Plasma concentrations of organohalogenated contaminants in white-tailed eagle nestlings – The role of age and diet

[en] Concentrations of organohalogenated contaminants (OHCs) can show significant temporal and spatial variation in the environment and wildlife. Most of the variation is due to changes in use and production, but environmental and biological factors may also contribute to the variation. Nestlings of top predators are exposed to maternally transferred OHCs in the egg and through their dietary intake after hatching. The present study investigated spatial and temporal variation of OHCs and the role of age and diet on these variations in plasma of Norwegian white-tailed eagle (Haliaeetus albicilla) nestlings. The nestlings were sampled at two locations, Smøla and Steigen, in 2015 and 2016. The age of the nestlings was recorded (range: 44 – 87 days old) and stable carbon and nitrogen isotopes (δ13C and δ15N) were applied as dietary proxies for carbon source and trophic position, respectively. In total, 14 polychlorinated biphenyls (PCBs, range: 0.82 – 59.05 ng/mL), 7 organochlorinated pesticides (OCPs, range: 0.89 – 52.19 ng/mL), 5 polybrominated diphenyl ethers (PBDEs, range: 0.03 – 2.64 ng/mL) and 8 perfluoroalkyl substances (PFASs, range: 4.58 – 52.94 ng/mL) were quantified in plasma samples from each location and year. The OHC concentrations, age and dietary proxies displayed temporal and spatial variations. The age of the nestlings was indicated as the most important predictor for OHC variation as the models displayed significantly decreasing plasma concentrations of PCBs, OCPs, and PBDEs with increasing age, while concentrations of PFASs were significantly increasing with age. Together with age, the variations in PCB, OCP and PBDE concentrations were also explained by δ13C and indicated decreasing concentrations with a more marine diet. Our findings emphasise age and diet as important factors to consider when investigating variations in plasma OHC concentrations in nestlings. © 2018 Elsevier Ltd

Disciplines :

Environmental sciences & ecology
Zoology

Author, co-author :

Løseth, M. E.; Department of Biology, Norwegian University of Science and Technology (NTNU), Høgskoleringen 5, Trondheim, 7491, Norway

Briels, N.; Department of Biology, Norwegian University of Science and Technology (NTNU), Høgskoleringen 5, Trondheim, 7491, Norway

Eulaers, I.; Department of Bioscience, Aarhus University, Fredriksborgvej 399, Roskilde, 4000, Denmark

Nygård, T.; Norwegian Institute for Nature Research (NINA), Høgskoleringen 9, Trondheim, 7034, Norway

Malarvannan, G.; Toxicological Centre, University of Antwerp, Universiteitsplein 1, Wilrijk, 2610, Belgium

Poma, G.; Toxicological Centre, University of Antwerp, Universiteitsplein 1, Wilrijk, 2610, Belgium

Covaci, A.; Toxicological Centre, University of Antwerp, Universiteitsplein 1, Wilrijk, 2610, Belgium

Herzke, D.; Norwegian Institute for Air Research (NILU), FRAM - High North Research Centre on Climate and the Environment, Tromsø, 9007, Norway

Bustnes, J. O.; Norwegian Institute for Nature Research (NINA), FRAM - High North Research Centre on Climate and the Environment, Tromsø, 9007, Norway

Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique

Jenssen, B. M.; Department of Biology, Norwegian University of Science and Technology (NTNU), Høgskoleringen 5, Trondheim, 7491, Norway, Department of Bioscience, Aarhus University, Fredriksborgvej 399, Roskilde, 4000, Denmark

Jaspers, V. L. B.; Department of Biology, Norwegian University of Science and Technology (NTNU), Høgskoleringen 5, Trondheim, 7491, Norway

Language :

English

Title :

Plasma concentrations of organohalogenated contaminants in white-tailed eagle nestlings – The role of age and diet

Publication date :

2019

Journal title :

Environmental Pollution

ISSN :

0269-7491

eISSN :

1873-6424

Publisher :

Elsevier Ltd

Volume :

246

Pages :

527-534

Peer reviewed :

Peer Reviewed verified by ORBi

Name of the research project :

230465

Funders :

UA - Universiteit Antwerpen

Available on ORBi :

since 07 January 2019

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Bibliography

Bearhop, S., Waldron, S., Votier, S.C., Furness, R.W., Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol. Biochem. Zool. 75 (2002), 451–458, 10.1086/342800.
Bohlin-Nizzetto, P., Aas, W., Monitoring of Environmental Contaminants in Air and Precipitation, Annual Report 2015., 2016, Norwegian Environmental Agency ISBN: 978-82-425-2841-4.
Bohlin-Nizzetto, P., Aas, W., Warner, N., Monitoring of Environmental Contaminants in Air and Precipitation, Annual Report 2016., 2017, Norwegian Environmental Agency ISBN: 978-82-425-2888-9.
Borgå K., Fisk, A.T., Hoekstra, P.E., Muir, D.C.G., Biological and chemical factors of importance in the bioaccumulation and trophic transfer of persistent organochlorine contaminants in Arctic marine food webs. Environ. Toxicol. Chem. 23 (2004), 2367–2385, 10.1897/03-518.
Bourgeon, S., Leat, E.K.H., Furness, R.W., Borgå K., Hanssen, S.A., Bustnes, J.O., Dietary versus maternal sources of organochlorines in top predator seabird chicks: an experimental approach. Environ. Sci. Technol. 47 (2013), 5963–5970, 10.1021/es400442q.
Bustnes, J.O., Bårdsen, B.J., Herzke, D., Johnsen, T.V., Eulaers, I., Ballesteros, M., Hanssen, S. a, Covaci, A., Jaspers, V.L.B., Eens, M., Sonne, C., Halley, D., Moum, T., Nøst, T.H., Erikstad, K.E., Ims, R.A., Plasma concentrations of organohalogenated pollutants in predatory bird nestlings: associations to growth rate and dietary tracers. Environ. Toxicol. Chem. 32 (2013), 2520–2527, 10.1002/etc.2329.
Bustnes, J.O., Bangjord, G., Ahrens, L., Herzke, D., Yoccoz, N.G., Perfluoroalkyl substance (PFAS) concentrations in a terrestrial raptor: relationships to environmental conditions and individual traits. Environ. Toxicol. Chem. 34 (2015), 184–191, 10.1002/etc.2782.
Cassone, C.G., Vongphachan, V., Chiu, S., Williams, K.L., Letcher, R.J., Pelletier, E., Crump, D., Kennedy, S.W., In ovo effects of perfluorohexane sulfonate and perfluorohexanoate on pipping success, development, mRNA expression, and thyroid hormone levels in chicken embryos. Toxicol. Sci. 127 (2012), 216–224, 10.1093/toxsci/kfs072.
Dauwe, T., Jaspers, V.L.B., Covaci, A., Eens, M., Accumulation of organochlorines and brominated flame retardants in the eggs and nestlings of great tits, Parus major. Environ. Sci. Technol. 40 (2006), 5297–5303, 10.1021/es060747a.
Elliott, J.E., Brogan, J., Lee, S.L., Drouillard, K.G., Elliott, K.H., PBDEs and other POPs in urban birds of prey partly explained by trophic level and carbon source. Sci. Total Environ. 524–525 (2015), 157–165, 10.1016/j.scitotenv.2015.04.008.
Eulaers, I., Covaci, A., Hofman, J., Nygård, T., Halley, D.J., Pinxten, R., Eens, M., Jaspers, V.L.B., A comparison of non-destructive sampling strategies to assess the exposure of white-tailed eagle nestlings (Haliaeetus albicilla) to persistent organic pollutants. Sci. Total Environ. 410–411 (2011), 258–265, 10.1016/j.scitotenv.2011.09.070.
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, 10.1016/j.envint.2010.12.007.
Eulaers, I., Jaspers, V.L.B., Bustnes, J.O., Covaci, A., Johnsen, T.V., Halley, D.J., Moum, T., Ims, R.A., Hanssen, S.A., Erikstad, K.E., Herzke, D., Sonne, C., Ballesteros, M., Pinxten, R., Eens, M., Ecological and spatial factors drive intra- and interspecific variation in exposure of subarctic predatory bird nestlings to persistent organic pollutants. Environ. Int. 57–58 (2013), 25–33, 10.1016/j.envint.2013.03.009.
Eulaers, I., Jaspers, V.L.B., Halley, D.J., Lepoint, G., Nygård, T., Pinxten, R., Covaci, A., Eens, M., Brominated and phosphorus flame retardants in white-tailed eagle Haliaeetus albicilla nestlings: bioaccumulation and associations with dietary proxies (δ13C, δ15N and δ34S). Sci. Total Environ. 478 (2014), 48–57, 10.1016/j.scitotenv.2014.01.051.
Faxneld, S., Berger, U., Helander, B., Danielsson, S., Miller, A., Nyberg, E., Persson, J.-O., Bignert, A., Temporal trends and geographical differences of perfluoroalkyl acids in Baltic Sea herring and white-tailed sea eagle eggs in Sweden. Environ. Sci. Technol. 50 (2016), 13070–13079, 10.1021/acs.est.6b03230.
Fry, B., Stable Isotope Ecology. 2006, Springer Science, USA, 10.1007/0-387-33745-8.
Gebbink, W.A., Letcher, R.J., Hebert, C.E., Chip Weseloh, D.V., Twenty years of temporal change in perfluoroalkyl sulfonate and carboxylate contaminants in herring gull eggs from the Laurentian Great Lakes. J. Environ. Monit. 13 (2011), 3365–3372, 10.1039/c1em10663e.
Gómez-Ramírez, P., Bustnes, J.O., Eulaers, I., Herzke, D., Johnsen, T.V., Lepoint, G., Pérez-García, J.M., García-Fernández, A.J., Jaspers, V.L.B., Per- and polyfluoroalkyl substances in plasma and feathers of nestling birds of prey from northern Norway. Environ. Res. 158 (2017), 277–285, 10.1016/j.envres.2017.06.019.
Guo, J., Simon, K., Romanak, K., Bowerman, W., Venier, M., Accumulation of flame retardants in paired eggs and plasma of bald eagles. Environ. Pollut. 237 (2018), 499–507, 10.1016/j.envpol.2018.02.056.
Haukås, M., Berger, U., Hop, H., Gulliksen, B., Gabrielsen, G.W., Bioaccumulation of per- and polyfluorinated alkyl substances (PFAS) in selected species from the Barents Sea food web. Environ. Pollut. 148 (2007), 360–371, 10.1016/j.envpol.2006.09.021.
Helander, B., Bignert, A., Asplund, L., Using raptors as environmental sentinels: monitoring the white-tailed sea eagle Haliaeetus albicilla in Sweden. AMBIO A J. Hum. Environ. 37 (2008), 425–431, 10.1579/0044-7447(2008)37.
Helander, B., Hailer, F., Vilà C., Morphological and genetic sex identification of white-tailed eagle Haliaeetus albicilla nestlings. J. Ornithol. 148 (2007), 435–442, 10.1007/s10336-007-0156-y.
Helgason, L.B., Barrett, R., Lie, E., Polder, A., Skaare, J.U., Gabrielsen, G.W., Levels and temporal trends (1983-2003) of persistent organic pollutants (POPs) and mercury (Hg) in seabird eggs from Northern Norway. Environ. Pollut. 155 (2008), 190–198, 10.1016/j.envpol.2007.10.022.
Herzke, D., Nygård, T., Berger, U., Huber, S., Røv, N., Perfluorinated and other persistent halogenated organic compounds in European shag (Phalacrocorax aristotelis) and common eider (Somateria mollissima) from Norway: a suburban to remote pollutant gradient. Sci. Total Environ. 408 (2009), 340–348, 10.1016/j.scitotenv.2009.08.048.
Houde, M., De Silva, A.O., Muir, D.C.G., Letcher, R.J., Canada, E., Saint-laurent, C., Street, M., Monitoring of perfluorinated compounds in aquatic biota : an updated review. Environ. Sci. Technol. 45 (2011), 7962–7973, 10.1021/es104326w.
Hung, H., Katsoyiannis, A.A., Brorström-Lundén, E., Olafsdottir, K., Aas, W., Breivik, K., Bohlin-Nizzetto, P., Sigurdsson, A., Hakola, H., Bossi, R., Skov, H., Sverko, E., Barresi, E., Fellin, P., Wilson, S., 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, 10.1016/j.envpol.2016.01.079.
Inger, R., Bearhop, S., Applications of stable isotope analyses to avian ecology. Ibis (Lond. 1859), 2008, 447–461, 10.1111/j.1474-919X.2008.00839.x.
Jenssen, B.M., Aarnes, J.B., Murvoll, K.M., Herzke, D., Nygård, T., Fluctuating wing asymmetry and hepatic concentrations of persistent organic pollutants are associated in European shag (Phalacrocorax aristotelis) chicks. Sci. Total Environ. 408 (2010), 578–585, 10.1016/j.scitotenv.2009.10.036.
Kelly, B.C., Ikonomou, M.G., Blair, J.D., Surridge, B., Hoover, D., Grace, R., Gobas, F.A.P.C., Perfluoroalkyl contaminants in an Arctic marine food web: trophic magnification and wildlife exposure. Environ. Sci. Technol. 43 (2009), 4037–4043, 10.1021/es9003894.
Kelly, J.F., Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can. J. Zool. 78 (2000), 1–27, 10.1139/z99-165.
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.
Lau, C., Anitole, K., Hodes, C., Lai, D., Pfahles-Hutchens, A., Seed, J., Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol. Sci. 99 (2007), 366–394, 10.1093/toxsci/kfm128.
Leat, E.H.K., Bourgeon, S., Borgå K., Strøm, H., Hanssen, S.A., Gabrielsen, G.W., Petersen, Æ., Olafsdottir, K., Magnusdottir, E., Fisk, A.T., Ellis, S., Bustnes, J.O., Furness, R.W., Effects of environmental exposure and diet on levels of persistent organic pollutants (POPs) in eggs of a top predator in the North Atlantic in 1980 and 2008. Environ. Pollut. 159 (2011), 1222–1228, 10.1016/j.envpol.2011.01.036.
Leat, E.H.K., Bourgeon, S., Eze, J.I., Muir, D.C.G., Williamson, M., Bustnes, J.O., Furness, R.W., Borgå K., Perfluoroalkyl substances in eggs and plasma of an avian top predator, great skua (Stercorarius skua), in the north Atlantic. Environ. Toxicol. Chem. 32 (2013), 569–576, 10.1002/etc.2101.
Løseth, M.E., Briels, N., Flo, J., Malarvannan, G., Poma, G., Covaci, A., Herzke, D., Nygård, T., Bustnes, J.O., Jenssen, B.M., Jaspers, V.L.B., White-tailed eagle (Haliaeetus albicilla) feathers from Norway are suitable for monitoring of legacy, but not emerging contaminants. Sci. Total Environ. 647 (2019), 525–533, 10.1016/j.scitotenv.2018.07.333.
Mackay, D., Shiu, W.Y., Ma, K., Lee, S.C., Halogenated hydrocarbons, second edi. Handbook of Physical-chemical Properties and Environmental Fate for Organic Chemicals, second ed., 2006, CRC Press, Taylor & Francis Group.
Miller, A., Elliott, J.E., Elliott, K.H., Lee, S., Cyr, F., Temporal trends of perfluoroalkyl substances (PFAS) in eggs of coastal and offshore birds: increasing PFAS levels associated with offshore bird species breeding on the Pacific coast of Canada and wintering near Asia. Environ. Toxicol. Chem. 34 (2015), 1799–1808, 10.1002/etc.2992.
Muir, D.C.G., de Wit, C.A., Trends of legacy and new persistent organic pollutants in the circumpolar arctic: overview, conclusions, and recommendations. Sci. Total Environ. 408 (2010), 3044–3051, 10.1016/j.scitotenv.2009.11.032.
Murvoll, K.M., Skaare, J.U., Anderssen, E., Jenssen, B.M., Exposure and effects of persistent organic pollutants in European shag (Phalacrocorax aristotelis) hatchlings from the coast of Norway. Environ. Toxicol. Chem. 25 (2006), 190–198, 10.1897/04-333R.1.
Nadjafzadeh, M., Voigt, C.C., Krone, O., Spatial, sesonal and individual variation of the diet of white-tailed eagles Haliaeetus albicilla assessed using stable isotope ratios. Ibis 158 (2016), 1–15, 10.1111/ibi.12311.
Nakagawa, S., Schielzeth, H., A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4 (2013), 133–142, 10.1111/j.2041-210x.2012.00261.x.
Nordlöf, U., Helander, B., Bignert, A., Asplund, L., Levels of brominated flame retardants and methoxylated polybrominated diphenyl ethers in eggs of white-tailed sea eagles breeding in different regions of Sweden. Sci. Total Environ. 409 (2010), 238–246, 10.1016/j.scitotenv.2010.09.042.
Nøst, T.H., Helgason, L.B., Harju, M., Heimstad, E.S., Gabrielsen, G.W., Jenssen, B.M., Halogenated organic contaminants and their correlations with circulating thyroid hormones in developing Arctic seabirds. Sci. Total Environ. 414 (2012), 248–256, 10.1016/j.scitotenv.2011.11.051.
Nygård, T., Polder, A., Miljøgifter I Rovfuglegg I Norge. Tilstand Og Tidstrender., 2012, Norwegian Institute for Nature research (NINA) report 834. ISBN: 978-82-426-2429-1.
Olsson, A., Ceder, K., Bergman, Å., Helander, B., Nestling blood of the white-tailed sea eagle (Haliaeetus albicilla) as an indicator of territorial exposure to organohalogen compounds - an evaluation. Environ. Sci. Technol. 34 (2000), 2733–2740, 10.1021/es991426k.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., Heisterkamp, S., Van Willigen, B., Nlme: linear and nonlinear mixed effects models. R Package version 3 (2018), 1–131.
Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J., Montaña, C.G., Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152 (2007), 179–189, 10.1007/s00442-006-0630-x.
Powley, C.R., George, S.W., Ryan, T.W., Buck, R.C., Matrix effect-free amalytical methods for determination of perflurinated carboxylic acids in environmental matrixes. Anal. Chem. 77 (2005), 6353–6358, 10.1021/ac0508090.
R Development Core Team, R: a Language and Environment for Statistical Computing. 2008.
Route, W.T., Key, R.L., Russell, R.E., Lindstrom, A.B., Strynar, M.J., Spatial and temporal patterns in concentrations of perfluorinated compounds in bald eagle nestlings in the upper Midwestern United States. Environ. Sci. Technol. 48 (2014), 6653–6660, 10.1021/es501055d.
Sletten, S., Bourgeon, S., Bårdsen, B.-J., Herzke, D., Criscuolo, F., Massemin, S., Zahn, S., Johnsen, T.V., Bustnes, J.O., Organohalogenated contaminants in white-tailed eagle (Haliaeetus albicilla) nestlings: an assessment of relationships to immunoglobulin levels, telomeres and oxidative stress. Sci. Total Environ. 539 (2016), 337–349, 10.1016/j.scitotenv.2015.08.123.
UNEP (United Nations Environmental Programme), The stockholm convention on persistent organic pollutants. United Nations, adoption of amendments to annexes A, B and C. Stock. Conv. URL: http://chm.pops.int/Convention/ConventionText/tabid/2232/Default.aspx, 2009.
Vicente, J., Sanpera, C., García-Tarrasón, M., Pérez, A., Lacorte, S., Perfluoroalkyl and polyfluoroalkyl substances in entire clutches of Audouin's gulls from the ebro delta. Chemosphere 119 (2015), S62–S68, 10.1016/j.chemosphere.2014.04.041.
Voorspoels, S., Covaci, A., Maervoet, J., Schepens, P., Relationship between age and levels of organochlorine contaminants in human serum of a Belgian population. Bull. Environ. Contam. Toxicol. 69 (2002), 22–29, 10.1007/s00128-002-0004-y.
Wang, Z., Cousins, I.T., Scheringer, M., Buck, R.C., Hungerbühler, K., Global emission inventories for C4-C14 perfluoroalkyl carboxylic acid (PFCA) homologues from 1951 to 2030, Part I: production and emissions from quantifiable sources. Environ. Int. 70 (2014), 62–75, 10.1016/j.envint.2014.04.013.
Wierda, M.R., Leith, K.F., Roe, A.S., Grubb, T.G., Sikarskie, J.G., Best, D.A., Pittman, H.T., Fuentes, L., Simon, K.L., Bowerman, W., Using bald eagles to track spatial (1999–2008) and temporal (1987–1992, 1999–2003, and 2004–2008) trends of contaminants in Michigan's aquatic ecosystems. Environ. Toxicol. Chem. 35 (2016), 1995–2002, 10.1002/etc.3523.
Willgohs, J.F., Havørn i Norge: Næring, forplantningsøkologi, konkurrenter og fiender. 1984, Direktoratet for vilt og ferskvannsfisk, Trondheim ISSN:032-5008.
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, 10.1111/j.2041-210X.2009.00001.x.
Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., Smith, G.M., Mixed Effects Models and Extensions in Ecology with R. 2009, Springer, 10.1017/CBO9781107415324.00.