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Lead poisoning and other human-related factors cause significant mortality in white-tailed eagles

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Abstract

The white-tailed eagle (Haliaeetus albicilla) suffered a severe population decline due to environmental pollutants in the Baltic Sea area ca. 50 years ago but has since been recovering. The main threats for the white-tailed eagle in Finland are now often related to human activities. We examined the human impact on the white-tailed eagle by determining mortality factors of 123 carcasses collected during 2000–2014. Routine necropsy with chemical analyses for lead and mercury were done on all carcasses. We found human-related factors accounting for 60% of the causes of death. The most important of these was lead poisoning (31% of all cases) followed by human-related accidents (e.g. electric power lines and traffic) (24%). The temporal and regional patterns of occurrence of lead poisonings suggested spent lead ammunition as the source. Lead shot was found in the gizzards of some lead-poisoned birds. Scavenging behaviour exposes the white-tailed eagle to lead from spent ammunition.

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References

  • Arnemo, J., O. Andersen, S. Stokke, V.G. Thomas, O. Krone, D.J. Pain, and R. Mateo. 2016. Health and environmental risks from lead-based ammunition: Science versus socio-politics. EcoHealth 13: 618–622.

    Article  Google Scholar 

  • Balotari-Chiebao, F., A. Villers, A. Ijäs, O. Ovaskainen, S. Repka, and T. Laaksonen. 2016. Post-fledging movements of white-tailed eagles: Conservation implications for wind-energy development. Ambio 45: 831–840.

    Article  Google Scholar 

  • Bevanger, K., F. Berntsen, S. Clausen, E.L. Dahl, Ø. Flagstad, A. Follestad, D. Halley, F. Hanssen, et al. 2010. Pre- and post-construction studies of conflicts between birds and wind turbines in coastal Norway (Bird-Wind). Report on findings 2007–2010. NINA Report 620, Trondheim, Norway.

  • Brooke, C.J., and T.V. Riley. 1999. Erysipelothrix rhusiopathiae: bacteriology, epidemiology and clinical manifestations of an occupational pathogen. Journal of Medical Microbiology 48: 789–799.

    Article  CAS  Google Scholar 

  • Burnham, K.P., and D.R. Anderson. 2002. Model selection and multimodel inference: A practical information- theoretic approach, 2nd ed. New York: Springer.

    Google Scholar 

  • Dahl, E.L., K. Bevanger, G. Nygård, E. Røskaft, and B.G. Stokke. 2012. Reduced breeding success in white-tailed eagles at Smøla windfarm, western Norway, is caused by mortality and displacement. Biological Conservation 145: 79–85.

    Article  Google Scholar 

  • Damerau, A., E.R. Venäläinen, and K. Peltonen. 2012. Heavy metals in meat of Finnish city rabbits. Food Additives & Contaminants 5: 246–250.

    Article  CAS  Google Scholar 

  • Delahay, R.J., and C.J. Spray (eds.). 2015. Proceedings of the Oxford Lead Symposium. Lead Ammunition: understanding and minimising the risks to human and environmental health. Oxford: Edward Grey Institute, The University of Oxford.

  • Ecke, F., N.J. Singh, J.M. Arnemo, A. Bignert, B. Helander, Å.M.M. Berglund, H. Borg, C. Bröjer, et al. 2017. Sublethal lead exposure alters movement behavior in free-ranging golden eagles. Environmental Science and Technology 51: 5729–5736.

    Article  CAS  Google Scholar 

  • EFSA (European Food Safety Authority). 2013. Scientific opinion on lead in food. Retrieved 11 April, 2017, from http://www.efsa.europa.eu/en/efsajournal/pub/1570.

  • Ekblad, C.M.S., S. Sulkava, T.G. Stjernberg, and T.K. Laaksonen. 2016. Landscape-scale gradients and temporal changes in the prey species of the white-tailed eagles (Haliaeetus albicilla). Annales Zoologici Fennici 53: 228–240.

    Article  Google Scholar 

  • Franson, C. 1996. Interpretation of tissue lead residues in birds other than waterfowl. In Environmental contaminants in wildlife—interpreting tissue concentrations, ed. W.N. Beyer, G.H. Heinz, and A.W. Redmon-Norwood, 265–279. Boca Raton, FL: CRC.

    Google Scholar 

  • Franson, J.C., and R.E. Russell. 2014. Lead and eagles: demographic and pathological characteristics of poisoning, and exposure levels associated with other causes of mortality. Ecotoxicology 23: 1722–1731.

    Article  CAS  Google Scholar 

  • Heatley, J.J., M.M. Mitchell, A. Roy, D.Y. Cho, D.L. Williams, and T.N. Tully. 2007. Disseminated Mycobacteriosis in a Bald Eagle Haliaeetus leucocephalus. Journal of Avian Medicine and Surgery 21: 201–209.

    Article  Google Scholar 

  • Heinz, G.H. 1996. Mercury poisoning in wildlife. In Noninfectious diseases of wildlife, ed. A. Fairbrother, G.L. Hoff, and L.N. Locke, 118–127. Ames, IA: Iowa State University Press.

    Google Scholar 

  • Heinz, G.H., and D.J. Hoffman. 1998. Methylmercury chloride and selenomethionine interactions on health and reproduction in mallards. Environmental Toxicology and Chemistry 17: 139–145.

    Article  CAS  Google Scholar 

  • Helander, B., and T. Stjernberg. 2002. Action Plan for the conservation of White-tailed Sea Eagle (Haliaeetus albicilla). Strasbourg: Birdlife International.

    Google Scholar 

  • Helander, B., A. Olsson, A. Bignert, L. Asplund, and K. Litzén. 2002. The role of DDE, PCB, coplanar PCB and eggshell parameters for reproduction in the white-tailed sea eagle (Haliaeetus albicilla) in Sweden. Ambio 31: 386–403.

    Article  Google Scholar 

  • Helander, B., A. Bignert, and L. Asplund. 2008. Using raptors as environmental sentinels: Monitoring the white-tailed sea eagle Haliaeetus albicilla in Sweden. Ambio 37: 425–431.

    Article  Google Scholar 

  • Helander, B., J. Axelsson, H. Borg, K. Holm, and A. Bignert. 2009. Ingestion of lead from ammunition and lead concentrations in white-tailed sea eagles (Haliaeetus albicilla) in Sweden. Science of the Total Environment 407: 5555–5563.

    Article  CAS  Google Scholar 

  • HELCOM (Helsinki Commision). 2010. Hazardous substances in the Baltic Sea – An integrated thematic assessment of hazardous substances in the Baltic Sea. Baltic Sea Environment Proceedings No. 120B. Retrieved February, 2018, from http://www.helcom.fi/Lists/Publications/BSEP120B.pdf.

  • Henriksson, K., E. Karppanen, and M. Helminen. 1966. High residues of mercury in Finnish white-tailed eagles. Ornis Fennica 43: 38–45.

    Google Scholar 

  • Herrmann, C., O. Krone, T. Stjernberg, and B. Helander. 2011. Population development of baltic bird species: White-tailed sea eagle (Haliaeetus albicilla). HELCOM Baltic Sea Environment Fact Sheets. Retrieved May, 2017, from http://www.helcom.fi/baltic-sea-trends/environment-fact-sheets/.

  • Hoffman, D.J., O.H. Pattee, S.N. Wiemeyer, and B. Mulhern. 1981. Effects of lead shot ingestion on δ-aminolevulinic acid dehydratase activity, hemoglobin concentration and serum chemistry in bald eagles. Journal of Wildlife Diseases 17: 423–431.

    Article  CAS  Google Scholar 

  • Hunt, W.G. 2012. Implications of sublethal lead exposure in avian scavengers. Journal of Raptor Research 46: 389–393.

    Article  Google Scholar 

  • Hunt, W.G., W. Burnham, C.N. Parish, K.K. Burnham, B. Mutch, and J.L. Oaks. 2006. Bullet fragments in deer remains: Implications for lead exposure in avian scavengers. Wildlife Society Bulletin 34: 167–170.

    Article  Google Scholar 

  • Iwata, H., M. Watanabe, E.-Y. Kim, R. Gotori, G. Yasunaga, S. Tanabe, Y. Masuda, and S. Fujita. 2000. Contamination by chlorinated hydrocarbons and lead in Steller’s Sea-Eagle and White-tailed Eagle from Hokkaido, Japan. In First symposium on Steller’s and white-tailed eagles in East Asia, ed. M. Ueta, and M.J. McGrady, 96–106. Tokyo: Wild Bird Society of Japan.

    Google Scholar 

  • Kalisinska, E., J. Gorecki, N. Lanocha, A. Okonska, J.B. Melgarejo, H. Budis, I. Rzad, and J. Golas. 2014. Total and methylmercury in soft tissues of white-tailed eagle (Haliaeetus albicilla) and Osprey (Pandion haliaetus) collected in Poland. Ambio 43: 858–870.

    Article  CAS  Google Scholar 

  • Kenntner, N., F. Tataruch, and O. Krone. 2001. Heavy metals in soft tissue of white-tailed eagles found dead or moribund in Germany and Austria from 1993 to 2000. Environmental Toxicology and Chemistry 20: 1831–1837.

    Article  CAS  Google Scholar 

  • Koivusaari, J., T. Stjernberg, H. Ekblom, and J. Högmander. 2003. Daily body weight, amount of food and time of feeding of white-tailed sea eagles at Finnish winter feeding stations 1992–2000. In: SEA EAGLE 2000. Proceedings from an international conference at Björkö, Sweden, 13–17 September 2000, ed. B. Helander, M. Marquiss, and W. Bowerman. Stockholm: Swedish Society for Nature Conservation/SNF & Åtta.45 Tryckeri AB.

  • Krone, O., F. Wille, N. Kenntner, D. Boertmann, and F. Tataruch. 2004. Mortality factors, environmental contaminants, and parasites of white-tailed sea eagles from Greenland. Avian Diseases 48: 417–424.

    Article  Google Scholar 

  • Krone, O., T. Stjernberg, N. Kenntner, F. Tataruch, J. Koivusaari, and I. Nuuja. 2006. Mortality factors, helminth burden, and contaminant residues in white-tailed sea eagles (Haliaeetus albicilla) from Finland. Ambio 35: 98–104.

    Article  CAS  Google Scholar 

  • Krone, O., N. Kenntner, A. Trinogga, M. Nadjafzadeh, F. Scholz, J. Sulawa, K. Totschek, P. Schuck-Wersig, et al. 2008. Lead poisoning in white-tailed sea eagles: causes and approaches to solutions in Germany. In Ingestion of lead from spent ammunition: Implications for wildlife and humans, ed. R.T. Watson, M. Fuller, M. Pokras, and W.G. Hunt. Boise, ID: The Peregrine Fund.

    Google Scholar 

  • Krone, O., N. Kenntner, and F. Tataruch. 2009. Gefährdungsursachen des Seeadlers. Denisia 27: 139–146 (In German).

    Google Scholar 

  • Mateo, R. 2009. Lead poisoning in wild birds in Europe and the regulations adopted in different countries. In Ingestion of lead from spent ammunition: Implications for wildlife and humans, ed. R.T. Watson, M. Fuller, M. Pokras, and W.G. Hunt. Boise, ID: The Peregrine Fund.

    Google Scholar 

  • Müller, K., R. Altenkamp, and L. Brunnberg. 2007. Morbidity of free-ranging white-tailed sea eagles (Haliaeetus albicilla) in Germany. Journal of Avian Medicine and Surgery 21: 265–274.

    Article  Google Scholar 

  • Nadjafzadeh, M., H. Hofer, and O. Krone. 2013. The link between feeding ecology and lead poisoning in white-tailed eagles. Journal of Wildlife Management 77: 48–57.

    Article  Google Scholar 

  • Newth, J.L., E.C. Rees, R.L. Cromie, R.A. McDonald, S. Bearhop, D.J. Pain, G.J. Norton, C. Deacon, et al. 2016. Widespread exposure to lead affects the body condition of free-living whooper swans Cygnus cygnus wintering in Britain. Environmental Pollution 209: 60–67.

    Article  CAS  Google Scholar 

  • Nuuja, I. (ed.). 2017. Merikotkien puolesta—WWF:n merikotkatyöryhmän vuosikymmenten taival. Helsinki: WWF Finland report. (For the white-tailed eagles—the journey of the WWF white-tailed eagle working group. In Finnish).

  • OIE (World Organisation for Animal Health). 2017. Update on highly pathogenic avian influenza in animals (types H5 and H7). Retrieved December, 2017, from: http://www.oie.int/animal-health-in-the-world/update-on-avian-influenza/.

  • Pain, D.J., I.J. Fisher and V.G. Thomas. 2009. A global update of lead poisoning in terrestrial birds from ammunition sources. In: Ingestion of Lead from Spent Ammunition: implications for wildlife and Humans, ed. R.T.Watson, M. Fuller, M. Pokras, and W.G. Hunt. Boise, ID: The Peregrine Fund.

    Google Scholar 

  • Provencher, J.F., M.R. Forbes, H.L. Hennin, O.P. Love, B.M. Braune, M.L. Mallory, and H.G. Gilchrist. 2016. Implications of mercury and lead concentrations on breeding physiology and phenology in an Arctic bird. Environmental Pollution 218: 1014–1022.

    Article  CAS  Google Scholar 

  • Redig, P.T., E.M. Lawler, S. Schwartz, J.L. Dunnette, B. Stephenson, and G.E. Duke. 1991. Effects of chronic exposure to sublethal concentrations of lead acetate on heme synthesis and immune function in red-tailed hawks. Archives of Environmental Contamination and Toxicology 21: 72–77.

    Article  CAS  Google Scholar 

  • Saurola, P., J. Valkama, and W. Velmala. 2013. The finnish bird ringing Atlas, vol. I. Helsinki: Finnish Museum of Natural History and Ministry of Environment.

    Google Scholar 

  • Stauber, E., N. Finch, P.A. Talcott, and J.M. Gay. 2010. Lead poisoning of bald (Haliaeetus leucocephalus) and golden (Aquila chrysaetos) eagles in the US Inland Pacific Northwest Region—an 18-year retrospective study: 1991–2008. Journal of Avian Medicine and Surgery 24: 279–287.

    Article  Google Scholar 

  • Stjernberg, T., J. Koivusaari, J. Högmander, T. Ollila, S. Keränen, G. Munsterhjelm, and H. Ekblom. 2009. Population size and nesting success of the White-tailed Sea Eagle (Haliaeetus albicilla) in Finland, 2007–2008. Linnut-vuosikirja 2008: 14–21. (in Finnish, English summary).

  • Sulkava, S., R. Tornberg, and J. Koivusaari. 1997. Diet of the white-tailed eagle Haliaeetus albicilla in Finland. Ornis Fennica 74: 65–78.

    Google Scholar 

  • Thomas, N.J., D.B. Hunter, and C.T. Atkinson (eds.). 2007. Infectious diseases of wild birds, 9th ed. Ames, ID: Blackwell Publishing.

    Book  Google Scholar 

  • Tiainen, J., M. Mikkola-Roos, A. Below, A. Jukarainen, A. Lehikoinen, T. Lehtiniemi, J. Pessa, A. Rajasärkkä, et al. 2016. Suomen lintujen uhanalaisuus 2015—the 2015 red list of Finnish bird species. Helsinki: Ympäristöministeriö & Suomen ympäristökeskus.

    Google Scholar 

  • Wayland, M., and T. Bollinger. 1999. Lead exposure and poisoning in bald eagles and golden eagles in the Canadian prairie provinces. Environmental Pollution 104: 341–350.

    Article  CAS  Google Scholar 

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Acknowledgements

We want to express our thanks to the people who submitted or reported dead or diseased white-tailed eagles suitable for this study. We warmly thank the competent staff of the Finnish Food Safety Authority, especially Minna Nylund, Perttu Koski, Nina Aalto and Annette Brockmann for their help in post-mortem examinations.

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Authors and Affiliations

  1. Wild and Aquatic Animal Pathology Section, Veterinary Bacteriology and Pathology Research Unit, Finnish Food Safety Authority Evira, Elektroniikkatie 3, 90590, Oulu, Finland

    Marja Isomursu & Varpu Hirvelä-Koski

  2. Västervikintie 346, 65280, Vaasa, Finland

    Juhani Koivusaari

  3. Finnish Museum of Natural History, University of Helsinki, PB 17, 00014, University of Helsinki, Finland

    Torsten Stjernberg

  4. Chemistry Research Unit, Finnish Food Safety Authority Evira, Mustialankatu 3, 00790, Helsinki, Finland

    Eija-Riitta Venäläinen

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  1. Marja Isomursu
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  2. Juhani Koivusaari
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Correspondence to Marja Isomursu.

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Isomursu, M., Koivusaari, J., Stjernberg, T. et al. Lead poisoning and other human-related factors cause significant mortality in white-tailed eagles. Ambio 47, 858–868 (2018). https://doi.org/10.1007/s13280-018-1052-9

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