Ecological differences in response of bird
species to radioactivity from Chernobyl and
Fukushima
A. P. Møller, T. A. Mousseau,
I. Nishiumi & K. Ueda

Journal of Ornithology
ISSN 2193-7192
J Ornithol
DOI 10.1007/s10336-015-1173-x

1 23

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Author's personal copy
J Ornithol
DOI 10.1007/s10336-015-1173-x

REVIEW

Ecological differences in response of bird species to radioactivity
from Chernobyl and Fukushima
A. P. Møller • T. A. Mousseau • I. Nishiumi •K. UedaReceived: 18 October 2014 / Revised: 19 January 2015 / Accepted: 2 February 2015
Ó Dt. Ornithologen-Gesellschaft e.V. 2015

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, migrationand pigments of plumage would predict the impact of radiation on abundance through effects on relative foodconsumption rates, free radicals and antioxidants. We made2,398 breeding bird censuses and quantified the impact ofradiation 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
Communicated by E. Matthysen.

Electronic supplementary material The online version of thisarticle (doi:10.1007/s10336-015-1173-x) contains supplementarymaterial, which is available to authorized users.
A. P. Møller (&)
Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR
8079, Université Paris-Sud, Bâtiment 362, 91405 Orsay Cedex,
Francee-mail: anders.moller@u-psud.fr
T. A. Mousseau
Department of Biological Sciences and the Environment
and Sustainability Program, University of South Carolina,
Columbia, SC 29208, USAe-mail: mousseau@sc.edu
I. Nishiumi
Department of Zoology, National Museum of Natureand Science, 4-1-1 Amakubo, Tsukuba, Ibaraki 305-0005, Japane-mail: nishiumi@kahaku.go.jp
K. UedaDepartment of Life Science, Rikkyo University,
3-34-1 Nishi-ikebukuro, Toshima-ku, Tokyo 171-8501, Japane-mail: keisuke@rikkyo.ac.jp

small body size and hence relatively high food consumption rates were more negatively impacted. Secondary
consumers showed stronger negative effects of radiation onabundance than herbivores, especially at Fukushima. There
was no main effect of migration, but migrants were morenegatively impacted at Chernobyl, while residents weremore negatively impacted at Fukushima. Carotenoid andpheomelanin 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 induration of exposure, differences in radioactive isotopes
and differences in accumulation of mutations.
Keywords Birds  Chernobyl  Coloration  Fukushima 
Pigments  Radiation resistanceIntroduction
There is considerable interspecific variation among organisms in their susceptibility to radiation effects (e.g.,Asker et al. 2011; Romanovskaya et al. 2002; Dighton
et al. 2008; Møller and Mousseau 2013). Why that is thecase remains an open question. This may arise from differences in exposure and hence differences in the intensityof natural selection that have resulted in the evolution of
mechanisms that sustain or even nullify such effects ofionizing radiation. This interesting scientific question hasreceived little attention despite the fact that many species
are tolerant to extreme levels of radiation (review in Møller
and Mousseau 2013). A few studies have attempted toassess interspecific differences in susceptibility to radiation

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and interspecific differences in their ecological correlates(Møller and Mousseau 2007b, 2011b; Galván et al. 2011,2014). Ionizing radiation produces free radicals and thus
promotes the generation of reactive oxidative species that
deplete antioxidant levels in animals (Riley 1994; Ivaniota
et al. 1998; Neyfakh et al. 1998). Not surprisingly, interspecific variation in susceptibility to radiation can be directly linked to ecological traits that are associated withhigh rates of use of antioxidants such as long-distancemigration, dispersal, allocation of antioxidants to coloration and allocation of antioxidants by mothers to theiroffspring (Møller and Mousseau 2007b). Field studies ofindividual birds in the vicinity of Chernobyl have shown
increased rates of DNA damage at higher levels of background radiation (Bonisoli-Alquati et al. 2010b), and thiseffect can be linked directly to an increased level of oxidative stress caused by background radiation (BonisoliAlquati et al. 2010a).
Among the pigments responsible for integument color,melanins and carotenoids are some of the most prominent
and widespread. Phaeomelanin- and carotenoid-based colors share a strong dependence on antioxidant status. Vertebrates synthesize two main forms of melanin: eumelaninand pheomelanin, with the latter producing lighter colors
than the former. Glutathione (GSH) levels determine themelanin form that is synthesized, as melanogenesis caneither lead to the production of eumelanin when the activity of tyrosinase is high and the ratio of cysteine:dopaquinone is low, or to the production of pheomelanin oreven an absence of melanin synthesis under opposite
conditions (Ozeki et al. 1997; Galván and Alonso-Alvarez2009). Therefore, eumelanogenesis takes place when thelevels of GSH are low and pheomelanogenesis when thelevels of GSH are high, implying that pheomelanogenesis
proceeds with higher levels of endogenous oxidative stressas compared to eumelanogenesis (Galván and Solano2009). The evolutionary implication of this mechanism isthat species in which natural selection has favored thedevelopment of pheomelanic traits may have a decreased
capacity to combat oxidative stress as compared to species
with eumelanic traits, as the maintenance of high GSHlevels as required by pheomelanogenesis might bemetabolically costly under adverse environmental conditions that generate oxidative stress and thus consume GSH
resources (Galván and Alonso-Alvarez 2009; Galván and
Solano 2009).
GSH is one of the antioxidants most susceptible to radiation (Bump and Brown 1990; Navarro et al. 1997;
Vartanian et al. 1994). Therefore, species which have themolecular basis to produce large amounts of pheomelanin
may be more limited in their use of GSH to combat oxidative stress, and may thus be more susceptible to ionizing
radiation than species in which melanogenesis has been123

selected to be directed toward the production of eumelanin(Galván et al. 2011). Adaptation to radiation in radioactively contaminated areas and naturally contaminated areas
alike may result in increased glutathione levels and body
condition, while oxidative stress and DNA damage has
decreased with increasing background radiation (Galván
et al. 2014). This apparent adaptation to radiation appears
to be linked to larger amounts of pheomelanin and smaller
amounts of eumelanin being costly, as shown from decreased glutathione levels, increased oxidative stress and
DNA damage, and reduced body condition (Galván et al.
2014). Finally, pheomelanin has been shown to induce achange towards the production of less pro-oxidant forms ofpheomelanin that may help acclimatize birds to radiation
exposure (Galván et al. 2014). Indeed, levels of gluthathione and pheomelanin are significantly correlated (Galván et al. 2014).
Here, we report the results of analyses of unique data on
the abundance of breeding birds at Fukushima, Japan and
Chernobyl, Ukraine, in relation to background levels ofradiation. There has been accumulation of mutations at
Chernobyl since 1986 for more than 20 generations formany small birds that typically have very short lifespan,(Møller and Mousseau 2011b), while only a couple ofgenerations have passed since the accident at Fukushima in
2011. Thus, we predicted significant differences in theassociation between abundance and radiation between
Chernobyl and Fukushima for different species of birds,
implying a significant area by ecological variableinteraction.
The objectives of this study were to test (1) whether
the effect of radiation reduced the abundance of birds;(2) whether this effect differed among species; (3)whether body mass, diet, migration and pigment-based
coloration affected the abundance of birds; and (4)whether the effects of these predictors differed between
Fukushima and Chernobyl, as predicted from their different histories of exposure to radioactive contaminants.
Small-sized species have relatively higher metabolism,
higher intake rates and hence higher ingestion of radionuclides. Similarly, species at higher trophic levels
should suffer more from radioactive contamination as aresult of bioaccumulation. Migratory birds through theirhigh metabolic rate and use of antioxidants should differ
in impact of radiation compared to residents. Indeed,
negative impacts of radiation on abundance are stronger
on the abundance of migrants than resident species(Møller and Mousseau 2007b). This is contrary to expectation because migrants spend less time in the contaminated breeding areas than residents. However,migrants deplete their stores of antioxidants during migration resulting in very low levels upon arrival (Ninni
et al. 2004). This effect is detrimental because breedingAuthor's personal copy
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birds start establishing territories, nest building and egg
formation upon arrival, causing antioxidant levels to be
severely depleted (Møller et al. 2005). Finally, there is atrade-off between allocation of antioxidants to productionof feather color and self-maintenance in birds with carotenoid- and pheomelanin-based plumage. Therefore, any
individual that allocated a large fraction of antioxidant
resources to plumage coloration without consideration of
future uses for protection against oxidative stress causedby radiation would be at a selective disadvantage.
Likewise, such individuals would also risk increased
rates of mutations due to the lack of protection against
oxidative stress thus reducing survival prospects.

Methods
Study sites
The breeding bird census points were located at ca. 100-mintervals in forested areas west of the exclusion zone
around the Fukushima Daiichi power plants in 2011–2014(Fig. 1a) or in forested areas within the Chernobyl Exclusion Zone or adjacent areas, or in areas in southern Belarus
around Gomel during the breeding seasons 2006–2009(Fig. 1b). At least one local ornithologist participated in thecensuses in Japan to confirm the identity of some difficult
bird species.
Census methods
We adopted the point count census method, which provides
reliable information on relative abundance of birds (Blondel et al. 1970; Møller 1983; Bibby et al. 2005; Vořı́šek
et al. 2010). The method is based on an observer recording
for a period of 5 min all birds seen and heard. Extensive
national monitoring programs for breeding and wintering
birds based on point counts take place in many different
countries, and this effort is part of environmental
monitoring by the European Union (Vořı́šek et al. 2010).
This method has provided highly repeatable results forbirds and other animals at Chernobyl (Møller and Mousseau 2011a). It consists of counts lasting 5 min during
which the number of birds seen or heard is recorded.
A.P.M. conducted these standard point counts during 29
May–9 June 2006, 1–11 June 2007, 29 May–5 June 2008,
1–6 June 2009 in the surroundings of Chernobyl (898census points) and during 11–15 July 2011, 14–19 2012,
14–19 2013 and 11–16 2014 at Fukushima (1,500 census
points). Thus, one single 5-min count was recorded foreach point in each of the study years. The fact that one
person made all counts eliminates any variance in results
due to inter-observer variability. There are no bird census

Fig. 1 Approximate location of census areas around Fukushima, Japan
indicated by dark blue dots (a) and Chernobyl, Ukraine and Belarus
indicated by light blue dots (b). Note that levels of radiation have only
been recorded at a limited number of sites (color figure online)

data from Chernobyl or Fukushima before the accidents,
nor to the best of our knowledge have other scientists
conducted bird censuses comparable to ours in the years
following the accidents.
We directly tested the reliability of our counts by letting
two persons independently perform counts, and the degreeof consistency was high for both species richness, totalabundance and abundance of individual species (details
reported by Møller and Mousseau 2007a for Chernobyl;

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similar results exist for Fukushima: A. P. Møller, I. Nishiumi and T. A. Mousseau, unpublished data).
Abundance estimates can be affected by numerous
confounding variables (Vořı́šek et al. 2010), and, therefore,
it is important to control such variables statistically toassess the underlying relationship between radiation andspecies richness and abundance. We classified habitats(agricultural habitats with grassland or shrub, deciduous
forest, or coniferous forest) and estimated to the nearest
10 % ground cover by herbs, shrub, trees, agricultural
habitat, deciduous forest and coniferous forest within adistance of 50 m from the census points. We recorded
altitude to the nearest foot (c.30 cm), using GPS. Weather
conditions can affect animal activity and hence census
results (Vořı́šek et al. 2010), and we recorded cloud coverat the start of each point count (to the nearest eighth),temperature (°C), and wind force (Beaufort). For each
census point, we recorded time of day when the count wasstarted (to the nearest minute). Because activity may show
a curvilinear relationship with time of day, with high levelsof bird activity in the morning and to a lesser extent in theevening (Vořı́šek et al. 2010), we also included timesquared as an explanatory variable.

extensive measurements of internal dose in hundreds ofbirds at Chernobyl and found very strong positive correlations between internal dose and background radiation level(A. P. Møller and T. A. Mousseau, unpublished).

Background radiation

Migration distance

We measured radiation in the field and cross-validated thesemeasurements with those reported by the Ukrainian Ministryof Emergencies. Once having finished the 5-min census, wemeasured a, b, and c radiation levels at ground level directly inthe field at each point where were censused invertebrates usinga hand-held dosimeter (Model: Inspector; SE International,
Summertown, TN, USA). We measured levels two–threetimes at each site and averaged the results. We cross-validated
our measurements in Ukraine against data from the governmental measurements published by Shestopalov (1996), estimated as the mid-point of the ranges published. This analysis
revealed a very strong positive relationship [linear regression
on log–log transformed data: F = 1546.49, df = 1, 252,
r2 = 0.86, P \ 0.0001, slope (SE) = 1.28 (0.10)], suggestingthat our field estimates of radiation provided reliable measurements of levels of radiation among sites.
At Fukushima, we used the same dosimeters, and themeasurements were cross-validated with readings with adosimeter that had been recently calibrated and certified tobe accurate by the factory (International Medcom, Sebastopol, CA, USA). We cross-validated tests at Fukushimaby comparing our own measurements with measurements
obtained at the same locations with a TCS 171-ALOKA
used by Japanese authorities. Again, there was a very strong
positive relationship [linear regression on log–log transformed data: F = 2427.97, df = 1, 20, r2 = 0.99,
P \ 0.0001, slope (SE) = 1.120 (0.023)]. We have madeWe estimated migration distance as the difference in latitude between the mean of the northernmost and thesouthernmost breeding distribution and the mean of thenorthernmost and the southernmost winter distribution,
relying on information in Cramp and Perrins (1977–1994)
and del Hoyo et al. (1992–2011). A strict classification of
species as either residents or migrants resulted in similar
conclusions (unpublished data).

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Ecological variables
Body mass
We extracted mean body mass of males and females during
the breeding season from Cramp and Perrins (1977–1994),
Lislevand et al. (2007) and del Hoyo et al. (1992–2011).
Body mass was estimated as the mean value of the means
for males and females.
Diet
We scored the diet of different species on a two-levelclassification based on information in Cramp and Perrins(1977–1994) and del Hoyo et al. (1992–2011): (0) mainly
plant material, especially outside the breeding season; and(1) primary predators eating herbivores such as insects andspiders, but also vertebrates.

Carotenoid-based coloration
We only considered pigment-based coloration in this study
because we did not have information on structural color forthe species considered. The extent of plumage patches
colored by carotenoids was determined by examining illustrations of adult breeding birds in Cramp and Perrins(1977–1994) and Wild Bird Society of Japan (1982). We
considered colors that were yellow, orange and red to becaused by carotenoids (Tella et al. 2004; Olson and Owens
2005). We assigned scores that ranged from 0 (total lack ofcarotenoid-based color) to 5 (all carotenoid-based).
Melanin-based coloration
We used a method for assigning coloration to melanindeveloped by (Galván et al. 2011). Information on melanin-based plumage coloration was obtained by examining

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illustrations of bird species censused at Chernobyl and
Fukushima in Cramp and Perrins (1977–1994) and Wild
Bird Society of Japan (1982). Eumelanic and pheomelanic
traits are generally of distinctive colors, the former being
responsible for black and gray colors and the latter foryellowish, reddish, chestnut and brown colors (Toral et al.
2008). Eumelanin and pheomelanin normally occur simultaneously in tissues (Ozeki et al. 1997), but the darker
colors conferred by eumelanin (Toral et al. 2008) makeevident the lower content of this pigment in chestnut andbrown as compared to black and gray colors (Galván andAlonso-Alvarez 2009). Furthermore, many bird species
have feather melanin contents of high purity ([90 % ofeither eumelanin or pheomelanin; McGraw and Wakamatsu 2004; J.J. Negro, personal communication). Therefore, we considered that black and gray plumage colors
were predominantly generated by eumelanin, while chestnut and brown colors were predominantly generated bypheomelanin. We did not consider conspicuous yellow or
red colorations assumed to be generated by other pigments(i.e. carotenoids), unless chemically identified as melaninbased by Toral et al. (2008). Although a rough approximation to the real proportion of eumelanic andpheomelanic plumage, the assumption that black-graycolors are eumelanic and brown-chestnut colors arepheomelanic should be adequate for comparative purposes(Owens and Hartley 1998). Thus, we quantified the proportion of melanic plumage parts by examining illustrations in Cramp and Perrins (1977–1994) and and Wild Bird
Society of Japan (1982). Illustrations of both resting andflying adult birds in breeding plumage were examined. The
method used by Beauchamp and Heeb (2001) and Galván(2008) was followed to obtain estimates of the proportionof eu- and pheomelanic color present in the plumage ofeach species, assigning scores that ranged from 0 (totallack of melanic color) to 5 (all melanic). When a species
was sexually dichromatic regarding melanin-based coloration, eumelanic and pheomelanic scores were the average obtained for males and females. When a species had
different subspecies or color morphs differing in extent ortype of melanin-based coloration, we used the nominate
subspecies or the most common morph, respectively. It
must be noted that eu- and pheomelanic color patches cancoexist in the same feathers, and thus the sum of both color
scores, in a species that presents both color types, is notalways necessarily 5, but higher values are also possible.
All interspecific data are reported in Appendix 1 in theelectronic supplementary material.
Statistical analyses
Body mass, migration distance and radiation level were
log10-transformed and coverage with agricultural land,herbs, shrub and trees, deciduous forest, coniferous forestand cloud cover were square-root arcsine-transformed before analyses.
We quantified the relationship between abundance ofdifferent species and level of radiation by estimating the
Kendall rank-order correlation for the relationship between
abundance and log10-transformed radiation while including
all potentially confounding variables in the statisticalmodels (coverage by herbs, shrub, trees, agricultural
habitat, deciduous forest and coniferous forest, altitude,
cloud cover, temperature, wind force, time of day and timeof day squared). We used non-parametric rank order correlations because the assumptions of parametric analyses
were violated. We have previously shown that statisticalcontrol for the confounding variables listed above did notaffect the conclusions of analyses (Møller and Mousseau
2011a). Therefore, we used the Kendall rank-order correlations from analyses of abundance in relation to radiation
rather than partial rank-order correlations in the subsequent
analysis. In this model, we included slope as the response
variable and body mass, diet, migration distance and area
and the two-way interactions between body mass, diet,migration distance and area as predictors. We did not include other interactions because there were no a priori
predictions.
It is a common underlying assumption of most statisticalanalyses that each data point provides equally precise information about the deterministic part of total process
variation, i.e. the standard deviation of the error term isconstant over all values of the predictor variable(s) (Sokal
and Rohlf 1995). Because estimates of slopes depend on
sample sizes, and because sample sizes vary considerably
among bird species, such variation can have serious consequences for conclusions (Garamszegi and Møller 2010,2011). The standard solution to this problem is to weight
each observation by sampling effort in order to use all data
relative to their importance, by giving each datum a weightthat reflects its degree of precision due to sampling effort(Draper and Smith 1981; Neter et al. 1996; Garamszegi and
Møller 2010). Therefore, we weighted the statistical modelby sample size. All analyses were made with JMP (SAS2012).

Results
We investigated the impact of low-dose radiation on theabundance of 154 species of birds using 2,398 standardized
point counts, which resulted in records of 15,811 individual
birds. A total of 14 species are common to Chernobyl and
Fukushima allowing for comparison of the effect of radiation on abundance of the same species in two different
environments (Møller et al. 2012a). The three species

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showing the strongest negative correlated with level ofbackground radiation level at Chernobyl were Yellowhammer Emberiza citrinella, Chaffinch Fringilla coelebs and Blackcap Sylvia atricapilla. At Fukushima they
were Tree Sparrow Passer montanus, Carrion Crow Corvus
corone and Barn Swallow Hirundo rustica. The mean
Kendall rank-order correlation between abundance andradiation was -0.109 (SE = 0.012), n = 154 species,differing significantly from the expected value zero in theabsence of any effect of radiation (t = 9.18, df = 153,
P \ 0.0001). The mean correlation was -0.047 (0.008) at
Chernobyl, but almost three-fold stronger at -0.150(SE = 0.022) at Fukushima, with both the mean and thevariance being significantly larger at Fukushima than at
Chernobyl (Welch ANOVA: F = 19.04, df = 1, 11,735,
P \ 0.0001; Levene’s test, F = 21.73, df = 1, 152,
P \ 0.0001).
The statistical model explaining variation in the correlations between abundance and background radiation fordifferent species accounted for 64 % of the variance(Table 1). Five out of seven main effects were significant
as were five out of six interaction effects between area andecological variables (Table 1). The correlations between
abundance and radiation level were more negative in species with smaller body mass, and this effect differed significantly between Chernobyl and Fukushima as shown by
the significant interaction (Fig. 2; Table 1). Carnivorous
species showed more strongly negative correlations thanherbivorous species and this effect differed between areas
with a larger difference at Fukushima than at Chernobyl(Fig. 3; Table 1). Migration distance did not show a significant main effect, but the migration effect differed be-

Table 1 Model of slope of therelationship between abundance
and level of backgroundradiation in relation to bodymass (g), diet (0—hervivory,
1—carnivory), migration
distance (8 latitude), carotenoid
score, eumelanin score,pheomelanin score, area
(Chernobyl, Fukushima), area 9
body mass, area 9 diet, area 9
migration distance, area 9
carotenoids, area 9 eumelanin,
area 9 pheomelanin in a model
weighted by sample size

The model had the statistics
F = 22.16, df = 13, 140,
r2 = 0.64, P \ 0.0001

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SourceFig. 2 Slope of the relationship between abundance and backgroundradiation in relation to body mass (g) in different species of birds

Fig. 3 Slope of the relationship between abundance and backgroundradiation in relation to diet in different species of birds

df

Sum of squares

F

P

Estimate

Error
0.050

\0.0001-0.267

Body mass1

17.33021.85\0.0001

0.099

0.021

Diet

1

10.30310.30

0.0004-0.045

0.012
0.014

Intercept

Migration distance

1

0.237

0.30

0.59

-0.008Carotenoids

1

10.82113.65

0.0003

0.034

0.009

Eumelanin

1

3.019

3.81

0.053

-0.0160.008

Pheomelanin

1

0.201

0.25

0.62

0.004

0.007

Area

1

22.62022.62\0.0001

0.073

0.014

Area 9 body mass1

10.36113.07

0.0004-0.076

0.021

Area 9 diet1

15.95920.12\0.0001

0.056

0.012

Area 9 migration distance1

12.14815.31\0.0001

0.055

0.014

Area 9 carotenoids

1

25.77132.50\0.0001-0.052

0.009

Area 9 eumelanin

1

0.302

0.38

0.54

-0.0160.008

122.58328.48\0.0001-0.0380.007

153

111.023

Area 9 pheomelanin
Error

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tween Chernobyl and Fukushima with a stronger negative
effect in migrants at Chernobyl, and a stronger negative
effect in residents at Fukushima (Fig. 4; Table 1).
Plumage color pigments showed different relationships
with impact of radiation on abundance. Species with carotenoid-based coloration showed a weaker negative effectthan species without carotenoid-based coloration (Table 1).
The interaction between carotenoids and area was significant with a stronger negative effect in species with than
without carotenoid-based plumage at Chernobyl, and aweaker negative effect in species with than without suchplumage at Fukushima (Fig. 5a). There was only a weakand non-significant main effect of eumelanin and no significant effect of the interaction (Fig. 5b; Table 1). There
was no significant main effect of pheomelanin (Table 1). A
strong interaction between pheomelanin and area implies
that at Chernobyl species with pheomelanin-based coloration experienced stronger negative effects of radiation
than species without such coloration, while at Fukushimaspecies with pheomelanin showed weaker negative effects
than species without pheomelanin in their plumage(Fig. 5c).

Body size is an important correlate of life history,
physiology and ecology (Bennett and Owens 2002). Small
species eat disproportionately more for their body size thanlarge species due to their surface to volume ratio. Therefore, we should expect small species to ingest disproportionately more radionuclides than large species. Among
bird species at Fukushima, there was a stronger negative
relationship between abundance and radiation in smallbodied species than among large species, and a similar

Discussion
The main findings of this extensive study of breeding birds
at Chernobyl and Fukushima were a negative impact ofionizing radiation on abundance and a number of ecological characteristics explaining variation in heterogeneityof this effect. We found significant main effects of bodymass, diet, migration and feather pigments on the impact ofradiation on abundance. Importantly, there were significant
interactions between area and ecological characteristics,
implying that the effects of radiation were not the same at
Chernobyl and Fukushima. We will briefly discuss thesefindings.

Fig. 4 Slope of the relationship between abundance and backgroundradiation in relation to migration in different species of birds

Fig. 5 Slope of the relationship between abundance and backgroundradiation in relation to plumage color based on a carotenoids,b eumelanin and c pheomelanin in different species of birds

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relationship was found at Chernobyl with a significant interaction between radiation and area. Higher metabolism
and higher rates of ingestion by small species should also
result in greater production of free radicals and hence
greater competition for anti-oxidants between use formetabolism and use due to radiation exposure.
Diet and its interaction with study area was a significant
predictor of impact of radiation on abundance. We predicted and found an effect of bioaccumulation of radionuclides in the food web (Voitovich and Afonin 2002;
Yakushev et al. 1999). Animals at higher trophic levels
generally have higher levels of radionuclide concentrations
than animals at lower levels (e.g., Kryshev and Ryabov
1990; Kryshev et al. 1992; Smith et al. 2002). Here, we
found a stronger negative effect in secondary consumers
compared to herbivores, and the interaction between dietand area was statistically significant, with a stronger effectat Fukushima compared to Chernobyl.
Long-distance migration involves high metabolic effort
and extensive use of antioxidants. Møller and Mousseau(2007b) have previously reported for birds from Chernobyl
that species with longer migrations had a lower abundanceat high radiation levels. Here, we were unable to document
a significant main effect of migration on the impact ofradiation on abundance. However, we did show a stronger
negative impact of radiation on migrants at Chernobyl, but
on residents at Fukushima. The Japanese and the European
avifaunas differ in their migration distance because morethan twice as many species of birds at Fukushima wereresidents (54 % of 57 species) as the species at Chernobyl(21 % of 97 species). Furthermore, Western Palearctic
species migrate longer distances and cross more inhospitable deserts than Eastern Palearctic migrants, while Japanese migrants have the possibility to stop at any of themany archipelagos during migration. Thus, it appears that
it is whether or not a species is migrating rather than theactual migration distance that is the important predictor of
the effects of radiation on abundance.
The slope of the relationship between abundance andradiation was significantly related to whether plumage
color was based on carotenoids and pheomelanin. At
Fukushima, species without carotenoids in their plumage
had lower abundance at high radiation levels, while thatwas not the case for species with carotenoid-based plumage
color. We have previously reported for Chernobyl thatspecies with carotenoid-based plumage are more strongly
negatively impacted (Møller and Mousseau 2007b), as wereport here. The slope of the relationship between abundance and background radiation differed between species
with and without plumage containing carotenoids andphaeomelanin, but not eumelanin, as we a priori had predicted. The two former kinds of pigment-based coloration
impose a trade-off between antioxidant use for123

maintenance caused by radiation and use of antioxidant
pigments allocated to plumage (Møller and Mousseau
2007b; Galván et al. 2011). Interestingly, these effects
differed between Fukushima and Chernobyl for carotenoidand phaeomelanin-based coloration, but not for eumelanincoloration. The main difference between Fukushima andChernobyl is the duration of chronic exposure to radiation(3 vs. 28 years), the duration of accumulation of deleterious mutations (Møller and Mousseau 2011b) and differences in composition of radionuclides (cesium at
Fukushima and strontium, cesium and plutonium at Chernobyl). Galván et al. (2014) have previously suggested andprovided evidence for pheomelanin playing an active role
in resistance to radiation.
We have previously investigated the importance ofsimilarity in effect of ionizing radiation on abundance due
to common phylogenetic descent, showing that conclusions
are independent of phylogeny (Møller and Mousseau
2007b; Galván et al. 2011, 2014). Hence, this justifies theabsence of phylogenetic analyses in the present study.
There may be many causes for differences in population
trends of birds. Here, we have attempted to control statistically for a number of such factors. We have previously
shown that a habitat preference for human proximity andother factors did not account for differences in population
trends among species (Møller et al. 2012a, b).
In conclusion, we have provided extensive informationon the impact of radiation on the abundance of breeding
birds at Chernobyl and Fukushima, and the ecologicalcharacteristics associated with such impacts generally
confirmed findings from previous studies at Chernobyl,
although most characteristics showed significant differences between Chernobyl and Fukushima. This level of
replication suggests that birds may constitute a usefulmodel system for investigating the impact of radiation andthe evolution of radiation-resistance in vertebrates.
Acknowledgments We gratefully acknowledge logistic support andhelp by Professor A. Hagiwara, T. Kanagawa, K. Kawai, Professor K.
Kawatsu and A.M. Smith in Japan. We are especially grateful toNamie-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, theUniversity 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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