[en] Our study reports the first data on mercury (Hg) isotope composition in marine European fish, for
seven distinct populations of the European seabass, Dicentrarchus labrax. The use of δ20230 Hg and Δ19931 Hg values in SIBER enabled us to estimate Hg isotopic niches, successfully discriminating several populations. Recursive-partitioning analyses demonstrated the relevance of Hg stable isotopes as discriminating tools. Hg isotopic values also provided insight on Hg contamination sources for biota in coastal environment. The overall narrow range of δ202 Hg around Europe was suggested to be related to a global atmospheric contamination while δ202 Hg at some sites was linked either to background ontamination, or with local contamination sources. Δ199 Hg was related to Hg levels of fish but we also suggest a relation with ecological conditions. Throughout this study, results from the Black Sea population stood out, displaying a Hg cycling similar to fresh water lakes. Our findings bring out the possibility to use Hg isotopes in order to discriminate distinct populations, to explore the Hg cycle on a large scale (Europe) and to distinguish sites contaminated by global versus local Hg source. The interest of using Hg sable isotopes to investigate the whole European Hg cycle is clearly highlighted.
Research center :
MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture [BE] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] ULg FSR - Université de Liège. Fonds spéciaux pour la recherche [BE]
National Research Council; Comittee on the toxicological effects of Methylmercury; Board on Environmental Studies and Toxicology; Toxicological Effects of Methylmercury; National Academy Press: Washington DC, 2000.
Boening, D. W. Ecological effects, transport, and fate of mercury: a general review Chemosphere 2000, 40 (12) 1335-1351 10.1016/S0045-6535(99)00283-0
OSPAR Commission. Quality status report 2010; The Commission, 2010.
UNEP. Global Mercury Assessment 2013: Sources, Emissions, Releases and Environmental Tansport; Geneva, Switzerland, 2013.
Storelli, M. M.; Giacominelli-Stuffler, R.; Marcotrigiano, G. Mercury accumulation and speciation in muscle tissue of different species of sharks from Mediterranean Sea, Italy Bull. Environ. Contam. Toxicol. 2002, 68 (2) 201-210 10.1007/s001280239
Storelli, M. M.; Ceci, E.; Storelli, A.; Marcotrigiano, G. O. Polychlorinated biphenyl, heavy metal and methylmercury residues in hammerhead sharks: contaminant status and assessment Mar. Pollut. Bull. 2003, 46 (8) 1035-1039 10.1016/S0025-326X(03)00119-X
Storelli, M. M.; Storelli, A.; Giacominelli-Stuffler, R.; Marcotrigiano, G. O. Mercury speciation in the muscle of two commercially important fish, hake (Merluccius merluccius) and striped mullet (Mullus barbatus) from the Mediterranean sea: estimated weekly intake Food Chem. 2005, 89 (2) 295-300 10.1016/j.foodchem.2004.02.036
Habran, S.; Debier, C.; Crocker, D. E.; Houser, D. S.; Das, K. Blood dynamics of mercury and selenium in northern elephant seals during the lactation period Environ. Pollut. 2011, 159 (10) 2523-2529 10.1016/j.envpol.2011.06.019
Das, K.; Siebert, U.; Gillet, A.; Dupont, A.; Di-Poï, C.; Fonfara, S.; Mazzucchelli, G.; De Pauw, E.; De Pauw-Gillet, M. C. Mercury immune toxicity in harbour seals: links to in vitro toxicity Environ. Health 2008, 7 (1) 52 10.1186/1476-069X-7-52
Bergquist, B. A.; Blum, J. D. The odds and evens of mercury isotopes: Applications of mass-dependent and mass-independent isotope fractionation Elements 2009, 5 (6) 353-357 10.2113/gselements.5.6.353
Lin, C. J.; Singhasuk, P.; Pehkonen, S. O. Environmental Chemistry and Toxicology of Mercury; Liu, G.; Cai, Y.; O'Driscoll, N., Eds.; John Wiley & Sons, Inc.: Hoboken, NJ, 2011.
Wiederhold, J. G.; Skyllberg, U.; Drott, A.; Jiskra, M.; Jonsson, S.; Björn, E.; Bourdon, B.; Kretzschmar, R. Mercury isotope signatures in contaminated sediments as a tracer for local industrial pollution sources Environ. Sci. Technol. 2015, 49 (1) 177-185 10.1021/es5044358
Blum, J. D.; Popp, B. N.; Drazen, J. C.; Anela Choy, C.; Johnson, M. W. Methylmercury production below the mixed layer in the North Pacific Ocean Nat. Geosci. 2013, 6 (10) 879-884 10.1038/ngeo1918
Fitzgerald, W. F.; Lamborg, C. H.; Hammerschmidt, C. R. Marine biogeochemical cycling of mercury Chem. Rev. 2007, 107 (2) 641-662 10.1021/cr050353m
Kwon, S. Y.; Blum, J. D.; Chen, C. Y.; Meattey, D. E.; Mason, R. P. Mercury Isotope Study of Sources and Exposure Pathways of Methylmercury in Estuarine Food Webs in the Northeastern U.S Environ. Sci. Technol. 2014, 48 (17) 10089-10097 10.1021/es5020554
Bergquist, B. A.; Blum, J. D. Mass-dependent and-independent fractionation of Hg isotopes by photoreduction in aquatic systems Science (Washington, DC, U. S.) 2007, 318 (5849) 417-420 10.1126/science.1148050
Blum, J. D.; Bergquist, B. A. Reporting of variations in the natural isotopic composition of mercury Anal. Bioanal. Chem. 2007, 388 (2) 353-359 10.1007/s00216-007-1236-9
Rodŕiguez-Gonźalez, P.; Epov, V. N.; Bridou, R.; Tessier, E.; Guyoneaud, R.; Monperrus, M.; Amouroux, D. Species-specific stable isotope fractionation of mercury during Hg(II) methylation by an anaerobic bacteria (Desulfobulbus propionicus) under dark conditions Environ. Sci. Technol. 2009, 43 (24) 9183-9188 10.1021/es902206j
Kritee, K.; Barkay, T.; Blum, J. D. Mass dependent stable isotope fractionation of mercury during mer mediated microbial degradation of monomethylmercury Geochim. Cosmochim. Acta 2009, 73 (5) 1285-1296 10.1016/j.gca.2008.11.038
Chen, C. Y.; Borsuk, M. E.; Bugge, D. M.; Hollweg, T.; Balcom, P. H.; Ward, D. M.; Williams, J.; Mason, R. P. Benthic and Pelagic Pathways of Methylmercury Bioaccumulation in Estuarine Food Webs of the Northeast United States PLoS One 2014, 9 (2) e89305 10.1371/journal.pone.0089305
Foucher, D.; Hintelmann, H. Tracing mercury contamination from the Idrija mining region (Slovenia) to the Gulf of Trieste using Hg isotope ratio measurements Environ. Sci. Technol. 2008, 43 (1) 33-39 10.1021/es801772b
Gehrke, G. E.; Blum, J. D.; Marvin-DiPasquale, M. Sources of mercury to San Francisco Bay surface sediment as revealed by mercury stable isotopes Geochim. Cosmochim. Acta 2011, 75 (3) 691-705 10.1016/j.gca.2010.11.012
Sherman, L. S.; Blum, J. D.; Dvonch, J. T.; Gratz, L. E.; Landis, M. S. The use of Pb, Sr, and Hg isotopes in Great Lakes precipitation as a tool for pollution source attribution Sci. Total Environ. 2015, 502, 362-374 10.1016/j.scitotenv.2014.09.034
Laffont, L. Fractionnement des isotopes stables de mercure dans un écosystème tropical en Amazonie bolivienne et dans les cheveux de populations humaines exposées; Université de Toulouse, Université Toulouse III-Paul Sabatier, 2009.
Gantner, N.; Hintelmann, H.; Zheng, W.; Muir, D. C. Variations in stable isotope fractionation of Hg in food webs of arctic lakes Environ. Sci. Technol. 2009, 43 (24) 9148-9154 10.1021/es901771r
Senn, D. B.; Chesney, E. J.; Blum, J. D.; Bank, M. S.; Maage, A.; Shine, J. P. Stable isotope (N, C, Hg) study of methylmercury sources and trophic transfer in the Northern Gulf of Mexico Environ. Sci. Technol. 2010, 44 (5) 1630-1637 10.1021/es902361j
Kwon, S. Y.; Blum, J. D.; Chirby, M. A.; Chesney, E. J. Application of mercury isotopes for tracing trophic transfer and internal distribution of mercury in marine fish feeding experiments Environ. Toxicol. Chem. 2013, 32 (10) 2322-2330 10.1002/etc.2313
Day, R. D.; Roseneau, D. G.; Berail, S.; Hobson, K. A.; Donard, O. F. X.; Vander Pol, S. S.; Pugh, R. S.; Moors, A. J.; Long, S. E.; Becker, P. R. Mercury Stable Isotopes in Seabird Eggs Reflect a Gradient from Terrestrial Geogenic to Oceanic Mercury Reservoirs Environ. Sci. Technol. 2012, 46 (10) 5327-5335 10.1021/es2047156
Loizeau, V.; Abarnou, A.; Ménesguen, A. A steady-state model of PCB bioaccumulation in the seabass (Dicentrarchus labrax) food web from the Seine estuary, France Estuaries 2001, 24 (6) 1074-1087 10.2307/1353019
Schnitzler, J. G.; Thomé, J. P.; Lepage, M.; Das, K. Organochlorine pesticides, polychlorinated biphenyls and trace elements in wild European seabass (Dicentrarchus labrax) off European estuaries Sci. Total Environ. 2011, 409 (19) 3680-3686 10.1016/j.scitotenv.2011.06.018
Pickett, G. D.; Pawson, M. G. Seabass: Biology, Exploitation and Conservation; Springer, 1994; Vol. 12.
Coelho, J. P.; Pereira, M. E.; Duarte, A.; Pardal, M. A. Macroalgae response to a mercury contamination gradient in a temperate coastal lagoon (Ria de Aveiro, Portugal) Estuarine, Coastal Shelf Sci. 2005, 65 (3) 492-500 10.1016/j.ecss.2005.06.020
Maury-Brachet, R.; Durrieu, G.; Dominique, Y.; Boudou, A. Mercury distribution in fish organs and food regimes: Significant relationships from twelve species collected in French Guiana (Amazonian basin) Sci. Total Environ. 2006, 368 (1) 262-270 10.1016/j.scitotenv.2005.09.077
Fritsch, M. Traits biologiques et exploitation du bar commun Dicentrarchus labrax (L.) dans les pêcheries françaises de la Manche et du golfe de Gascogne; Université de Bretagne Occidentale, 2005.
Remy, F.; Darchambeau, F.; Melchior, A.; Lepoint, G. Impact of food type on respiration, fractionation and turnover of carbon and nitrogen stable isotopes in the marine amphipod Gammarus aequicauda (Martynov, 1931) J. Exp. Mar. Biol. Ecol. 2017, 486, 358-367 10.1016/j.jembe.2016.10.031
Post, D. M. Using stable isotopes to estimate trophic position: models, methods, and assumptions Ecology 2002, 83 (3) 703-718 10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
Habran, S.; Crocker, D. E.; Debier, C.; Das, K. How are trace elements mobilized during the postweaning fast in Northern elephant seals? Environ. Toxicol. Chem. 2012, 31 (10) 2354-2365 10.1002/etc.1960
Rodríguez Martín-Doimeadios, R. C.; Krupp, E.; Amouroux, D.; Donard, O. F. X. Application of Isotopically Labeled Methylmercury for Isotope Dilution Analysis of Biological Samples Using Gas Chromatography/ICPMS Anal. Chem. 2002, 74 (11) 2505-2512 10.1021/ac011157s
Jackson, A. L.; Inger, R.; Parnell, A. C.; Bearhop, S. Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses in R J. Anim. Ecol. 2011, 80 (3) 595-602 10.1111/j.1365-2656.2011.01806.x
Therneau, T. M.; Atkinson, B. R port by Brian Ripley. rpart: Recursive Partitioning, R. 2011.
Team, R. C. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2014.
Strobl, C.; Malley, J.; Tutz, G. An introduction to recursive partitioning: rationale, application, and characteristics of classification and regression trees, bagging, and random forests Psychol. Methods 2009, 14 (4) 323 10.1037/a0016973
Zhang, H. Recursive partitioning and tree-based methods. In Handbook of computational statistics; Springer, 2012; pp 853-882.
Climate Europe www.climatedata.eu (accessed Mar 13, 2015).
Canty, J.; Frischling, B.; Frischling, D. Weatherbase www.weatherbase.com (accessed March 13, 2015).
Acquavita, A.; Covelli, S.; Emili, A.; Berto, D.; Faganeli, J.; Giani, M.; Horvat, M.; Koron, N.; Rampazzo, F. Mercury in the sediments of the Marano and Grado Lagoon (northern Adriatic Sea): Sources, distribution and speciation Estuarine, Coastal Shelf Sci. 2012, 113, 20-31 10.1016/j.ecss.2012.02.012
Bloom, N. S. On the Chemical Form of Mercury in Edible Fish and Marine Invertebrate Tissue Can. J. Fish. Aquat. Sci. 1992, 49 (5) 1010-1017 10.1139/f92-113
Trudel, M.; Rasmussen, J. B. Bioenergetics and mercury dynamics in fish: a modelling perspective Can. J. Fish. Aquat. Sci. 2006, 63 (8) 1890-1902 10.1139/f06-081
Kidd, K.; Clayden, M.; Jardine, T. Bioaccumulation and biomagnification of mercury through food webs. Environ. Chem. Toxicol. Mercury; Wiley: Hoboken, 2012, 455-499.
Scheuhammer, A. M.; Meyer, M. W.; Sandheinrich, M. B.; Murray, M. W. Effects of Environmental Methylmercury on the Health of Wild Birds, Mammals, and Fish Ambio 2007, 36 (1) 12-19 10.1579/0044-7447(2007)36[12:EOEMOT]2.0.CO;2
Mason, R. P.; Laporte, J. M.; Andres, S. Factors Controlling the Bioaccumulation of Mercury, Methylmercury, Arsenic, Selenium, and Cadmium by Freshwater Invertebrates and Fish Arch. Environ. Contam. Toxicol. 2000, 38 (3) 283-297 10.1007/s002449910038
Hrenchuk, L. E.; Blanchfield, P. J.; Paterson, M. J.; Hintelmann, H. H. Dietary and Waterborne Mercury Accumulation by Yellow Perch: A Field Experiment Environ. Sci. Technol. 2011, 46 (1) 509-516 10.1021/es202759q
Lorrain, A.; Graham, B. S.; Popp, B. N.; Allain, V.; Olson, R. J.; Hunt, B. P. V.; Potier, M.; Fry, B.; Galván-Magaña, F.; Menkes, C. E. R. et al. Nitrogen isotopic baselines and implications for estimating foraging habitat and trophic position of yellowfin tuna in the Indian and Pacific Oceans Deep Sea Res., Part II 2015, 113, 188-198 10.1016/j.dsr2.2014.02.003
Hobson, A. K. Tracing origins and migration of wildlife using stable isotopes: a review Oecologia 1999, 120 (3) 314-326 10.1007/s004420050865
França, S.; Vasconcelos, R. P.; Tanner, S.; Máguas, C.; Costa, M. J.; Cabral, H. N. Assessing food web dynamics and relative importance of organic matter sources for fish species in two Portuguese estuaries: a stable isotope approach Mar. Environ. Res. 2011, 72 (4) 204-215 10.1016/j.marenvres.2011.09.001
Pasquaud, S.; Elie, P.; Jeantet, C.; Billy, I.; Martinez, P.; Girardin, M. A preliminary investigation of the fish food web in the Gironde estuary, France, using dietary and stable isotope analyses Estuarine, Coastal Shelf Sci. 2008, 78 (2) 267-279 10.1016/j.ecss.2007.12.014
Barnes, C.; Jennings, S.; Polunin, N. V. C.; Lancaster, J. E. The importance of quantifying inherent variability when interpreting stable isotope field data Oecologia 2008, 155 (2) 227-235 10.1007/s00442-007-0904-y
Jennings, S.; van der Molen, J. Trophic levels of marine consumers from nitrogen stable isotope analysis: estimation and uncertainty ICES J. Mar. Sci. 2015, 72 (8) 2289-2300 10.1093/icesjms/fsv120
Spitz, J.; Chouvelon, T.; Cardinaud, M.; Kostecki, C.; Lorance, P. Prey preferences of adult seabass Dicentrarchus labrax in the northeastern Atlantic: implications for bycatch of common dolphin Delphinus delphis ICES J. Mar. Sci. 2013, 70 (2) 452-461 10.1093/icesjms/fss200
Das, K.; Holsbeek, L.; Browning, J.; Siebert, U.; Birkun, A.; Bouquegneau, J.-M. Trace metal and stable isotope measurements (delta13C and delta15N) in the harbour porpoise Phocoena phocoena relicta from the Black Sea Environ. Pollut. 2004, 131 (2) 197-204 10.1016/j.envpol.2004.02.006
Çoban-Ylldlz, Y.; Altabet, M. A.; Yllmaz, A.; Tuǧrul, S. Carbon and nitrogen isotopic ratios of suspended particulate organic matter (SPOM) in the Black Sea water column Deep Sea Res., Part II 2006, 53 (17-19) 1875-1892 10.1016/j.dsr2.2006.03.021
Joiris, C. R.; Holsbeek, L.; Bolba, D.; Gascard, C.; Stanev, T.; Komakhidze, A.; Baumgärtner, W.; Birkun, A. Total and Organic Mercury in the Black Sea Harbour Porpoise Phocoena phocoena relicta Mar. Pollut. Bull. 2001, 42 (10) 905-911 10.1016/S0025-326X(01)00049-2
Harmelin-Vivien, M.; Cossa, D.; Crochet, S.; Bǎnaru, D.; Letourneur, Y.; Mellon-Duval, C. Difference of mercury bioaccumulation in red mullets from the north-western Mediterranean and Black seas Mar. Pollut. Bull. 2009, 58 (5) 679-685 10.1016/j.marpolbul.2009.01.004
Akbal, F.; Gürel, L.; Bahadlr, T.; Güler, İ.; Bakan, G.; Büyükgüngör, H. Water and sediment quality assessment in the mid-Black Sea coast of Turkey using multivariate statistical techniques Environ. Earth Sci. 2011, 64 (5) 1387-1395 10.1007/s12665-011-0963-6
Sorokin, Y. U. I. The Black Sea. In Etuaries and Enclosed Seas: Ecosystems of the World; Elsevier: Amsterdam, 1983; pp 253-291.
Lamborg, C. H.; Yiǧiterhan, O.; Fitzgerald, W. F.; Balcom, P. H.; Hammerschmidt, C. R.; Murray, J. Vertical distribution of mercury species at two sites in the Western Black Sea Mar. Chem. 2008, 111 (1-2) 77-89 10.1016/j.marchem.2007.01.011
Driscoll, C. T.; Chen, C. Y.; Hammerschmidt, C. R.; Mason, R. P.; Gilmour, C. C.; Sunderland, E. M.; Greenfield, B. K.; Buckman, K. L.; Lamborg, C. H. Nutrient supply and mercury dynamics in marine ecosystems: A conceptual model Environ. Res. 2012, 119, 118-131 10.1016/j.envres.2012.05.002
Wang, W. X.; Wong, R. S. K. Bioaccumulation kinetics and exposure pathways of inorganic mercury and methylmercury in a marine fish, the sweetlips Plectorhinchus gibbosus Mar. Ecol.: Prog. Ser. 2003, 261, 257-268 10.3354/meps261257
Lin, C.-C.; Yee, N.; Barkay, T. Microbial transformations in the mercury cycle Environ. Chem. Toxicol. Mercur. 2012, 155-191 10.1002/9781118146644.ch5
Gehrke, G. E.; Blum, J. D.; Slotton, D. G.; Greenfield, B. K. Mercury Isotopes Link Mercury in San Francisco Bay Forage Fish to Surface Sediments Environ. Sci. Technol. 2011, 45 (4) 1264-1270 10.1021/es103053y
Point, D.; Sonke, J. E.; Day, R. D.; Roseneau, D. G.; Hobson, K. A.; Vander Pol, S. S.; Moors, A. J.; Pugh, R. S.; Donard, O. F. X.; Becker, P. R. Methylmercury photodegradation influenced by sea-ice cover in Arctic marine ecosystems Nat. Geosci. 2011, 4 (3) 188-194 10.1038/ngeo1049
Borysova, O.; Kondakov, A.; Paleari, S.; Rautalahti-Miettinen, E.; Stolberg, F.; Daler, D. Eutrophication in the Black Sea Region; Impact Assessment and Causal Chain Analysis; Kalmar, Sweden, 2005.
Perrot, V.; Pastukhov, M. V.; Epov, V. N.; Husted, S.; Donard, O. F. X.; Amouroux, D. Higher Mass-Independent Isotope Fractionation of Methylmercury in the Pelagic Food Web of Lake Baikal (Russia) Environ. Sci. Technol. 2012, 46 (11) 5902-5911 10.1021/es204572g
Kritee, K.; Blum, J. D.; Johnson, M. W.; Bergquist, B. A.; Barkay, T. Mercury stable isotope fractionation during reduction of Hg (II) to Hg (0) by mercury resistant microorganisms Environ. Sci. Technol. 2007, 41 (6) 1889-1895 10.1021/es062019t
Perrot, V.; Epov, V. N.; Pastukhov, M. V.; Grebenshchikova, V. I.; Zouiten, C.; Sonke, J. E.; Husted, S.; Donard, O. F. X.; Amouroux, D. Tracing Sources and Bioaccumulation of Mercury in Fish of Lake Baikal- Angara River Using Hg Isotopic Composition Environ. Sci. Technol. 2010, 44 (21) 8030-8037 10.1021/es101898e
Kwon, S. Y.; Blum, J. D.; Carvan, M. J.; Basu, N.; Head, J. A.; Madenjian, C. P.; David, S. R. Absence of Fractionation of Mercury Isotopes during Trophic Transfer of Methylmercury to Freshwater Fish in Captivity Environ. Sci. Technol. 2012, 46 (14) 7527-7534 10.1021/es300794q
Wang, R.; Feng, X.-B.; Wang, W.-X. In Vivo Mercury Methylation and Demethylation in Freshwater Tilapia Quantified by Mercury Stable Isotopes Environ. Sci. Technol. 2013, 47 (14) 7949-7957 10.1021/es3043774
Štrok, M.; Baya, P. A.; Hintelmann, H. The mercury isotope composition of Arctic coastal seawater C. R. Geosci. 2015, 347 (7) 368-376 10.1016/j.crte.2015.04.001
Mieiro, C.; Pacheco, M.; Pereira, M.; Duarte, A. Mercury Organotropism in Feral European Seabass (Dicentrarchus labrax) Arch. Environ. Contam. Toxicol. 2011, 61 (1) 135-143 10.1007/s00244-010-9591-5
