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

Abstract

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.

Full text

1 23
Journal of Ornithology
ISSN 2193-7192
J Ornithol
DOI 10.1007/s10336-015-1197-2
Cumulative effects of radioactivity from
Fukushima on the abundance and
biodiversity of birds
A.P.Møller, I.Nishiumi &
T.A.Mousseau

1 23
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REVIEW
Cumulative effects of radioactivity from Fukushima
on the abundance and biodiversity of birds
A. P. Møller
1
•I. Nishiumi
2
•T. A. Mousseau
3,4
Received: 18 October 2014 / Revised: 3 March 2015 / Accepted: 3 March 2015
ÓDt. Ornithologen-Gesellschaft e.V. 2015
Abstract Species differ in their susceptibility to ra-
diation because of differences in their ability to sustain
toxic and genetic effects caused by radiation. We cen-
sused breeding birds in Fukushima Prefecture, Japan,
during 2011-2014 to test whether the abundance and di-
versity of birds became increasingly negatively affected
by radiation over time. The abundance of birds decreased
with increasing levels of background radiation, with sig-
nificant 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.
Keywords Birds Chernobyl Fukushima Radiation
resistance
Introduction
Radiation has been demonstrated to have diverse nega-
tive effects on animals and plants under natural condi-
tions (Møller and Mousseau 2011b). There are highly
radiation-resistant bacteria and fungi that are able to
cope with extreme natural levels of radiation (Dada-
chova et al. 2004;Daly2009), but such organisms seem
to be exceptions rather than the rule. While natural
levels of radiation vary worldwide with significant ef-
fects on the incidence of disease in humans (e.g., Lubin
and Boice 1997;Hendryetal.2009), and by implication
also on other organisms (Møller and Mousseau 2011b),
there are significant radiation effects involving DNA
damage and mutations (e.g., Ghiassi-Nejad et al. 2004),
following the original observation that radiation is a
powerful mutagen (Nadson and Philippov 1925). Re-
cently, interest in the effects of low-dose radiation on
public health but also on free-living organisms has been
increasing following the nuclear accidents at Chernobyl
and Fukushima.
Acute exposure to radiation has negative effects on a
number of physiological processes such as oxidative stress
and immune function, while chronic exposure across ex-
tended periods of time can result in severe accumulations
Communicated by E. Matthysen.
Electronic supplementary material The online version of this
article (doi:10.1007/s10336-015-1197-2) contains supplementary
material, which is available to authorized users.
&A. P. Møller
anders.moller@u-psud.fr
I. Nishiumi
nishiumi@kahaku.go.jp
T. A. Mousseau
mousseau@sc.edu
1
Laboratoire d’Ecologie, Syste
´matique et Evolution, CNRS
UMR 8079, Universite
´Paris-Sud, Ba
ˆtiment 362,
91405 Orsay Cedex, France
2
Department of Zoology, National Museum of Nature and
Science, 3-23-1 Haykunin-cho, Shinjuku-ku,
Tokyo 169-0073, Japan
3
Department of Biological Sciences, University of South
Carolina, Columbia, SC 29208, USA
4
Department of Environmental Biology, Biosciences, and
Biotechnology, Chubu University, Kasugai, Aichi 487-8501,
Japan
123
J Ornithol
DOI 10.1007/s10336-015-1197-2
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of effects of mutations during the lifespan of individuals,
but also across generations. Current studies, generally
conducted under laboratory conditions, typically rely on
acute exposure, while the chronic effects of extended ex-
posure are rarely considered. We previously showed that
the abundance and diversity of birds and other organisms at
Chernobyl were more strongly negatively impacted by a
given level of radiation than those affected by similar
levels of exposure at Fukushima (Møller et al. 2012). Thus,
the difference in the actual levels of radiation in Chernobyl
and Fukushima is not the cause since the effects were
quantified as effects per unit of background radiation.
Some studies suggested that the negative impact of ra-
diation may become ameliorated over time because of
adaptation in terms of improved DNA repair (Boubriak
et al. 2008). The stronger negative effects at Chernobyl
than at Fukushima that we previously documented (Møller
et al. 2012) may be associated with a longer history of
exposure, although alternative explanations such as dif-
ferences in radionuclides and their toxicity may also play a
role.
Here we report the results of analyses of unique data on
the abundance of breeding birds in Fukushima, Japan, in
relation to the background level of radiation during the
2011–2014 period. This period covers the radiation effects
just after the Fukushima accident, but also the subsequent
chronic effects accumulated during the following 3 years.
This is the first study quantifying such cumulative temporal
effects of radiation over time.
The objectives of this study were to test (1) whether
the effect of radiation reduced the abundance and species
richness of birds, (2) whether this effect differed among
species, and (3) whether such negative effects of ra-
diation accumulated over time. Ionizing radiation at
Chernobyl and Fukushima had negative effects on the
abundance and species richness of birds and other or-
ganisms (Møller and Mousseau 2007a,b;Mølleretal.
2011a,b,2012). Such effects vary considerably among
species because of differences in the physiology and
ecology (Møller and Mousseau 2007b;Galva
´netal.
2011,2014). Unfortunately, there are no population
studies or studies of a broad range of species dating back
to the period prior to the accidents at Chernobyl in 1986
or Fukushima in 2011. We conducted the first stan-
dardized counts of breeding birds in 2006 in Chernobyl,
20 years after the accident. We started bird counts in
Fukushima already in 2011, allowing for tests of effects
of ionizing radiation directly from the start of radiation
exposure. Here we present analyses of these unique data
on the effects of radiation since 2011 at Fukushima in an
attempt to determine whether such negative effects of
radiation on the abundance and diversity of birds accu-
mulate over time.
Methods
Study sites
We conducted breeding bird censuses at a total of 400
sampling points (in 2011 only 300 points) in forested areas
around the Fukushima Daiichi power plants in 2011–2014,
totaling 1,500 sampling events (Fig. 1). At least one local
ornithologist (Satoe Kasahara, Shin Matsui, Isao Nishiumi
or Keisuke Ueda) participated in approximately a quarter
of the censuses in Japan to confirm the identity of some
difficult bird species. However, all analyses presented here
were based on the data recorded by APM. All sampling
sites were localized using GPS coordinates, and altitude
was estimated to the nearest foot using a GPS.
Census methods
The point count census method provides reliable informa-
tion on the relative abundance of birds (Blondel et al. 1970;
Møller 1983; Bibby et al. 2005; Vor
ˇı
´s
ˇek et al. 2010). This
method has provided highly repeatable results for birds 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. Each census point was
separated from the previous point by a minimum distance of
100 m. In Fukushima APM with the help of IN conducted
these standard point counts on 11–15 July 2011, 14–19 July
2012, 14–19 July 2013 and 11–16 July 2014. The fact that
one person made all counts analyzed here eliminates any
variance in results due to interobserver variability.
Fig. 1 Location of census areas around Fukushima, Japan, indicated
by lines of dark blue dots in relation to the background radiation
level. Circles show distances of 5 and 50 km from the reactors.
Radiation level increases from the lowest level for light blue to the
highest level for the darkest shade of red. Adapted from http://www.
nnistar.com/gmap/fukushima, generated by the Japanese Ministry of
Education, Culture, Sports, Science and Technology (MEXT) and
local government (color figure online)
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We directly tested the reliability of our counts by letting
two persons independently perform counts, and the degree
of consistency was high for both species richness and
abundance (details reported by Møller and Mousseau
2007a). The Pearson product-moment correlation between
species richness in two series of counts conducted by two
different persons was r=0.99, t=42.06, df =8,
P\0.0001, and for abundance it was equally high at
r=0.99, t=12.47, df =8, P\0.0001.
Abundance estimates can be affected by numerous
confounding variables (Vor
ˇı
´s
ˇek et al. 2010); therefore, it is
important to control such variables statistically to assess
the underlying relationship between radiation and species
richness and abundance. We classified habitats in the field
directly at the census points immediately following the
5-min count [agricultural habitats with grassland or shrubs
(either currently or previously cultivated), deciduous forest
or coniferous forest] and estimated to the nearest 10 %
ground coverage by herbs, shrubs, trees, agricultural
habitat, deciduous forest and coniferous forest within a
distance of 50 m from the census points. Weather condi-
tions can affect animal activity and hence census results
(Vor
ˇı
´s
ˇek et al. 2010), and we recorded cloud cover at the
start of each point count (to the nearest eighth), tem-
perature (degrees Celsius) and wind force (Beaufort). For
each census point, we recorded the time of day when the
count was started (to the nearest minute). Our bird counts
were concentrated in the morning with counts extending
across the entire day depending on other research activities.
Because bird activity may show a curvilinear relationship
with time of day, for example, with high levels of activity
in the morning and to a lesser extent in the evening for
birds (Vor
ˇı
´s
ˇek et al. 2010), we also included time squared
as an explanatory variable in the statistical analyses.
Background radiation
Radiation measurements at Fukushima were obtained using
the same dosimeters (model: Inspector, SE International,
Inc., Summertown, TN, USA) cross-validated with read-
ings from a dosimeter that had been calibrated and certified
to be accurate by the factory during the weeks preceding
the study (International Medcom, Sebastopol, CA, USA).
All radiation measurements were made at the census points
immediately after each bird count. We also made a cross-
validation test by comparing our own measurements using
the Inspector dosimeter with measurements obtained at the
same locations with a TCS 171-ALOKA used by Japanese
authorities. There was a very strong positive relationship
[linear regression on log-log transformed data:
F=2427.97, df =1, 20, r
2
=0.99, P\0.0001, slope
(SE) =1.120 (0.023)]. All data are reported in Electronic
Supplementary Material Table S1.
Diet
We scored the species as herbivores if they mainly fed on
foliage or seeds, primary consumers if they mainly fed on
insects, spiders and other invertebrates, and as top con-
sumers if they mainly fed on vertebrates, relying on in-
formation presented in del Hoyo et al. (1992–2011).
Statistical analyses
Radiation levels were log
10
transformed, and coverage with
agricultural land, herbs, shrubs and trees, deciduous forest,
coniferous forest and cloud cover was square-root arcsine
transformed before analyses.
We quantified the relationship between the abundance of
different bird species and level of radiation by estimating
the slope of the relationship between abundance and log
10
-
transformed radiation while including potentially con-
founding variables in the statistical models (coverage by
herbs, shrubs, trees, agricultural habitat, deciduous forest
and coniferous forest, altitude, cloud cover, temperature,
wind force, time of day and time of day squared). The
resulting species-specific partial slopes for bird abundance
with radiation were used for subsequent analyses. This
approach is extremely conservative because it reduces the
total counts of the entire study to a single estimate per
species or in some analyses a single estimate per species
and year. We quantified species richness as the total
number of species recorded at a given observation point
under the assumption that such estimates would be dis-
tributed randomly across radiation levels if there were no
negative effects of radiation on species richness.
A common underlying assumption of most statistical
analyses is 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 is
constant 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 species, this can have serious consequences for
conclusions (Garamszegi and Møller 2010,2011). The
standard solution to violations of this assumption is to weigh
each observation by sampling effort in order to use all data,
by giving each datum a weight that reflects its degree of
precision due to sampling effort (Draper and Smith 1981;
Neter et al. 1996; Garamszegi and Møller 2010). Therefore,
we weighted statistical models by sample size in order to use
all data in relation to the precision of the estimates. Even a
single observation of a species was included in the analyses
because such an observation could theoretically be recorded
at any of the observation points with a single point having an
observation of 1 and all other points an observation of 0. The
null hypothesis is that the slope in this case will be zero,
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while non-random locations of observations will be con-
centrated at low radiation levels if radiation has a negative
effect on the presence and the abundance of birds.
We tested whether the abundance of species was related
to the level of radiation, species and the interaction be-
tween radiation and species. Next we tested whether there
was a temporal trend in slope of the relationship between
abundance and background radiation under the prediction
that the extent of negative effects would accumulate across
years. Finally, we tested whether the slope of the rela-
tionship between abundance and radiation differed among
categories of main diet: herbivory or carnivory, or herbi-
vores, primary consumers or top consumers. All standard
least squares analyses or in case of data that were not
normally distributed non-parametric tests were made with
JMP (SAS 2012).
Results
Tests for interspecific differences in the effect
of radiation on abundance
The number of individual birds of the 57 different species
recorded at Fukushima ranged from 1 to 1,715, mean
(SE) =166.7 (48.6), median =22 individuals.
There was a significant decline in the level of back-
ground radiation across years (Fig. 2;F=1736.70,
df =3, 1097, P\0.0001) with additional variation among
census points (F=43.53, df =399, 1097, P\0.0001).
The abundance of birds at Fukushima differed sig-
nificantly among species, decreasing with increasing levels
of background radiation, and this decrease differed among
species as reflected by the significant species by radiation
interaction (Table 1). There was a strong negative rela-
tionship between species richness and radiation level
across the census points (Fig. 3A; F=6.73, df =1, 1495,
P\0.0001), and there was an equally strong negative
relationship between the total number of individuals and
radiation level across the census points (Fig. 3b;
F=18.11, df =1, 1495, P\0.0001).
The slope of the relationship between abundance and
background radiation for 57 different species of birds
ranged from -0.525 to ?0.107, mean (SE) =-0.162
(0.023) (Table 2). The mean slope differed significantly
from zero in an analysis weighted by sample size (one-
sample t-test, t=-7.16, df =56, P\0.0001). This im-
plies that species were on average less abundant at high
levels of radiation.
Differences in slopes among years
Correlation coefficients between abundance and radiation
differed among years in an analysis weighted by sample
size (Fig. 4;F=5.25, df =3, 107, r
2
=0.05, P=
0.0020) in a model that accounted for species (F=73.17,
df =56, 107, P\0.0001).
We compared the slope of the relationship between
abundance and radiation for the same species in different
years under the assumption that the relationship for slopes
of different species in subsequent years should be positive
with a slope of one. Any deviation from this null expec-
tation would imply that factors other than statistical de-
pendence were involved. There was a significant change in
slope across years with 57 species for which there were
data for at least 3 years (Kendall s=-0.192, SE =0.074,
P=0.012). While the relationship between abundance and
background radiation on average was weakly negative in
2011, it became on average more strongly negative in 2012
(Fig. 5a), and on average it became even more strongly
negative in 2013 compared to 2012 (Fig. 5b). Please note
that the relationship between abundance and radiation for
the different species in 2011 was positively related to the
relationship for different species in 2012, and the rela-
tionship between abundance and radiation for different
species in 2012 was positively related to the relationship
for different species in 2013. Thus, species tended to be-
come more negatively affected by radiation over time. In
contrast, there was no evidence that the relationship
between abundance and background radiation changed
with sample size in the species for which there were data
for at least 3 years (Kendall s=-0.060, SE =0.098,
P=0.542).
There was a significant difference in slope between
species with a herbivorous and a carnivorous diet (F=
Fig. 2 Box plots of background radiation (lSv/h) at census points
during the years 2011–2014. The box plots show median, quartiles,
5th and 95th percentiles and extreme observations
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25.20, df =1, 55, r
2
=0.30, P\0.0001). Surprisingly
herbivorous species had a more strongly negative slope
(-0.32 (SE =0.04), N=10) than carnivorous species
(-0.10 (0.02), N=47). There was also a significant
positive association between the slope of the relationship
between abundance and radiation and trophic level
(F=12.52, df =2, 54, r
2
=0.29, P\0.0001). The
mean slope was the steepest for primary consumers [-0.32
(SE =0.04, N=10) over low level predators (-0.10
(0.02), N=38) to top predators (-0.04 (0.13), N=9)].
Discussion
The main results of this study of radiation and species
richness and abundance of birds at Fukushima, Japan,
during 2011–2014 were that (1) overall abundance and
diversity of species on average decreased with increasing
levels of background radiation, (2) the relationship differed
among species, with most species decreasing, but some
species increasing in abundance with increasing levels of
radiation, and (3) the relationship became more strongly
negative across years, while there was no effect of change
in abundance.
The overall negative relationship between abundance
and level of background radiation differed among species.
This result parallels previous findings from Chernobyl
(Møller and Mousseau 2007a). We conducted our censuses
under the assumption that there would be no significant
difference in abundance because radiation should be dis-
tributed randomly across habitats that were censused.
Therefore, we should expect the effect of radiation to re-
main after controlling statistically for the confounding ef-
fects of habitat, weather and time of day. We suggest that
the difference in the effect of radiation on abundance be-
tween Fukushima and Chernobyl could be ascribed to
differences in duration of exposure to radiation with (1)
mutations accumulating for longer time in Chernobyl and
(2) selection due to radiation not having acted for equally
long time in the two areas.
We had expected an effect of bioaccumulation of ra-
dionuclides in the food web because bioaccumulation is
common (Voitovich and Afonin 2002; Yakushev et al.
1999) and 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). However, the evidence
suggested an opposite effect, with more strongly negative
effects of radiation on abundance at low trophic levels. Our
findings are therefore possibly more consistent with the
hypothesis that oxidative stress in contaminated areas and
reduced antioxidant levels (Møller et al. 2005) are a con-
sequence of chronic radiation exposure (Møller and
Mousseau 2007b), with negative effects on reproduction
and survival and ultimately population trends.
Fig. 3 a Number of bird species and bnumber of bird individuals at
census points in relation to background radiation (lSv/h). The lines
are the linear regression lines
Table 1 Abundance of
different species of birds in
relation to radiation level in
Fukushima
Sum of squares df F P Estimate (SE)
Radiation (R) 0.123 1 12.39 0.0004 -0.0063 (0.0018)
Species (S) 45.583 44 103.75 0.0001
R9S 3.587 44 8.16 \0.0001
Error 133.902 13410
The overall model had the statistics F
89,13410
=55.47, r
2
=0.27, P\0.0001
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This study has implications for the assessment of bio-
logical effects of ionizing radiation on free-living organ-
isms. We have shown that the negative impact of radiation
on abundance and species richness changes over time, and
this effect varies among species. If we had not conducted
the first breeding bird census in 2011 immediately after the
Fukushima accident, we would not have been able to
document a temporal change in abundance as we have
reported here. Although bird species on average declined in
abundance with increasing background radiation, there
were several species that clearly increased in abundance.
The reason for such changes can be changes in land use or
release from competition due to reductions in the abun-
dance of other species. The patterns of change in
Fig. 4 Box plots of the correlation coefficients between abundance
and background radiation during the years 2011–2014. The box plots
show median, quartiles, 5th and 95th percentiles and extreme
observations
Table 2 Slope of the relationship between abundance and level of
radiation after controlling statistically for potentially confounding
variables (see ‘‘Methods’’) based on observations from 1,500 census
points, level of significance of this relationship and the number of
individuals that were censused for different species of birds
Species Slope PNo. individuals
Accipiter gentilis 0.0004 0.8295 3
Acrocephalus arundinaceus -0.1579 \0.0001 180
Aegithalos caudatus 0.0470 0.2411 54
Alauda arvensis 0.0020 0.4439 5
Alcedo atthis 0.0008 0.4939 1
Anas poecilorhyncha -0.0018 0.6089 8
Apus affinis -0.0067 0.2466 6
Ardea cinerea -0.0129 0.0316 22
Bambusicola thoracica 0.0022 0.1675 2
Butastur indicus 0.0054 0.2859 14
Buteo buteo -0.0812 \0.0001 99
Carduelis sinica -0.0681 0.2086 238
Cettia diphone -0.1798 \0.0001 1715
Cinclus pallasii 0.0030 0.4338 5
Cisticola juncidis 0.0023 0.1475 2
Corvus corone -0.3069 \0.0001 559
Corvus macrorhynchos 0.0362 0.2644 446
Cuculus canorus 0.0049 0.1743 10
Cuculus poliocephalus -0.0534 0.0027 284
Cuculus saturatus 0.0019 0.1014 1
Cyanopica cyanus -0.0015 0.7763 13
Cyanoptila cyanomelana 0.0035 0.1278 4
Delichon urbica -0.0056 0.4656 20
Dendrocopos kizuki 0.0137 0.1192 56
Emberiza cioides -0.1896 \0.0001 703
Eophona personata -0.0015 0.2039 1
Falco peregrinus -0.0009 0.4416 1
Falco tinnunculus -0.0002 0.8821 1
Ficedula narcissina 0.0344 \0.0001 53
Garrulax canorus -0.0248 0.0402 94
Garrulus glandarius 0.0139 0.0077 36
Hirundo rustica -0.2201 \0.0001 419
Hypsipetes amaurotis -0.0494 0.2069 1618
Lanius bucephalus -0.0156 0.1086 71
Milvus migrans -0.0011 0.9104 56
Motacilla alba -0.0161 0.0044 19
Motacilla cinerea -0.0640 \0.0001 66
Motacilla grandis -0.0487 \0.0001 44
Parus ater 0.0345 \0.0001 45
Parus major 0.0315 0.0315 137
Parus montanus 0.0037 0.5879 23
Parus varius 0.0072 0.2133 22
Passer montanus -0.5249 \0.0001 1114
Pericrocotus divaricatus -0.0004 0.9180 1
Phalacrocorax carbo 0.0012 0.5993 4
Table 2 continued
Species Slope PNo. individuals
Phasianus colchicus -0.0041 0.5560 7
Phasianus soemmeringii -0.0056 0.0446 6
Picus awokera 0.0047 0.2158 1
Regulus regulus 0.0028 0.1519 3
Streptopelia orientalis 0.1067 \0.0001 155
Sturnus cineraceus -0.0088 0.6979 55
Tarsiger cyanurus -0.0001 0.9510 2
Terpsiphone atrocaudata 0.0036 0.1166 2
Troglodytes troglodytes 0.0008 0.4784 1
Turdus cardis 0.0038 0.0032 8
Urosphena squameiceps -0.0015 0.7906 26
Zosterops japonica 0.0222 0.0831 118
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abundance with radiation level were only weakly species-
specific, and even closely related species such as barn
swallow Hirundo rustica and house martin Delichon ur-
bica, carrion crow Corvus corone and jungle crow Corvus
macrorhynchos, and great tit Parus major and varied tit
Parus varius varied significantly in the impact of radiation
on abundance (Table 2). This makes it unlikely that com-
petitive release is an important factor.
Although there has been great public interest concerning
the ecological, genetic and potential health consequences
of the Fukushima radiological disaster, basic research to
date has been surprisingly limited with only a handful of
studies published since the disaster. A recent study of bull
sperm and testis from the Fukushima region found no
evidence for significant histological changes in the testes or
sperm morphology (Yamashiro et al. 2013), although this
study was very preliminary with only two bulls from a
relatively uncontaminated part of Fukushima represented
for the analysis of sperm. A study of aphids revealed large
effects of radiation on morphology, although aberrant
forms were only reported for one location in an area of
relatively low contamination (Akimoto 2014). Similarly, a
recent study of Japanese macaques found evidence for ra-
diation effects on various characteristics of their blood, but
individuals used in this study were obtained from areas
surrounding Fukushima City where contamination levels,
though measurable, are low relative to other parts of
Fukushima Prefecture (Ochiai et al 2014). Ishida (2013)
reported on surveys of some bird populations living in
more heavily contaminated areas of the region and sug-
gested that there was no evidence of significant declines
resulting from the disaster. However, the number of sites
surveyed was relatively few (56 in May and 38 in June
2012), and the analyses did not control for the many other
potentially confounding factors that influence bird abun-
dance and distribution, making this study very preliminary.
Recent seminal studies of butterflies exposed to radioactive
contaminants associated with the Fukushima disaster found
strong evidence for increased mutation rates, develop-
mental abnormalities and population effects as a direct
consequence of exposure to radionuclides (Hiyama et al.
2012,2013). These studies by Hiyama et al. (2012,2013)
were greatly strengthened by laboratory experiments that
used both internal and external radiation sources, and these
unambiguously supported observations of the elevated
mutation rates and phenotypic effects observed in the field
(Møller and Mousseau 2013), although, as with other
studies, the number of populations studied, and hence the
level of replication of observations, was very limited.
Murase et al. (2015) made an equally compelling case for
radiation having a negative impact on reproductive per-
formance in the decline of Japanese goshawks Accipiter
gentilis fujijamae compared to the pre-accident years, the
progressive decline over time being directly linked to the
air dose rate.
In conclusion, we have shown substantial evidence
based on rigorous and highly replicated observations across
space and time that is consistent with the hypothesis that
the species richness and abundance of different species of
birds were suppressed at high levels of background ra-
diation in Fukushima. The relationship between abundance
and radiation differed significantly among species, with
most species decreasing, but some species increasing in
abundance with increasing levels of radiation. Importantly,
the relationship between abundance and radiation became
more strongly negative over the 4 years studied, while
there was no change in the effect of radiation on abundance
with change in abundance over years.
Acknowledgments We gratefully acknowledge the lo-
gistic support and help in Japan by Prof. A. Hagiwara, Prof.
Fig. 5 Relationship between correlation coefficients for abundance
of different bird species and background radiation (lSv/h) at census
points during (a) 2011 and 2012 and (b) 2012 and 2013
J Ornithol
123
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K. Ueda, Prof. K. Kawatsu, S. Matsui, S. Kasahara, T.
Kanagawa, K. Kawai, H. Suzuki and K. Koyama. We are
especially grateful to the people of Fukushima Prefecture
who permitted us to conduct this study. We thank Dr.
S. Welch for help in preparing the contamination map of
Fukushima Prefecture. We gratefully acknowledge support
from the US National Science Foundation, the University
of South Carolina School of the Environment, the NATO
CLG program, the CRDF, the Fulbright Program, the Na-
tional Geographic Society and the Samuel Freeman
Charitable Trust for Research in Chernobyl, and the
University of South Carolina, the Samuel Freeman
Charitable Trust, Qiagen GmbH, the Chubu University
Science and Technology Center and anonymous gifts from
individual citizens for research in Japan.
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