Insight on trace element detoxification in the Black-tailed Godwit (Limosa limosa) through genetic, enzymatic and metallothionein analyses

Science of the Total Environment

Volumn 423, Issue , 2012, Pages 73-83

  Lucia, Magali ^a   Bocher, Pierrick ^a   Cosson, Richard P ^b   Churlaud, Carine ^a   Robin, Frédéric ^a   Bustamante, Paco ^a  

^a UNIVERSITÉ DE LA ROCHELLE   (France)

^b UNIVERSITÉ DE NANTES   (France)

Author keywords

Bioaccumulation; Biomarker; Genomic expression; Mercury; Metals; Shorebird

Indexed keywords

ANTIOXIDANT ENZYME ACTIVITY; ATLANTIC COASTS; BODY MASS; CARBON AND NITROGEN; CONTAMINANT CONCENTRATIONS; DETOXIFICATION MECHANISM; DIETARY PATTERNS; ELEVATED CONCENTRATIONS; GENOMIC EXPRESSION; GLUTATHIONE PEROXIDASE; METALLOTHIONEINS; MITOCHONDRIAL METABOLISM; PRELIMINARY ASSESSMENT; QUANTITATIVE REAL TIME PCR; REACTIVE OXYGEN SPECIES; SHOREBIRD; SUPER OXIDE DISMUTASE; THRESHOLD LEVELS; TRACE ELEMENT CONCENTRATIONS; TROPHIC POSITION; WHETHER DIFFERENCES;

BIOACCUMULATION; BIOCHEMISTRY; BIOMARKERS; CADMIUM; COPPER; DETOXIFICATION; GENE EXPRESSION; ISOTOPES; LEAD; MANGANESE; MERCURY (METAL); METALS; MUSCLE; NUTRITION; OXYGEN; POLYMERASE CHAIN REACTION; SILVER; TOXICITY;

POLLUTION;

ACETYL COENZYME A CARBOXYLASE; ARSENIC; BETA ACTIN; CADMIUM; CARBON; CATALASE; CHROMIUM; COBALT; COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C OXIDASE; FATTY ACID SYNTHASE; GLUTATHIONE PEROXIDASE; IRON; LEAD; LIPOPROTEIN LIPASE; MALATE DEHYDROGENASE (NADP); MANGANESE; MANGANESE SUPEROXIDE DISMUTASE; MERCURY; METALLOTHIONEIN; NICKEL; NITROGEN; REACTIVE OXYGEN METABOLITE; SELENIUM; SILVER; SUPEROXIDE DISMUTASE; TRACE ELEMENT; ZINC;

BIOACCUMULATION; BIOMARKER; CARBON ISOTOPE RATIO; CONCENTRATION (COMPOSITION); DETOXIFICATION; ENZYME; FEATHER; GENE EXPRESSION; GENETIC ANALYSIS; GENOMICS; MERCURY (ELEMENT); METABOLISM; METALLOTHIONEIN; MUSCLE; NITROGEN ISOTOPE; STABLE ISOTOPE; SUBLETHAL EFFECT; TOXICITY; TRACE ELEMENT; WADER;

ACC GENE; ACT GENE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIRD; BODY MASS; CAT GENE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORRELATION ANALYSIS; COX1 GENE; DETOXIFICATION; EATING HABIT; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; ENZYME ANALYSIS; FAS GENE; FEATHER; FOOD INTAKE; FRANCE; GENE; GENE EXPRESSION; GENETIC ANALYSIS; LINKAGE ANALYSIS; LIVER PARENCHYMA; LPL GENE; ME GENE; MITOCHONDRIAL RESPIRATION; MOLTING; MT GENE; MUSCLE TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SEASHORE; SOD1 GENE; SOD2 GENE;

ANIMALS; ARSENIC; AVIAN PROTEINS; BODY SIZE; CHARADRIIFORMES; DIET; FEATHERS; FEEDING BEHAVIOR; FRANCE; GENE EXPRESSION REGULATION; KIDNEY; LIVER; METABOLIC DETOXICATION, DRUG; METALLOTHIONEIN; METALS, HEAVY; MOLTING; MUSCLES; OXIDATIVE STRESS; SELENIUM;

AVES; LIMOSA; LIMOSA LIMOSA;

EID: 84859005548     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2012.02.005     Document Type: Article

References (77)

1. Adams S.M., Giesy J.P., Tremblay L.A., Eason C.T. The use of biomarkers in ecological risk assessment: recommendations from the Christchurch Conference on Biomarkers in Ecotoxicology. Biomarkers 2001, 6:1-6.
2. Alerstam T., Lindström A. Optimal bird migration: the relative importance of time, energy and safety. Bird migration: the physiology and ecophysiology 1990, 331-351. Springer, New York. E. Gwinner (Ed.).
3. Alerstam T., Hedenström A., Akesson S. Long-distance migration: evolution and determinants. Oikos 2003, 103:247-260.
4. Arai T., Ikemoto T., Hokura A., Terada Y., Kunito T., Tanabe S., et al. Chemical forms of mercury and cadmium accumulated in marine mammals and seabirds as determined by XAFS analysis. Environ Sci Technol 2004, 15:6468-6474.
5. Bearhop S., Waldron S., Thompson D., Furness R. Bioamplification of mercury in Great Skua Catharacta skua Chicks: the influence of trophic status as determined by stable isotope signatures of blood and feathers. Mar Pollut Bull 2000, 40:181-185.
6. Braune B.M., Noble D.G. Environmental contaminants in Canadian shorebirds. Environ Monit Assess 2009, 148:185-204.
7. Brdička A.R. Polarographic studies with the dropping mercury method. A new test for proteins in the presence of cobalt salts in ammoniacal solution of ammonium chloride. Collect Czech Chem Commun 1933, 7:112-128.
8. Burger J. Metals in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 1993, 5:203-311.
9. Burger J., Gochfeld M. Marine birds as sentinels of environmental pollution. Ecohealth 2004, 1:263-274.
10. Bustamante P., Miramand P. Interspecific and geographical variations of trace element concentrations in Pectinidae from European waters. Chemosphere 2004, 57:1355-1362.
11. Bustamante P., Miramand P. Subcellular and body distributions of 17 trace elements in the variegated scallop Chlamys varia from the Charente-Maritime coast (Bay of Biscay, France). Sci Total Environ 2005, 337:59-79.
12. Bustamante P., Lahaye V., Durnez C., Churlaud C., Caurant F. Total and organic Hg concentrations in cephalopods from the North East Atlantic waters: influence of geographical origin and feeding ecology. Sci Total Environ 2006, 368:585-596.
13. Cherel Y., Le Corre M., Jaquemet S., Ménard F., Richard P., Weimerskirch H. Resource partitioning within a tropical seabird community: new information from stable isotopes. Mar Ecol Prog Ser 2008, 366:281-291.
14. Cosson R.P., Amiard-Triquet C., Amiard J.C. Metallothionein and detoxification. Is the use of detoxification proteins for MTs a language abuse?. Water Air Soil Pollut 1991, 57-58:555-567.
15. De Luca-Abbott S.B., Wong B.S., Peakall D.B., Lam P.K., Young L., Lam M.H., et al. Review of effects of water pollution on the breeding success of waterbirds, with particular reference to ardeids in Hong Kong. Ecotoxicology 2001, 10:327-349.
16. Deisseroth A., Dounce A.L. Catalase: physical and chemical properties, mechanisms of catalysis, and physiological role. Physiol Rev 1970, 50:319-375.
17. Delany S., Scott D. Waterbird population estimates 2006, Wetlands International, Wageningen. 4th ed.
18. Delany S., Scott D., Dobman T., Stroud D. An atlas of wader population in Africa and Western Eurasia 2009, Wetlands International, Wageningen.
19. Donaldson G.M., Braune B.M. Sex-related levels of selenium, heavy metals, and organochlorine compounds in American White Pelicans (Pelecanus erythrorhyncos). Arch Environ Contam Toxicol 1999, 37:110-114.
20. Eisler R. A review of arsenic hazards to plants and animals with emphasis on fishery and wild life resources. Part II: human health and ecosystem effects 1994, 185-259. Wiley, New York. J.O. Nriagu (Ed.).
21. Eisler R. Silver hazards to fish, wildlife and invertebrates: a synoptic review. US Department of the Interior, National Biological Service, Report 32 1996.
22. Elliott J.E., Scheuhammer A.M. Heavy metal and metallothionein concentrations in seabirds from the Pacific coast of Canada. Mar Pollut Bull 1997, 34:794-801.
23. Elliott J.E., Scheuhammer A.M., Leighton F.A., Pearce P.A. Heavy metal and metallothionein concentrations in Atlantic Canadian seabirds. Arch Environ Contam Toxicol 1992, 22:63-73.
24. Gallien I., Caurant F., Bordes M., Bustamante P., Miramand P., Fernandez B., et al. Cadmium-containing granules in kidney tissue of the Atlantic white-sided dolphin (Lagenorhyncus acutus) off the Faroe Islands. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 2001, 130:389-395.
25. Gérard-Monnier D., Erdelmeier I., Régnard K., Moze-Henry N., Yadan J., Chaudière J. Reactions of 1-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Analytical applications to a colorimetric assay of lipid peroxidation. Chem Res Toxicol 1998, 11:1176-1183.
26. Gill J.A., Norris K., Potts P.M., Gunnarsson T.G., Atkinson P.W., Sutherland W.J. The buffer effect and large-scale population regulation in migratory birds. Nature 2001, 412:436-438.
27. Gill J.A., Langston R.H.W., Alves J.A., Atkinson P.W., Bocher P., Vieira N.C., et al. Contrasting trends in two Black-tailed Godwit populations: a review of causes and recommendations. Wader Study Group Bull 2007, 114:43-50.
28. Gochfeld M., Belant J.L., Shukla T., Benson T., Burger J. Heavy metals in laughing gulls: gender, age and tissue differences. Environ Toxicol Chem 1996, 15:2275-2283.
29. Gonzalez P., Dominique Y., Massabuau J.C., Boudou A., Bourdineaud J.P. Comparative effects of dietary methylmercury on gene expression in liver, skeletal muscle, and brain of the Zebrafish (Danio rerio). Environ Sci Technol 2005, 39:3972-3980.
30. Groen N.M., Hemerik L. Reproductive success and survival of black-tailed godwits Limosa limosa in a declining local population in The Netherlands. Ardea 2002, 90:239-248.
31. Hall B.D., Bodaly R.A., Fudge R.J.P., Rudd J.W.M., Rosenberg D.M. Food as the dominant pathway of methylmercury uptake by fish. Water Air Soil Pollut 1997, 100:13-24.
32. Halpern B.S., Walbridge S., Selkoe K.A., Kappel C.V., Micheli F., D'Agrosa C., et al. A global map of human impact on marine ecosystems. Science 2008, 319:948-952.
33. Heinz G.H. Selenium in birds. Environmental contaminants in wildlife: interpreting tissue concentrations 1996, 447-458. SETAC CRC, Lewis Publishers, Boca Raton. W.N. Beyer, G.H. Heinz, A.W. Redmon-Norwood (Eds.).
34. Henderson B.M., Winterfield R.W. Acute copper toxicosis in the Canada goose. Avian Dis 1975, 19:385-387.
35. Jardine T.D., Kidd K.A., Fisk A.T. Applications, considerations, and sources of uncertainty when using stable isotope analysis in ecotoxicology. Environ Sci Technol 2006, 40:7501-7511.
36. Kägi J.H. Overview of metallothionein. Methods Enzymol 1991, 205:613-626.
37. Kojadinovic J., Bustamante P., Churlaud C., Cosson R.P., Le Corre M. Mercury in seabird feathers: Insight on dietary habits and evidence for exposure levels in the western Indian Ocean. Sci Total Environ 2007, 384:194-204.
38. Kojadinovic J., Cosson R.P., Le Corre M., Bustamante P. Trace elements in three marine birds breeding on Reunion Island (Western Indian Ocean). Part 2: factors influencing their detoxification. Arch Environ Contam Toxicol 2007, 52:431-440.
39. Kunito T., Kubota R., Fujihara J., Agusa T., Tanabe S. Arsenic in marine mammals, seabirds, and sea turtles. Rev Environ Contam Toxicol 2008, 195:31-69.
40. Lourenço P.M., Piersma T. Stopover ecology of black-tailed godwits Limosa limosa limosa in Portuguese rice fields: a guide on where to feed in winter. Bird study 2008, 55:194-202.
41. Lucia M., André J.M., Gonzalez P., Baudrimont M., Gontier K., Maury-Brachet R., et al. Impact of cadmium on aquatic bird Cairina moschata. Biometals 2009, 22:843-853.
42. Lucia M., André J.M., Gonzalez P., Baudrimont M., Bernadet M.D., Gontier K., et al. Effect of dietary cadmium on lipid metabolism and storage of aquatic bird Cairina moschata. Ecotoxicology 2010, 19:163-170.
43. Luna-Acosta A., Bustamante P., Godefroy J., Fruitier-Arnaudin I., Thomas-Guyon H. Seasonal variation of pollution biomarkers to assess the impact on health status of juvenile Pacific oysters Crassostrea gigas exposed in situ. Environ Sci Pollut Res 2010, 17:999-1008.
44. ème contribution française aux dénombrements internationaux des oiseaux d'eau organisés par Wetlands International 2010, Office national de la chasse et de la faune Sauvage.
45. McCarty L.S., Munkittrick K.R. Environmental biomarkers in aquatic toxicology: fiction, fantasy, or functional?. Hum Environ Risk Assess 1996, 2:268-274.
46. Métian M., Bustamante P., Hédouin L., Warnau M. Accumulation of nine metals and one metalloid in the tropical scallop Comptopallium radula from coral reefs in New Caledonia. Environ Pollut 2008, 152:543-552.
47. Michener R.H., Kaufman L. Stable isotope ratios as tracers in marine food webs: an update. Stable isotopes in ecology and environmental science 2007, 238-282. Blackwell Publishing. R.H. Michener, K. Lajtha (Eds.).
48. Nam D.H., Anan Y., Ikemoto T., Kim E.Y., Tanabe S. Distribution of trace elements in subcellular fractions of three aquatic birds. Mar Pollut Bull 2005, 51:750-756.
49. Neff J.M. Ecotoxicology of arsenic in the marine environment. Environ Toxicol Chem 1997, 16:917-927.
50. Nigro M., Leonzio C. Intracellular storage of mercury and selenium in different marine vertebrates. Mar Ecol Prog Ser 1996, 135:137-143.
51. Nriagu J.O. A history of global metal pollution. Science 1996, 272:223-224.
52. Orieux N., Cambier S., Gonzalez P., Morin B., Adam C., Garnier-Laplace J., et al. Genotoxic damages in zebrafish submitted to a polymetallic gradient displayed by the Lot River (France). Ecotoxicol Environ Saf 2011, 74:974-983.
53. Outridge P.M., Scheuhammer A.M., Fox G.A., Braune B.M., White L.M., Gregorich L.J. An assessment of the potential hazards of environmental selenium for Canadian wildlife. Environ Rev 1999, 7:81-96.
54. Paglia D.E., Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967, 70:158-169.
55. Perez-Hurtado A., Goss-Custard J.D., Garcia F. The diet of wintering waders in Cádiz Bay, southwest Spain. Bird Study 1997, 44:45-52.
56. Peterson S.A., Ralston N.V.C., Peck D.V., Van Sickle J., Robertson J.D., Spate V.L., et al. How might selenium moderate the toxic effects of mercury in stream fish of the Western U.S.?. Environ Sci Technol 2009, 43:3919-3925.
57. Pierron F., Baudrimont M., Bossy A., Bourdineaud J.P., Brèthes D., Elie P., et al. Impairment of lipid storage by cadmium in the European eel (Anguilla anguilla). Aquat Toxicol 2007, 81:304-311.
58. Piersma T., van Gils J.A. The flexible phenotype: a body-centred integration of ecology, physiology and behaviour 2011, Oxford University Press Inc., New York. 1st ed.
59. Pigeot J., Miramand P., Guyot T., Sauriau P.G., Fichet D., Le Moine O., et al. Cadmium pathways in an exploited intertidal ecosystem with chronic cadmium inputs (Marennes-Oléron, Atlantic coast, France). Mar Ecol Prog Ser 2006, 307:101-114.
60. Quaintenne G., van Gils J.A., Bocher P., Dekinga A., Piersma T. Diet selection in a molluscivore shorebird across Western Europe: does it show short- or long-term intake rate-maximization?. J Anim Ecol 2010, 79:53-62.
61. Robin F. Dynamique de la distribution, sélection de l'habitat et stratégie d'alimentation chez la barge à queue noire limosa limosa à l'échelle des sites d'hivernage français 2011, University of La Rochelle, France.
62. Roodbergen M., Klok C., van der Hout A. Transfer of heavy metals in the food chain earthworm Black-tailed Godwit (Limosa limosa): comparison of a polluted and a reference site in The Netherlands. Sci Total Environ 2008, 406:407-412.
63. Rubenstein D.R., Hobson K.A. From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol Evol 2004, 19:256-263.
64. Schekkerman H., Teunissen W., Oosterveld E. Mortality of Black-tailed Godwit Limosa limosa and Northern Lapwing Vanellus vanellus chicks in wet grasslands: influence of predation and agriculture. J Ornithol 2009, 150:133-145.
65. Scheuhammer A.M. The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 1987, 46:263-295.
66. Skorupa J.P., Morman S.P., Sefchick-Edwards J.S. Guidelines for interpreting selenium exposure of biota associated with nonmarine aquatic habitats 1996, U.S. Fish and Wildlife Service, National Irrigation Water Quality Program.
67. Smith P., Khron R., Hermanson G., Mallia A., Gartner F., Provanzano M., et al. Measurement of protein using bicinchoninic acid. Anal Biochem 1985, 150:76-85.
68. Spallholz J.E., Hoffman D.J. Selenium toxicity: cause and effects in aquatic birds. Aquat Toxicol 2002, 57:27-37.
69. Stewart F.M., Furness R.W., Monteiro L.R. Relationships between heavy metal and metallothionein concentrations in lesser black-backed gulls, Larus fuscus, and Cory's shearwater, Calonectris diomedea. Arch Environ Contam Toxicol 1996, 30:299-305.
70. Stewart M.S., Neldner K.H., Spallholz J.E., Pence B.C. Selenite, selenocystamine, and selenomethionine have disparate abilities to impose oxidative stress and induce apoptosis in mouse keratinocytes. Free Radic Biol Med 1999, 26:42-48.
71. Stroud D.A., Baker A., Blanco D.E., Davidson N.C., Delany S., Ganter B., et al. The conservation and population status of the world's waders at the turn of the millennium. Waterbirds around the world 2006, 643-648. The Stationery Office, Edinburgh. G.C. Boere, C.A. Galbraith, D.A. Stroud (Eds.).
72. Thomas C.D., Cameron A., Green R.E., Bakkenes M., Beaumont L.J., Collingham Y.C., et al. Extinction risk from climate change. Nature 2004, 427:145-148.
73. Thompson J.A.J., Cosson R.P. An improved electrochemical method for the quantification of metallothionein in marine organism. Mar Environ Res 1984, 11:137-152.
74. Triplet P., Mahéo R. Le Drean Quenec'hdu S. La Barge à queue noire Limosa limosa islandica hivernant en France-Littoral Manche Atalntique, 1977-2006. Alauda 2007, 75:389-398.
75. Vitousek P.M., Mooney H.A., Lubchenco J., Melillo J.M. Human domination of Earth's ecosystems. Science 1997, 277:494-499.
76. Weber L.M., Haig S.M. Shorebird diet and size selection of Nereid Polychaetes in South Carolina coastal diked wetlands. J Field Ornithol 1997, 68:358-366.
77. Wooliams J.A., Wiener G., Anderson P.H., McMurray C.H. Variation in the activities of glutathione peroxidase and superoxide dismutase and in the concentration of copper in the blood in various breed crosses of sheep. Res Vet Sci 1983, 34:253-256.