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Environmental Pollution 164 (2012) 36e39

Contents lists available at SciVerse ScienceDirect

Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Rapid communication

Abundance of birds in Fukushima as judged from Chernobyl
Anders Pape Møller a, *, Atsushi Hagiwara b, Shin Matsui c, Satoe Kasahara c, Kencho Kawatsu d,Isao Nishiumi e, Hiroyuki Suzuki f, Keisuke Ueda c, Timothy A. Mousseau gaLaboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, F-91405 Orsay Cedex, France
Laboratory of Aquaculture Biology, Faculty of Fisheries, Nagasaki University, Nagasaki 852-8521, Japanc
Department of Life Sciences, Rikkyo University, 3-34-1 Nishi-Ikebukuro, Toshima-ku, Tokyo 171-8501, Japand
Graduate School of Symbiotic Systems Science and Technology, Fukushima University, 1 Kanayagawa, Fukushima City 960-1296, Japane
Department of Zoology, National Museum of Nature and Science, 3-23-1 Haykunin-cho, Shinjuku-ku, Tokyo 169-0073, Japanf
Value Frontier Co., Ltd., 4-13-7, Minamiazabu, Minato, Tokyo 106-0047, Japang
Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USAba r t i c l e i n f o

a b s t r a c t

Article history:
Received 6 November 2011
Received in revised form
11 January 2012
Accepted 12 January 2012

The effects of radiation on abundance of common birds in Fukushima can be assessed from the effects ofradiation in Chernobyl. Abundance of birds was negatively related to radiation, with a signiﬁcantdifference between Fukushima and Chernobyl. Analysis of 14 species common to the two areas revealeda negative effect of radiation on abundance, differing between areas and species. The relationshipbetween abundance and radiation was more strongly negative in Fukushima than in Chernobyl for thesame 14 species, demonstrating a negative consequence of radiation for birds immediately after theaccident on 11 March 2011 during the main breeding season in MarcheJuly, when individuals work close
to their maximum sustainable level.
Ó 2012 Elsevier Ltd. All rights reserved.

Keywords:
Birds
Chronic radiation
Population trends
Radiation

1. Introduction
Animal abundances provide reliable early warning signals of the
impact of environmental perturbations on biological systems(e.g. Vorísek et al., 2010). For example, a wide range of animals
show reduced abundance in areas with high background radiationnear Chernobyl (Møller and Mousseau, 2011a; Mousseau andMøller, 2011), allowing us to use the relationship between abundance and radiation in Chernobyl as a yardstick for assessing themagnitude of other nuclear accidents such as that at the
Fukushima-Daiichi Nuclear Power Plant on 11 March 2011. The
nuclear accidents at both Chernobyl and Fukushima contaminatedlarge areas in the neighborhood of the reactors (Fig. 1), but also
many neighboring countries. While the magnitude of the nuclear
disaster has been assessed as seven on the ofﬁcial IAEA INES scale(on par with Chernobyl (http://www.iaea.org/Publications/
Factsheets/English/ines.pdf)), the biological magnitude of nuclear
disasters has so far eluded assessment.
Previous studies of the effects of low-dose radiation on animals
and plants have been extremely limited, and when it comes to* Corresponding author.
E-mail address: anders.moller@u-psud.fr (A.P. Møller).
0269-7491/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.envpol.2012.01.008

extensive surveys that use standardized, widely approved census
methods to relate abundance of free-living organisms to the level ofbackground radiation, there are only a handful of such studies
available (Krivolutsky and Pokarshevsky, 1992; Maksimova, 2002;
Møller and Mousseau, 2006, 2007; Galván et al., 2011). Thesestudies consistently show negative relationships between abundance and radiation, even when statistically controlling for potentially confounding habitat factors and other variables. The results
are repeatable among observers (Møller and Mousseau, 2011a),they are repeatable among areas (Ukraine vs. Belarus) (Møller andMousseau, 2011a), and they are repeatable among years (Møller
and Mousseau, 2011a), showing that similarly negative effects canbe demonstrated using stringent methodology. The nuclear accident at Fukushima-Daiichi provides a novel opportunity to assesspreviously reported effects by increasing the level of replication,
which is a hallmark of scientiﬁc enquiry. Obviously, Chernobyl and
Fukushima differ in terms of environmental conditions, the amountand composition of radionuclides, prevailing weather and timesince the nuclear accident. However, vast amounts of radioactivity
remain in areas surrounding Chernobyl, due to the long half-lives of
plutonium, cesium and strontium, making a comparison of theeffects of a given level of radiation on abundance of any group oforganisms possible and justiﬁable. Furthermore, the two disasterzones show similarities by both being heavily contaminated, both

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A.P. Møller et al. / Environmental Pollution 164 (2012) 36e39

37(iii) species would show species-speciﬁc responses that differed
between areas. We tested these predictions by conducting extensive breeding bird censuses in Chernobyl during four years
2006e2009 and in Fukushima in 2011, using exactly the same
methods, procedures and individuals to conduct the censuses. In
addition, we compare the response of the same 14 species thatco-occur in both areas to radiation, allowing for stringent tests thatwould be independent of differences in ecology and evolutionary
history.
2. Material and methods
Breeding bird censuses were conducted within the Chernobyl Exclusion Zone
or adjacent areas on the southern and western borders with a permit from the
Ukrainian authorities and in areas in southern Belarus around Gomel during thebreeding seasons 2006e2009 (Fig. 1A). We conduced similar censuses at a total of
300 sampling points in forested areas west of the exclusion zone around the
Fukushima Daiichi power plants in 2011 (Fig. 1B). Information on census
methods, confounding variables, repeatability of density estimates, radiation
measurements and statistical analyses are reported in Electronic Supplementary
Material 1.

3. Results and discussion

Fig. 1. Location of bird census areas around (A) Chernobyl, Ukraine and Belarus (bluedots) and (B) Fukushima, Japan (black dots). (A) was adapted from Shestopalov (1996)
and (B) from http://www.nnistar.com/gmap/fukushima, generated by the Japanese
Ministry of Education, Culture, Sports, Science and Technology (MEXT) and local
government. (For interpretation of the references to color in this ﬁgure legend, thereader is referred to the web version of this article.)being composed of farmland and forests, and both being located intemperate climates in the same zoogeographic region. If there weresimilar negative relationships between abundance and a given levelof background radiation in the vicinity of Chernobyl and Fukushima, we could conclude that the underlying factor responsible forthese effects was most likely the same. Chernobyl and Fukushima
are both located in the Palearctic zoogeographic region, implyingthat numerous taxa occur in both areas despite the areas being
separated by a distance of more than 7000 km. We explicitly
exploited that situation by investigating the response of the same
set of species in Chernobyl and Fukushima to low-dose radiation.
Here we assessed the predictions that (i) the effects of radiation
on abundance of birds would be negative; (ii) the effect would bestronger in the area more recently exposed to radiation; and thatRadioactive contamination can negatively affect the abundanceof living beings through the toxic effects of radionuclides or
through effects related to the accumulation of mutations (Møller
and Mousseau, 2006). We related bird abundance to backgroundradiation level after controlling statistically for potentially confounding effects of time of day, weather and habitat on abundanceof birds (Møller and Mousseau, 2011a; Electronic Supplementary
Material 2). Bird abundances showed a signiﬁcant decline withincreasing background radiation both in Chernobyl and Fukushima(F1,1194 ¼ 66.49, P < 0.0001, slope (SE) ¼ 0.092 (0.011)), with nosigniﬁcant effect of study area (Chernobyl or Fukushima:
F1,1194 ¼ 0.43, p ¼ 0.51) or difference in effect of radiation between
areas (interaction between radiation and area: F1,1194 ¼ 1.45,
P ¼ 0.23). This implies that for the same level of radiation we founda similar decline in abundance with increasing level of radiation.
This result implies that differences between the two disaster zones
are much less important than the similarities, most likely caused byradioactive contamination.
Most species had reduced population density at higher levels of
background radiation (Fig. 2), after controlling for potentiallyconfounding variables (Møller and Mousseau, 2011a; Electronic
Supplementary Material 2). The slope describing the relationshipbetween abundance and radiation was on average strongly negative both in Chernobyl (0.063 (SE ¼ 0.007), N ¼ 80 species,
one-sample t-test, t79 ¼ 8.69, P < 0.0001) and in Fukushima(0.040 (SE ¼ 0.008), N ¼ 45 species, one-sample t-test,
t44 ¼ 4.81, P < 0.0001). Thus, the effect of radiation on abundance
was stronger in species breeding in Chernobyl than in Fukushima(F1,123 ¼ 3.80, r2 ¼ 0.03, P ¼ 0.040).
We used extensive and unique data obtained from large-scale
censuses of breeding birds in the vicinity of Chernobyl in Ukraine
and Belarus and in the vicinity of Fukushima in Japan to test for aneffect of radiation on abundance. There was extensive evidence
consistent with the hypothesis that low-dose radiation has significant negative consequences for birds because most species had
suppressed populations in more contaminated areas (Fig. 2).
A direct comparison of these negative effects in the two disasterzones revealed for 80 species in Chernobyl a more strongly negative
effect of radiation on abundance than for the 45 species recorded in
Fukushima. These effects were independent of habitat, weather andtime of day when the censuses were conducted, making it unlikelythat any uncontrolled, additional variables could be the underlying
cause for the negative relationships. Our previous studies in theAuthor's personal copy

38

A.P. Møller et al. / Environmental Pollution 164 (2012) 36e39

Fig. 2. Frequency distribution of the number of bird species with different slopes of
the relationship between abundance and background radiation level, after controlling
statistically for the potentially confounding effects of habitat variables, weather, andtime of day. See Materials and methods for further details. Note that there are many
more negative slopes than would be expected by chance alone, implying that most
species have declines in abundance in more heavily contaminated areas.

vicinity of Chernobyl have also revealed very similar results independent of statistical control for effects of potentially confounding
variables (Møller and Mousseau, 2011a).
To further assess the possible effects of radiation, we analyzed the
14 bird species that were breeding both in Fukushima and Chernobyl, relating their abundance to radiation without the potentiallyconfounding effects of differences in ecology among species anddifferent phylogenetic histories that could have affected the analysesof all species. In these 14 bird species there was a signiﬁcant negative
relationship between abundance and radiation (Table 1), as found forall bird species, and there was also a signiﬁcant difference between
areas, with density being higher in Fukushima than in Chernobyl(Table 1). Species differed signiﬁcantly in abundance (Table 1). The
radiation effect differed between areas, as shown by the interaction
between radiation and area (Table 1). The mean slope of the relationship between abundance and radiation for the 14 species of birds
in Fukushima (0.067 (SE ¼ 0.011)) was more negative than themean slope for the same 14 species in Chernobyl (0.008 (0.001);
paired t-test, t13 ¼ 3.32, P ¼ 0.0055). This difference in effectbetween Fukushima and Chernobyl is unbiased by effects due toecology and common phylogenetic descent and is therefore morereliable than the apparently stronger effect for Chernobyl than for
Fukushima, when analyzing all species (see above). The stronger
negative effect for the same level of background radiation onabundance of exactly the same bird species in Fukushima than in
Chernobyl may be interpreted as being due to (1) selection alreadyhaving eliminated individuals with accumulated mutations inTable 1Abundance of the same 14 species of birds in Chernobyl and Fukushima in relation toradiation level at 1198 census points (898 in Chernobyl and 300 in Fukushima). The
overall model had the statistics F55,16716 ¼ 47.60, r2 ¼ 0.14, P < 0.0001.

Radiation (R)Area (A)Species (S)
RA
RS
AS
RAS
Error

Sum of squares

d.f.

F

P

Estimate (SE)

1.019
0.412
7.102
0.240
1.354
6.846
1.210
124.47

1
1
13
1
13
13
13
16,716136.81
55.29
73.36
32.28
13.99
70.72
12.50

<0.0001<0.0001<0.0001<0.0001<0.0001<0.0001<0.0001

0.011 (0.0014)
0.013 (0.0011)

Chernobyl to a greater extent than in Fukushima; (2) the composition of radionuclides being more dangerous for birds in Fukushima
than in Chernobyl (perhaps an unlikely explanation); or (3) the
higher density in Fukushima than in Chernobyl increasing theintensity of intraspeciﬁc competition and therefore the negative
effects of radiation. The relationship between abundance and radiation also differed signiﬁcantly among species, as shown by theinteraction between radiation and species (Table 1). The difference inabundance between Chernobyl and Fukushima differed among
species, as shown by the signiﬁcant area by species interaction(Table 1). Finally, the different effect of radiation on species was not
the same in the two areas, as shown by the interaction between
radiation, area and species (Table 1).
Although Chernobyl and Fukushima are located more than7000 km apart, they still share a large number of species due to thefact that the two sites are both located in the Palearctic zoogeographic region. We identiﬁed 14 species of birds that were common
to the two sites, allowing us to conduct a particularly stringent test of
the hypothesis that radiation would differ negative impact onabundance even when comparing populations of the same species inthe two areas. Detailed analyses of species common to the twodisaster zones revealed a more strongly negative relationshipbetween abundance and radiation at Fukushima than at Chernobyl,
demonstrating an immediate negative consequence of radiation forbirds during the main breeding season MarcheJuly 2011, when
individual birds are known to work close to their maximum
sustainable level (Drent and Daan, 1980). Previous research at
Chernobyl has shown that bird species with high metabolic rates andhence high rate of use of antioxidants suffer disproportionately fromthe negative effects of radiation on the production of free radicals(Galván et al., 2011; Bonisoli-Alquati et al., 2010b). A reduction in thelevel of free radicals will have consequences for damage to DNA(Bonisoli-Alquati et al., 2010a), the ability to reproduce and survive(Møller et al., 2005), and normal development of neurological tissues(e.g. brains) (Almond et al., 2007; Møller et al., 2011).
In conclusion, the data presented here constitute the ﬁrst
investigation of initial biological community responses to theradioactive fallout from the Fukushima disaster. The parallels andcontrasts with prior results from Chernobyl suggest that organismal responses to radionuclides can be immediate and large. The
prolonged, relatively larger impacts on Chernobyl communities
point to possible sustained, longer term impacts on organisms that
may reﬂect cumulative, multigenerational consequences of mutation accumulation within populations, as suggested by Møller andMousseau (2011a,b). The disaster at Chernobyl, and now Fukushima, provide unique opportunities to assess the risks and hazards ofprolonged exposure to mutagenic contaminants that likely haverelevance for other communities inhabiting the regions affected bythese disasters.
Acknowledgments
We gratefully acknowledge logistic support and help by I. Chizhevsky and G. Milinevski. We also acknowledge support from the US
National Science Foundation, the University of South Carolina Schoolof the Environment, the NATO CLG program, the CNRS, the CRDF, theFulbright Program, the National Geographic Society, and the SamuelFreeman Charitable Trust for research in Chernobyl, and the
University of South Carolina, the CNRS and Qiagen GmbH for researchin Japan.

0.008 (0.0014)

Appendix. Supplementary material
Supplementary material associated with this article can befound, in the online version, at doi:10.1016/j.envpol.2012.01.008.

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A.P. Møller et al. / Environmental Pollution 164 (2012) 36e39

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