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Ecological differences in response of bird species to radioactivity from Chernobyl and Fukushima

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Abstract

Organisms differ in their susceptibility to ionizing radiation, although the ecological basis for such differences remain poorly understood. We hypothesized that ecological characteristics such as body size, diet, migration and pigments of plumage would predict the impact of radiation on abundance through effects on relative food consumption rates, free radicals and antioxidants. We made 2,398 breeding bird censuses and quantified the impact of radiation on abundance at Chernobyl and Fukushima providing statistical replication, but also analyses of interaction effects. The impact of radiation on abundance of birds was stronger at Fukushima than at Chernobyl. Species with small body size and hence relatively high food consumption rates were more negatively impacted. Secondary consumers showed stronger negative effects of radiation on abundance than herbivores, especially at Fukushima. There was no main effect of migration, but migrants were more negatively impacted at Chernobyl, while residents were more negatively impacted at Fukushima. Carotenoid and pheomelanin plumage pigments associated with antioxidant status showed stronger negative effects, especially at Chernobyl compared to Fukushima, while eumelanic coloration which is not related to antioxidant status did not show such an effect. These differences between Chernobyl and Fukuskima may reflect differences in duration of exposure, differences in radioactive isotopes and differences in accumulation of mutations.

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References

  • Asker D, Awad TS, McLandsborough L, Beppu T, Ueda K (2011) Deinococcus depolymerans sp. nov., a gamma- and UV-radiation-resistant bacterium, isolated from a naturally radioactive site. Int J Syst Evol Microbiol 61:1448–1453

    Article  PubMed  CAS  Google Scholar 

  • Beauchamp G, Heeb P (2001) Social foraging and the evolution of white plumage. Evol Ecol Res 3:703–720

    Google Scholar 

  • Bennett PM, Owens IPF (2002) Evolutionary ecology of birds. Oxford University Press, Oxford

    Google Scholar 

  • Bibby CJ, Hill DA, Burgess ND, Mustoe S (2005) Bird census techniques. Academic, London

    Google Scholar 

  • 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 38:55–71

    Google Scholar 

  • Bonisoli-Alquati A, Mousseau TA, Møller AP, Caprioli M, Saino N (2010a) Increased oxidative stress in barn swallows from the Chernobyl region. Comp Biochem Physiol A 155:205–210

    Article  Google Scholar 

  • Bonisoli-Alquati A, Voris A, Mousseau TA, Møller AP, Saino N, Wyatt M (2010b) DNA damage in barn swallows (Hirundo rustica) from the Chernobyl region detected by use of the Comet assay. Comp Biochem Physiol C 151:271–277

    Google Scholar 

  • Bump EA, Brown JM (1990) Role of glutathione in the radiation response of mammalian cells in vitro and in vivo. Pharmacol Therapeut 47:117–136

    Article  CAS  Google Scholar 

  • Cramp S, Perrins CM (1977–1994) The birds of the Western Palearctic, vol 1–9. Oxford University Press, Oxford

  • del Hoyo J, Elliott A, Sagatal J, Christie DA (eds) (1992–2011) Handbook of the birds of the World. Lynx, Barcelona

  • Dighton J, Tugay T, Zhdanova N (2008) Fungi and ionizing radiation from radionuclides. FEMS Microbiol Lett 281:109–120

    Article  PubMed  CAS  Google Scholar 

  • Draper NR, Smith H (1981) Applied regression analysis, 2nd edn. Wiley, New York

    Google Scholar 

  • Galván I (2008) The importance of white on black: unmelanized plumage proportion predicts display complexity in birds. Behav Ecol Sociobiol 63:303–311

    Article  Google Scholar 

  • Galván I, Alonso-Alvarez C (2009) The expression of melanin-based plumage is separately modulated by exogenous oxidative stress and a melanocortin. Proc R Soc Lond B 276:3089–3097

    Article  Google Scholar 

  • Galván I, Solano F (2009) The evolution of eu- and pheomelanic traits may respond to an economy of pigments related to environmental oxidative stress. Pigment Cell Melanoma Res 22:339–342

    Article  PubMed  Google Scholar 

  • 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 165:827–835

    Article  PubMed  Google Scholar 

  • 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 28:1387–1403

    Article  Google Scholar 

  • Garamszegi LZ, Møller AP (2010) Effects of sample size and intraspecific variation in phylogenetic comparative studies: a meta-analytic review. Biol Rev 85:797–805

    PubMed  Google Scholar 

  • Garamszegi LZ, Møller AP (2011) Nonrandom variation in within-species sample size and missing data in phylogenetic comparative studies. Syst Biol 60:676–680

    Article  Google Scholar 

  • Ivaniota L, Dubchak AS, Tyshchenko VK (1998) Free radical oxidation of lipids and antioxidant system of blood in infertile women in a radioactive environment. Ukr Biochim Zh 70:132–135 (in Russian)

    CAS  Google Scholar 

  • 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 116–121

    Google Scholar 

  • Kryshev I, Alexakhin R, Makhonko K (1992) Radioecological consequences of the Chernobyl accident. Nuclear Society, Moscow

    Google Scholar 

  • Lislevand T, Figuerola J, Székely T (2007) Avian body sizes in relation to fecundity, mating system, display behavior, and resource sharing. Ecology 88:1605

    Article  Google Scholar 

  • McGraw KJ, Wakamatsu K (2004) Melanin basis of ornamental feather colors in male Zebra Finches. Condor 106:686–690

    Article  Google Scholar 

  • Møller AP (1983) Methods for monitoring bird populations in the Nordic countries. Nordic Council of Ministers, Oslo

    Google Scholar 

  • Møller AP, Mousseau TA (2007a) Species richness and abundance of birds in relation to radiation at Chernobyl. Biol Lett 3:483–486

    Article  PubMed  PubMed Central  Google Scholar 

  • Møller AP, Mousseau TA (2007b) Determinants of interspecific variation in population declines of birds from exposure to radiation at Chernobyl. J Appl Ecol 44:909–919

    Article  Google Scholar 

  • Møller AP, Mousseau TA (2011a) Efficiency of bio-indicators for low-level radiation under field conditions. Ecol Indic 11:424–430

    Article  Google Scholar 

  • Møller AP, Mousseau TA (2011b) Conservation consequences of Chernobyl and other nuclear accidents. Biol Cons 144:2787–2798

    Article  Google Scholar 

  • Møller AP, Mousseau TA (2013) The effects of natural variation in background radioactivity on humans, animals and other organisms. Biol Rev 88:226–254

    Article  PubMed  Google Scholar 

  • Møller AP, Surai PF, Mousseau TA (2005) Antioxidants, radiation and mutation in barn swallows from Chernobyl. Proc R Soc Lond B 272:247–253

    Article  Google Scholar 

  • Møller AP, Hagiwara A, Matsui S, Kasahara S, Kawatsu K, Nishiumi I, Suzuki H, Ueda K, Mousseau TA (2012a) Abundance of birds in Fukushima as judged from Chernobyl. Environ Poll 164:36–39

    Article  Google Scholar 

  • Møller AP, Nishiumi I, Suzuki H, Ueda K, Mousseau TA (2012b) Differences in effects of radiation on abundance of animals in Fukushima and Chernobyl. Ecol Indic 24:75–81

    Article  Google Scholar 

  • Navarro J, Obrador E, Pellicer JA, Asensi M, Viña J, Estrela JM (1997) Blood glutathione as an index of radiation-induced oxidative stress in mice and humans. Free Radic Biol Med 22:1203–1209

    Article  PubMed  CAS  Google Scholar 

  • Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models. Irwin, Chicago

    Google Scholar 

  • Neyfakh EA, Alimbekova AI, Ivanenko GF (1998) Radiation-induced lipoperoxidative stress in children coupled with deficit of essential antioxidants. Biochim (Moscow) 63:977–987

    CAS  Google Scholar 

  • Ninni P, de Lope F, Saino N, Haussy C, Møller AP (2004) Antioxidants and condition-dependence of arrival date in a migratory passerine. Oikos 105:55–64

    Article  Google Scholar 

  • Olson V, Owens IPF (2005) Interspecific variation in the use of carotenoid-based coloration in birds: diet, life history and phylogeny. J Evol Biol 18:1534–1546

    Article  PubMed  CAS  Google Scholar 

  • Owens IPF, Hartley IR (1998) Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proc R Soc Lond B 265:397–407

    Article  Google Scholar 

  • Ozeki H, Ito S, Wakamatsu K, Ishiguro I (1997) Chemical characterization of pheomelanogenesis starting from dihydroxyphenylalanine or tyrosine and cysteine. Effects of tyrosinase and cysteine concentrations and reaction time. Biochim Biophys Acta 1336:539–548

    Article  PubMed  CAS  Google Scholar 

  • Riley PA (1994) Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol 65:27–33

    Article  PubMed  CAS  Google Scholar 

  • Romanovskaya VA, Rokitko PV, Mikheev AN, Gushcha NI, Malashenko YR, Chernaya NA (2002) The effect of γ-radiation and desiccation on the viability of the soil bacteria isolated from the alienated zone. Microbiology 71:608–613

    Article  CAS  Google Scholar 

  • SAS Institute Inc (2012) JMP. SAS Institute, Cary

    Google Scholar 

  • Shestopalov VM (1996) Atlas of Chernobyl exclusion zone. Ukrainian Academy of Science, Kiev

    Google Scholar 

  • 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. In: Proc Int Symp: transfer of radionuclides in biosphere: prediction and assessment, Mito, Japan, pp 37–48, December 18–19, 2002

  • Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New York

    Google Scholar 

  • Tella JL, Figuerola J, Negro JJ, Blanco G, Rodríguez-Estrella R, Forero MG, Blazquez MC, Green AJ, Hiraldo F (2004) Ecological, morphological and phylogenetic correlates of interspecific variation in plasma carotenoid concentration in birds. J Evol Biol 17:156–164

    Article  PubMed  CAS  Google Scholar 

  • Toral GM, Figuerola J, Negro JJ (2008) Multiple ways to become red: pigment identification in red feathers using spectrometry. Comp Biochem Physiol B 150:147–152

    Article  PubMed  CAS  Google Scholar 

  • Vartanian LS, Gurevich S, Kozachenko AI, Nagler LG, Burlakova EB (1994) Age-related peculiarities of effect of low dose ionizing radiation on blood antioxidant enzyme system status in Chernobyl’s accident liquidation participant. Adv Gerontol 14:48–54 (in Russian)

    Google Scholar 

  • 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, Russia, pp 340–343, 16–20

  • Voříšek P, Klvanova A, Wotton S, Gregory RD (2010) A best practice guide for wild bird monitoring schemes. European Union, Bruxelles

    Google Scholar 

  • Wild Bird Society of Japan (1982) A field guide to the birds of Japan. Wild Bird Society of Japan, Tokyo

    Google Scholar 

  • 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 841–844

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Acknowledgments

We gratefully acknowledge logistic support and help by Professor A. Hagiwara, T. Kanagawa, K. Kawai, Professor K. Kawatsu and A.M. Smith in Japan. We are especially grateful to Namie-cho and the people of Fukushima Prefecture who permitted and supported us to conduct this study in the field. We gratefully acknowledge support from the US National Science Foundation, the University of South Carolina College of Arts and Sciences, CNRS (France), the Samuel Freeman Charitable Trust, Qiagen GmbH, JSPS KAKENHI Grant Number 26440254, and anonymous gifts from individuals in Japan.

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Correspondence to A. P. Møller.

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Communicated by E. Matthysen.

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Møller, A.P., Mousseau, T.A., Nishiumi, I. et al. Ecological differences in response of bird species to radioactivity from Chernobyl and Fukushima. J Ornithol 156 (Suppl 1), 287–296 (2015). https://doi.org/10.1007/s10336-015-1173-x

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