.
60. Mateo R., Beyer W.N., Spann J.W., Hoffman D.J., Ramis A. Relationship between oxidative stress, pathology, and behavioral signs of lead poisoning in mallards. J. Toxicol. Environ. Health Part A 2003, 66:1371-1389.
61. Mateo R., Hoffman D.J. Differences in oxidative stress between young Canada geese and mallards exposed to lead-contaminated sediment. J. Toxicol. Environ. Health Part A 2001, 64:531-545.
62. Mateo R., Taggart M., Meharg A.A. Lead and arsenic in bones of birds of prey from Spain. Environ. Pollut. 2003, 126:107-114.
63. McGowan C., Donaldson W. Changes in organ nonprotein sulfhydryl and glutathione concentrations during acute and chronic administration of inorganic lead to chicks. Biol. Trace Elem. Res. 1986, 10:37-46.
64. Order 1 Orden 1/2011, de 1 de julio, de la Conselleria de Infraestructuras, Territorio y Medio Ambiente, por la que se fijan los períodos hábiles de caza y se establecen las Vedas especiales para la temporada 2011-2012 en la Comunitat Valenciana. D. Ofic. Comunidad Valencia. 2011, 6560:27462-27469.
65. Pillai A., Laxmi Priya P.N., Gupta S. Effects of combined exposure to lead and cadmium on pituitary membrane of female rats. Arch. Toxicol. 2002, 76:671-675.
66. Polo F.J., Celdrán J.F., Peinado V.I., Viscor G., Palomeque J. Hematological values for four species of birds of prey. Condor 1992, 94:1007-1013.
67. Price D.J., Joshi J.G. Ferritin. Binding of beryllium and other divalent metal ions. J. Biol. Chem. 1983, 258:10873-10880.
68. Prohaska J.R., Ganther H.E. Glutathione peroxidase activity of glutathione-S-transferases purified from rat liver. Biochem. Biophys. Res. Commun. 1977, 76:437-445.
69. Rattan S.I.S. Hormesis in aging. Ageing Res. Rev. 2008, 7:63-78.
70. Reglero M.M., Taggart M.A., Monsalve-González L., Mateo R. Heavy metal exposure in large game from a lead mining area: effects on oxidative stress and fatty acid composition in liver. Environ. Pollut. 2009, 157:1388-1395.
71. Royal Decree 581 Royal Decree 581/2001, of June the 1st, on the prohibition of the use of hunting, leaded ammunition in certain protected wetlands. BOE 2001, 143:21284-21285.
72. Sandhir R., Gill K.D. Effect of lead on lipid peroxidation in liver of rats. Biol. Trace Elem. Res. 1995, 48:91-97.
73. Sandhir R., Julka D., Gill K.D. Lipoperoxidative damage on lead exposure in rat brain and its implications on membrane bound enzymes. Pharmacol. Toxicol. 1994, 74:66-71.
74. Schrauzer G.N. Effects of selenium antagonists on cancer susceptibility: new aspects of chronic heavy metal toxicity. J. UOEH 1987, 9:208-215.
75. Shaikh Z.A., Vu T.T., Zaman K. Oxidative stress as a mechanism of chronic cadmium-induced hepatotoxicity and renal toxicity and protection by antioxidants. Toxicol. Appl. Pharmacol. 1999, 154:256-263.
76. Shlosberg A., Wu Q., Rumbeiha W.K., Lehner A., Cuneah O., King R., Hatzofe O., Kannan K., Johnson M. Examination of Eurasian griffon vultures (Gyps fulvus fulvus) in Israel for exposure to environmental toxicants using dried blood spots. Arch. Environ. Contam. Toxicol. 2012, 62:502-511.
77. Snoeijs T., Dauwe T., Pinxten R., Vandesande F., Eens M. Heavy metal exposure affects the humoral immune response in a free-living small songbird, the Great Tit (Parus major). Arch. Environ. Contam. Toxicol. 2004, 46:399-404.
78. Somashekaraiah B.V., Padmaja K., Prasad A.R. Lead-induced lipid peroxidation and antioxidant defense components of developing chick embryos. Free Radic. Biol. Med. 1992, 13:107-114.
79. Stohs S.J., Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 1993, 18:321-336.
80. Sullivan J.F., Jetton M.M., Hahn H.K., Burch R.E. Enhanced lipid peroxidation in liver microsomes of zinc-deficient rats. Am. J. Clin. Nutr. 1980, 33:51-56.
81. Valavanidis A., Vlahogianni T., Dassenakis M., Scoullos M. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol. Environ. Saf. 2006, 64:178-189.
82. Villegas A., Sánchez J.M., Costillo E., Corbacho C. Blood chemistry and haematocrit of the black vulture (Aegypius monachus). Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 2002, 132:489-497.
83. Zolfaghari G., Esmaili-Sari A., Ghasempouri S.M., Kiabi B.H. Examination of mercury concentration in the feathers of 18 species of birds in southwest Iran. Environ. Res. 2007, 104:258-265.