Biomonitoring; Erythrocytes; Feather; Metals; Red blood cells; Environmental Pollutants; Mercury; Animals; Environmental Monitoring; Feathers/chemistry; Norway; Environmental Pollutants/analysis; Eagles; Mercury/analysis; Birds of prey; Dry weight; Erythrocyte; Hg concentrations; Isotope signatures; Mercury exposure; Red blood cell; Stable carbon and nitrogen isotopes; Toxicology; Pollution; Health, Toxicology and Mutagenesis; General Medicine
Abstract :
[en] Mercury (Hg) and stable carbon and nitrogen isotope ratios were analysed in body feathers from nestlings of white-tailed eagles (Haliaeetus albicilla) (WTE; n = 13) and Northern goshawks (Accipiter gentilis) (NG; n = 8) and in red blood cells (RBC) from NG (n = 11) from Norway. According to linear mixed model, species factor was significant in explaining the Hg concentration in feathers (LMM; p < 0.001, estimate (WTE) = 2.51, 95% CI = 1.26, 3.76), with concentrations higher in WTE (3.01 ± 1.34 µg g-1 dry weight) than in NG (0.51 ± 0.34 µg g-1 dry weight). This difference and the isotopic patterns for each species, likely reflect their diet, as WTE predominantly feed on a marine and higher trophic-chain diet compared to the terrestrial NG. In addition, Hg concentrations in RBCs of NG nestlings were positively correlated with feather Hg concentrations (Rho = 0.77, p = 0.03), supporting the potential usefulness of nestling body feathers to biomonitor and estimate Hg exposure. Hg levels in both species were generally below the commonly applied toxicity threshold of 5 µg g-1 in feathers, although exceeded in two WTE (6.08 and 5.19 µg g-1 dry weight).
Disciplines :
Environmental sciences & ecology Zoology
Author, co-author :
Gómez-Ramírez, Pilar ; Toxicology Group, Department of Health Sciences, Faculty of Veterinary, University of Murcia, Campus de Espinardo, 30100, Murcia, Spain. pilargomez@um.es
Bustnes, Jan Ove; Norwegian Institute for Nature Research, Fram Centre, 9296, Tromsø, Norway
Eulaers, Igor; Department of Bioscience, Faculty of Technical Sciences, Aarhus University, Frederiksborgvej 399, PO Box 358, 4000, Roskilde, Denmark
Johnsen, Trond Vidar; Norwegian Institute for Nature Research, Fram Centre, 9296, Tromsø, Norway
Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution
Pérez-García, Juan Manuel; Ecology Area, Department of Applied Biology, University Miguel Hernández, 03202, Elche, Spain
García-Fernández, Antonio Juan; Toxicology Group, Department of Health Sciences, Faculty of Veterinary, University of Murcia, Campus de Espinardo, 30100, Murcia, Spain
Espín, Silvia; Toxicology Group, Department of Health Sciences, Faculty of Veterinary, University of Murcia, Campus de Espinardo, 30100, Murcia, Spain
Jaspers, Veerle Leontina Bernard; Environmental Toxicology Group, Department of Biology, Norwegian University of Science and Technology (NTNU), 7024, Trondheim, Norway. veerle.jaspers@ntnu.no
Language :
English
Title :
Mercury Exposure in Birds of Prey from Norway: Relation to Stable Carbon and Nitrogen Isotope Signatures in Body Feathers.
Publication date :
02 June 2023
Journal title :
Bulletin of Environmental Contamination and Toxicology
UCM - Universidad Complutense de Madrid [ES] MICINN - Ministerio de Ciencia e Innovacion [ES] NTNU - Norges Teknisk-Naturvitenskapelige Universitet [NO] RCN - Research Council of Norway [NO] NINA - Norsk Institutt for Naturforskning [NO] Universidad de Murcia [ES]
Funding text :
Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. P. Gómez-Ramírez was supported by a grant from Iceland, Liechtenstein and Norway through the EEA Financial Mechanism, operated by Universidad Complutense de Madrid. The Norwegian Research Council and NTNU funded the project NEWRAPTOR and V.L.B. Jaspers. Additional funding was provided by the Hazardous Substances Flagship (the Raptor project) at the Fram Centre in Tromsø. Hg analysis was supported by the Service of Toxicology and Forensic Veterinary at the University of Murcia. Silvia Espín and Juan M. Pérez-García were supported by Ministerio de Ciencia, Innovación y Universidades (Juan de la Cierva-Incorporación contracts IJCI-2017–34653 and IJC-2019–038968, respectively).
Badry A, Palma L, Beja P et al (2019) Using an apex predator for large-scale monitoring of trace element contamination: associations with environmental, anthropogenic and dietary proxies. Sci Total Environ 676:746–755. 10.1016/j.scitotenv.2019.04.217 DOI: 10.1016/j.scitotenv.2019.04.217
Barnes JG, Gerstenberger SL (2015) Using feathers to determine mercury contamination in peregrine falcons and their prey. J Raptor Res 49:43–58. 10.3356/jrr-14-00045.1 DOI: 10.3356/jrr-14-00045.1
Bearhop S, Waldron S, Thompson D, Furness R (2000) Bioamplification of mercury in great Skua Catharacta skua Chicks: the influence of trophic status as determined by stable isotope signatures of blood and feathers. Mar Pollut Bull 40:181–185. 10.1016/S0025-326X(99)00205-2 DOI: 10.1016/S0025-326X(99)00205-2
Berglund M, Lind B, Björnberg KA et al (2005) Inter-individual variations of human mercury exposure biomarkers: a cross-sectional assessment. Environ Heal A Glob Access Sci Source. 10.1186/1476-069X-4-20 DOI: 10.1186/1476-069X-4-20
Bond AL (2010) Relationships between stable isotopes and metal contaminants in feathers are spurious and biologically uninformative. Environ Pollut 158:1182–1184. 10.1016/j.envpol.2010.01.004 DOI: 10.1016/j.envpol.2010.01.004
Boutton TW (1991) Stable carbon isotope ratios of natural materials: II. Atmospheric, terrestrial, marine, and freshwater environments. In: Coleman DC, Fry B (eds) Carbon isotope techniques. Academic Press Inc., San Diego, pp 173–183 DOI: 10.1016/B978-0-12-179730-0.50016-3
Burger J, Gochfeld M (1997) Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. Environ Res 75:160–172. 10.1006/enrs.1997.3778 DOI: 10.1006/enrs.1997.3778
Burger J, Jehl JR, Gochfeld M (2013) Selenium:mercury molar ratio in eared grebes (Podiceps nigricollis) as a possible biomarker of exposure. Ecol Indic 34:60–68. 10.1016/J.ECOLIND.2013.04.001 DOI: 10.1016/J.ECOLIND.2013.04.001
Bustnes JO, Bårdsen B-JJ, Bangjord G et al (2013) Temporal trends (1986–2005) of essential and non-essential elements in a terrestrial raptor in northern Europe. Sci Total Environ 458–460:101–106. 10.1016/j.scitotenv.2013.04.027 DOI: 10.1016/j.scitotenv.2013.04.027
Carravieri A, Cherel Y, Blévin P et al (2014) Mercury exposure in a large subantarctic avian community. Environ Pollut 190:51–57. 10.1016/j.envpol.2014.03.017 DOI: 10.1016/j.envpol.2014.03.017
Cherel Y, Barbraud C, Lahournat M et al (2018) Accumulate or eliminate? Seasonal mercury dynamics in albatrosses, the most contaminated family of birds. Environ Pollut 241:124–135. 10.1016/j.envpol.2018.05.048 DOI: 10.1016/j.envpol.2018.05.048
Climate and Pollution Agency (2010) The mercury problem: reducing and eliminating mercury pollution in Norway. Retrieved from http://www.mercury.org.cn/zcfg/gj/202107/P020210715338600571869.pdf
Dolan KJ, Ciesielski TM, Lierhagen S et al (2017) Trace element concentrations in feathers and blood of Northern goshawk (Accipiter gentilis) nestlings from Norway and Spain. Ecotoxicol Environ Saf 144:564–571. 10.1016/j.ecoenv.2017.06.062 DOI: 10.1016/j.ecoenv.2017.06.062
Einoder LD, MacLeod CK, Coughanowr C (2018) Metal and isotope analysis of bird feathers in a contaminated estuary reveals bioaccumulation, biomagnification, and potential toxic effects. Arch Environ Contam Toxicol. 10.1007/s00244-018-0532-z DOI: 10.1007/s00244-018-0532-z
Eisler R (1987) Mercury hazards to fish, wildlife and invertebrates: a synoptic review. Biological Report 85 (1.10) Contaminant Hazard Review, No. 10. US Fish and Wildlife Research centre
Ekblad C, Eulaers I, Schulz R et al (2021) Spatial and dietary sources of elevated mercury exposure in white-tailed eagle nestlings in an Arctic freshwater environment. Environ Pollut 290:117952. 10.1016/j.envpol.2021.117952 DOI: 10.1016/j.envpol.2021.117952
Espín S, Martínez-López E, León-Ortega M et al (2014a) Factors that influence mercury concentrations in nestling Eagle Owls (Bubo bubo). Sci Total Environ 470–471:1132–1139. 10.1016/j.scitotenv.2013.10.063 DOI: 10.1016/j.scitotenv.2013.10.063
Espín S, Martínez-López E, León-Ortega M et al (2014b) Oxidative stress biomarkers in Eurasian eagle owls (Bubo bubo) in three different scenarios of heavy metal exposure. Environ Res 131:134–144. 10.1016/j.envres.2014.03.015 DOI: 10.1016/j.envres.2014.03.015
Espín S, García-Fernández AJJ, Herzke D et al (2016) Tracking pan-continental trends in environmental contamination using sentinel raptors-what types of samples should we use? Ecotoxicology 25:777–801. 10.1007/s10646-016-1636-8 DOI: 10.1007/s10646-016-1636-8
Espín S, Andevski J, Duke G et al (2021) A schematic sampling protocol for contaminant monitoring in raptors. Ambio 50:95–100. 10.1007/s13280-020-01341-9 DOI: 10.1007/s13280-020-01341-9
Eulaers I, Jaspers VLB, Bustnes JO et al (2013) Ecological and spatial factors drive intra- and interspecific variation in exposure of subarctic predatory bird nestlings to persistent organic pollutants. Environ Int 57–58:25–33. 10.1016/j.envint.2013.03.009 DOI: 10.1016/j.envint.2013.03.009
Eulaers I, Jaspers VLB, Halley DJ et al (2014) 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 478:48–57. 10.1016/j.scitotenv.2014.01.051 DOI: 10.1016/j.scitotenv.2014.01.051
Frank RA, Lutz RS (1999) Productivity and survival of Great horned owls exposed to dieldrin. Condor 101:331–339 DOI: 10.2307/1369996
Furness RW, Muirhead SJ, Woodburn M (1986) Using bird feathers to measure mercury in the environment: relationships between mercury content and moult. Mar Pollut Bull 17:27–30. 10.1016/0025-326X(86)90801-5 DOI: 10.1016/0025-326X(86)90801-5
Gómez-Ramírez P, Shore RF, van den Brink NW et al (2014) An overview of existing raptor contaminant monitoring activities in Europe. Environ Int 67:12–21 DOI: 10.1016/j.envint.2014.02.004
Gómez-Ramírez P, Bustnes JO, Eulaers I et al (2017) Per- and polyfluoroalkyl substances in plasma and feathers of nestling birds of prey from northern Norway. Environ Res 158:277–285. 10.1016/j.envres.2017.06.019 DOI: 10.1016/j.envres.2017.06.019
Góngora E, Braune BM, Elliott KH (2018) Nitrogen and sulfur isotopes predict variation in mercury levels in Arctic seabird prey. Mar Pollut Bull 135:907–914. 10.1016/j.marpolbul.2018.07.075 DOI: 10.1016/j.marpolbul.2018.07.075
Guigueno MF, Elliott KH, Levac J, et al (2012) Differential exposure of alpine ospreys to mercury: melting glaciers, hydrology or deposition patterns? Environ Int 40:24–32. 10.1016/j.envint.2011.11.004 DOI: 10.1016/j.envint.2011.11.004
Harmens H, Norris DA, Koerber GR et al (2008) Temporal trends (1990–2000) in the concentration of cadmium, lead and mercury in mosses across Europe. Environ Pollut 151:368–376. 10.1016/j.envpol.2007.06.043 DOI: 10.1016/j.envpol.2007.06.043
Herring G, Ackerman JT, Herzog MP (2012) Mercury exposure may suppress baseline corticosterone levels in juvenile birds. Environ Sci Technol 46:6339–6346. 10.1021/es300668c DOI: 10.1021/es300668c
Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis (lond 1859) 150:447–461. 10.1111/j.1474-919X.2008.00839.x DOI: 10.1111/j.1474-919X.2008.00839.x
Kelly JF (2000) Stable isotopes of carbon and in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27 DOI: 10.1139/z99-165
Keyel ER, Etterson MA, Niemi GJ, et al (2020) Feather mercury increases with feeding at higher trophic levels in two species of migrant raptors, Merlin (Falco columbarius) and Sharp-shinned Hawk (Accipiter striatus). Condor 122:duz069. 10.1093/condor/duz069 DOI: 10.1093/condor/duz069
Lodenius M, Solonen T (2013) The use of feathers of birds of prey as indicators of metal pollution. Ecotoxicology 22:1319–1334. 10.1007/s10646-013-1128-z DOI: 10.1007/s10646-013-1128-z
Løseth ME, Briels N, Eulaers I et al (2019) Plasma concentrations of organohalogenated contaminants in white-tailed eagle nestlings–the role of age and diet. Environ Pollut 246:527–534. 10.1016/j.envpol.2018.12.028 DOI: 10.1016/j.envpol.2018.12.028
Peterson SH, Ackerman JT, Toney M, Herzog MP (2019) Mercury concentrations vary within and among individual bird feathers: a critical evaluation and guidelines for feather use in mercury monitoring programs. Environ Toxicol Chem 38:1164–1187 DOI: 10.1002/etc.4430
Ramos R, González-Solís J (2012) Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Front Ecol Environ 10:258–266. 10.1890/110140 DOI: 10.1890/110140
Rattner BA, Golden NH, Toschik PC et al (2008) Concentrations of metals in blood and feathers of nestling ospreys (Pandion haliaetus) in Chesapeake and Delaware Bays. Arch Environ Contam Toxicol 54:114–122. 10.1007/s00244-007-9004-6 DOI: 10.1007/s00244-007-9004-6
Rodríguez A, Acosta M, Mugica L et al (2013) Assessment of trace elements and stable isotopes of three ardeid species at Birama Swamp Cuba. Arch Environ Contam Toxicol 65:24–32. 10.1007/s00244-013-9887-3 DOI: 10.1007/s00244-013-9887-3
Roque I, Lourenço R, Marques A et al (2016) Barn owl feathers as biomonitors of mercury: sources of variation in sampling procedures. Ecotoxicology 25:469–480. 10.1007/s10646-015-1604-8 DOI: 10.1007/s10646-015-1604-8
Solonen T, Lodenius M (1990) Feathers of birds of prey as indicators of mercury contamination in southern Finland. Holarct Ecol 13:229–237. 10.1111/j.1600-0587.1990.tb00613.x DOI: 10.1111/j.1600-0587.1990.tb00613.x
Sun J, Bustnes JO, Helander B et al (2019) Temporal trends of mercury differ across three northern white-tailed eagle (Haliaeetus albicilla) subpopulations. Sci Total Environ 687:77–86. 10.1016/j.scitotenv.2019.06.027 DOI: 10.1016/j.scitotenv.2019.06.027
UNEP (2013) Global mercury assessment 2013: sources, emissions, releases, and environmental transport. UNEP Chemicals Branch, Geneva, Switzerland