[en] The spatiotemporal trends of mercury (Hg) are crucial for the understanding of this ubiquitous and toxic contaminant. However, uncertainties often arise from comparison among studies using different species, analytical and statistical methods. The long-term temporal trends of Hg exposure were reconstructed for a key sentinel species, the white-tailed eagle (Haliaeetus albicilla). Body feathers were sampled from museum collections covering 150 years in time (from 1866 to 2015) from West Greenland (n=124), Norway (n=102), and Sweden (n=87). A significant non-linear trend was observed in the Norwegian subpopulation, with a 60% increase in exposure occurring from 1866 to 1957 followed by a 40% decline until 2015. In the Swedish subpopulation, studied at a later period, the Hg exposure showed a drastic decline of 70% from 1967 to 2011. In contrast, no significant trend could be observed in the Greenland subpopulation. The additional analysis of dietary proxies (δ13C and δ15N) in general increased performance of the temporal trend models, but this was dependent on the subpopulation and study period. The downward trend of Hg coincided with the decreasing δ13C and δ15N in the Norwegian subpopulation, suggesting a potential dietary mitigation of Hg contamination. Hg exposure in both the Greenland and Norwegian subpopulations was consistently below the suggested threshold for adverse health effects (40 μg g−1), while the maximum exposure in the Swedish subpopulation was distinctively elevated (median: 46.0 μg g−1) and still remains well above natural background concentrations (maximum 5 μg g−1).
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Disciplines :
Zoology Environmental sciences & ecology
Author, co-author :
Sun, Jiachen; Universiteit Antwerpen - UA > Biology > Behavioural ecology and ecophysiology
Bustnes, Jan Ove; Norwegian Institute for Nature Research (NINA) > Artic ecology department
Helander, Björn; Museum of Natural History > Environmental Research & Monitoring
Bårdsen, Bård-Jørgen; Norwegian Institute for Nature Research > Arctic Ecology Department
Boertmann, David
Dietz, Rune
Jaspers, Veerle L.B.
Labansen, Aili Lage
Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
AMAP, AMAP assessment 2011: mercury in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), 2011, 193.
Appelquist, H., Asbirk, S., Drabæk, I., Mercury monitoring: mercury stability in bird feathers. Marine. Poll. Bull. 15 (1984), 22–24.
Beattie, S.A., Armstrong, D., Chaulk, A., Comte, J., Gosselin, M., Wang, F., Total and methylated mercury in Arctic multiyear sea ice. Environ. Sci. Technol. 48 (2014), 5575–5582.
Berg, W., Johnels, A., Sjöstrand, B., Westermark, T., Mercury content in feathers of Swedish birds from the past 100 years. Oikos 17 (1966), 71–83.
Bignert, A., Bäcklin, B.-M., Helander, B., Roos, A., Contaminants and health of aquatic wildlife. Norrgren, L., Levengood, J.M., (eds.) Ecosystem Health and Sustainable Agriculture. Ecology and Animal Health, 2012, Uppsala University, Uppsala, 73–85.
Bignert, A., Dahlgren, H., Danielsson, S., Faxneld, S., Kylberg, E., Nyberg, E., Vasileiou, M., Staveley Öhlund, J., Berger, U., Borg, H., Comments concerning the national Swedish contaminant monitoring programme in marine biota, 2014. Report 1. Swedish Museum of Natural History, 2014, 62–75.
Bignert, A., Danielsson, S., Faxneld, S., Nyberg, E., Comments Concerning the National Swedish Contaminant Monitoring Programme in Marine Biota, 2016. Report 5. 2016, Swedish Museum of Natural History, 73–85.
Blévin, P., Carravieri, A., Jaeger, A., Chastel, O., Bustamante, P., Cherel, Y., Wide range of mercury contamination in chicks of southern ocean seabirds. PLoS One, 8, 2013, e54508.
Boening, D.W., Ecological effects, transport, and fate of mercury: a general review. Chemosphere 40 (2000), 1335–1351.
Bond, A.L., Hobson, K.A., Branfireun, B.A., Rapidly increasing methyl mercury in endangered ivory gull (Pagophila eburnea) feathers over a 130 year record. Proc. R. Soc. B, 282, 2015, 20150032.
Bortolotti, G.R., Flaws and pitfalls in the chemical analysis of feathers: bad news–good news for avian chemoecology and toxicology. Ecol. Appl. 20 (2010), 1766–1774.
Bowerman, W.W., Evans, E.D., Giesy, J.P., Postupalsky, S., Using feathers to assess risk of mercury and selenium to bald eagle reproduction in the Great Lakes region. Arch. Environ. Contam. Toxicol. 27 (1994), 294–298.
Braune, B.M., Gaskin, D.E., Mercury levels in Bonaparte's gulls (Larus philadelphia) during autumn molt in the Quoddy region, New Brunswick, Canada. Arch. Environ. Contam. Toxicol. 16 (1987), 539–549.
Braune, B.M., Donaldson, G.M., Hobson, K.A., Contaminant residues in seabird eggs from the Canadian Arctic. II. Spatial trends and evidence from stable isotopes for intercolony differences. Environ. Pollut. 117 (2002), 133–145.
Braune, B.M., Gaston, A.J., Hobson, K.A., Gilchrist, H.G., Mallory, M.L., Changes in food web structure alter trends of mercury uptake at two seabird colonies in the Canadian Arctic. Environ. Sci. Technol. 48 (2014), 13246–13252.
Braune, B.M., Gaston, A.J., Mallory, M.L., Temporal trends of legacy organochlorines in eggs of Canadian Arctic seabirds monitored over four decades. Sci. Total Environ. 646 (2019), 551–563.
Burger, J., Gochfeld, M., Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. Environ. Res. 75 (1997), 160–172.
Burgess, N.M., Bond, A.L., Hebert, C.E., Neugebauer, E., Champoux, L., Mercury trends in herring gull (Larus argentatus) eggs from Atlantic Canada, 1972–2008: temporal change or dietary shift?. Environ. Pollut. 172 (2013), 216–222.
Chen, L., Zhang, W., Zhang, Y., Tong, Y., Liu, M., Wang, H., Xie, H., Wang, X., Historical and future trends in global source-receptor relationships of mercury. Sci. Total Environ. 610-611 (2018), 24–31.
Corman, A.-M., Schwemmer, P., Mercker, M., Asmus, H., Rüdel, H., Klein, R., Boner, M., Hofem, S., Koschorreck, J., Garthe, S., Decreasing δ13C and δ15N values in four coastal species at different trophic levels indicate a fundamental food-web shift in the southern North and Baltic Seas between 1988 and 2016. Environ. Monit. Assess., 190, 2018, 461.
Crewther, W.G., Fraser, R.D., Lennox, F.G., Lindley, H., The chemistry of keratins. Adv. Protein Chem. 20 (1965), 191–346.
Dietz, R., Riget, F., Cleemann, M., Aarkrog, A., Johansen, P., Hansen, J.C., Comparison of contaminants from different trophic levels and ecosystems. Sci. Total Environ. 245 (2000), 221–231.
Dietz, R., Riget, F., Boertmann, D., Sonne, C., Olsen, M.T., Fjeldså, J., Falk, K., Kirkegaard, M., Egevang, C., Asmund, G., Wille, F., Moller, S., Time trends of mercury in feathers of West Greenland birds of prey during 1851−2003. Environ. Sci. Technol. 40 (2006), 5911–5916.
Dietz, R., Outridge, P.M., Hobson, K.A., Anthropogenic contributions to mercury levels in present-day Arctic animals—a review. Sci. Total Environ. 407 (2009), 6120–6131.
Dietz, R., Mosbech, A., Flora, J., Eulaers, I., Interactions of climate, socio-economics, and global mercury pollution in the North Water. Ambio 47 (2018), 281–295.
Dittmann, T., Becker, P.H., Bakker, J., Bignert, A., Nyberg, E., Pereira, M.G., Pijanowska, U., Shore, R.F., Stienen, E., Toft, G.O., Marencic, H., Large-scale spatial pollution patterns around the North Sea indicated by coastal bird eggs within an EcoQO programme. Environ. Sci. Pollut. R. 19 (2012), 4060–4072.
Elmgren, R., Man's impact on the ecosystem of the Baltic sea: energy flows today and at the turn of the century. Ambio 18 (1989), 326–332.
EPA, U.S., Mercury in Solids and Solutions by Thermal Decomposition, Amalgamation, and Atomic Absorption Spectrophotometry. 1998, Environmental Protection Agency, Washington, DC.
Espín, S., García-Fernández, A., Herzke, D., Shore, R., van Hattum, B., Martínez-López, E., Coeurdassier, M., Eulaers, I., Fritsch, C., Gómez-Ramírez, P., Sampling and contaminant monitoring protocol for raptors. Research Networking Programme-EURAPMON, Research and Monitoring for and With Raptors in Europe, 2014.
Espín, S., García-Fernández, A.J., Herzke, D., Shore, R.F., van Hattum, B., Martínez-López, E., Coeurdassier, M., Eulaers, I., Fritsch, C., Gómez-Ramírez, P., Tracking pan-continental trends in environmental contamination using sentinel raptors—what types of samples should we use?. Ecotoxicology 25 (2016), 777–801.
Evers, D.C., Savoy, L.J., DeSorbo, C.R., Yates, D.E., Hanson, W., Taylor, K.M., Siegel, L.S., Cooley, J.H., Bank, M.S., Major, A., Munney, K., Mower, B.F., Vogel, H.S., Schoch, N., Pokras, M., Goodale, M.W., Fair, J., Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17 (2008), 69–81.
Falandysz, J., Jakuczun, B., Mizera, T., Metals and organochlorines in four female white-tailed eagles. Marine. Poll. Bull. 19 (1988), 521–526.
Farmer, R.G., Leonard, M.L., Long-term feeding ecology of great black-backed gulls (Larus marinus) in the northwest Atlantic: 110 years of feather isotope data. Can. J. Zool. 89 (2011), 123–133.
Forsman, D., The Raptors of Europe and the Middle East: A Handbook of Field Identification. 1999 (London).
Frederick, P.C., Hylton, B., Heath, J.A., Spalding, M.G., A historical record of mercury contamination in southern Florida (USA) as inferred from avian feather tissue: contribution R-09888 of the. Journal Series, Florida Agricultural Experiment Station. Environ. Toxicol. Chem. 23 (2009), 1474–1478.
Frøslie, A., Holt, G., Norheim, G., Mercury and persistent chlorinated hydrocarbons in owls Strigiformes and birds of prey Falconiformes collected in Norway during the period 1965–1983. Environ. Pollut. B. 11 (1986), 91–108.
Fu, L., Moncher, R.B., Severity distributions for GLMs: gamma or lognormal? Evidence from Monte Carlo simulations. Casualty Actuarial Society Discussion Paper Program, 2004, 149–230.
Goede, A.A., De Bruin, M., The use of bird feather parts as a monitor for metal pollution. Environ. Pollut. B. 8 (1984), 281–298.
Gruber, N., Keeling, C.D., Bacastow, R.B., Guenther, P.R., Lueker, T.J., Wahlen, M., Meijer, H.A., Mook, W.G., Stocker, T.F., Spatiotemporal patterns of carbon-13 in the global surface oceans and the oceanic Suess effect. Glob. Biogeochem. Cycles 13 (1999), 307–335.
Hailer, F., Helander, B., Folkestad, A., Ganusevich, S., Garstad, S., Hauff, P., Koren, C., Masterov, V., Nygård, T., Rudnick, J., Phylogeography of the white-tailed eagle, a generalist with large dispersal capacity. J. Biogeogr. 34 (2007), 1193–1206.
Head, J.A., DeBofsky, A., Hinshaw, J., Basu, N., Retrospective analysis of mercury content in feathers of birds collected from the state of Michigan (1895–2007). Ecotoxicology 20 (2011), 1636–1643.
Helander, B., Food Ecology of the White-tailed Sea Eagle Haliaeetus albicilla in Sweden, in: Reproduction of the White-tailed Sea Eagle Haliaeetus albicilla, in Relation to Food and Residue Levels of Organochlorine and Mercury Compounds in the Eggs. 1983 (Stockholm).
Helander, B., Olsson, M., Reutergårdh, L., Residue levels of organochlorine and mercury compounds in unhatched eggs and the relationships to breeding success in white-tailed sea eagles Haliaeetus albicilla in Sweden. Ecography 5 (1982), 349–366.
Helander, B., Marquiss, M., Bowerman, B., Sea Eagle 2000: Proceedings from the International Sea Eagle Conference in Björkö, Sweden, 13–17 September 2000. 2003 (Stockholm).
Honda, K., Min, B.Y., Tatsukawa, R., Distribution of heavy metals and their age-related changes in the Eastern great white egret, Egretta alba modesta, in Korea. Arch. Environ. Contam. Toxicol. 15 (1986), 185–197.
Jensen, S., Johnels, A.G., Olsson, M., Otterlind, G., DDT and PCB in herring and cod from the Baltic, the Kattegat and the Skagerrak. Ambio Special Report, 1972, 71–85.
Johnels, A., Germund, T., Westermark, T., A history of mercury levels in Swedish fauna. Ambio 8 (1979), 160–168.
Koivusaari, J., Nuuja, I., Palokangas, R., Hattula, M.-L., Chlorinated hydrocarbons and total mercury in the prey of the white-tailed eagle (Haliaeetus albicilla L.) in the Quarken Straits of the Gulf of Bothnia, Finland. Bull. Environ. Contam. Toxicol. 15 (1976), 235–241.
Koivusaari, J., Nuuja, I., Palokangas, R., Finnlund, M., Relationships between productivity, eggshell thickness and pollutant contents of addled eggs in the population of white-tailed eagles Haliaëtus albicilla L. in Finland during 1969–1978. Environ. Pollut. 23 (1980), 41–52.
Körtzinger, A., Quay, P.D., Sonnerup, R.E., Relationship between anthropogenic CO2 and the 13C Suess effect in the North Atlantic Ocean. Glob. Biogeochem. Cycles 17 (2003), 1–20.
Kovács, A., Mammen, U.C.C., Wernham, C.V., European monitoring for raptors and owls: state of the art and future needs. Ambio 37 (2008), 408–412.
Lehtonen, K.K., Bignert, A., Bradshaw, C., Broeg, K., Schiedek, D., Chemical pollution and ecotoxicology. Snoeijs-Leijonmalm, P., Schubert, H., Radziejewska, T., (eds.) Biological Oceanography of the Baltic Sea, 2017, Springer Netherlands, Dordrecht, 547–587.
Lindberg, P., Odsjö, T., Mercury levels in feathers of peregrine falcon Falco peregrinus compared with total mercury content in some of its prey species in Sweden. Environ. Pollut. B. 5 (1983), 297–318.
Lindqvist, O., Johansson, K., Bringmark, L., Timm, B., Aastrup, M., Andersson, A., Hovsenius, G., Håkanson, L., Iverfeldt, Å., Meili, M., Mercury in the Swedish environment — recent research on causes, consequences and corrective methods. Water Air Soil Pollut. 55 (1991), 1–261.
Marra, G., Wood, S.N., Practical variable selection for generalized additive models. Comput. Stat. Data Anal. 55 (2011), 2372–2387.
Mizutani, H., Fukuda, M., Kabaya, Y., Wada, E., Carbon isotope ratio of feathers reveals feeding behavior of cormorants. Auk 107 (1990), 400–403.
Mizutani, H., Fukuda, M., Kabaya, Y., C13 and N15 enrichment factors of feathers of 11 species of adult birds. Ecology 73 (1992), 1391–1395.
Mlíkovský, J., The food of the white-tailed sea eagle (Haliaeetus albicilla) at Lake Baikal, East Siberia. Slovak Raptor J 3 (2009), 35–39.
Monteiro, L.R., Furness, R.W., Kinetics, dose−response, and excretion of methylmercury in free-living adult Cory's shearwaters. Environ. Sci. Technol. 35 (2001), 739–746.
Movalli, P., Bode, P., Dekker, R., Fornasari, L., van der Mije, S., Yosef, R., Retrospective biomonitoring of mercury and other elements in museum feathers of common kestrel Falco tinnunculus using instrumental neutron activation analysis (INAA). Environ. Sci. Pollut. R. 24 (2017), 25986–26005.
Pettersson, O., Lehman, H., Reduced pesticide use in Scandinavian agriculture. Crit. Rev. Plant Sci. 13 (1994), 43–55.
Provencher, J.F., Mallory, M.L., Braune, B.M., Forbes, M.R., Gilchrist, H.G., Mercury and marine birds in Arctic Canada: effects, current trends, and why we should be paying closer attention. Environ. Rev. 22 (2014), 244–255.
R Core Team, R: A Language and Environment for Statistical Computing, Vienna. https://www.R-project.org/, 2018.
Renedo, M., Bustamante, P., Tessier, E., Pedrero, Z., Cherel, Y., Amouroux, D., Assessment of mercury speciation in feathers using species-specific isotope dilution analysis. Talanta 174 (2017), 100–110.
Rigét, F., Dietz, R., Born, E.W., Sonne, C., Hobson, K.A., Temporal trends of mercury in marine biota of west and northwest Greenland. Marine. Poll. Bull. 54 (2007), 72–80.
Rigét, F., Braune, B., Bignert, A., Wilson, S., Aars, J., Born, E., Dam, M., Dietz, R., Evans, M., Evans, T., Temporal trends of Hg in Arctic biota, an update. Sci. Total Environ. 409 (2011), 3520–3526.
Scheuhammer, A.M., Effects of acidification on the availability of toxic metals and calcium to wild birds and mammals. Environ. Pollut. 71 (1991), 329–375.
Skurdal, J., Qvenild, T., Skogheim, O.K., Mercury accumulation in five species of freshwater fish in Lake Tyrifjorden, south-east Norway, with emphasis on their suitability as test organisms. Environ. Biol. Fish 14 (1985), 233–237.
Sulkava, S., Tornberg, R., Koivusaari, J., Diet of the white-tailed eagle Haliaeetus albicilla in Finland. Ornis Fennica 74 (1997), 65–78.
Tagliabue, A., Bopp, L., Towards understanding global variability in ocean carbon-13. Glob. Biogeochem. Cycles 22 (2008), 1–13.
Thompson, D.R., Furness, R.W., Comparison of the levels of total and organic mercury in seabird feathers. Marine. Poll. Bull. 20 (1989), 577–579.
Thompson, D.R., Furness, R.W., Lewis, S.A., Diets and long-term changes in δ15N and δ13C values in northern fulmars Fulmarus glacialis from two northeast Atlantic colonies. Mar. Ecol. Prog. Ser. 125 (1995), 3–11.
Thompson, D.R., Bearhop, S., Speakman, J.R., Furness, R.W., Feathers as a means of monitoring mercury in seabirds: insights from stable isotope analysis. Environ. Pollut. 101 (1998), 193–200.
Vo, A.T.E., Bank, M.S., Shine, J.P., Edwards, S.V., Temporal increase in organic mercury in an endangered pelagic seabird assessed by century-old museum specimens. Proc. Natl. Acad. Sci. 108 (2011), 7466–7471.
Weech, S.A., Scheuhammer, A.M., Elliott, J.E., Mercury exposure and reproduction in fish-eating birds breeding in the Pinchi Lake region, British Columbia. Canada. Environ. Toxicol. Chem 25 (2009), 1433–1440.
Westermark, T., Odsjö, T., Johnels, A., Mercury content of bird feathers before and after Swedish ban on alkyl mercury in agriculture. Ambio 4 (1975), 87–92.
Wille, F., Kampp, K., Food of the white-tailed eagle Haliaeetus albicilla in Greenland. Ecography 6 (1983), 81–88.
Willgohs, J.F., The White-tailed Eagle Haliaëtus albicilla albicilla (Linné) in Norway. 1961 (Trondheim).
Wood, S.N., Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. Royal Stat. Soc. B. 73 (2011), 3–36.
Wood, S.N., P-splines with derivative based penalties and tensor product smoothing of unevenly distributed data. Stat. Comput. 27 (2017), 985–989.
Åkerblom, S., Bignert, A., Meili, M., Sonesten, L., Sundbom, M., Half a century of changing mercury levels in Swedish freshwater fish. Ambio 43 (2014), 91–103.