Temporal trends of legacy organochlorines in different white-tailed eagle (Haliaeetus albicilla) subpopulations: A retrospective investigation using archived feathers
Sun, Jiachen; Covaci, Adrian; Bustnes, Jan Oveet al.
2020 • In Environment International, 138, p. 105618
POPs; Museum collection; Organochlorines; Stable isotopes; Body feathers
Abstract :
[en] Understanding the spatiotemporal patterns of legacy organochlorines (OCs) is often difficult because monitoring practices differ among studies, fragmented study periods, and unaccounted confounding by ecological variables. We therefore reconstructed long-term (1939–2015) and large-scale (West Greenland, Norway, and central Sweden) trends of major legacy OCs using white-tailed eagle (Haliaeetus albicilla) body feathers, to understand the exposure dynamics in regions with different contamination sources and concentrations, as well as the effectiveness of legislations. We included dietary proxies (δ13C and δ15N) in temporal trend models to control for potential dietary plasticity. Consistent with the hypothesised high local pollution sources, levels of polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethanes (DDTs) and hexachlorocyclohexanes (HCHs) in the Swedish subpopulation exceeded those in the other subpopulations. In contrast, chlordanes (CHLs) and hexachlorobenzene (HCB) showed higher concentrations in Greenland, suggesting the importance of long-range transport. The models showed significantly decreasing trends for all OCs in Sweden in 1968–2011 except for CHLs, which only decreased since the 1980s. Nevertheless, median concentrations of DDTs and PCBs remained elevated in the Swedish subpopulation throughout the 1970s, suggesting that the decreases only commenced after the implementation of regulations during the 1970s. We observed significant trends of increasing concentrations of PCBs, CHLs and HCB in Norway from the 1930s to the 1970s/1980s and decreasing concentrations thereafter. All OC concentrations, except those of PCBs were generally significantly decreasing in the Greenland subpopulation in 1985-2013. All three subpopulations showed generally increasing proportions of the more persistent compounds (CB 153, p.p′-DDE and β-HCH) and decreasing proportions of the less persistent ones (CB 52, p.p′-DDT, α- and γ-HCH). Declining trends of OC concentrations may imply the decreasing influence of legacy OCs in these subpopulations. Finally, our results demonstrate the usefulness of archived museum feathers in retrospective monitoring of spatiotemporal trends of legacy OCs using birds of prey as sentinels.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
Disciplines :
Zoology Environmental sciences & ecology
Author, co-author :
Sun, Jiachen
Covaci, Adrian
Bustnes, Jan Ove
Jaspers, Veerle L. B.
Helander, Björn
Bårdsen, Bård-Jørgen
Boertmann, David
Dietz, Rune
Labansen, Aili Lage
Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Temporal trends of legacy organochlorines in different white-tailed eagle (Haliaeetus albicilla) subpopulations: A retrospective investigation using archived feathers
Andersson, O., Linder, C.E., Olsson, M., Reutergardh, L., Uvemo, U.B., Wideqvist, U., Spatial differences and temporal trends of organochlorine compounds in biota from the northwestern hemisphere. Arch. Environ. Contam. Toxicol. 17 (1988), 755–765.
Bagge, P., Pesticide residues in some Baltic animals-a review of selected literature. Pure Appl. Chem. 42 (1975), 129–137.
Bailey, R.E., Global hexachlorobenzene emissions. Chemosphere 43 (2001), 167–182.
Barber, J.L., Sweetman, A.J., Van Wijk, D., Jones, K.C., Hexachlorobenzene in the global environment: emissions, levels, distribution, trends and processes. Sci. Total Environ. 349 (2005), 1–44.
Barrett, R.T., Skaare, J.U., Norheim, G., Vader, W., Frøslie, A., Persistent organochlorines and mercury in eggs of Norwegian seabirds 1983. Environ. Pollut. A 39 (1985), 79–93.
Berggren, P., Ishaq, R., Zebühr, Y.U., Näf, C., Bandh, C., Broman, D., Patterns and levels of organochlorines (DDTs, PCBs, non-ortho PCBs and PCDD/Fs) in male harbour porpoises (Phocoena phocoena) from the Baltic Sea, the Kattegat-Skagerrak Seas and the west coast of Norway. Mar. Pollut. Bull. 38 (1999), 1070–1084.
Bignert, A., Göthberg, A., Jensen, S., Litzén, K., Odsjö, T., Olsson, M., Reutergårdh, L., The need for adequate biological sampling in ecotoxicological investigations: A retrospective study of twenty years pollution monitoring. Sci. Total Environ. 128 (1993), 121–139.
Bignert, A., Helander, B.O., Monitoring of contaminants and their effects on the common guillemot and the white-tailed sea eagle. J. Ornithol. 156 (2015), S173–S185.
Bignert, A., Olsson, M., Persson, W., Jensen, S., Zakrisson, S., Litzén, K., Eriksson, U., Häggberg, L., Alsberg, T., Temporal trends of organochlorines in Northern Europe, 1967–1995. Relation to global fractionation, leakage from sediments and international measures. Environ. Pollut. 99 (1998), 177–198.
Braune, B.M., Temporal trends of organochlorines and mercury in seabird eggs from the Canadian Arctic, 1975–2003. Environ. Pollut. 148 (2007), 599–613.
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.
Breivik, K., Pacyna, J.M., Münch, J., Use of α-, β- and γ-hexachlorocyclohexane in Europe, 1970–1996. Sci. Total Environ. 239 (1999), 151–163.
Breivik, K., Sweetman, A., Pacyna, J.M., Jones, K.C., Towards a global historical emission inventory for selected PCB congeners — A mass balance approach: 1. Global production and consumption. Sci. Total Environ. 290 (2002), 181–198.
Brevik, E.M., Bjerk, J.E., Kveseth, N.J., Organochlorines in codfish from harbours along the Norwegian coast. Bull. Environ. Contam. Toxicol. 20 (1978), 715–720.
Bruhn, R., Kannan, N., Petrick, G., Schulz-Bull, D.E., Duinker, J.C., Persistent chlorinated organic contaminants in harbour porpoises from the North Sea, the Baltic Sea and Arctic waters. Sci. Total Environ. 237–238 (1999), 351–361.
Campbell, L.M., Drevnick, P.E., Use of catalogued long-term biological collections and samples for determining changes in contaminant exposure to organisms. Blais, J.M., Rosen, M.R., Smol, J.P., (eds.) Environmental Contaminants, vol. 18, 2015, Springer, Dordrecht, 431–459.
Cribari-Neto, F., Zeileis, A., Beta regression in R. J. Stat. Softw. 34 (2009), 1–24.
Dauwe, T., Jaspers, V.L.B., Covaci, A., Schepens, P., Eens, M., Feathers as a nondestructive biomonitor for persistent organic pollutants. Environ. Toxicol. Chem. 24 (2005), 442–449.
De Voogt, P., Brinkman, U., Production, properties and usage of polychlorinated biphenyls. Kimbrough, R.D., Jensen, A.A., (eds.) Halogenated biphenyls, terphenyls, naphthalenes, dibenzodioxins related products, 1989, Elsevier Science Publishers B.V, Amsterdam, 3–45.
EFSA, Chlordane as undesirable substance in animal feed - Scientific Opinion of the Panel on Contaminants in the Food Chain. EFSA J., 5, 2007, 582.
Espín S., García-Fernández A., Herzke D., Shore R., van Hattum B., Martínez-López E., Coeurdassier M., Eulaers I., Fritsch C., Gómez-Ramírez P., 2014. Sampling and contaminant monitoring protocol for raptors. Research Networking Programme-EURAPMON, Research and monitoring for and with raptors in Europe.
Eulaers, I., Covaci, A., Herzke, D., Eens, M., Sonne, C., Moum, T., Schnug, L., Hanssen, S.A., Johnsen, T.V., Bustnes, J.O., Jaspers, V.L.B., A first evaluation of the usefulness of feathers of nestling predatory birds for non-destructive biomonitoring of persistent organic pollutants. Environ. Int. 37 (2011), 622–630.
Eurochlor, 2015. Hexachlorobenzene – Sources, environmental fate and risk characterisation. In: Barber, J., Sweetman, A., Jones, K. (Eds.), Eurochlor, Brussels, Belgium.
Falandysz, J., Organochlorine pesticides and polychlorinated biphenyls in herring from the southern Baltic, 1981. Eur. Food Res. Technol. 179 (1984), 20–23.
Falandysz, J., Organochlorine pesticides and polychlorinated biphenyls in sprats from the southern Baltic, 1983. Eur. Food Res. Technol. 181 (1985), 482–485.
Falandysz, J., Kannan, K., Tanabe, S., Tatsukawa, R., Organochlorine pesticides and polychlorinated-biphenyls in cod-liver oils: North-Atlantic, Norwegian Sea, North-Sea and Baltic Sea. Ambio 23 (1994), 288–293.
Fenstad, A.A., Jenssen, B.M., Gabrielsen, K.M., Ost, M., Jaatinen, K., Bustnes, J.O., Hanssen, S.A., Moe, B., Herzke, D., Krokje, A., Persistent organic pollutant levels and the importance of source proximity in Baltic and Svalbard breeding common eiders. Environ. Toxicol. Chem. 35 (2016), 1526–1533.
Fryer, R.J., Nicholson, M.D., The power of a contaminant monitoring programme to detect linear trends and incidents. ICES J. Mar. Sci. 50 (1993), 161–168.
Gauthier, L.T., Hebert, C.E., Weseloh, D.C., Letcher, R.J., Dramatic changes in the temporal trends of polybrominated diphenyl ethers (PBDEs) in herring gull eggs from the Laurentian Great Lakes: 1982–2006. Environ. Sci. Technol. 42 (2008), 1524–1530.
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.
Goldberg, E., Synthetic organohalides in the sea. Proc. R. Soc. Lond. B Biol. Sci. 189 (1975), 277–289.
Granby, K., Kinze, C.C., Organochlorines in Danish and West Greenland harbor porpoises. Mar. Pollut. Bull. 22 (1991), 458–462.
Haahti, H., Perttila, M., Levels and trends of organochlorines in cod and herring in the Northern Baltic. Mar. Pollut. Bull. 19 (1988), 29–32.
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.
Hebert, C.E., Weseloh, D.V.C., Adjusting for temporal change in trophic position results in reduced rates of contaminant decline. Environ. Sci. Technol. 40 (2006), 5624–5628.
Helander, B., Food ecology of the white-tailed sea eagle Haliaeetus albicilla in Sweden. 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, University of Stockholm, Swedish Society for the Conservation of Nature, Stockholm, 87–155.
Helander, B., 2003. The international colour-ringing programme – Adult survival, homing and the expansion of the white-tailed sea eagle in Sweden. In: Sea Eagle 2000: Proceedings from the international sea eagle conference in Björkö, Sweden, 13-17 September 2000. Swedish Society for Nature Conservation (SNF), pp. 145–154.
Helander, B., Olsson, A., Bignert, A., Asplund, L., Litzén, K., The role of DDE, PCB, coplanar PCB and eggshell parameters for reproduction in the white-tailed sea eagle (Haliaeetus albicilla) in Sweden. Ambio 31 (2002), 386–403.
Holden, A.V., Marsden, K., Organochlorine pesticides in seals and porpoises. Nature 216 (1967), 1274–1276.
Hung, H., Katsoyiannis, A.A., Brorström-Lundén, E., Olafsdottir, K., Aas, W., Breivik, K., Bohlin-Nizzetto, P., Sigurdsson, A., Hakola, H., Bossi, R., Temporal trends of Persistent Organic Pollutants (POPs) in arctic air: 20 years of monitoring under the Arctic Monitoring and Assessment Programme (AMAP). Environ. Pollut. 217 (2016), 52–61.
Jaspers, V.L.B., Covaci, A., Herzke, D., Eulaers, I., Eens, M., Bird feathers as a biomonitor for environmental pollutants: prospects and pitfalls. TrAC-Trends Anal. Chem. 118 (2019), 223–226.
Jaspers, V.L.B., Rodriguez, F.S., Boertmann, D., Sonne, C., Dietz, R., Rasmussen, L.M., Eens, M., Covaci, A., Body feathers as a potential new biomonitoring tool in raptors: A study on organohalogenated contaminants in different feather types and preen oil of West Greenland white-tailed eagles (Haliaeetus albicilla). Environ. Int. 37 (2011), 1349–1356.
Jaspers, V.L.B., Sonne, C., Soler-Rodriguez, F., Boertmann, D., Dietz, R., Eens, M., Rasmussen, L.M., Covaci, A., Persistent organic pollutants and methoxylated polybrominated diphenyl ethers in different tissues of white-tailed eagles (Haliaeetus albicilla) from West Greenland. Environ. Pollut. 175 (2013), 137–146.
Jaspers, V.L.B., Voorspoels, S., Covaci, A., Eens, M., Can predatory bird feathers be used as a non-destructive biomonitoring tool of organic pollutants?. Biol. Lett. 2 (2006), 283–285.
Jaspers, V.L.B., Voorspoels, S., Covaci, A., Lepoint, G., Eens, M., Evaluation of the usefulness of bird feathers as a non-destructive biomonitoring tool for organic pollutants: A comparative and meta-analytical approach. Environ. Int. 33 (2007), 328–337.
Jensen, S., Report of a new chemical hazard. New Sci., 15, 1966, 612.
Jensen, S., Johnels, A.G., Olsson, M., Otterlind, G., DDT and PCB in marine animals from Swedish waters. Nature 224 (1969), 247–250.
Jorundsdottir, H., Bignert, A., Svavarsson, J., Nygard, T., Weihe, P., Bergman, A., Assessment of emerging and traditional halogenated contaminants in Guillemot (Uria aalge) egg from North-Western Europe and the Baltic Sea. Sci. Total Environ. 407 (2009), 4174–4183.
Kveseth, N.J., Bjerk, J.E., Fimreite, N., Stenersen, J., Residues of DDT in a Norwegian fruitgrowing district two and four years after the termination of DDT usage. Arch. Environ. Contam. Toxicol. 8 (1979), 201–212.
Li, Y.-F., Scholtz, M.T., Van Heyst, B.J., Global gridded emission inventories of β-hexachlorocyclohexane. Environ. Sci. Technol. 37 (2003), 3493–3498.
Luckas, B., Harms, U., Characteristic levels of chlorinated hydrocarbons and trace metals in fish from coastal waters of North and Baltic sea. Int. J. Environ. Anal. Chem. 29 (1987), 215–225.
Luckas, B., Vetter, W., Fischer, P., Heidemann, G., Plotz, J., Characteristic chlorinated-hydrocarbon patterns in the blubber of seals from different marine regions. Chemosphere 21 (1990), 13–19.
Lyngs, P., Migration and winter ranges of birds in Greenland, vol. 97, 2003, Danish Ornithological Society, Copenhagen.
Ma, J., Hung, H., Tian, C., Kallenborn, R., Revolatilization of persistent organic pollutants in the Arctic induced by climate change. Nat. Clim. Chang. 1 (2011), 255–260.
Marcotte, S., Estel, L., Leboucher, S., Minchin, S., Occurrence of organic biocides in the air and dust at the Natural History Museum of Rouen, France. J. Cult. Herit. 15 (2014), 68–72.
Moilanen, R., Pyysalo, H., Wickstrom, K., Linko, R., Time trends of chlordane, DDT, and PCB concentrations in pike (Esox lucius) and Baltic herring (Clupea harengus) in the Turku Archipelago, Northern Baltic Sea for the period 1971–1982. Bull. Environ. Contam. Toxicol. 29 (1982), 334–340.
Muir, D.C., Norstrom, R.J., Geographical differences and time trends of persistent organic pollutants in the Arctic. Toxicol. Lett. 112 (2000), 93–101.
Nyberg, E., Faxneld, S., Danielsson, S., Eriksson, U., Miller, A., Bignert, A., Temporal and spatial trends of PCBs, DDTs, HCHs, and HCB in Swedish marine biota 1969–2012. Ambio 44 (2015), 484–497.
Olsson, M., Bignert, A., Eckhéll, J., Jonsson, P., Comparison of temporal trends (1940s–1990s) of DDT and PCB in Baltic sediment and biota in relation to eutrophication. Ambio 29 (2000), 195–201.
R Core Team, R: A language and environment for statistical computing. 2018, R Foundation for Statistical Computing, Vienna.
Rigét, F.F., Bignert, A., Braune, B., Dam, M., Dietz, R., Evans, M., Green, N., Gunnlaugsdóttir, H., Hoydal, K.S., Kucklick, J., Letcher, R., Muir, D., Schuur, S., Sonne, C., Stern, G., Tomy, G., Vorkamp, K., Wilson, S., Temporal trends of persistent organic pollutants in Arctic marine and freshwater biota. Sci. Total Environ. 649 (2019), 99–110.
Rocque, D.A., Winker, K., Use of bird collections in contaminant and stable-isotope studies. Auk 122 (2005), 990–994.
Roots, O., Organochlorine pesticides and polychlorinated biphenyls in the ecosystem of the Baltic Sea. Chemosphere 31 (1995), 4085–4097.
Sabatier, P., Poulenard, J., Fanget, B., Reyss, J.-L., Develle, A.-L., Wilhelm, B., Ployon, E., Pignol, C., Naffrechoux, E., Dorioz, J.-M., Montuelle, B., Arnaud, F., Long-term relationships among pesticide applications, mobility, and soil erosion in a vineyard watershed. Proc. Natl. Acad. Sci. 111 (2014), 15647–15652.
Sapota, G., Decreasing trend of persistent organic pollutants (POPs) in herring from the southern Baltic Sea. Oceanol. Hydrobiol. Stud. 35 (2006), 15–21.
Schmidt, O., Insecticide contamination at the National Museum of Denmark: A case study. The contamination of museum materials and the repatriation process for native California: Proceedings of a working conference., vol. 16, 2000, 92–95.
Skåre, J.U., Stenersen, J., Kveseth, N., Polder, A., Time trends of organochlorine chemical residues in seven sedentary marine fish species from a Norwegian fjord during the period 1972–1982. Arch. Environ. Contam. Toxicol. 14 (1985), 33–41.
Skeff, W., Neumann, C., Schulz-Bull, D.E., Glyphosate and AMPA in the estuaries of the Baltic Sea method optimization and field study. Mar. Pollut. Bull. 100 (2015), 577–585.
Strandberg, B., Strandberg, L., van Bavel, B., Bergqvist, P.A., Broman, D., Falandysz, J., Naf, C., Papakosta, O., Rolff, C., Rappe, C., Concentrations and spatial variations of cyclodienes and other organochlorines in herring and perch from the Baltic Sea. Sci. Total Environ. 215 (1998), 69–83.
Sun, J., Bossi, R., Bustnes, J.O., Helander, B., Boertmann, D., Dietz, R., Herzke, D., Jaspers, V.L.B., Labansen, A.L., Lepoint, G., Schulz, R., Sonne, C., Thorup, K., Tøttrup, A.P., Zubrod, J.P., Eens, M., Eulaers, I., White-tailed eagle (Haliaeetus albicilla) body feathers document spatiotemporal trends of perfluoroalkyl substances in the northern environment. Environ. Sci. Technol. 53 (2019), 12744–12753.
Sun, J., Bustnes, J.O., Helander, B., Bårdsen, B.-J., Boertmann, D., Dietz, R., Jaspers, V.L.B., Labansen, A.L., Lepoint, G., Schulz, R., Søndergaard, J., Sonne, C., Thorup, K., Tøttrup, A.P., Zubrod, J.P., Eens, M., Eulaers, I., Temporal trends of mercury differ across three northern white-tailed eagle (Haliaeetus albicilla) subpopulations. Sci. Total Environ. 687 (2019), 77–86.
UNEP, 2006. Norwegian implementation plan for the Stockholm convention on persistent organic pollutants (POPs). Norwegian Pollution Control Authority and the Norwegian Food Safety Authority.
UNEP, 2008. Listing of POPs in the Stockholm Convention.
UNEP, 2017a. National implementation plan for the Stockholm Convention Sweden. Report 6794. Swedish Environmental Protection Agency.
UNEP, 2017b. Norwegian implementation plan for the Stockholm convention on persistent organic pollutants (POPs). Norwegian Environment Agency.
van den Berg, H., Manuweera, G., Konradsen, F., Global trends in the production and use of DDT for control of malaria and other vector-borne diseases. Malar. J., 16, 2017, 401.
Vijgen, J., The legacy of lindane HCH isomer production. A Global Overview of Residue Management, Formulation and Disposal. 2006, International HCH & Pesticides Association, 384.
Vijgen, J., Abhilash, P., Li, Y., Lal, R., Forter, M., Torres, J., Singh, N., Yunus, M., Tian, C., Schäffer, A., HCH isomers as new Stockholm Convention POPs - Are we on the way to manage lindane (γ-HCH), and waste HCH isomer (α-and β-HCH) pollution around the world. Environ. Sci. Pollut. R. 5 (2010), 363–393.
Weber, R., Schlumpf, M., Nakano, T., Vijgen, J., The need for better management and control of POPs stockpiles. Environ. Sci. Pollut. R. 22 (2015), 14385–14390.
Weissglas, G., Swedish legislation on pesticides. Arh. Hig. Rada. Toksikol. 24 (1973), 405–410.
Westöö, G., Changes in the levels of environmental pollutants (Hg, DDT, dieldrin, PCB) in some Swedish foods. Ambio 3 (1974), 79–83.
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, Norwegian Universities Press, Trondheim, Norway.
Wood, S.N., Generalized additive models: An introduction with R. Second Edition, 2017, Chapman and Hall/CRC, Boca Raton.
Zuur, A F, Ieno, E N, Elphick, C S, A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1 (2010), 3–14.