Journal of Ornithology

, Volume 156, Supplement 1, pp 297–305 | Cite as

Cumulative effects of radioactivity from Fukushima on the abundance and biodiversity of birds

  • A. P. Møller
  • I. Nishiumi
  • T. A. Mousseau


Species differ in their susceptibility to radiation because of differences in their ability to sustain toxic and genetic effects caused by radiation. We censused breeding birds in Fukushima Prefecture, Japan, during 2011-2014 to test whether the abundance and diversity of birds became increasingly negatively affected by radiation over time. The abundance of birds decreased with increasing levels of background radiation, with significant interspecific variation. Even though levels of background radiation decreased over time, the relationship between abundance and radiation became more negative over time. The relationship between abundance and radiation became less negative with increasing trophic levels. These findings are consistent with the hypothesis that the negative effects of radiation on abundance and species richness accumulate over time.


Birds Chernobyl Fukushima Radiation resistance 

Supplementary material

10336_2015_1197_MOESM1_ESM.doc (224 kb)
Supplementary material 1 (DOC 369 kb)


  1. Akimoto S (2014) Morphological abnormalities in gall-forming aphids in a radiation-contaminated area near Fukushima Daiichi: Selective impact of fallout? Ecol Evol 4:355–369PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bibby CJ, Hill DA, Burgess ND, Mustoe S (2005) Bird census techniques. Academic Press, London, UKGoogle Scholar
  3. Blondel J, Ferry C, Frochot B (1970) La méthode des indices ponctuels d’abondance (I.P.A.) au des relevés d’avifaune par “stations d’ecoute”. Alauda 38:55–71Google Scholar
  4. Boubriak II, Grodzinsky DM, Polischuk VP, Naumenko VD, Gushcha NP, Micheev AN, McCready SJ, Osborne DJ (2008) Adaptation and impairment of DNA repair function in pollen of Betula verrucosa and seeds of Oenothera biennis from differently radionuclide-contaminated sites of Chernobyl. Ann Bot 101:267–276PubMedPubMedCentralCrossRefGoogle Scholar
  5. Dadachova E, Howell RW, Bryan RA, Frenkel A, Nosanchuck JD, Casadevall A (2004) Susceptibility of the human pathogenic fungi Cryptococcus neoformans and Histoplasma capsulatum to gamma-irradiation versus radioimmunotherapy with alpha- and beta-emitting radioisotopes. J Nuclear Med 45:313–320Google Scholar
  6. Daly MJ (2009) A new perspective on radiation resistance based on Deinococcus radiodurans. Nature Rev Microbiol 7:237–245CrossRefGoogle Scholar
  7. del Hoyo J, Elliott A, Sagartal J (eds) (1992–2011) Handbook of the birds of the World. Lynx, Barcelona, SpainGoogle Scholar
  8. Draper NR, Smith H (1981) Applied regression analysis, 2nd edn. John Wiley, New York, NYGoogle Scholar
  9. Galván I, Bonisoli-Alquati A, Jenkinson S, Ghanem G, Wakamatsu K, Mousseau TA, Møller AP (2014) Chronic exposure to low-dose radiation at Chernobyl favors adaptation to oxidative stress in birds. Funct Ecol 28:1387–1403CrossRefGoogle Scholar
  10. Galván I, Mousseau TA, Møller AP (2011) Bird population declines due to radiation exposure at Chernobyl are stronger in species with pheomelanin-based coloration. Oecologia 165:827–835PubMedCrossRefGoogle Scholar
  11. Garamszegi LZ, Møller AP (2010) Effects of sample size and intraspecific variation in phylogenetic comparative studies: A meta-analytic review. Biol Rev 85:797–805PubMedGoogle Scholar
  12. Garamszegi LZ, Møller AP (2011) Nonrandom variation in within-species sample size and missing data in phylogenetic comparative studies. Syst Biol in press. doi: 10.1093/sysbio/syr060.
  13. Ghiassi-Nejad M, Zakeri F, Assaei Kariminia A (2004) Long-term immune and cytogenetic effects of high level natural radiation on Ramsar inhabitants in Iran. J Environ Radioact 74:107–116PubMedCrossRefGoogle Scholar
  14. Hendry JH, Simon SL, Wojcik A, Sohrabi M, Burkart W, Cardis E, Laurier D, Tirmarche M, Hayata I (2009) Human exposure to high natural background radiation: What can it teach us about radiation risks? J Radiol Protect 29(2A):A29–A42CrossRefGoogle Scholar
  15. Hiyama A, Nohara C, Kinjo S, Taira W, Gima S, Tanahara A, Otaki JM (2012) The biological impacts of the Fukushima nuclear accident on the pale grass blue butterfly. Sci Rep 2:570PubMedPubMedCentralCrossRefGoogle Scholar
  16. Hiyama A, Nohara C, Taira W, Kinjo S, Iwata M, Otaki JM (2013) The Fukushima nuclear accident and the pale grass blue butterfly: Evaluating biological effects of long-term low-dose exposures. BMC Evol Biol 13:168PubMedPubMedCentralCrossRefGoogle Scholar
  17. Ishida K (2013) Contamination of wild animals: Effects on wildlife in high radioactivity areas of the agricultural and forest landscape. In: Nakanishi TM, Tanoi K (eds) Agricultural Implications of the Fukushima Nuclear Accident. Springer, Japan, pp 119–129CrossRefGoogle Scholar
  18. Kryshev I, Alexakhin R, Makhonko K (1992) Radioecological consequences of the Chernobyl accident. Nuclear Society, Moscow, RussiaGoogle Scholar
  19. Kryshev II, Ryabov IN (1990) About the efficiency of trophic level in the accumulation of Cs-137 in fish of the Chernobyl NPP cooling pond. In: Ryabov IN, Ryabtsev IA (eds) Biological and radioecological aspects of the consequences of the Chernobyl accident. USSR Academy of Sciences, Moscow, pp 116–121Google Scholar
  20. Lubin J, Boice J Jr (1997) Lung cancer risk from residential radon: meta-analysis of eight epidemiologic studies. J Natl Cancer Inst 89:49–57PubMedCrossRefGoogle Scholar
  21. Møller AP (1983) Methods for monitoring bird populations in the Nordic countries. Nordic Council of Ministers, Oslo, NorwayGoogle Scholar
  22. Møller AP, Hagiwara A, Matsui S, Kasahara S, Kawatsu K, Nishiumi I, Suzuki H, Ueda K, Mousseau TA (2012) Abundance of birds in Fukushima as judged from Chernobyl. Environ. Poll. 164:36–39CrossRefGoogle Scholar
  23. Møller AP, Mousseau TA (2007a) Species richness and abundance of birds in relation to radiation at Chernobyl. Biol Lett 3:483–486PubMedPubMedCentralCrossRefGoogle Scholar
  24. Møller AP, Mousseau TA (2007b) Determinants of interspecific variation in population declines of birds from exposure to radiation at Chernobyl. J Appl Ecol 44:909–919CrossRefGoogle Scholar
  25. Møller AP, Mousseau TA (2011a) Efficiency of bio-indicators for low-level radiation under field conditions. Ecol Indicators 11:424–430CrossRefGoogle Scholar
  26. Møller AP, Mousseau TA (2011b) Conservation consequences of Chernobyl and other nuclear accidents. Biol Cons 114:2787–2798CrossRefGoogle Scholar
  27. Møller AP, Mousseau TA (2013) Low-dose radiation, scientific scrutiny, and requirements for demonstrating effects. BMC Biol 11(92)Google Scholar
  28. Møller AP, Surai PF, Mousseau TA (2005) Antioxidants, radiation and mutation in barn swallows from Chernobyl. Proc R Soc Lond B 272:247–253CrossRefGoogle Scholar
  29. Murase K, Murase J, Horie R, Endo K (2015) Effects of the Fukushima Daiichi nuclear accident on goshawk reproduction. Sci Rep (in press)Google Scholar
  30. Nadson GA, Philippov GS (1925) Influence des rayon’s x sur la sexualité et la formation des mutantes chez les champignons inferieurs (Mucorinées). C R Soc Biol Filiales 93:473–474Google Scholar
  31. Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models. Irwin, Chicago, ILGoogle Scholar
  32. Ochiai K, Hayama S, Nakiri S, Nakanishi S, Ishii N, Uno T, Kato T, Konno F, Kawamoto Y, Tsuchida S, Omi T (2014) Low blood cell counts in wild Japanese monkeys after the Fukushima Daiichi nuclear disaster. Sci Rep 4:5793PubMedGoogle Scholar
  33. SAS Institute Inc (2012) JMP. SAS Institute Inc., Cary, NCGoogle Scholar
  34. Smith MH, Oleksyk TK, Tsyusko O (2002) Effects of trophic position and ecosystem type on the form of the frequency distribution of radiocesium at Chornobyl and nuclear sites in the United States. Proc Int Symp: Transfer of Radionuclides in Biosphere: Prediction and Assessment, December 18–19, 2002. Mito, Japan, pp 37–48Google Scholar
  35. Sokal RR, Rohlf FJ (1995) Biometry. W. H, Freeman, New YorkGoogle Scholar
  36. Voitovich AM, Afonin VYu (2002) DNA damages and radionuclide accumulation in wild small vertebrates. In: Environmental Radioactivity in the Arctic and Antarctic, Proceedings of the 5th International Conference, St. Petersburg, 16-20 June 2002, Russia, pp. 340–343Google Scholar
  37. Voříšek P, Klvanova A, Wotton S, Gregory RD (2010) A best practice guide for wild bird monitoring schemes. European Union, Bruxelles, BelgiumGoogle Scholar
  38. Yakushev BI, Budkevich TA, Zabolotny AI, Mironov V, Kudryashov VP (1999) Contamination of vegetation in Belarus by transuranium radionuclides due to Chernobyl NPP accident. In: Goossens LHJ (ed) Proc 9th Ann Conf “Risk analysis: Facing the new millennium”, October 10–13, 1999. Delft University Press, Rotterdam, pp 841–844Google Scholar
  39. Yamashiro H, Abe Y, Fukuda T, Kino Y, Kawaguchi I, Kuwahara Y, Fukumoto M, Takahashi S, Suzuki M, Kobayashi J, Uematsu E, Tong B, Yamada T, Yoshida S, Sato E, Shinoda H, Sekine T, Isogai E, Fukumoto M (2013) Effects of radioactive caesium on bull testes after the Fukushima nuclear plant accident. Sci Rep 3:2850PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2015

Authors and Affiliations

  1. 1.Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079Université Paris-SudOrsay CedexFrance
  2. 2.Department of ZoologyNational Museum of Nature and ScienceTokyoJapan
  3. 3.Department of Biological SciencesUniversity of South CarolinaColumbiaUSA
  4. 4.Department of Environmental Biology, Biosciences, and BiotechnologyChubu UniversityKasugaiJapan

Personalised recommendations