Per- and polyfluoroalkyl substances in plasma and feathers of nestling birds of prey from northern Norway

[en] Plasma samples from nestlings of two top predators, White-tailed eagle (Haliaeetus albicilla) and Northern goshawk (Accipiter gentilis) from northern Norway were analysed for a wide range of per- and polyfluoroalkyl substances (PFASs). Body feathers from the White-tailed eagles were also analysed and significant associations between specific PFASs in blood plasma and body feathers were found (0.36 < R2 < 0.67; all p < 0.05). This result suggests that analysing body feathers of White-tailed eagle could potentially be a useful non-invasive strategy to monitor PFASs exposure in nestlings of this species. White-tailed eagles showed significantly higher levels of contaminants than Northern goshawks (plasma ∑PFASs Median = 45.83 vs 17.02 ng mL−1, p <0.05). The different exposure between both species seemed to be related to different dietary input, as quantified by stable carbon and nitrogen isotope analysis of body feathers. A priori, the bird of prey populations studied are not at risk for PFASs, since the levels in plasma of both species were hundreds to thousand times lower than the toxic reference values reported for predatory birds. However, further studies on larger sample sizes are needed to confirm this hypothesis since toxic thresholds for nestling birds of prey are not established.

Disciplines :

Zoology
Environmental sciences & ecology

Author, co-author :

Gómez-Ramírez, P.; University of Murcia > Faculty of Veterinary > Area of Toxicology

Bustnes, J. O.

Eulaers, I.

Herzke, D.

Johnsen, T. V.

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

Pérez-García, J. M.

García-Fernández, A. J.

Jaspers, V. L. B.

Language :

English

Title :

Per- and polyfluoroalkyl substances in plasma and feathers of nestling birds of prey from northern Norway

Publication date :

2017

Journal title :

Environmental Research

ISSN :

0013-9351

eISSN :

1096-0953

Publisher :

Academic Press, New York, United States - New York

Volume :

158

Pages :

277-285

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://www.sciencedirect.com/science/article/pii/S0013935117304814

Available on ORBi :

since 27 June 2017

Statistics

Number of views

51 (5 by ULiège)

Number of downloads

2 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Andersen, D.E., Survey techniques. Bird, D.M., Bildstein, K.L., (eds.) Raptor Research and Management Techniques, 2007, Hancock House Publishers Ltd, Canada and Hancock House Publishers, USA, 89–100.
Barón, E., Giménez, J., Verborgh, P., Gauffier, P., De Stephanis, R., Eljarrat, E., Barceló, D., Bioaccumulation and biomagnification of classical flame retardants, related halogenated natural compounds and alternative flame retardants in three delphinids from Southern European waters. Environ. Pollut. 203 (2015), 107–115.
Bearhop, S., Furness, R.W., Hilton, G.M., Votier, S.C., Waldron, S., A forensic approach to understanding diet and habitat use from stable isotope analysis of (avian) claw material. Funct. Ecol. 17 (2003), 270–275.
Bearhop, S., Adams, C.E., Waldron, S., Fuller, R.A., MacLeod, H., Determining trophic niche width: a novel approach using stable isotope analysis. J. Anim. Ecol. 73:5 (2004), 1007–1012.
Benskin, J.P., De Silva, A.O., Martin, L.J., Arsenault, G., McCrindle, R., Riddell, N., Mabury, S.A., Martin, J.W., Disposition of perfluorinated acid isomers in Sprague-Dawley rats; Part 1: single dose. Environ. Toxicol. Chem. 28 (2009), 542–554.
Berger, U., Haukas, M., Validation of a screening method based on liquid chromatography coupled to high-resolution mass spectrometry for analysis of perfluoroalkylated substances in biota. J. Chromatogr. A 1081 (2005), 210–217.
BirdLife International, 2014. Species factsheet: Haliaeetus albicilla. Downloaded from 〈 http://www.birdlife.org〉 on 06/11/2014.
Borg, D., Håkansson, H., Environmental and health risk assessment of perfluoroalkylated and polyfluoroalkylated substances (PFASs) in Sweden. Swed. Environ. Prot. Agency Report., 6513, 2012.
Boutton, T.W., Stable carbon isotope ratios of natural materials: II. Atmospheric, terrestrial, marine, and freshwater environments. Coleman, D.C., Fry, B., (eds.) Carbon Isotope Techniques, 1991, Academic Press Inc, San Diego, 173–183.
Buck, R.C., Franklin, J., Berger, U., Conder, J.M., Cousins, I.T., Voogt, P., De, Jensen, A.A., Kannan, K., Mabury, S.A., van Leeuwen, S.P.J., Perfluoroalkyl and polyfluoroalkyl substances in the environment: terminology, classification, and origins. Integr. Environ. Assess. Manag. 7 (2011), 513–541.
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.
Coplen, T., Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun. Mass Spectrom. 25 (2011), 2538–2560.
Domingo, J.L., Nadal, M., Per-and polyfluoro alkyl substances (PFASs) in food and human dietary intake: a review of the recent scientific literature. J. Agric. Food Chem. 65 (2017), 533–543.
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.
Elliott, K.H., Cesh, L.S., Dooley, J.A., Letcher, R.J., Elliott, J.E., PCBs and DDE, but not PBDEs, increase with trophic level and marine input in nestling bald eagles. Sci. Total Environ. 407 (2009), 3867–3875.
Espín, S., Martínez-López, E., Gómez-Ramírez, P., María-Mojica, P., García-Fernández, A.J., Razorbills (Alca torda) as bioindicators of mercury pollution in the southwestern Mediterranean. Mar. Pollut. Bull. 64 (2012), 2461–2470.
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., Jaspers, V.L.B., Krone, O., Duke, G., Helander, B., Mateo, R., Movalli, P., Sonne, C., van den Brink, N.W., Sampling and contaminant monitoring protocol for raptors. research networking programme. EURAPMON, 2014 〈www.eurapmon.net〉.
Espín, S., García-Fernández, A.J., Herzke, D., Shore, R.F., Hattum, B., Van, Martínez-López, E., Coeurdassier, M., Eulaers, I., Fritsch, C., Gómez-Ramírez, P., Jaspers, V.L., Krone, O., Duke, G., Helander, B., Mateo, R., Movalli, P., Sonne, C., van den Brink, N.W., Tracking pan-continental trends in environmental contamination using sentinel raptors-what types of samples should we use?. Ecotoxicology 25 (2016), 777–801.
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.
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.
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.
Eulaers, I., Jaspers, V.L.B., Pinxten, R., Covaci, A., Eens, M., Legacy and current-use brominated flame retardants in the Barn Owl. Sci. Total Environ. 472 (2014), 454–462.
Frank, R., Lutz, R.S., Productivity and survival of great horned owls exposed to dieldrin. Condor 101 (1999), 331–339.
García-Fernández, A.J., María-Mojica, P., Contaminantes Ambientales y su Repercusión Sobre la Fauna Silvestre. 2000, Ministerio de Agricultura, Pesca yAlimentación, 215–227.
García-Fernández, A.J., Calvo, J.F., Martínez-López, E., María-Mojica, P., Martínez, J.E., Raptor ecotoxicology in Spain: a review on persistent environmental contaminants. Ambio 37 (2008), 432–439.
García-Fernández, A.J., Espín, S., Martínez-López, E., Feathers as a biomonitoring tool of polyhalogenated compounds: a review. Environ. Sci. Technol. 47 (2013), 3028–3043.
Gebbink, W.A., Letcher, R.J., Linear and branched perfluorooctane sulfonate isomer patterns in herring gull eggs from colonial sites across the Laurentian Great Lakes. Environ. Sci. Technol. 44 (2010), 3739–3745.
Gebbink, W.A., Letcher, R.J., Burgess, N.M., Champoux, L., Elliott, J.E., Hebert, C.E., Martin, P., Wayland, M., Weseloh, D.V., Wilson, L., Perfluoroalkyl carboxylates and sulfonates and precursors in relation to dietary source tracers in the eggs of four species of gulls (Larids) from breeding sites spanning Atlantic to Pacific Canada. Environ. Int. 37:7 (2011), 1175–1182.
Giesy, J.P., Naile, J.E., Khim, J.S., Jones, P.D., Newsted, J.L., Aquatic toxicology of perfluorinated chemicals. Whiteacre, D.M., (eds.) Reviews of Environmental Contamination and Toxicology, 2010, Springer, New York, 1–52.
Gjershaug, J.O., Kålås, J.A., Nygård, T., Herzke, D., Folkestad, A.O., Monitoring of raptors and their contamination levels in Norway. Ambio 37 (2008), 420–424.
Gómez-Ramírez, P., Shore, R.F., van den Brink, N.W., van Hattum, B., Bustnes, J.O., Duke, G., Fritsch, C., García-Fernández, A.J., Helander, B.O., Jaspers, V., Krone, O., Martínez-López, E., Mateo, R., Movalli, P., Sonne, C., An overview of existing raptor contaminant monitoring activities in Europe. Environ. Int. 67 (2014), 12–21.
Greaves, A.K., Letcher, R.J., Linear and branched perfluorooctane sulfonate (PFOS) isomer patterns differ among several tissues and blood of polar bears. Chemosphere 93 (2013), 574–580.
Hanssen, L., Dudarev, A.A., Huber, S., Odland, J.Ø., Nieboer, E., Sandanger, T.M., Partition of perfluoroalkyl substances (PFASs) in whole blood and plasma, assessed in maternal and umbilical cord samples from inhabitants of arctic Russia and Uzbekistan. Sci. Total Environ. 447 (2013), 430–437.
Hardey, J., Crick, H., Wernham, C., Riley, H., Etheridge, B., Thompson, D., Raptors: A Field Guide for Surveys and Monitoring, 2nd ed., 2009, The Stationery Office, Edinburgh.
Herzke, D., Kallenborn, R., Nygård, T., Organochlorines in egg samples from Norwegian birds of prey: congener-, isomer-and enantiomer specific considerations. Sci. Total Environ. 291 (2002), 59–71.
Herzke, D., Berger, U., Kallenborn, R., Nygård, T., Vetter, W., Brominated flame retardants and other organobromines in Norwegian predatory bird eggs. Chemosphere 61 (2005), 441–449.
Herzke, D., Nygård, T., Berger, U., Huber, S., Rov, 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.
Herzke, D., Jaspers, V.L.B., Boertmann, D., Rasmussen, L.M., Sonne, C., Dietz, R., Covaci, A., Eens, M., Bustnes, J.O., PFCs in feathers of white tailed eagles (Haliaeetus albicilla) from Greenland and Norway; useful for non-destructive monitoring?. Organomet. Compd. 73 (2011), 1337–1339.
Houde, M., Czub, G., Small, J.M., Backus, S.M., Wang, X., Alaee, M., Muir, D.C.G., Fractionation and bioaccumulation of perfluorooctane sulfonate (PFOS) isomers in a Lake Ontario food web. Environ. Sci. Technol. 42 (2008), 9397–9403.
Inger, R., Bearhop, S., Applications of stable isotope analyses to avian ecology. Ibis 150 (2008), 447–461.
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. 80 (2011), 595–602.
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. 40 (2006), 7501–7511.
Jaspers, V.L., 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.
Jaspers, V.L.B., Herzke, D., Eulaers, I., Gillespie, B.W., Eens, M., Perfluoroalkyl substances in soft tissues and tail feathers of Belgian barn owls (Tyto alba) using statistical methods for left-censored data to handle non-detects. Environ. Int. 52 (2013), 9–16.
Jones, P.D., Hu, W., De Coen, W., Newsted, J.L., Giesy, J.P., Binding of perfluorinated fatty acids to serum proteins. Environ. Toxicol. Chem. 22 (2003), 2639–2649.
Kärrman, A., van Bavel, B., Järnberg, U., Hardell, L., Lindström, G., Perfluorinated chemicals in relation to other persistent organic pollutants in human blood. Chemosphere 64 (2006), 1582–1591.
Keller, J.M., Kucklick, J.R., Harms, C.A., McClellan-Green, P.D., Organochlorine contaminants in sea turtles: correlations between whole blood and fat. Environ. Toxicol. Chem. 23 (2004), 726–738.
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.
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.
Layman, C.A., Allgeier, J.E., Characterizing trophic ecology of generalist consumers: a case study of the invasive lionfish in the Bahamas. Mar. Ecol. Prog. 448 (2012), 131–141.
Lindstrom, A.B., Strynar, M.J., Libelo, E.L., Polyfluorinated compounds: past, present, and future. Environ. Sci. Technol. 45 (2011), 7954–7961.
Matthews, B., Mazumder, A., A critical evaluation of intrapopulation variation of δ13C and isotopic evidence of individual specialization. Oecologia 140 (2004), 361–371.
Meyer, J., Jaspers, V.L., Eens, M., de Coen, W., The relationship between perfluorinated chemical levels in the feathers and livers of birds from different trophic levels. Sci. Total Env. 407 (2009), 5894–5900.
Newsome, S.D., Del Rio, C.M., Bearhop, S., Phillips, D.L., A niche for isotopic ecology. Front. Ecol. Environ. 5 (2007), 429–436.
Newsted, J.L., Jones, P.D., Coady, K., Giesy, J.P., Avian toxicity reference values for perfluorooctane sulfonate. Environ. Sci. Technol. 39 (2005), 9357–9362.
Newsted, J.L., Coady, K.K., Beach, S.A., Butenhoff, J.L., Gallagher, S., Giesy, J.P., Effects of perfluorooctane sulfonate on mallard and Northern bobwhite quail exposed chronically via the diet. Environ. Toxicol. Pharmacol. 23 (2007), 1–9.
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.
NRC (U.S. National Research Council), Animals as Sentinels of Environmental Health Hazards. 1991, National Academy Press, Washington.
O'Brien, J.M., Kennedy, S.W., Chu, S., Letcher, R.J., Isomer-specific accumulation of perfluorooctane sulfonate in the liver of chicken embryos exposed in ovo to a technical mixture. Environ. Toxicol. Chem. 30 (2011), 226–231.
Pearson, S.F., Levey, D.J., Greenberg, C.H., del Rio, C.M., Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135 (2003), 516–523.
Peig, J., Green, A.J., New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118 (2009), 1883–1891.
Powley, C.R., George, S.W., Ryan, T.W., Buck, R.C., Matrix effect-free analytical methods for determination of perfluorinated carboxylic acids in environmental matrixes. Anal. Chem. 77 (2005), 6353–6358.
R Core Team, R: A Language and Environment for Statistical Computing. 2015, R Foundation for Statistical Computing, Vienna, Austria (URL) 〈https://www.R-project.org/〉.
Route, W.T., Russell, R.E., Lindstrom, A.B., Strynar, M.J., Key, R.L., 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.
Senthilkumar, K., Fluorinated organic chemicals: a review. Res. J. Chem. Environ. 9 (2005), 50–79.
Seow, J., 2013. Firefighting foams with perfluorochemicals — environmental review. 〈http://www.hemmingfire.com/news/get_file.php3/id/287/file/Seow_WA-DEC_PFCs_Firefighting_Foam_final_version_7June 2013.pdf〉 (2013).
Sergio, F., Newton, I., Marchesi, L., Conservation: top predators and biodiversity. Nature, 436, 2005, 192.
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.
Sonne, C., Bustnes, J.O., Herzke, D., Jaspers, V.L.B., Covaci, A., Eulaers, I., Halley, D.J., Moum, T., Ballesteros, M., Eens, M., Ims, R.A., Hanssen, S.A., Erikstad, K.E., Johnsen, T.V., Rigét, F.F., Jensen, A.L., Kjelgaard-Hansen, M., Blood plasma clinical–chemical parameters as biomarker endpoints for organohalogen contaminant exposure in Norwegian raptor nestlings. Ecotoxicol. Environ. Saf. 80 (2012), 76–83.
UNEP (United Nations Environmental Programme), The Stockholm Convention on Persistent Organic Pollutants. 2009, United Nations, adoption of amendments to Annexes A, B and C.
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.
Wang, Z., Cousins, I.T., Scheringer, M., Hungerbuehler, K., Hazard assessment of fluorinated alternatives to long-chain perfluoroalkyl acids (PFAAs) and their precursors: status quo, ongoing challenges and possible solutions. Environ. Int. 75 (2015), 172–179.
Zhang, H., Ding, L., Fang, X., Shi, Z., Zhang, Y., Chen, H., Yan, X., Dai, J., Biological responses to perfluorododecanoic acid exposure in rat kidneys as determined by integrated proteomic and metabonomic studies. PLoS ONE, 6(6), 2011, e20862.