Feathers as an integrated measure of organohalogen contamination, its dietary sources and corticosterone in nestlings of a terrestrial bird of prey, the northern Goshawk (Accipiter gentilis).
Randulff, Sina T; Abbasi, Naeem A; Eulaers, Igoret al.
2022 • In Science of the Total Environment, p. 154064
Body feather; Corticosterone; Northern goshawk nestlings; Plasma; Preen oil; Stable isotopes; Pollution; Waste Management and Disposal; Environmental Chemistry; Environmental Engineering
Abstract :
[en] In this study, we evaluated the suitability of body feathers, preen oil and plasma for estimation of organohalogen compound (OHC) exposure in northern goshawk Accipiter gentilis nestlings (n = 37; 14 nests). In addition, body feathers received further examination concerning their potential to provide an integrated assessment of (1) OHC exposure, (2) its dietary sources (carbon sources and trophic position) and (3) adrenal gland response (corticosterone). While tetrabromobisphenol A was not detected in any sample, the presence of polychlorinated biphenyls, organochlorine pesticides, polybrominated diphenyl ethers and hexabromocyclododecane in body feathers (median: 23, 19, 1.6 and 3.5 ng g-1 respectively), plasma (median: 7.5, 6.2, 0.50 and 1.0 ng g-1 ww, respectively) and preen oil (median: 750, 600, 18 and 9.57 ng g-1 ww, respectively) suggests analytical suitability for biomonitoring of major OHCs in the three matrices. Furthermore, strong and significant associations (0.20 ≤ R2 ≤ 0.98; all P < 0.05) among the OHC concentrations in all three tissues showed that body feathers and preen oil reliably reflect circulating plasma OHC levels. Of the dietary proxies, δ13C (carbon source) was the most suitable predictor for variation in feather OHCs concentrations, while no significant relationships between body feather OHCs and δ15N (trophic position) were found. Finally, body feather corticosterone concentrations were not related to variation in OHC concentrations. This is the first study to evaluate feathers of a terrestrial bird of prey as an integrated non-destructive tool to jointly assess nestling ecophysiology and ecotoxicology.
Disciplines :
Environmental sciences & ecology Zoology
Author, co-author :
Randulff, Sina T; Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway
Abbasi, Naeem A; College of Earth and Environmental Sciences (CEES), University of the Punjab, Quaid-e-Azam campus, Lahore, Pakistan. Electronic address: abbasi_akhtar4045@yahoo.com
Eulaers, Igor; Arctic Research Centre, Department of Bioscience, Aarhus University, Roskilde, Denmark
Nygård, Torgeir; Unit for Terrestrial Ecology, Norwegian Institute for Nature Research, Trondheim, Norway
Covaci, Adrian; Toxicological Centre, Department of Pharmaceutical Sciences, University of Antwerp, Wilrijk, Belgium
Eens, Marcel; Behavioural Ecology & Ecophysiology Group, Department of Biology, University of Antwerp, Wilrijk, Belgium
Malarvannan, Govindan; Toxicological Centre, Department of Pharmaceutical Sciences, University of Antwerp, Wilrijk, Belgium
Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire d'Ecologie trophique et isotopique
Løseth, Mari E; Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway, Norwegian Geotechnical Institute (NGI), Oslo, Norway
Jaspers, Veerle L B; Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway. Electronic address: veerle.jaspers@ntnu.no
Language :
English
Title :
Feathers as an integrated measure of organohalogen contamination, its dietary sources and corticosterone in nestlings of a terrestrial bird of prey, the northern Goshawk (Accipiter gentilis).
Abbasi, N.A., Eulaers, I., Jaspers, V.L.B., Chaudhry, M.J.I., Frantz, A., Ambus, P.L., Covaci, A., Malik, R.N., The first exposure assessment of legacy and unrestricted brominated flame retardants in predatory birds of Pakistan. Environ. Pollut. 220 (2017), 1208–1219.
Abbasi, N.A., Arukwe, A., Jaspers, V.L.B., Eulaers, I., Mennillo, E., Ibor, O.R., Frantz, A., Covaci, A., Malik, R.N., Oxidative stress responses in relationship to persistent organic pollutant levels in feathers and blood of two predatory bird species from Pakistan. Sci. Total Environ. 580 (2017), 26–33.
Bortolotti, G.R., Marchant, T.A., Blas, J., German, T., Corticosterone in feathers is a long-term, integrated measure of avian stress physiology. Funct. Ecol. 22 (2008), 494–500.
Bourgeon, S., Leat, E.H., Magnusdottir, E., Fisk, A.T., Furness, R.W., Strom, H., Hanssen, S.A., Petersen, A., Olafsdottir, K., Borga, K., Gabrielsen, G.W., Bustnes, J.O., Individual variation in biomarkers of health: influence of persistent organic pollutants in great skuas (Stercorarius skua) breeding at different geographical locations. Environ. Res. 118 (2012), 31–39.
Briels, N., Torgersen, L.N., Castaño-Ortiz, J.M., Løseth, M.E., Herzke, D., Nygård, T., Bustens, J.O., Ciesielski, T.M., Poma, G., Malarvannan, G., Jaspers, V.L.B., Covaci, A., Integrated exposure assessment of northern goshawk (Accipiter gentilis) nestlings to legacy and emerging organic pollutants using non-destructive samples. Environ. Research, 178, 2019, 108678.
Bustnes, J.O., Bardsen, 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., Nost, 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.
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 Wit, C.A., Herzke, D., Vorkamp, K., Brominated flame retardants in the Arctic environment–trends and new candidates. Sci. Total Environ. 408 (2010), 2885–2918.
Drouillard, K., Norstrom, R., Fox, G., Gilman, A., Peakall, D., Development and validation of a herring gull embryo toxicokinetic model for PCBs. Ecotoxicology 12 (2003), 55–68.
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. 407:12 (2009), 3867–3875.
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., 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., Nygard, 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., 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.
Fairhurst, G.D., Vogeli, M., Serrano, D., Delgado, A., Tella, J.L., Bortolotti, G.R., Can synchronizing feather-based measures of corticosterone and stable isotopes help us better understand habitat-physiology relationships?. Oecologia 173 (2013), 731–743.
Fairhurst, G.D., Bond, A.L., Hobson, K.A., Ronconi, R.A., Feather-based measures of stable isotopes and corticosterone reveal a relationship between trophic position and physiology in a pelagic seabird over a 153-year period. Ibis 157 (2015), 273–283.
Ganz, K., Jenny, D., Kraemer, T., Jenni, L., Jenni-Eiermann, S., Prospects and pitfalls of using feathers as a temporal archive of stress events and environmental pollutants: a review and case study. J. Ornithol. 159:3 (2018), 771–783.
Garcia-Fernandez, A.J., Calvo, J.F., Martinez-Lopez, E., Maria-Mojica, P., Martinez, J.E., Raptor ecotoxicology in Spain: a review on persistent environmental contaminants. Ambio 37 (2008), 432–439.
Garcia-Fernandez, A.J., Espin, S., Martinez-Lopez, E., Feathers as a biomonitoring tool of polyhalogenated compounds: a review. Environmental Science & Technology 47 (2013), 3028–3043.
Harms, N.J., Fairhurst, G.D., Bortolotti, G.R., Smits, J.E., Variation in immune function, body condition, and feather corticosterone in nestling tree swallows (Tachycineta bicolor) on reclaimed wetlands in the Athabasca oil sands, Alberta, Canada. Environ. Pollut. 158 (2010), m841–m848.
Helander, B., Hailer, F., Vila, C., Morphological and genetic sex identification of white-tailed eagle Haliaeetus albicilla nestlings. J. Ornithol. 148 (2007), 435–442.
Jaspers, V.L.B., Covaci, A., Voorspoels, S., Dauwe, T., Eens, M., Schepens, P., Brominated flame retardants and organochlorine pollutants in aquatic and terrestrial predatory birds of Belgium: levels, patterns, tissue distribution and condition factors. Environ. Pollut. 139 (2006), 340–352.
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., Covaci, A., van den Steen, E., Eens, M., Is external contamination with organic pollutants important for concentrations measured in bird feathers?. Environ. Int. 33 (2007), 766–772.
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.
Jaspers, V.L.B., Covaci, A., Deleu, P., Neels, H., Eens, M., Preen oil as the main source of external contamination with organic pollutants onto feathers of the common magpie (Pica pica). Environ. Int. 34 (2008), 741–748.
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.
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.
Kenward, R., The Goshawk. 2010, Bloomsbury Publishing.
Letcher, R.J., Bustnes, J.O., Dietz, R., Jenssen, B.M., Jorgensen, E.H., Sonne, C., Verreault, J., Vijayan, M.M., Gabrielsen, G.W., Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci. Total Environ. 408 (2010), 2995–3043.
Løseth, M.E., Flo, J., Sonne, C., Krogh, A.K.H., Nygård, T., Bustnes, J.O., Jenssen, B.M., Jaspers, V.L.B., The influence of natural variation and organohalogenated contaminants on physiological parameters in white-tailed eagle (Haliaeetus albicilla) nestlings from Norway. Environ. Res., 177, 2019, 108586.
Løseth, M.E., Briels, N., Flo, J., Malarvannan, G., Poma, G., Covaci, A., Herzke, D., Nygard, T., Bustens, 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.
Love, O.P., Bird, D.M., Shutt, L.J., Plasma corticosterone in american kestrel siblings: effects of age, hatching order, and hatching asynchrony. Horm. Behav. 43 (2003), 480–488.
Love, O.P., Shutt, L.J., Silfies, J.S., Bortolotti, G.R., Smits, J.E., Bird, D.M., Effects of dietary PCB exposure on adrenocortical function in captive American kestrels (Falco sparverius). Ecotoxicology 12 (2003), 199–208.
Martínez-Padilla, J., Mougeot, F., García, J.T., Arroyo, B., Bortolotti, G.R., Feather corticosterone levels and carotenoid-based coloration in common buzzard (Buteo buteo) nestlings. J. Raptor Res. 47 (2013), 161–173.
Monclús, L., Lopez-Bejar, M., de la Puente, J., Covaci, A., Jaspers, V.L.B., Can variability in corticosterone levels be related to POPs and OPEs in feathers from nestling cinereous vultures (Aegypius monachus)?. Sci. Total Environ. 650 (2019), 184–192.
Nordstad, T., Moe, B., Bustnes, J.O., Bech, C., Chastel, O., Goutte, A., Sagerup, K., Trouvé, C., Herzke, D., Gabrielsen, G.W., Relationships between POPs and baseline corticosterone levels in black-legged kittiwakes (Rissa tridactyla) across their breeding cycle. Environ. Pollut. 164 (2012), 219–226.
Noyes, P.D., McElwee, M.K., Miller, H.D., Clark, B.W., van Tiem, L.A., Walcott, K.C., Erwin, K.N., Levin, E.D., The toxicology of climate change: environmental contaminants in a warming world. Environ. Int. 35 (2009), 971–986.
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.
Pinheiro, J., Bates, D., Debroy, S.D.S., Team, R.C., NLME, Linear and Nonlinear Mixed Effects Models. R Package, Version 3, 57, 2015, 1–89.
R Core Team, R: A Language and Environment for Statistical Computing Reference Index. 2014.
Ramos, R., González-Solís, J., Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Front. Ecol. Environ. 10 (2012), 258–266.
Rigét, F.F., Bignert, A., Braune, B., Stow, J., Wilson, S., Temporal trends of legacy POPs in Arctic biota, an update. Sci. Total Environ. 408 (2010), 2874–2884.
Schoech, S.J., Rensel, M.A., Heiss, R.S., Short- and long-term effects of developmental corticosterone exposure on avian physiology, behavioral phenotype, cognition, and fitness: a review. Curr. Zool. 57 (2011), 514–530.
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.
Strong, R.J., Pereira, M.G., Shore, R.F., Henrys, P.A., Pottinger, T.G., Feather corticosterone content in predatory birds in relation to body condition and hepatic metal concentration. Gen. Comp. Endocrinol. 214 (2015), 47–55.
Tartu, S., Angelier, F., Herzke, D., Moe, B., Bech, C., Gabrielsen, G.W., Bustens, J.O., Chastel, O., The stress of being contaminated? Adrenocortical function and reproduction in relation to persistent organic pollutants in female black legged kittiwakes. Sci. Total Environ. 476 (2014), 553–560.
Yamashita, S., Evaluation of noninvasive approach for monitoring PCB pollution of seabirds using preen gland oil. Environ. Sci. Technol. 41 (2007), 4901–4906.
Yamashita, R., Takada, H., Nakazawa, A., Takahashi, A., Ito, M., Yamamoto, T., Watanuki, Y., Global monitoring of persistent organic pollutants (POPs) using seabird preen gland oil. Arch. Environ. Contam. Toxicol. 75:4 (2018), 545–556.
Yu, L.H., Luo, X.J., Wu, J.P., Liu, L.Y., Song, J., Sun, Q.H., Mai, B.X., Biomagnification of higher brominated PBDE congeners in an urban terrestrial food web in North China based on field observation of prey deliveries. Environ. Sci. Technol. 45:12 (2011), 5125–5131.
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.
