Journal of Environmental Radioactivity 169-170 (2017) 159e173

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Journal of Environmental Radioactivity

journal homepage: www.elsevier.com/locate/jenvrad

On the divergences in assessment of environmental impacts

from ionising radiation following the Fukushima accident
P. Strand a, *, S. Sundell-Bergman c, J.E. Brown b, M. Dowdall b
a
CERAD, Norwegian University of Life Sciences, 1430 Ås, Norway
b
Norwegian Radiation Protection Authority, Grini næringspark 13, 1332 Østerås, Norway
c
Department of Soil and Environment, Swedish University of Agricultural Sciences (SLU), Box 7014, 750 07 Uppsala, Sweden

a r t i c l e i n f o a b s t r a c t

Article history: The accident at the Fukushima-Daiichi Nuclear Power Station on March 11, 2011, led to significant
Received 24 October 2016 contamination of the surrounding terrestrial and marine environments. Whilst impacts on human health
Received in revised form remain the primary concern in the aftermath of such an accident, recent years have seen a significant
16 December 2016
body of work conducted on the assessment of the accident’s impacts on both the terrestrial and marine
Accepted 16 December 2016
environment. Such assessments have been undertaken at various levels of biological organisation, for
different species, using different methodologies and coming, in many cases, to divergent conclusions as
to the effects of the accident on the environment. This article provides an overview of the work con-
Keywords:
Environmental radiological assessment
ducted in relation to the environmental impacts of the Fukushima accident, critically comparing and
Fukushima contrasting methodologies and results with a view towards finding reasons for discrepancies, should
they indeed exist. Based on the outcomes of studies conducted to date, it would appear that in order to
avoid the fractured and disparate conclusions drawn in the aftermath of previous accidents, radioactive
contaminants and their effects can no longer simply be viewed in isolation with respect to the ecosys-
tems these effects may impact. A combination of laboratory based and field studies with a focus on
ecosystem functioning and effects could offer the best opportunities for coherence in the interpretation
of the results of studies into the environmental impacts of ionising radiation.
© 2017 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160
2. Theoretical/desk-based assessments by international organisations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161
3. Studies where radiometric data from the field have been used to provide information on environmental exposures . . . . . . . . . . . . . . . . . . . . . . . . . . 162
3.1. Terrestrial . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162
3.2. Freshwater . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163
3.3. Marine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164
4. Direct analyses of biological effects in the field . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164
4.1. Molecular, cellular damage and morphological effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164
4.2. Effects at the population level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165
5. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167
5.1. Are the findings of UNSCEAR and IAEA assessments backed up by empirical study? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167
5.2. Consistency between published ad hoc studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168
5.3. Limitations regarding the various categories of studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168
5.4. Suggestions towards resolving some of the discrepancies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171

* Corresponding author.
E-mail address: per.strand@nrpa.no (P. Strand).

http://dx.doi.org/10.1016/j.jenvrad.2016.12.005
0265-931X/© 2017 Elsevier Ltd. All rights reserved.
160 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
1. Introduction
The accident of March 11, 2011 at the Fukushima-Daiichi Nuclear
Power Station (FDNPS), resulted in atmospheric releases of signif-
icant amounts of radioactive substances leading to the contami-
nation of the surrounding terrestrial (and freshwater) environment
through deposition processes and interception by vegetation. In-
puts of radioactivity to the marine environment also occurred
through (i) atmospheric releases plus deposition to the sea surface
and (ii) runoff of seawater used to cool the reactors during the
accident plus leakage of wastewaters from damaged containment
structures. The major releases primarily took place from 12 to 23
March 2011 i.e. in early spring. According to the International
Atomic Energy Agency, IAEA (2015), atmospheric releases
(excluding uncertain early estimates) of the key radionuclides 137Cs
and 131I amounted to 7e20 PBq and 100e400 PBq respectively. Of
these inventories, somewhere between 0.18 and 10 PBq 137Cs and
60e100 PBq 131I were estimated to have been deposited across the
Pacific Ocean. Direct releases of contaminated water were esti-
mated to have been 1e6 PBq 137Cs (IAEA, 2015), bearing in mind
that larger estimates have been published (e.g. Bailly du Bois et al.,
2012). While a broad range of radioactive isotopes were released,
the releases contained only very low levels of isotopes of strontium
and actinides (owing to the nature of the accident), in contrast to
the Chernobyl accident in 1986 (IAEA, 2015). Furthermore, the at-
mospheric releases were substantially smaller than those associ-
ated with the Chernobyl accident. In this regard, for the earlier
accident, the releases were estimated to have been about 85 PBq
137
Cs and 1.76
103 PBq 131I by the United Nations Scientific
Committee on the Effects of Atomic Radiation (UNSCEAR, 2000).
In the aftermath of the FDNPS accident, the protection of human
health from radiation exposures was of foremost importance, a
radius of 20 km from the site being evacuated on March 12, 2011
due to the risk of high radiation exposures. In contrast, the expo-
sure to radiation of non-human organisms which inhabited the
most affected areas, was inevitable. From the perspective of
communicating the broader implications of the accident and
informing decisions regarding management alternatives, an eval-
uation of the radiological consequences on the environment is
important (see ICRP, 2014). In a general sense, the assessment of
impacts on the environment from ionizing radiation is a subject
that has received increased attention in recent years with initial
focus on developing a system in relation to individual organisms
but with less emphasis on establishing the consequences of expo-
sures to radiation at an ecosystem level. The putative inertia against
addressing ecosystem impacts is plausibly a reflection of the state
of knowledge and the challenges associated with addressing a
complex ecological situation.
Fig. 1. Schematic of what is meant by “effects to individuals” versus “effects to populations” and “effects to ecosystems”. Adapted from Bradshaw et al. (2014).
Great progress has been made over the last two decades in
expanding radiological assessment systems to encompass envi-
ronmental perspectives. Of particular note were the activities of the
International Union of Radioecology, which were key to providing
momentum in moving the subject forward (IUR, 2000; IUR, 2002).
Various internationally supported methods and norms have been
developed (see ICRP, 2008, 2009, 2014) in this period, which allow
environmental exposures to be quantified and contextualised. The
impact on the environment may be manifested at all levels of
organisation but the major societal concern is to protect ecosys-
tems and natural populations with due consideration of those that
have been provided legislative protection on the individual level,
such as species considered as being endangered. However, as sys-
tem relevance increases, from an ecological perspective, there is a
concomitant increase in the system complexity and a resultant
difficulty in assessing the response(s) to a stressor. Toxicological
investigations, as a result of this, usually are oriented towards
simpler systems, or towards tissue and individual effects but at-
tempts must then be made to extrapolate this information to
populations and higher levels of biological organisation (Garnier-
Laplace et al., 2004). It seems logical to assume that the most
pertinent biological endpoint in individuals after radiation expo-
sure will be disturbances in reproduction, especially in view of
known radiation sensitivities of the various concomitant stages
(oocytes, spermatogonia, newborn etc.) and the importance of the
endpoint for population sustainability. This point is recognized by
the ICRP (ICRP, 2008). With this in mind, information regarding
radiation induced effects in wild plants and animals has been
collated under umbrella endpoints by the ICRP such as mortality,
morbidity and reduced reproductive capacity. Through the work of
the ICRP and others (see e.g. Strand et al., 2000; Strand and Larsson,
2001. Larsson, 2008; Vives i Batlle et al., 2007, Strand et al., 2014),
various methods/methodologies are available to facilitate the pro-
cess of assessing the impact of exposures in a robust manner. In
recent years, the IUR has identified a need to move radiological
impact assessments towards a more ecosystem based approach
drawing on the advances made in other environmental science
disciplines (IUR, 2012; IUR, 2015). An overview of the various ef-
fects commonly considered at different levels of biological orga-
nisation is given in Fig. 1.
Analyses of impacts on the environment following a nuclear
accident are, of course, not without precedent. The temporal
development of radiation impacts on plants and animals following
nuclear accidents have been described in relation to the Chernobyl
and Kyshtym accidents (e.g. Gerask'in et al., 2008; Alexakhin, 2009).
After the Chernobyl accident, severe impacts were observed in areas
near to the nuclear plant (Kryshev et al., 2005). The Chernobyl ac-
cident occurred in spring with accelerated growth in the natural
 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
ecosystems while the FDNPS accidents occurred earlier in the year.
The effects observed after Chernobyl in the most affected environ-
ment were due to acute damage i.e. high external doses delivered at
high dose rates. Pine trees became necrotic some weeks after the
accident mainly from b-radiation (lethal doses estimated to
20e100 Gy) as well as deciduous trees close to the reactor site,
while no lethal effects were observed on herbaceous plants. An
increased level of somatic mutations in plants around Chernobyl
was observed during the first years after the accident but then
declined in the proceeding years. Soil fauna along with the abun-
dance and species diversity of insects were affected in the near zone
of Chernobyl immediately after the accident. In addition, vertebrate
animals also received high doses to the thyroid as a result of internal
exposure from radioiodine during this early period. Based on the
experience gained from the Chernobyl accident, distinct phases are
apparent after radiation accidents. These are characterised by an
intensive, “acute” period followed by a rapid fall off in exposure
levels and a subsequent long-term period exhibiting a slow decline
in the dose rate. Most serious and immediate ecological impacts
arise from the first acute period of exposure. For the Chernobyl
accident, approximately 80% of the total radiation dose accumu-
lated by plants and animals was received within 3 months of the
accident, and over 90% of this was due to beta radiation (UNSCEAR,
1996). In the final (third) and continuing phase of radiation expo-
sure (commencing about 1 y post-accident) dose rates have been
chronic, 1% of the initial values, and derived mainly from 137Cs
contamination. (Hinton et al., 2007). The protracted response is
more indirect due to death of organisms or inhibition of processes in
the ecosystems, but also related to the evacuation of people and
domestic animals and remediation occurring. Although populations
of biota around the Chernobyl NPP have recovered substantially
during the years following the accident (IAEA, 2006; Kryshev et al.,
2005), the nature and scale of the recovery has been confounded by
drastic changes in human activity, including cessation of agricul-
tural and industrial activity. As a result, the populations (in terms of
numbers of individuals) of many plants and animals have increased,
although the long-term ecological effects confounded by human
evacuation are still unclear and debated.
The IAEA observed (IAEA, 2015) that releases of radionuclides in
the terrestrial environment, and the corresponding doses to
nonhuman biota occupying areas of high deposition in Japan, were
much lower than in areas around Chernobyl. From this, it was
argued that severe detriments would not be expected, a view that
appeared to be supported by the absence of observations of severe
acute radiation effects immediately after the accident. Nevertheless,
the IAEA highlighted the need to investigate more subtle potential
effects in the longer term. This would need to be achieved bearing in
mind the observation that the severe earthquake and tsunami, per
se, resulted in environmental stress of a significant nature to the
terrestrial and marine environments extending over the north-
eastern coast of Honshu, putatively far in excess of that caused by
radiation exposure. The earthquake induced topographic changes
to the sea floor, and inundation following the tsunami resulted in
the transfer of large volumes of marine sediments onshore. Elevated
deposition of sediment affected the abundance of several benthic
biota and may have a significant impact on the sediment with
respect to biological function for years to come (Oguri et al., 2013).
The Biodiversity Center of Japan (BCOJ, 2014).] has conducted an
investigation on the impact of this event on the environment,
excluding the radiation impact from the Fukushima Daiichi accident
(MRIJ, 2007). For these reasons, the need to disentangle con-
founding factors should lead to focus being placed on areas affected
by radioactive contamination but not by the tsunami itself.
In recent years, numerous studies have been undertaken to
quantify the amount of radioactivity released and deposited on
161
land and water with a more limited subset focussing on the impact
that the radionuclide releases have had on wild plants and animals
following the FDNPS accident. These have taken the form of theo-
retical (i.e. desk-based) assessments, field-based analyses and lab-
oratory experiments, in some cases combining these components.
Now that over 5 years have elapsed since the accident occurred, an
opportune moment has arrived to take stock of the information
that has been published, with a view to drawing some general
observations about the environmental impacts arising from radia-
tion exposures in the aftermath of the FDNPS accident. A similar
type of synthesis has been conducted by Aliyu et al. (2015) as part of
a cursory review that also addresses subjects including the source
term, radionuclide transport processes and human impacts in
Japan. These broad subjects have also been addressed in a more
comprehensive manner by UNSCEAR (UNSCEAR, 2014, 2015) and
the IAEA (IAEA, 2015). In the current review, as presented in the
subsequent pages, a more in-depth appraisal of information on
environmental impacts than previously achieved will be presented.
In so doing, a greater consideration will be given to where dis-
crepancies between studies lie, elaborating on potential causes for
any differences where this is deemed pertinent.
2. Theoretical/desk-based assessments by international
organisations
The consequences of radiation exposures for people and the
environment from the FDNPS accident have been summarised by
the United Nations Scientific Committee on the Effects of Atomic
Radiation, UNSCEAR (UNSCEAR, 2014) and the International Atomic
Energy Agency, IAEA (2015). The desk-based/theoretical environ-
mental impact assessments conducted in both cases have been
based on the approach promulgated by the ICRP (ICRP, 2008, 2009)
but with some modifications. This involved the use of reference
transfer and, in the case of UNSCEAR, kinetic models to allow ex-
posures to be calculated in terms of dose and dose-rates to non-
human biota in units of Gy and Gy per unit time respectively.
From this, possible impacts could be inferred via comparison with
dose-effects benchmarks derived from earlier reviews of dose-
response empirical studies covering a wide range of organisms
(e.g. UNSCEAR, 2011; IAEA, 1992; ICRP, 2008) and from the radio-
biological literature in general.
Within the UNSCEAR (2014) approach, data resulting from
monitoring programmes, indicative of conditions during the first
year after the accident and collated from publically available in-
formation, were employed, in addition to other pertinent reports
and scientific reports available in the literature. The radiation ex-
posures were evaluated within the context of, firstly, the more
dynamic, “intermediate” phase after the accident approximating to
the first three months during which radioisotopes of short half-life
such as 131I cannot be ignored and, secondly, the “late” phase
extending out to 1 year after the accident during which the external
exposure was, to a large extent, dominated by radioisotopes of
cesium. Radiation doses for non-human organisms were estimated
using the ERICA Tool (Brown et al., 2008), a process that comprised
of the selection of representative species (derived primarily from
ERICA reference organisms) and radionuclides, i.e., 134Cs, 137Cs, 89Sr,
90
Sr, 239Pu, 240Pu, 129mTe, 110mAg, and 131I. The assessment was
conducted using measurements of activity concentration in plants
and animals directly whenever this was practicable and such data
were given preference over using soil and/or water activity con-
centration in tandem with a transfer model. The available biota
measurements were available from different locations and sampled
at different times. In addition, the ERICA Approach involves an
equilibrium-based assessment conducted with the use of concen-
tration ratios (Beresford et al., 2008a; Hosseini et al., 2008) for the
162 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
derivation of biota radionuclide concentrations from soil and water.
Such an approach for modelling transfer was adopted by UNSCEAR
(2014) for intermediate and late phases but kinetic models (Vives i
Batlle et al. (2008); Avila et al. (2004); Sazykina (2000); Beresford
et al. (2010)). were also employed by UNSCEAR to estimate time-
dependent concentrations in biota with both approaches using
measured concentrations in media as input data. Subsequent dose
calculations are then performed employing dose conversion co-
efficients (DCCs, in micrograys per hour per becquerel per kilogram
as compiled within the ERICA Tool) and estimating temporal pro-
jections of dose rate from which cumulative doses can be derived.
Using the results, radiation risks to biota could be estimated based
on collated effects data, a priori, and benchmarks derived from such
collations (UNSCEAR (2011); ICRP (2008); Garnier-Laplace et al.
(2008); Andersson et al. (2009); Real et al. (2004); Gerask'in et al.
(2008); Garnier-Laplace et al. (2006); UNSCEAR (1996)).
The dose assessment undertaken for the purposes of IAEA
(2015) paralleled that of UNSCEAR (2014) in the sense that it was
comprised of two distinct components and employed essentially
the same dosimetric models. The first part concerned the applica-
tion of environmental media activity concentrations of radionu-
clides (i.e. water, sediment and soil or deposition) to derive doses to
adult Reference Animals and Plants (RAPs), in accordance with the
ICRP approach, following the releases from the Fukushima Daiichi
NPP. The use of such data reflected the absence, or sporadic
coverage, of direct radionuclide activity concentrations measure-
ments in plants and animals for this period and required the
application of transfer models in deriving the levels of radionu-
clides associated with wildlife. Dose rates to biota were estimated
for defined periods following the releases from the FDNPS by the
IAEA. The source of the input datasets for this part of the assess-
ment was the same as those used by UNSCEAR (2014); however, the
methodology applied, in particular the methodology for modelling
transfer in the environment, was different and specific to the
application of RAPs. Whereas the UNSCEAR (2014) approach
adopted fully kinetic models (parametrised using transfer rates
between compartments) to resolve the changes of activity con-
centrations in different components of the environment with a
high temporal resolution for the intermediate phase, the approach
used by the IAEA involved the use of time-integrated activity
concentrations over longer periods and the application of
equilibrium-based concentration ratios in all phases. The exposures
assessment conducted by the IAEA was thus divided into three
distinct periods in order to take into account the time dependence
of the delivery of dose. The dose was estimated with respect to
time-integrated activity concentrations in soil, fresh water and sea
water (water and sediment) for the periods listed below:
 An early, acute period, during which exposures from short lived
radionuclides, occurred (30 days, mid-Marchemid-April 2011);
 An intermediate period after 31e90 days (mid-Mayemid-
September 2011), when data on activity concentrations in the
environment were available;
 Late period after 90 days (up to one year), when equilibrium is
assumed, especially for radiocaesium.
The second part of the IAEA assessment was based on data
pertaining to directly measured activity concentrations in non-
human biota (and their habitats). These data provide the most
precise estimates of doses, because the approach avoids the use of
transfer models with their concomitant uncertainties. Reference
dosimetric models for RAPs were used in the exposure estimates
for the second part of the assessment, whenever possible. In some
cases, bespoke models were required where the biota differed
considerably from those included in the list of RAPs. In a similar
fashion to the approach adopted by UNSCEAR, the IAEA looked at a
range of dose and dose-rate benchmarks, e.g. ICRP, 2008; UNSCEAR,
2011, for the sake of comparison with exposure estimates and the
inference of possible effects.
The UNSCEAR concluded that, for both aquatic and terrestrial
biota, exposures following the accident had been generally too low
for observable acute effects. Some exceptions had been regarded as
possible because of locally elevated levels of contamination. The
Committee further concluded that, generally, population-relevant
biota effects in the marine environment would have been
confined to points where discharges or releases of highly radioac-
tive water into the ocean had taken place. With respect to terres-
trial species, whilst the Committee had not been able to exclude a
risk of effects to individuals, observable effects at the population
level were considered as unlikely. The overall conclusion of
UNSCEAR was that (any substantial) radiation effects would have
been localised to limited areas where deposition densities (or ac-
tivity concentrations) were greatest. These were considered by
UNSCEAR to be locations such as the Fukushima port in proximity
to the main release point (marine environment) and terrestrial
locations within Okuma Town. Beyond the most contaminated
areas, the potential for radiation effects on wild organisms were
considered as being insignificant.
Similarly, the IAEA concluded that no impacts on populations and
the ecosystems (both terrestrial, freshwater and marine environ-
ments) were expected. Furthermore, the IAEA concluded that long
term effects were unlikely, as the estimated doses over the short
term were generally substantially below levels at which observa-
tions of highly detrimental acute effects might be expected, and
there was a relatively rapid decline in dose rates after the accident.
3. Studies where radiometric data from the field have been
used to provide information on environmental exposures
The most common types of studies that have been conducted in
the environs of FDNPS post-accident can be broadly categorised as
those involving the characterisation of environmental radioactivity
levels without the provision of any information on particular bio-
logical effects. The category includes studies wherein (i) radionu-
clide activity concentrations in biota and their habitat were
determined and/or (ii) absorbed dose rates were measured or
calculated. Self-evidently, such information can be (or has been)
useful to estimate exposures and thereafter infer whether effects
might be expected or not. The collation made for this section has
not been exhaustive but a selection of relevant publications has
been made for illustrative purposes, i.e. to provide an indication of
exposure levels.
3.1. Terrestrial
The concentration of radiocaesium in leaves of Japanese cedar,
bamboo and Clinopodium gracile was measured by Tazoe et al.
(2012). Samples of Japanese cedar leaves collected in April and
June 2011, respectively, showed a much lower concentration of
radiocaesium than leaves from the bamboo (approximately
450 kBq/kg), which might be due to the differences in overlapping
branches (interception). Grass sampled from Namie Town showed a
maximum activity concentration of approximately 350 kBq/kg of
radiocaesium in April. Japanese mugwort showed very low con-
centrations (<0.5 Bq/kg), despite relatively high concentrations of
137
Cs in the soil (6.3e27.1 kBq/kg). Kuroda et al. (2013) investigated
the radiocaesium concentrations in the stemwood of major Japa-
nese tree species (oak, cedar and red pine trees) sampled at five
sites in Fukushima Prefecture. Half a year after the Fukushima
Daiichi accident, radiocaesium was distributed between bark,
 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
sapwood and heartwood, indicating a very rapid translocation of
radiocaesium into the wood. The concentration levels in the com-
ponents of the tree depended on the radiocaesium deposition
density. At all sites and for all species, radiocaesium activity con-
centrations were substantially greater in bark than they were in
sapwood and heartwood.
The concentrations of earthworms in forests of Fukushima
Prefecture were measured six months after the accident at three
forest sites located at distances of 26 kme134 km from the site of
the Fukushima Daiichi NPP (Hasegawa et al., 2013). The diversity of
terrestrial earthworms in Japan is relatively high, especially with
respect to the family Megascolecidae. Three plots were comprised of
Japanese cedar plantations (Cryptomeria japonica), and one plot
was characterised as a mixed forest of oak (Quercus serrata) and
pine (Pinus densiflora). The deposition densities of radiocaesium
(134þ137Cs) varied from 20 kBq/m2 at a site located 134 km from the
NPP to 1230 kBq/m2 at a site located 26 km from the plant. The
highest concentrations in earthworms were 61 ± 41 kBq/kg of
134
Cs; values of 70 ± 46 kBq/kg (dry weight) of 137Cs were also
found at this site. The lowest values d 1.26 ± 1.17 and
1.46 ± 1.17 kBq/kg (dry weight) for 134Cs and 137Cs, respectively d
were obtained for soil invertebrates sampled at the distance of
134 km from the Fukushima Daiichi NPP. No substantial differences
in 134þ137Cs concentrations were identified for different species of
earthworms on the same plots (Hasegawa et al., 2013).
Earthworms were studied by Fujiwara et al. (2015) in assessing
the uptake and retention of radiocaesium and concomitant absor-
bed dose rates to the organisms within areas impacted by the ac-
cident. The concentration ratios (CR) for 137Cs were higher early in
the culturing period with subsequent decreases observed over
time. Depuration of radiocaesium from earthworms was reported
as occurring over a period of days. Highest absorbed dose rates for
radiocaesium were calculated as being 1.9 mGy/day, the authors
concluding that such exposures would have no biological conse-
quences in actual earthworms. This conclusion was based upon
consideration of accepted benchmark levels rather than an empir-
ical study of biological effects. Recent reported work on exposures
to earthworms and similar biota species can be usefully con-
textualised by comparison with the results of Ohtsuka et al. (2015)
in determining background radiation dose-rates to such species,
due to naturally occurring radionuclides, prior to the accident. Re-
ported mean dose rates were 0.28 mGy/h for the earthworm species
and between 0.036 and 0.69 mGy/h for the arthropod species.
Concentrations of radiocesium in the species, Nephila clavata L.
Koch (Nephilidae: Arachnida), a large web spider, collected at three
sites at varying distances from the FDNPS were reported (Ayabe
et al., 2014). Samples were collected about 1.5 y after the acci-
dent. The concentrations were highest in samples drawn from a
secondary forest some 33 km northwest of the plant, exhibiting a
mean value of 2.4 Bq/g d.w. for 134Cs and approximately 4 Bq/g d.w.
for 137Cs. In a secondary forest some 37 km northwest of the plant,
the mean concentrations of 134Cs and 137Cs were 0.8 Bq/g d.w. and
1.5 Bq/g d.w. respectively. A pine forest, 62 km west of the plant,
contained very low radiocaesium concentrations in a limited
number of individuals. Concentrations of 134Cs and 137Cs in spiders
collected at each site exhibited a tendency towards correlation with
the air radiation dose rate observed at each site (Spearman Rank
correlation coefficient ¼ 1 but this was based on only 4 sampling
sites). The authors of the study considered that as spiders are key
components of forest food, the high concentrations in this species
suggest the transferral of radiocaesium to higher trophic levels.
Dose rates for Tohoku hynobiid salamanders (amphibian) from a
highly contaminated area of the Fukushima prefecture were esti-
mated by Fuma et al. (2015). The highest total dose rates estimates
were 50 mGy/h, the authors concluding that growth and survival of
163
this salamander, even for habitats in the severely contaminated
Fukushima Prefecture, would not be adversely affected. As the
dose-rates derived were in exceedance of some published bench-
marks, the authors could not conclusively assert that impacts in
relation to more sensitive endpoints, might occur.
Matsui et al. (2015) measured ambient dose equivalents and
137
Cs activities in bird nests at Ibaraki, 175 km southwest of the
plant. The study quantified correlations between dose rates within,
and external to, each nest and correlated the mass of, and activities
of 137Cs in, the nesting materials. The maximum dose rates reported
were 0.24 mGy/h. To place these dose rates into some kind of
context, typical background (weighted absorbed)) dose rates
arising from primordial radionuclides (excluding Rn-222) would be
approximately of this magnitude (see Beresford et al., 2008b).
Kubota et al. (2015a) estimated the absorbed dose rates for wild
rodents inhabiting a site severely contaminated by the FDNPS ac-
cident. Theoretical calculations were checked using abdominally
embedded glass dosimeters. The average internal absorbed dose
rate was markedly smaller than the average external dose rate
(<10% of the total absorbed dose rate). The average total absorbed
dose rate estimated for wild rodents living in the sampling area 3
years after the accident was approximately 52 mGy/h (1.2 mGy/d).
The authors of this paper noted that substantial differences were
observed, at the time of capture, in whole-body activity concen-
tration of radiocesium between individual rodents. They also drew
attention to the fact that calculated values fell above ICRPs’ derived
consideration levels suggestive of there being some chance of
deleterious effects occurring at the individual level.
Muscle concentrations of 134Cs and 137Cs in Japanese monkeys
(Macaca fuscata) inhabiting the forest area of Fukushima City were
measured by Hayama et al. (2013). Concentrations in muscle were
in the range of 6000 to 25 000 Bq/kg for monkeys captured in areas
with soil contamination levels in the range of 100 000 to 300 000
Bq/m2. Levels decreased rapidly during May and June 2011 and
reached an equilibrium value of around 1000 Bq/kg in monkeys
sampled during and after June, although substantial differences
between individuals were observed.
The radionuclide activity concentration data for terrestrial
ecosystems specified in Tazoe et al. (2012), Kuroda et al. (2013) and
Ayabe et al. (2014) were used by IAEA (2015) to derive dose-rates
for grasses, trees invertebrates and mammals. Dose-rates were
below 2 mGy/d for grass, below 0.1 mGy/d for trees and generally
below 0.4 mGy/d for animals. IAEA considered that exposures of
this magnitude would not be considered to be detrimental to
populations of these organism types.
3.2. Freshwater
An overview of radiocaesium in freshwater fish in Fukushima
Prefecture and eastern Japan was based on data published in
Mizuno and Kubo (2013). An isopleth map shows the radiocaesium
contamination of the Ayu (Plecoglossus) captured between May and
September 2011 in each prefecture in eastern Japan. At about
100 km from the Fukushima Daiichi NPP, the average concentration
was about 200 Bq/kg and decreased with larger distances. How-
ever, no information was given in the study about uncertainties or
variability. Nor was any information provided on where the fish
were caught. The data did indicate, however, that the levels of
concentration in fish were relatively low. Maximum activity con-
centrations, ca. 8000 Bq/kg f.w. 137Cs (along with similar levels of
134
Cs), from the publication Mizuno and Kubo (2013) were used by
the IAEA (2015) to derive dose-rates of 0.1 mGy/d and infer from
this that population impacts would not be probable.
Subsequent analyses have provided some confirmation sup-
porting the contention that the data used by IAEA were
164 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
representative. For example, Tsuboi et al. (2015) determined 134Cs
and 137Cs in riverbed samples of algae and silt and in the freshwater
fish ‘ayu’ in five river systems of Fukushima Prefecture between the
summer of 2011 and the autumn of 2013. Maximal activity con-
centrations in fish slightly are reported as exceeding 1000 Bq/kg f.w.
while levels in riverbed sediments were reported as being generally
below 10 kBq/kg w.w. Arai (2014) studied freshwater fish in the
Sousou region of Fukushima Prefecture for a three-year period from
May 2011 to March 2014. The highest concentration (of total
134
Cs þ 137Cs) was found in masu salmon (18700 Bq/kg) followed by
ayu (2900e4400 Bq/kg) with Japanese dace exhibiting 2500 Bq/kg.
The total radiocaesium concentrations were observed to decrease
gradually but significantly during the three-year period after the
accident, the tendencies varying among the studied species.
3.3. Marine
Activity concentrations in pelagic fish and plankton were
measured in samples collected at 50 stations at the Japanese coast
in June 2011 (Buesseler et al., 2012). The amount of radiocaesium
ranged from below the detection point to about 56 Bq/kg (dry
weight). Silver-110 m was occasionally detected in zooplankton,
with concentrations up to 23.6 Bq/kg (dry weight). The authors
concluded that “radiation risks due to these radionuclides are below
those generally considered harmful to marine animals and human
consumers” (Buesseler et al., 2012).
By October 2012, Wada et al. (2013) had measured 131I, 134Cs and
137
Cs concentrations in 6462 samples from 169 different marine
species collected off the coast of Fukushima Prefecture since April
2011. Two species only exceeded 2000 Bq/kg w.w. 131I during the
period immediately after the accident. In the years 2011 and 2012,
63 and 41 species respectively exceeded 100 Bq/kg w.w. for radi-
ocaesium. The overall radioactive Cs concentrations in marine
species were observed to have decreased significantly but the
trends in decline of radioactive Cs concentrations differed greatly
between taxa, habitats (pelagic/demersal), and spatial distribu-
tions. Higher concentrations were observed for shallower waters
south of the plant. For pelagic fish and some invertebrates, radio-
caesium concentrations decreased rapidly or were below detection
limits and declined steadily in seaweed, surf clams, and other or-
ganisms. Some coastal demersal fishes exhibited more gradual
declines and concentrations above the regulatory limit were
detected frequently, suggesting continued uptake of radiocaesium
through the benthic food web. There were substantial overlaps
with the data used by UNSCEAR (2014) in their evaluation of
environmental impacts based on radionuclide measurements in
biota. As noted by Vives i Batlle et al. (2014), the exposure levels
generally did not seem to indicate the potential for effects.
Baumann et al. (2013) discussed elevated levels of up to 800 Bq/
kg d.w. 134Cs and 137Cs in macroalgae and mussels within a few
months of the accident. Reported Cs concentrations in biota
sampled in early June 2011 were higher in areas south of Fukush-
ima than those sampled in the last third of the month north of
Fukushima. Activity concentrations of 134Cs and 137Cs in organisms
taken south of Fukushima were comparable to, or lower than, those
of 40K in the same samples.
Sohtome et al. (2014) discussed 134Cs and 137Cs concentrations
in benthic invertebrates, from 10 taxonomic classes and 46 iden-
tified families, collected off Fukushima Prefecture at depths be-
tween 3 and 500 m between July 2011, four months after the
accident, and August 2013 in order to facilitate elucidation of time-
series trends among taxa and areas. Cesium-137 was detected in
77% of 592 specimens, higher 137Cs concentrations being often
found in areas close to or south of the plant, consistent with the
reported spatial distribution of 137Cs concentrations in seawater
and sediments exhibiting high concentrations after the accident.
Overall 137Cs concentrations in invertebrates, maximal 137Cs levels
attaining 290 Bq/kg w.w. in the sea urchin (Glyptocidaris crenularis),
were low relative to many demersal fish, and fell exponentially over
time whilst exhibiting taxon-specific declines. Comparison of
invertebrate 137Cs concentrations with seawater and sediment
concentrations suggested that contaminated sediments are the
primary source of persistent contamination in benthic in-
vertebrates, especially with respect to Malacostraca and Poly-
chaeta. Shigenobu et al. (2014) determined 134Cs and 137Cs
contamination in greenlings (Hexagrammos otakii) taken off the
coast of Fukushima Prefecture. Samples taken near the plant itself
exhibited a geometric 137Cs mean of 17 364 Bq/kg w.w. with a
maximal value of 740 000 Bq/kg w.w. These were, by some margin,
the highest activity concentrations directly measured for any biota
species (for all ecosystems) and the levels in offshore samples were
substantially lower. The radiocaesium concentrations of individual
greenlings indicated that contamination levels in the northern
waters were low. In this area the radiocaesium concentrations of all
individuals caught after October 2012 were between levels that
were lower than detection limits and circa 39 Bq/kg w.w. The
radiocesium concentrations of greenlings caught in southern wa-
ters in May 2012 varied between 3 and 1070 Bq/kg w.w.
The publication of Johansen et al. (2015) includes, inter alia,
estimates of dose rates arising from radiocaesium and 90Sr to fish in
the port area near to the FDNPS including the highly elevated
values reported by Shigenobu et al. (2014) above. The authors drew
attention to the fact that the original predictions that can be
inferred from the marine models applied in UNSCEAR (2014) sug-
gest that exposure levels would have dropped off much more
rapidly following the first few months of exposure than was actu-
ally observed. Using publically available data on activity concen-
trations in the port area for levels in seawater, sediment and fish the
authors reported, for a period covering 2013e2014, dose rates of
1.1 mGy/d median, and 4.3 maximum mGy/d. These compare to a
maximum calculated by UNSCEAR (2014) for the FDNPS North
channel of 140 mGy/h (3.4 mGy/d) with a subsequent rapid fall to
levels in the order of tens of mGy/h within the first few months. The
persistent elevation of 134,137Cs in certain species was considered to
be likely mainly due to their sediment-associated food chains and
feeding behaviors. Although the maximum dose rates calculated in
this study of 4.3 mGy/d fell below UNSCEAR benchmark for aquatic
systems of 10 mGy/d (400 mGy/h) and the authors noted that
population effects had not been reported, nor indicated in their
study, the values were considered as being close enough to insti-
gate caution regarding the initial conclusions from UNSCEAR. They
furthermore identified the need for continued appraisal and
attention regarding exposures of benthos in the port area in prox-
imity to the FDNPS. The dose rates appeared to be at a level where
there was some expectation of observing damaging effects for some
individuals within the population.
4. Direct analyses of biological effects in the field
The reports of impacts on biota via the determination of the
various responses related to particular biological endpoints have
been solely restricted to the terrestrial and freshwater environment
around the FDNPS plausibly reflecting the practicalities of con-
ducting such studies.
4.1. Molecular, cellular damage and morphological effects
In studying exposure effects on the DNA (single- and double
strand breaks) of wild boar and earthworms, Fujita et al. (2014)
used comet assays on samples collected from regions exhibiting
 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
levels of contamination ranging from 0.28 mSv/h to 2.85 mSv/h. No
significant differences were observed with respect to levels of DNA
damage in wild boar captured in regions categorised as exhibiting
low levels or contamination relative to those captured in regions
categorised as being highly contaminated. However, earthworms
sampled from the region denoted as being highly contaminated
had a significantly greater extent of DNA damage relative to those
sampled from the less contaminated region, the authors discussing
the inherent difficulty in interpretation of molecular effects in
relation to possible biological function impairment.
Studies on five frog species collected during the autumn of 2012
both within and outside a 20 km radius of the FDNPS, were re-
ported upon by Matsushima et al. (2015). The highest reported
radiocaesium concentration was 47 279 Bq/kg wet weight. Histo-
logical examinations of ovaries and testes from the frog samples
indicated no clear abnormalities in the tissues, the authors
concluding that “exposure to radioactive materials does not seem to
have severely affected the reproductive behaviour or the maturation of
eggs and sperm in frogs.”
The occurrence of chromosomal aberrations in splenic lym-
phocytes of Japanese field (Apodemus argenteus) and house mice
(Mus musculus) from the Fukushima Prefecture was investigated by
Kubota et al. (2015b). In mice drawn from a lesser contaminated
area, the average frequency of dicentric chromosomes was reported
as being similar to mice from an uncontaminated control area. Mice
from moderately and heavily contaminated areas were stated to
have exhibited a significant increase in the average frequencies of
dicentric chromosomes. The total absorbed dose rate were esti-
mated to be of the order of 1 mGy/d and 3 mGy/d (pertaining to
moderately and heavily contaminated locations respectively).
Chromosomal aberrations were stated as having increased to some
extent with the dose rate; although the frequency of chromosomal
aberrations was considered as being proportional to the absorbed
dose, chromosomal aberrations in old mice (median age of 300
days), was not reported as having increased with radiation dose at
the same rate as that stated for young mice (median age of 105
days). For a study on large Japanese field mice (Apodemus speciosus)
in Fukushima, focusing on apoptosis in germ cells and abnormal
sperm morphologies, Okano et al. (2016) concluded that radiation
did not cause substantial male subfertility during 2013 and 2014.
A population of wild monkeys from the forest area of Fukushima
City, some 70 km from the plant itself, were the subject of a 1-year
haematological study by Ochiai et al. (2014) during 2012. For
comparative purposes, monkeys from the Shimokita Peninsula in
Aomori Prefecture, some 400 km from the plant, were also studied.
Total muscle caesium concentrations in the Fukushima monkeys
were reported as being between 78 and 1778 Bq/kg, levels being
undetectable in all Shimokita monkeys. Relative to the Shimokita
monkeys, Fukushima monkeys were stated as having exhibited
significantly lower white and red blood cell counts, haemoglobin
and haematocrit, the white blood cell count of immature monkeys
showing a significant negative correlation with muscle caesium
levels. Results suggested that the exposure to some form of radio-
active material contributed to haematological changes in Fukush-
ima monkeys, the authors opining that “low blood cell count does
not necessarily mean that the health of individual monkeys is at risk.
However, it may suggest that the immune system has been compro-
mised to some extent, potentially making individual animals and the
entire troop susceptible to, for example, epidemic infectious disease.”
Morphological effects have also been observed following the
FDNPS accident. The proportions of abnormalities and mortality
rates in gall-forming aphids were observed, by Akimoto (2014) to
be significantly higher in the Fukushima region than in control
areas. The author concluded that radioactive contamination had
deleterious effects on the process of embryogenesis in eggs
165
deposited on tree bark surfaces, but a negligible influence on sec-
ond generation aphids. Working with fir tree species, Watanabe
et al. (2015) investigated morphological changes in trees at loca-
tions near the plant. Populations at such locations were posited as
having exhibited a significantly increased number of morphological
defects relative to a control population distant from the plant. The
authors stated that defect frequency corresponded to radioactive
contamination levels at the study sites and suggested the possi-
bility that the contamination contributed to the defects while
considering that a range of confounding factors could account for
the morphological observations.
Suzuki (2015) studied Carp in small water bodies in the highly
contaminated Iitate Village, Fukushima Prefecture. Blood neutro-
phil, monocyte and lymphocyte counts in this species of fish from
three ponds in Fukushima were lower compared to fish from a non-
contaminated pond in Tochigi Prefecture. Histological observations
of the carp in Fukushima indicated abnormal hyperplasia of mac-
rophages in the liver, kidney, spleen and pancreas of the studied
fish. The presence of injurious effects on the health of carp due to
the radiation in Fukushima could not be confirmed as only a single
pond was available for comparative control purposes. Nor was the
author able to find any symptoms in the carp that could be corre-
lated with concentrations of internal caesium.
4.2. Effects at the population level
The effects of radiation exposure on the abundance of common
bird species in Fukushima compared with those observed in areas
contaminated after the Chernobyl accident were reported (Møller
et al., 2012). This was achieved by census surveys, i.e. deter-
mining the numbers of birds in a given area by field study, and
correlating bird abundance with external dose-rates with a statis-
tical control for possibly confounding factors such as time of day,
meteorological conditions and habitat on bird abundance. The
study indicated that the abundance of birds was negatively related
to radiation with, according to the authors, a significant difference
between Fukushima and Chernobyl. Through analysis of 14 species
that were common to the two areas studied, the authors revealed a
negative effect on abundance as a result of radiation that differed
between species and areas. The relationship between abundance
and radiation was considered to be more strongly negative for
Fukushima than for Chernobyl in relation to the same 14 species.
Møller et al. (2012) suggested that this demonstrated a negative
consequence of radiation for birds immediately after the Fukush-
ima accident during the main breeding season in MarcheJuly,
when individuals work close to their maximum sustainable level.
Mousseau and Møller (2014) later concluded that the abundance
and diversity of forest and grassland avian species in Chernobyl
were lower in contaminated areas, opining that this indicated a
type of dose response, similar but stronger patterns being reported
for birds in Fukushima during 2011. Ishida (2013) presented find-
ings from studies in the northern Abukuma Highlands related to
radioactivity measurements conducted on birds and other wild
animal species. The distribution of the bush warbler (C. diphone)
and brown-eared bulbul (H. amourotis) was reported as being not
related to the levels of radiocesium. Distributions during mid-July
2011, based on early surveys after the accident, were stated as
having resembled the results obtained in 2012. Ishida (2013) noted
that there was a distinct progressive change in character of a spe-
cies over the studied area of contamination and thus a design of the
bird count survey which did not account for this would be inap-
propriate for discriminating the effects of radioactivity from other
environmental factors.
Bonisoli-Alquati et al. (2015) hypothesized that the exposure of
barn swallow (Hirundo rustica) nestlings to low doses of radiation
166 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
increased genetic damage (quantified using Comet Assay) of pe-
ripheral erythrocytes. The abundance and local age ratio of barn
swallows was estimated across a range environmental radiation
levels - between 0.15 and 4.9 mGy (average exposure rates of
0.9 mG y/h). Exposure to radioactive contamination (measured with
hand held dosimeters at ground level under the nests and by
gamma ray spectrometer at the laboratory respectively) was not
reported to result in higher levels of genetic damage in nestlings. At
higher levels of contamination, the number of barn swallows was
reported to have declined and the fraction of juveniles decreased,
taken as being indicative of lower survival and reproduction and/or
fledging rate. Part of the database employed in the work had been
previously published in studies relating the abundance of birds in
the Fukushima region to the level of radioactive contamination
(Møller et al., 2012; 2013). Møller et al. (2015a), using census
methods, analysed further bird abundances at Fukushima and
Chernobyl. The conclusion was drawn that species with small body
size and relatively high food consumption rates were more nega-
tively impacted with secondary consumers being reported as
exhibiting stronger negative effects of radiation on abundance than
herbivores, especially at Fukushima. Møller et al. (2015b) present
yet another analyses of the census data on bird abundances around
Fuksuhima, but this time analysed the data in relation to temporal
developments. For the period 2011e2014 Møller et al. (2015b)
tested whether the abundance and diversity of birds became
more negatively affected by radiation over time. They concluded
that the abundance of birds decreased with increasing levels of
background radiation (as reported in earlier publications), with
significant interspecies variation (some species actually increased
in abundance with radiation level). Even though background radi-
ation levels exhibited a decrease with respect to time, the abun-
dance - radiation relationship was stated as becoming more
negative with time. The authors considered that their findings were
consistent with their hypothesis that the negative effects of radia-
tion on species richness and abundance accumulate over time.
Garnier-Laplace et al. (2015) modelled a reconstruction of the
radiological dose to birds at 300 census sites in the northwest area
affected by the Fukushima accident during 2011e2014 from the
earlier work of Møller et al. (2015b). The ambient dose rate
measured at the census points (between 0.16 and 31 mG y/hr) and
the dose rate reconstructed for adult birds of each species (between
0.3 and 97 mG y/hr), was purported as indicating that the overall
abundance of birds at Fukushima decreased with increasing total
external doses. The authors stated that the relationship reported
was directly consistent with exposure levels reported in the liter-
ature (ICRP, 2008) as causing physiological disturbances in birds.
The authors claimed that of the 57 species studied, 90% were
chronically exposed to a dose rate that could potentially affect their
reproductive success and that the data also indicated a significant
positive relationship between total dose and species diversity.
Murase et al. (2015) studied the reproductive performance of a
top avian predator before and after the Fukushima accident in an
area of relatively low contamination area some 100 km from the
plant. Observation data over 22 years, including information on
occupied nests, number of eggs incubated and hatched and number
of birds fledged, were used in the study, Bayesian methods being
employed to elaborate upon the relationship between these data
and dose rates determined under each nest. The reproductive
performance was reported as having declined to a marked degree
compared with the years pre-accident and progressively decreased
for the three post-accident study years. The authors suggested that
these declines were attributable to an increase in the air dose rates
measured under the nests; dramatic impacts on reproduction were
reported at air dose rates substantially below 1 mSv/h (the
maximum dose-rate being 0.85 mSv/h). To place this into some kind
of context, typical background (weighted absorbed) dose rates for
terrestrial biota from primordial radionuclides (excluding 222Rn)
may be of the magnitude 0.5 mGy/h (Beresford et al., 2008b).
Mousseau and Møller (2012b), in analysing invertebrate abun-
dances, reported differences in variation patterns between
Fukushima samples and those observed in Chernobyl - butterflies
and cicadas exhibiting lower abundances with increasing contam-
ination levels, an aspect not observed for bumblebees, dragonflies
or grasshoppers. Arachnids were stated to exhibit a statistically
significant increase at heavily contaminated sites, posited as being
due to the decrease in the abundance of birds reported upon in
these areas.
Genetic and morphological characteristics of the pale grass blue
butterfly (Zizeeria maha) studied was by Hiyama et al. (2012). They
collected 144 samples of first-voltine adults from locations in the
Fukushima area in May 2011, some of which exhibited relatively
mild abnormalities. The F1 offspring from the first-voltine females
(33 females totally collected) exhibited more pronounced abnor-
malities, subsequently inherited by the F2 generation (which
comprised of 10 samples). Mature butterflies collected in
September 2011 were shown to have more severe abnormalities
than those which had been collected in May. In conclusion, the
authors opined that artificial radionuclides from FDNPS were the
cause of genetic and physiological damage to this species and that
the cumulative effects of exposures could have caused a deterio-
ration in the population. In a follow up study, Hiyama et al. (2015)
investigated spatio-temporal changes in abnormality rates in both
adult populations (caught in the field) and laboratory-reared
offspring populations of the pale grass blue butterfly at 7 local-
ities (Fukushima, Motomiya, Hirono, Iwaki, Takahagi, Mito, and
Tsukuba) during spring and autumn between 2011 and 2013. The
abnormality rates in adults from the contaminated localities were
reported as having increased rapidly, attaining a maxima during
autumn 2011, this not having been observed in non-contaminated
localities. Total offspring abnormality rates, including deaths at
the larval, pre-pupal, and pupal stages and morphological abnor-
malities at the adult stage, were stated as having peaked either
during the autumn of 2011 or in the spring of 2012. The elevated
abnormality rates of the field and offspring populations reverted to
a normal level by the autumn of 2012 and by the spring of 2013,
respectively. Nohara et al. (2014) had reported on larvae of the
same species that, under laboratory conditions, were fed leaves
collected from localities contaminated by radionuclides from the
FDNPS accident. The sample specimens themselves were drawn
from Okinawa, which was a relatively uncontaminated locality in
Japan. Mortality and abnormality rates were stated as having
increased sharply at low doses in response to the ingested (radio)
caesium dose, activities reported as resulting in 50% lethality and
abnormality were 1.9 and 0.76 Bq radiocaesium per larva (corre-
sponding to 54 000 and 22 000 Bq/kg radiocaesium body weight,
respectively). The data was reportedly indicative of a non-linear
relationship between ingested (radio)caesium activity and
lethality and abnormality metrics with the reported maximum
effects occurring at relatively low activities (maximum mortality
at < 4 Bq compared to a maximum experimental application of ca.
16 Bq where mortality rates dropped by >10%). Taira et al. (2015)
elaborated upon the geographical, temporal, and temperature-
dependent changes of the forewing size of the same butterfly
species in Japan. After accounting for these factors, the authors
concluded that size reductions observed exclusively in Fukushima
Prefecture in 2011 were “caused by the environmental stress of
radioactive pollution”.
A somewhat different interpretation of the changes seen in in-
sect populations following the FDNPS accident is provided by
Yoshioka et al. (2015) drawing on the observation that human
 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
activities functioning to maintain biodiversity and ecosystem ser-
vices in the evacuation zone were effectively discontinued in 2011.
The results were indicative of the number of individuals of Xylocopa
appendiculata, the largest Apidae species in the region, being
significantly lower within the evacuation zone than without,
whereas similar metrics for other insects were not significantly
lower. The authors considered that, although flying insects and
their ecosystem services (i.e., benefits from them such as pollina-
tion) were not critically impacted 3 years after the disaster, the
long-term effects of the human evacuation on these biota types
required further attention.
5. Discussion
The maintenance (or restoration) of the ecological integrity of an
ecosystem is fundamental for the well-being of its populations and
leads to the support of a balanced, integrated, adaptive community
of organisms comparable to that of similar, undisturbed ecosys-
tems. Exposure to radioactive fallout may lead to direct observable
effects on living organisms and to indirect effects when specific
constituents of an ecosystem are disrupted, resulting in some
imbalance. The time-course of radiation impact on ecosystems
following nuclear accidents has been described elsewhere
(Alexakhin, 2009) and most probably applied and will apply to the
FDNPS accident. Initially, the dose rates decrease rapidly due to the
decay of short-lived radionuclides (e.g.131I). Then migration of the
deposited radionuclides (e.g. 137Cs) leads to heterogeneous expo-
sures and, in a longer time perspective (years), low exposures to the
organisms prevails over comparatively long periods.
Although the number of studies on potential effects on biota
induced by the deposited radioactive substances originating from
the FDNPS accident have increased markedly, there are few studies/
observation from the acute phase of the accident when the releases
of especially radioiodine dominated. Some initial effort have been
made to address certain aspects of this problem, as exemplified by
the work of Strand et al. (2014) with respect to 131I exposures for
mammals, but few other scientists have addressed the issue. In
attempting to elucidate possible impacts on the environment as a
result of radioactive contamination, we will attempt to draw out
some general patterns from the studies undertaken and elucidate
the main points where discrepancies exist between the reported
observations and the assessed consequences.
5.1. Are the findings of UNSCEAR and IAEA assessments backed up
by empirical study?
The UNSCEAR and the IAEA evaluation of the impact of the
FDNPS accident on the natural environment came to similar con-
clusions. The releases were unlikely to have caused any substantial
harm to the environment (i.e. discernible regional population im-
pacts on non-human biota) both in the short as well as long term.
Assessments of the radiological impact based primarily on
measured activity concentrations in the environment underpin
these judgements. Few observations of effects were reported at the
time of the UNSCEAR and IAEA evaluations and only a limited
number of investigations were then published.
The assessments of UNSCEAR (2014) and IAEA (2015) used
comprehensive datasets on activity concentrations including those
collated by official sources, e.g. Ministry of Education, Culture,
Sports, Science and Technology (MEXT) Japanese Ministry of Agri-
culture, Forestry and Fisheries (MAFF) and industry (e.g., TEPCO).
Some of these data were later published in the open literature as
exemplified above (e.g. Wada et al., 2013) so the consistency be-
tween the international evaluation and bespoke studies is not un-
expected. For the IAEA (2015), further use was made of published
167
activity concentration data, as noted above, obviating the need to
identify inconsistencies. In those cases where activity concentra-
tions and or dose-rates were determined in specific studies inde-
pendently from the assessments made by UNSCEAR and IAEA,
consistency was also generally high. For example, the exposure
estimates made by Kubota et al. (2015a) for rodents are remarkably
similar, i.e. differ by less than 20%, to estimates for the RAP ‘Rat’
presented in UNSCEAR (2014) for locations in Okuma Town in
rough proximity to the study locations of Kubota et al. (2015a).
Similarly, the dose rate estimates and measurements made by
Fuma et al. (2015) for amphibia were in reasonable agreement with
estimates made by UNSCEAR (2014) for frogs from a nearby area.
For this comparison, the dose estimates from the international
assessment and the bespoke research study differed by no more
than a factor of three. Nonetheless, a more pronounced discrepancy
might be evident in the marine environment. Although the
maximum dose rates for fish in the port area in proximity to the
FDNPS calculated by Johansen et al. (2015) and those from the
UNSCEAR analysis (UNSCEAR, 2014) correspond quite closely, the
similarities end there. The original predictions that can be inferred
from the marine models applied in UNSCEAR (2014) suggest that
exposure levels would have decreased much more rapidly,
following the first few months of exposure, than was actually the
case. This might constitute evidence that the transfer models
applied in the initial phase, by UNSCEAR (UNSCEAR, 2014),
following the accident may have substantial limitations in terms of
applications to later time periods (albeit that this was never the
intention). The initial argument, as adopted by UNSCEAR, to ignore
transfer to sediment and thus remove a focus on sediment-
associated food chains would appear to be inappropriate for long
term prognoses (post 1 year) although other considerations such as
protracted releases of radioactivity into the marine environemnt
might also (partly) explain the discrepancy between measured and
modelled data.
Neither UNSCEAR (2014) nor IAEA (2015) discounted the pos-
sibility that risks to individual organism could exist in highly
contaminated areas. For example, UNSCEAR (2014) noted, inter alia,
that: “For the late phase (months to years) after the accident, a risk of
effects to individuals of certain species, especially mammals, may exist
in areas of highest deposition density.” Furthermore, IAEA (2015)
noted, inter alia, that “the estimated dose rate of 1.7 mGy/d for the
period of 0e30 days falls just within the range (1e10 mGy/d) where
there is a potential for reduced reproductive success, owing to
increased male sterility.” In fact, some of the inferences made within
the aforementioned theoretical studies correspond quite convinc-
ingly with some of the more recent empirical observations. For pine
trees, the accumulated dose calculated within IAEA (2015) “was
approximately 0.6 Gy for the first 30 day. From data collated for forest
affected by deposition after the Chernobyl accident, UNSCEAR [246]
reported that minor damage characterized by disturbances in growth,
reproduction and morphology of conifers could be observed at doses
from 0.5 to 1.2 Gy” This observation is self-evidently quite consistent
with the morphological abnormalities in conifers reported by
Watanabe et al. (2015).
An issue that both IAEA and UNSCEAR reports were less
equivocal about was the possibility that there would be severe,
regional population level impacts on non-human biota. Such im-
pacts were considered unlikely from both assessments. This is in
contrast to studies (e.g. by Møller et al. Murase et al. and Hiyama
et al.) where substantial population impacts have been reported for
some types of organisms and identified, by the authors of these
works, as being caused by low-levels of radiation.
At a cursory level, there might appear to be some irreconcilable
differences between the conclusions drawn from the theoretical/
desk based studies and some of the empirical observations made
168 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
with regard to effects observed in the field. However, the consis-
tency between those studies characterising environmental radio-
activity levels (and exposure levels) in non-human biota and their
habitat in the field and the input datasets (and dose estimates) used
in desk-based assessments conducted by international organisa-
tions can generally be considered as high. Furthermore, there is no
inconsistency with the findings of UNSCEAR and IAEA vis-a
-vis
published studies concerning molecular, cellular and morpholog-
ical effects at the individual level.
5.2. Consistency between published ad hoc studies
Establishing whether there are discrepancies between studies in
the field focussing on (i) molecular/cellular effects and (ii) popu-
lation level effects is challenging because there is generally, as one
might expect for various studies conducted by distinct research
groups for different reasons, a lack of consistency with regards to
the species considered, experimental designs employed and sta-
tistical analyses applied.
In those studies on mechanisms where cytogenetic and
morphological effects have been observed (e.g. Fujita et al., 2014;
Kubota et al., 2015b; Watanabe et al., 2015), the authors are often
reluctant to make strong inferences regarding repercussions for the
physiological or functional attributes of individuals and/or impacts
on higher levels of biological organisation. This caution is under-
standable in view of the putative difficulties in extrapolating from
sub-cellular effects to impacts at the individual level especially
where knowledge is still rudimentary. Additionally, the concern for
biota is not individually based and furthermore, there is a challenge
to account for confounding factors due to limited, relevant datasets,
and/or the lack of appropriate experimental designs to quantify the
confounding variables.
The situation is different for humans. Chromosomal aberrations
such as dicentrics are used in biological dosimetry and there appear
to be close correlations between some types of chromosomal ab-
errations and cancer in humans (UNSCEAR, 2008). Stronger corre-
lations exist, in part, because some molecular biomarkers are
reasonable predictors of deleterious effects to individuals, the
endpoint of concern in human risk analyses. In contrast, the end-
points for ecological risk are at higher levels of biological organi-
zation, and a linkage between molecular-level effects via a
biomarker and quantifiable impacts observed in populations,
communities or ecosystems has not yet been found (Hinton and
Brechignac, 2004).
Where attempts have been made to establish a connection be-
tween sub-cellular aberrations and effects at higher levels of bio-
logical organisation, results tend to confuse rather than edify. In the
study of Bonisoli-Alquati et al. (2015), focussing on the analysis of
genetic damage and population effects in the same bird species,
low exposures, at 7 mGy/h, did not reveal any effect, although quite
significant population effects were documented. In this regard, the
authors considered that “genetic damage to nestlings does not
explain the decline of barn swallows in contaminated areas.”, which
would appear to be somewhat at odds with the widely held sup-
position that any impacts at the population level will be a conse-
quence of responses to irradiation that occur in the constituent
individuals (ICRP, 2008). However, a lack of increase in genetic
damage (DNA damage) as quantified by the comet assay is not
unexpected considering the very low doses involved and the limit
of sensitivity of the comet assay, which is more than 1 Gy for the
neutral version (Olive, 2009).
5.3. Limitations regarding the various categories of studies
Some further insights into the underlying causes governing the
discrepancies between assessments involving inferences of bio-
logical effects and those studies involving the study of impacts at
the population level may be achieved through a consideration of
the limitations and uncertainties associated with the various cat-
egories of analysis. Extrapolation from individual effects to pop-
ulations and to the structure and function of the ecosystem is not
straightforward. A traditional premise states that spatial and tem-
poral energy deposition patterns set the initial conditions for all
effects and responses to radiation-induced disturbances in all living
organisms (see Goodhead, 1989). Therefore, the level of dose to any
organism (the energy imparted to the body of an organism) and the
number of affected individuals will delineate the ultimate radiation
response of any population. However, interaction between species
and other constituents in the environment affected by radiation
may have indirect implications for ecosystem integrity (Bradshaw
et al., 2014) although such impacts might be difficult to discern
from effects on individuals.
As noted by UNSCEAR (2014), in relation to the desk-top/
theoretical study conducted as part of the Committee's assess-
ment of impacts from the FDNPS on non-human biota, un-
certainties can be substantial and need to be recognized when
interpreting results. As noted above, in both the UNSCEAR and IAEA
assessments, it was particularly difficult to account for short-lived
radionuclides in the initial post-accident period. Although esti-
mates were made for the terrestrial ecosystem, these were
considered highly uncertain. This is important because the critical
period for the delivery of dose, in terms of a potential to cause
harm, would have occurred primarily in the initial phases (first few
months) following the accident. If impacts on non-human biota are
attributable to radionuclide contamination, the exposures and ef-
fects in this early period require the closest of scrutiny and there is
arguably a need to determine accumulated dose in this period (and
possibly even adopt this metric as an independent variable in sta-
tistical analyses) and not just consider dose rates in the longer term.
The synthesis of information from earlier studies (at Chernobyl etc.)
provide evidence for this contention and further suggest ecosys-
tems recover rapidly, by immigration, succession, etc., and that
impacts, if any, will be ephemeral (IAEA, 2006; Deryabina et al.,
2015). Furthermore, there were limitations associated with the
modelling of external doses for the marine environment in the
UNSCEAR study because it was not practicable to include exposures
from sediment in some simulations for various reasons, and the
prolonged input from contaminated groundwater and spill over
from the reactor was not included. As noted by Strand et al. (2014),
the effect on total dose of neglecting sediment exposure ranges
from negligible in the acute phase (dynamic modelling) to a factor
of < 2 in the longer term (monitoring-based assessment). None-
theless, an inadequate characterisation of transfer through benthic
(sediment associated) food-chains might render the application of
dynamic models, as used in UNSCEAR, problematic in the long
term, as discussed above (with reference to Johansen et al., 2015).
Overall uncertainties associated with the types of transfer
models applied in the UNSCEAR and IAEA assessments, particularly
those that include a biological transfer aspect, may be characterised
as being large, as exemplified by Linkov and Burmistrov (2003) in
observing that estimations using different models often differ from
one another by more than an order of magnitude. For terrestrial
models, a substantial uncertainty is associated with exposures to I-
131. As a consequence (lack of early data), neither the method
applied by UNSCEAR nor that applied by IAEA accounted for this
adequately. In contrast, UNSCEAR estimates of dose rates using
empirically derived concentrations of radionuclides in biota had
uncertainties considered (by Strand et al., 2014) to be much lower
(typically < ±35%). Where comparison of terrestrial model pre-
dictions and empirical data was feasible, it was indicated that the
 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
estimates of activity concentrations in organisms could be consid-
ered as being reasonably robust (Strand et al., 2014). The results
from two dynamic marine biota models employed by UNSCEAR and
using the same input datasets exhibited close correspondence. In
addition, a reasonable degree of correspondence between empir-
ical measurements and radionuclide concentrations in biota pro-
duced by models was evident. When compared with modelled data
(except for the drainage channels of the FDNPS and nearby loca-
tions), empirically derived dose rates fell, generally, within an order
of magnitude (Strand et al., 2014).
A pragmatic approach to deal with uncertainty and conse-
quently lend credibility to an assessment involves the use of con-
servative assumptions. This is often the approach taken for
screening assessments when limited information is initially in hand
(IAEA, 2001). Conservatism has been introduced at various points
in the assessments undertaken by the IAEA and UNSCEAR. For
example, calculations were made for the most highly contaminated
locations even when they covered areas that were plausibly too
small to support viable populations of organisms and by adopting
higher end estimates (e.g. using 95th percentiles dose rates for
some calculations made by UNSCEAR).
The inference of effects from the assessments of the IAEA and
UNSCEAR rely on the use of benchmarks in conjunction with a
common knowledge of radiobiology. The dose-rate and dose
values, e.g. as given in UNSCEAR (1996, 2011), are based on an
extensive distillation of (dose-response) information primarily
derived from the radiobiological literature. This literature covers
experimental efforts conducted over many decades and (to a
limited extent) includes analyses of field studies and observations
from earlier, similar events. The benchmarks thus constitute a
synthesis concerning the doses at which biological effects are likely
to be identified. However, the screening levels suggested by
UNSCEAR or ICRP are not without ambiguity because they are based
on information with practically imposed limitations (e.g. it may not
be possible to have studied all organisms present in any given
ecosystem) and primarily relate to well controlled, acute exposure
conditions. The underlying data used for establishing benchmarks,
as exemplified by the FREDERICA database (Copplestone et al.,
2008), has poor coverage for certain wild-life groups, for various
life stages, and for many dose-rate ranges that may be of utility in
drawing inferences with regards to potential environmental im-
pacts. Nonetheless, published data on the exposures and effects on
non-human biota have been evaluated and reported by UNSCEAR
(UNSCEAR, 1996, 2011). The derived conclusions are that it is
improbable that chronic dose rates of less than 100 mGy/h delivered
to the individual organisms considered as being most highly-
exposed would have significant effects for the integrity of the
population with respect to most terrestrial communities and that it
was improbably that maximum dose rates of 400 mGy/h to any
individual of aquatic populations would have any detrimental ef-
fects at the population level. These values are in concurrence with
the values reported elsewhere (e.g. Rose, 1992; IAEA, 1992). It
should be remembered that these benchmarks are, largely, based
on expert judgment, an observation that also applies to the Derived
Consideration Reference Levels (DCRLs) of the ICRP. DCRLs have also
been employed in the interpretation of exposure levels following
the FDNPS accident. The selection of numerical values for DCRLs
was based upon review of literature data by ICRP on the effects of
radiation relevant to the RAPs (ICRP, 2008) and the estimates relate
to the individual level. It is, therefore, essential to not only consider
the spatial and temporal scales to which the values apply, but also
which organisms and life stages are exposed in order to be able to
make any judgement on population and ecosystem impacts in a
specific area.
Both UNSCEAR and IAEA assessments expressed reservations
169
with regards to some of the population studies (e.g. Hiyama et al.,
2012; Møller et al., 2012, 2013), noting that uncertainties with re-
gard to dosimetry, statistics and possible confounding aspects
complicated the substantiation of firm conclusions from the
referred to field studies. Similar views are reflected in comments on
the aforementioned studies from other scientists in recent years
(e.g. Beresford et al., 2012a,b; Ishida, 2013; Copplestone and
Beresford, 2014; Strand et al., 2014). Responses to criticisms
received have also been forthcoming. Mousseau and Møller (2012a)
noted that the statistical models employed in exploring the rela-
tionship between abundance of birds and radiation levels were
robust in the sense that each observation was weighted by sample
size in order to use all data in an unbiased fashion. They also argued
that since samples were taken on the western side of the coastal
mountains it was possible to rule out confounding factors such as
the effect of the tsunami itself on abundances. Finally, although
recognizing that hand held instruments do not necessarily reflect,
in an accurate way, the actual doses received by mobile animals,
they maintained that a strong relationship exists accounting for
more than half the variance between measured body burdens of Cs-
137 and Sr-90 and background radiation measured using such do-
simeters. However, besides a lack of rigorous dosimetry, a question
remains regarding other factors plausibly affecting the abundance
of birds. For example, it is commonly known that barn swallows
breed in buildings in close proximity to humans and domestic farm
animals (Svensson et al., 2009). It would have been of interest if the
influence of such factors had been addressed in the field in-
vestigations of the evacuated areas around both the Chernobyl (see
Smith, 2008) and Fukushima power plants.
Several papers (Hiyama et al., 2013; Nohara et al., 2014; Taira
et al., 2014) provide a comprehensive defence of an earlier publi-
cation detailing possible impacts of radionuclide releases on the
Pale Grass Blue Butterfly (Hiyama et al., 2012). The original paper
had received substantial criticism and the authors attempted to
counter the most important concerns through comprehensive
elaboration of the methodology employed and through the pre-
sentation of more detailed data analyses than previously achieved.
Furthermore, an attempt was made in one particular study (Nohara
et al., 2014) to augment the general earlier findings by studying the
impact of leaf ingestion, contaminated after the accident, on the
larvae of the previously studied butterfly species. The publications’
authors maintain that exposures from Fukushima releases would
have been the cause of mortality and abnormalities for the relevant
butterfly species and that the mutations would have been inherited
by the progeny and that population decreases would have been
considerable in areas near to the NPP. They reject the confounding
factors such as the non-radiation related impact of the tsunami.
There are notably some errors of a technical nature in a subset of
these publications, e.g. Nohara et al. (2014) exemplified by doses
being specified in Becquerels and references being made to inap-
propriate dose response models with respect to the endpoints that
are the subject of the studies (see Copplestone and Beresford,
2014). In line with some other field studies Møller et al., Bonisoli-
Alquati et al. etc, no alternative explanations are provided to the
reported observations despite the fact that the doses, although
improperly assessed, are extremely low and that appropriate con-
trols are lacking.
5.4. Suggestions towards resolving some of the discrepancies
There is a requirement for a robust characterisation of absorbed
dose and dose rates for plants and animals studied in the field in
areas contaminated by the FDNPS releases in order to attribute
biological effects to radiation exposures. Furthermore, it may be
useful to be well acquainted with the applied methodology and to
170 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
identify suitable biomarkers with relatively high sensitivities and
recognize the link between a primary response and the endpoint of
concern, which apparently is not an easy task. It should also be
emphasized that the exposures to biota in the field are by no means
homogeneous, which may add to the above-mentioned uncertainty
in any assessments of dose and dose rates, and the concomitant
biological impact. A robust characterisation acknowledging these
circumstances would facilitate a more convincing link to be made
with the dose-response behaviour of various organism groups
established under controlled laboratory conditions. Dose re-
constructions for (published) field-based data may have the po-
tential to provide more dependable dose-response relationships
(Garnier-Laplace et al., 2015) than originally achieved although
further refinements are clearly necessary in view of unsubstanti-
ated biological responses and the large uncertainties associated
with the aforementioned analysis.
Tools are available, such as ‘tried and tested’ biota dose con-
version coefficients (see Vives i Batlle et al., 2007), and their
application would appear to be a pre-requisite in the generation of
credible dose-response information. Furthermore, interpretations
of results can be challenging in the absence of reliable and repre-
sentative controls. In this regard, the inclusion of appropriate
controls was one of the main quality criteria employed in reviewing
references included in the comprehensive radiation effects data-
base - FREDERICA (Copplestone et al., 2008) albeit that the data
primarily had provenance in laboratory based experiment.
Although the inclusion of controls may be highly desirable, chal-
lenges exist in always being able to find appropriate reference sites
(Landis et al., 2011). In such cases, gradient experimental designs
may be suitable alternatives, capturing a range of exposures, from
high to low, near-background and accounting for patterns in
environmental variables that may exhibit correlation with levels of
contaminants (FCSAP, 2013). Concomitantly, the design of a study
as well as the selected methodology should be appropriate for the
purpose of the investigations. In this respect, the sensitivity of the
applied methods should be considered to avoid misinterpretations
and false results.
The information to hand with regards to the benchmarks
adopted by UNSCEAR and IAEA as described in the preceding sec-
tion pertains to exposures to only one stressor. There is a question
of limitation associated with applicability when information of this
type is extrapolated to infer effects for ecosystems that includes
many stressors (natural and anthropogenic) except ionizing radia-
tion. Interaction with other stressors in the environment could
exacerbate the radiotoxic manifestations by altering the suscepti-
bility of the organisms or induce impairments or alterations in
important biological processes and functions of individual organ-
isms (Eriksson et al., 2010). Interaction with other stressors may
also act as perturbation or disturbance initiators, which spread
through other organisational levels in ecosystems (Bradshaw et al.,
2014). There would seem to be some merit in continuing to treat
the original UNSCEAR (2011) conclusions, pertaining to dose-rates
below which population effects are not likely, as working hypoth-
eses awaiting more elucidation from field studies tailored to anal-
yse the impacts of ionising radiation on populations of wild
organisms interacting under the conditions prevalent within
contaminated ecosystems that includes many different stressors.
The possibly greater radiosensitivity of organisms in the field
compared to those kept under laboratory conditions (Garnier-
Laplace et al., 2013) is of considerable interest but requires
further testing and substantiation.
The studies on potential effects on biota that have emerged
during the five years after the accident warrant some general re-
marks. It takes a long time before precise dose estimates can be
provided after any accident because the sampling and the
subsequent radiometric determinations are time-consuming tasks.
Furthermore, the presence of large data gaps in the first weeks and
months following the accident, as exemplified by the lack of data on
short-lived radionuclides such as 132Te and 132I and a conspicuous
absence of direct radionuclide determinations for many biota cat-
egories in this period, can never be resolved because comprehen-
sive sampling, was not undertaken at that time. The assessment of
doses in the early and intermediate phase rely heavily on models
with their associated uncertainty (UNSCEAR, 2014; Strand et al.,
2014). This augments the requirement for some carefulness in the
interpretation of results pertaining to exposure levels (i.e. accu-
mulated dose and dose-rates). Contemporarily, in the evaluation of
impact with regard to direct observation of biological effects in the
field, the identification and analysis of reliable and representative
controls is commendable although utilization of appropriate
gradient designs (FCSAP, 2013), as considered above, may be
equally valid. This is especially germane, in view of the dosimetry
being unavoidably weaker in the initial phases following an acci-
dent. Furthermore, large groups of organisms (animals) may be
needed for biomonitoring due to the variation in sensitivity be-
tween individuals and species (Abramsson-Zetterberg et al., 1997).
Additionally, as already pointed out, the methodology applied for
the analysis must be relevant for the endpoint under investigation.
An appraisal of efforts in relation to elucidation of the envi-
ronmental impacts of the Fukushima Daichi accident indicate that a
number of aspects, as elaborated upon in detail above, may serve to
confound the establishment of a coherent picture with regard to
the extent, magnitude and type of effects that have been reported
and the overall meaning of such effects in understanding envi-
ronmental impacts. As discussed above, there is an apparent
disparity when one attempts to assess impact based on individuals
or small groups (and the endpoints associated with such assem-
blages) and the assessment of impact based on larger assemblages
such as populations or communities (which are assessed using a
different set of endpoints). Furthermore, it should be remembered
that the focus of protection is placed upon higher organisational
level while the primary response to low doses of ionising radiation
is on cells and tissues of individual organisms. Thus, this seemingly
lack of coherence serves to complicate efforts in relation to con-
textualising the accident in an environmental perspective as well as
exacerbating difficulties in ameliorating the impacts of the acci-
dent. While assessing impacts based on individuals or reference
organisms is in-line with that currently outlined by the ICRP (ICRP,
2008) and others, the divergences between what is assessed and
people's perception of environmental protection indicate the need
for a clearer linkage between impact assessment and environ-
mental concerns.
Distinct conceptual differences appear between the “reference
organism approach” on one side, as used most for current assess-
ments (IAEA, UNSCEAR), and the ecosystem approach” on the other
side, first mentioned in the early 2000s by Brechignac (2001, 2003).
The latter, although not fully developed to a degree that would
allow using it for regulatory purposes, would appear to align more
congruently with a number of the more controversial field obser-
vations and experiments on environmental effects associated with
Fukushima. Bre chignac et al. (2012) previously outlined the
possible advantages of such an ecosystem approach, more suited
than traditional methods to deal with population and ecosystem
effects within assessment of radiation impacts. The authors argue
that such a system would be both complementary to the reference
organism approach as well as being in-line with trajectories
adopted in other areas of environmental protection towards the use
of ecosystem services (see Millennium Ecosystem Assessment,
2003). It is clear, however, from the discussion above that such a
move towards an ecosystem approach in assessing radiation
 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
impacts has faltered despite the efforts of the IUR and others to
integrate the substantial developments made, in this regard, within
other disciplines into the field of radioecology. While at an early
stage of development with respect to assessment of environmental
radiological impacts, it is possible that such an approach may yield
mechanisms that could reconcile, in particular, disparities engen-
dered by assessing effects at different levels of biological organi-
sation. Towards such an end, a series of developments would be
required within a possible ecosystem approach. These de-
velopments would have to follow trajectories towards, amongst
other aspects, assessing inter-related responses to ionizing radia-
tion, as well as delayed effects, on a system level rather an indi-
vidual or group level. In following such a trajectory, the overall
functioning of a system or ecological structure would have to be
considered, possible candidates for assessment of this functionality
including, possibly, the productivity of the system, its energy bal-
ance or the flow and utilisation of nutrients within it. While rec-
ognising that a move towards system level assessments may
potentially offer a means of reconciling the differences evident in
today's systems of environmental assessment, it is apparent that a
parallel effort is required in quantifying the relationships between
(radiation-induced impacts at) the various levels of biological
organisation that currently constitute the backbone of the extant
assessment system. The focussing of more attention on represen-
tatives of trophic levels currently not studied in detail could pro-
vide a means of ameliorating the potential limitations that the
absence of these aspects engender within the current system of
environmental radiological protection. In addition, it will be
important to elaborate upon our understanding of environmental
radiation effects in areas such as hormesis and how ecosystems
adapt and acclimatize to radiation exposure. Such an elaboration
could be well served by the establishment of tighter conduits be-
tween field and laboratory studies, both at system and lower
organisational levels. In this manner, it is perhaps possible that
future incidents will be assessed by methods which stand on
common foundations such that fractures in the supporting struc-
tures upon which the assessment is based are not propagated
through to the end result. A recent symposium elaborated upon a
number of the abovementioned themes (Bre chignac et al., 2016)
resulting in several consensus statements that may provide a way
forward in the coming years (IUR, 2015).
Acknowledgements
This work was supported by the Research Council of Norway
through its Centre's of Excellence funding scheme, project number
223268/F50.
References
Abramsson-Zetterberg, L., Grawe , J., Zetterberg, G., 1997. Spontaneous and radia-
tioninduced micronuclei in erythrocytes from four species of wild rodents: a
comparison with CBA mice. Mutat. Res. 393, 55e71.
Akimoto, S., 2014. Morphological abnormalities in gall-forming aphids in a
radiation-contaminated area near Fukushima Daiichi: selective impact of
fallout? Ecol. Evol. 4 (4), 355e369.
Alexakhin, R.M., 2009. Remediationof areas contaminated after radiation acci-
dents». In: Voigt, G., Fesenko, S. (Eds.), Radioactivity in the Environment.
Elsevier, Oxford, pp. 177e222.
Aliyu, A.S., Evangeliou, N., Mousseau, T.A., Wu, J., Ramli, A.T., 2015. An overview of
current knowledge concerning the health and environmental consequences of
the Fukushima Daiichi Nuclear Power Plant (FDNPP) accident. Environ. Int. 85,
213e228.
Andersson, P.J., Garnier-Laplace, J., Beresford, N.A., Copplestone, D., Howard, B.J.,
Howe, P., Oughton, D., Whitehouse, P., 2009. Protection of the environment
from ionising radiation in a regulatory context (protect): proposed numerical
benchmark values. J. Environ. Radioact. 100, 1100e1108.
Arai, T., 2014. Radioactive Cesium Accumulation in Freshwater Fishes after the
Fukushima Nuclear Accident, vol. 3. Springerplus, p. 479.
171
Avila, R., Beresford, N., Broed, R., Brown, J., Iospje, M., Agüero, A., Robles, B.,
Suan ~ ez, A., 2004. Study of the uncertainty in estimation of the exposure of non-
human biota to ionizing radiation. J. Radiol. Prot. 24, A105eA122.
Ayabe, Y.T., Kanasashi, N. Hijii, Takenaka, C., 2014. Radiocesium contamination of
the web spider Nephila clavata (Nephilidae: Arachnida) 1.5 years after the
Fukushima Dai-ichi nuclear power plant accident. J. Environ. Radioact. 127,
105e110.
Bailly du Bois, P., Laguionie, P., Boust, D., Korsakissok, I., Didier, D., Fie vet, B., 2012.
Estimation of marine source-term following Fukushima Dai-ichi accident.
J. Environ. Radioact. 114, 2e9.
Baumann, Z., Casacuberta, N., Baumann, H., Masque , P., Fisher, N.S., 2013. Natural
and Fukushima-derived radioactivity in macroalgae and mussels along the
Japanese shoreline. Biogeosciences 10, 3809e3815.
BCOJ, 2014. Biodiversity Center of Japan. Official web site about the effect of the
earthquake and the tsunami (in Japanese), Accessed in 2014. http://www.
shiokaze.biodic.go.jp.
Beresford, N.A., Barnett, C.L., Howard, B.J., Scott, W.A., Brown, J.E., Copplestone, D.,
2008a. Derivation of transfer parameters for use within the ERICA Tool and the
default concentration ratios for terrestrial biota. J. Environ. Radioact. 99 (9),
1393e1407.
Beresford, N.A., Barnett, C.L., Jones, D.G., Wood, M.D., Appleton, J.D., Breward, N.,
Copplestone, D., 2008b. Background exposure rates of terrestrial wildlife in
England and Wales. J. Environ. Radioact. 99, 1430e1439.
Beresford, N.A., Barnett, C.L., Brown, J.E., Cheng, J.-J., Copplestone, D., Gaschak, S.,
Hosseini, A., Howard, B.J., Kamboj, S., Nedveckaite, T., Olyslaegers, G., Smith, J.T.,
Vives i Batlle, J., Vives- Lynch, S., Yu, C., 2010. Predicting the radiation exposure
of terrestrial wildlife in the Chernobyl exclusion zone: an international com-
parison of approaches. J. Radiol. Prot. 30, 341e373.
Beresford, N.A., Adam-Guillermin, C., Bonzom, J.-M., Garnier-Laplace, J., Hinton, T.,
Lecomte, C., Copplestone, D., 2012a. Comment on “Abundance of birds in
Fukushima as judged from Chernobyl” by Møller et al. (2012). Environ. Pollut.
169, 136.
Beresford, N.A., Adam-Guillermin, C., Bonzom, J.-M., Garnier-Laplace, J., Hinton, T.,
Lecomte, C., Copplestone, D., Della Vedova, C., Ritz, C., 2012b. Response to au-
thors' reply regarding “abundance of birds in Fukushima as judged from
Chernobyl” by Møller et al. (2012). Environ. Pollut. 169, 139e140.
Bonisoli-Alquati, A., Koyama, K., Tedeschi, D.J., Kitamura, W., Sukuzi, H.,
Ostermiller, S., Arai, E., Møller, A.P., Mousseau, T.A., 2015. Abundance and ge-
netic damage of barn swallows from Fukushima. Sci. Rep. 5, 9432.
Bradshaw, C.L., Kapustka, L., Barnthouse, J., Brown, P., Forbes, Ciffroy V., Geras'kin, S.,
Kautsky, U., Bre chignac, F., 2014. Using an ecosystem approach to complement
protection schemes based on organissssssssm-level endpoints. J. Environ.
Radioact. 136, 98e104.
chignac, F., 2001. Environment versus man radioprotection: the need for a new
Bre
conceptual approach? Radioprot. Colloq. 37 (C1), 161e166.
chignac, F., 2003. Protection of the environment: how to position radioprotec-
Bre
tion in an ecological risk assessment perspective. Sci. Total Environ. 307, 37e54.
chignac, F., Bradshaw, C., Carroll, S., Jaworska, A., Kapustka, L., Monte, L.,
Bre
Oughton, D., 2012. Towards an Ecosystem Approach for Environment Protection
with Emphasis on Radiological Hazards. International Union of Radioecology
Report no 7, Cadarache, France, 89 pp.
chignac, F., Oughton, D., Mays, C., Barnthouse, L., Beasley, J.C., Bonisoli-
Bre
Alquati, A., Bradshaw, C., Brown, J., Dray, S., Geras'kin, S., Glenn, T., Higley, K.,
Ishida, K., Kapustka, L., Kautsky, U., Kuhne, W., Lynch, M., Mappes, T., Mihok, S.,
Møller, A.P., Mothersill, C., Mousseau, T.A., Otaki, J.M., Pryakhin, E.,
Rhodes Jr., O.E., Salbu, B., Strand, P., Tsukada, H., 2016. Addressing ecological
effects of radiation on populations and ecosystems to improve protection of the
environment against radiation: agreed statements from a consensus sympo-
sium. J. Environ. Radioact. 158e159, 21e29.
Brown, J.E., Alfonso, B., Avila, R., Beresford, N.A., Copplestone, D., Pro €hl, G.,
Ulanovsky, A., 2008. The ERICA tool. J. Environ. Radioact. 99, 1371e1383.
Buesseler, K.O., Jayne, S.R., Fisher, N.S., Rypina, I.I., Baumann, H., Baumann, Z.,
Breier, C.F., Douglass, E.M., George, J., Macdonald, A.M., Miyamoto, H.,
Nishikawa, J., Pike, S.M., Yoshida, S., 2012. Fukushima-derived radionuclides in
the ocean and biota off Japan. PNAS 109 (16), 5984e5988.
Copplestone, D., Beresford, N., 2014. Questionable Studies Won't Help Identify
Fukushima's Effects. The Conversation. https://theconversation.com/
questionable-studies-wont-help-identify-fukushimas-effects-26772.
Copplestone, D., Hingston, J.L., Real, A., 2008. The development and purpose of the
FREDERICA radiation effects database. J. Environ. Radioact. 99, 1456e1463.
Deryabina, T.G., Kuchmel, S.V., Nagorskaya, L.L., Hinton, T.G., Beasley, J.C.,
Lerebours, A., Smith, J.T., 2015. Long term census data reveal abundant wildlife
populations at Chernobyl. Curr. Biol. 25 (19), R824eR826.
Eriksson, P., Fischer, C., Stenerlow, B., Fredriksson, A., Sundell Bergman, S., 2010.
Interaction of gamma-radiation and methyl mercury during a critical phase of
neonatal brain development in mice exacerbates developmental neuro-
behavioural effects. Neurotoxicology 31, 223e229.
FCSAP, 2013. Federal Contaminated Sites Action Plan (FCSAP) Ecological Risk
Assessment Guidance. Government of Canada, ISBN 978-1-100-22282-0. http://
www.federalcontaminatedsites.gc.ca/B15E990AC0A8-4780-
912407650F3A68EA/ERA%20Guidance%2030%20Marh%202012_FINAL_En.pdf.
Fujita, Y., Yoshihara, Y., Sato, I., Sato, S., 2014. Environmental radioactivity damages
the DNA of earthworms of Fukushima prefecture. Jpn. Eur. J. Wildl. Res. 60 (1),
145e148.
Fujiwara, K., Takahashi, T., Nguyen, P., Kubota, Y., Gamou, S., Sakurai, S.,
172 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
Takahashi, S., 2015. Uptake and retention of radio-caesium in earthworms
cultured in soil contaminated by the Fukushima nuclear power plant accident.
J. Environ. Radioact. 139, 135e139.
Fuma, S.S., Ihara, I., Kawaguchi, I., Ishikawa, T., Watanabe, Y., Kubota, Y., Sato, Y.,
Takahashi, H., Aono, T., Ishii, N., Soeda, H., Matsui, K., Une, Y., Minamiya, Y.,
Yoshida, S., 2015. Dose rate estimation of the Tohoku hynobiid salamander,
Hynobius lichenatus, in Fukushima. J. Environ. Radioact. 143, 123e134.
Garnier-Laplace, J., Gilek, M., Sundell-Bergman, S., Larsson, C.-M., 2004. Assessing
ecological effects of radionuclides: data gaps and extrapolation issues. J. Radiol.
Prot. 24, A139eA155.
Garnier-Laplace, J., Della-Vedova, C., Gilbin, R., Copplestone, D., Hingston, J.,
Ciffroy, P., 2006. First derivation of predicted-no-effect values for freshwater
and terrestrial ecosystems exposed to radioactive substances. Environ. Sci.
Technol. 40 (20), 6498e6505.
Garnier-Laplace, J., Copplestone, D., Gilbin, R., Alonzo, F., Ciffroy, P., Gilek, M.,
Agüero, A., Bjo €rk, M., Oughton, D.H., Jaworska, A., Larsson, C.M., Hingston, J.L.,
2008. Issues and practices in the use of effects data from FREDERICA in the
ERICA Integrated Approach. J. Environ. Radioact. 99 (9), 1474e1483.
Garnier-Laplace, J., Geras’kin, S., Della-Vedova, C., Beaugelin-Seiller, K., Hinton, T.G.,
Real, A., Oudalova, A., 2013. Are radiosensitivity data derived from natural field
conditions consistent with data from controlled exposures? a case study of
Chernobyl wildlife chronically exposed to low dose rates. J. Environ. Radioact.
121, 12e21.
Garnier-Laplace, J., Beaugelin-Seiller, K., Della-Vedova, C., Me tivier, J.-M., Ritz, C.,
Mousseau, T.A., Møller, A.P., 2015. Radiological dose reconstruction for birds
reconciles outcomes of Fukushima with knowledge of dose-effect relationships.
Sci. Rep. 5, 16594.
Gerask'in, S.A., Fesenko, S.V., Alexakhin, R.M., 2008. Effects of nonhuman species
irradiation after the Chernobyl NPP accident. Environ. Int. 34, 880e897.
Goodhead, D.T., 1989. The initial physical damage produced by ionising radiation.
Int. J. Radiat. Biol. 56 (5), 623e634.
Hasegawa, M., Ito, M.T., Kaneko, S., Kiyono, Y., Ikeda, S., Makino, S., 2013. Radio-
cesium concentrations in epigeic earthworms at various distances from the
Fukushima nuclear power plant 6 months after the 2011 accident. J. Environ.
Radioact. 126, 8e13.
Hayama, S., Nakiri, S., Nakanishi, S., Ishii, N., Uno, T., Kato, T., Konno, F.,
Kawamoto, Y., Tsuchida, S., Ochiai, K., Omi, T., 2013. Concentration of radio-
cesium in the wild Japanese monkey (Macaca fuscata) over the first 15 months
after the Fukushima Daiichi nuclear disaster. PLoS One 8 (7), e68530.
Hinton, T.G., Brechignac, F., 2004. A case against biomarkers as they are currently
used in radioecological risk analyses: a problem of linkage. In: Brechignac, F.,
Howard, B.J. (Eds.), Scientific Trends in Radiological Protection of the Environ-
ment. IRSN, France, pp. 123e136. ISBN: 2-7430-0880-8.
Hinton, T.G., Alexakhin, R., Balonov, M., Gentner, N., Hendry, J., Prister, B., Strand, P.,
Woodhead, D., 2007. Radiation-induced effects on plants and animals. Findings
of the UN Chernobyl Forum. Health Phys. 93, 427e440.
Hiyama, A., Nohara, C., Kinjo, S., Taira, W., Gima, S., Tanahara, A., et al., 2012. The
biological impacts of the Fukushima nuclear accident on the pale grass blue
butterfly. Sci. Rep. 2, 570 (2012).
Hiyama, A., Nohara, C., Taira, W., Kinjo, S., Iwata, M., Otaki, J.M., 2013. The
Fukushima nuclear accident and the pale grass blue butterfly: evaluating bio-
logical effects of long-term low-dose exposures. BMC Evol. Biol. 13, 168.
Hiyama, A., Taira, W., Nohara, C., et al., 2015. Spatiotemporal abnormality dynamics
of the pale grass blue butterfly: three years of monitoring (2011-2013) after the
Fukushima nuclear accident. BMC Evol. Biol. 15, 15.
Hosseini, A., Thørring, H., Brown, J.E., Saxe n, R., Ilus, E., 2008. Transfer of radionu-
clides in aquatic ecosystems: default concentration ratios for aquatic biota in
the ERICA Tool. J. Environ. Radioact. 99 (9), 1408e1429.
IAEA, 1992. Effects of Ionizing Radiation on Plants and Animals at Levels Implied by
Current Radiation Protection Standards. Technical Report Series No. 332. IAEA,
Vienna.
IAEA, 2001. Generic models for use in assessing the impact of discharges of
radioactive substances to the environment. IAEA Saf. Rep. Ser. 19, 216. STI/PUB/
1102.
IAEA, 2006. Environmental Consequences of the Chernobyl Accident and Their
Remediation : Twenty Years of Experience/Report of the Chernobyl Forum
Expert Group ‘Environment’. International Atomic Energy Agency, Vienna.
IAEA, 2015. The Fukushima Daiichi Accident. International Atomic Energy Agency,
2015, Vienna.
ICRP, 2008. Environmental protection: the concept and use of reference animals
and plants. ICRP Publication 108. Ann. ICRP 38 (4e6).
ICRP, 2009. Environmental protection: transfer parameters for reference animals
and plants. ICRP Publication 114. Ann. ICRP 39 (6).
ICRP, 2014. Protection of the environment under different exposure situations. ICRP,
2014 ICRP Publication 124, Ann ICRP 43 (1).
Ishida, K., 2013. Contamination of wild animals: effects on wildlife in high radio-
activity areas of the agricultural and forest landscape. In: Nakanishi, T.M.,
Tanoi, K. (Eds.), Agricultural Implications of the Fukushima Nuclear Accident.
Springer, Tokyo, pp. 119e129, 2013.
IUR, 2000. Dose and Effects in Non-human Systems. Summary of the Work of the
Action Group of IUR. IUR Report 01. International Union of Radioecology,
Østerås, Norway. http://www.iur-uir.org/en/.
IUR, 2002. Protection of the Environment : Current Status and Future Work. IUR
Report 03. International Union of Radioecology, Østerås, Norway. http://www.
iur-uir.org/en/.
IUR, 2012. Towards and Ecosystem Approach for Environment Protection with
Emphasison Radiological Hazards. IUR Report 07. International Union of
Radioecology, Østerås, Norway. http://www.iur-uir.org/en/.
IUR, 2015. IUR Consensus Symposium 2015-Ecological Effects of Radiation on
Populations and Ecosystems. The consensus statements. http://www.iur-uir.
org/en/conferences/id-90-iur-consensus-symposium-2015-ecological-effects-
of-radiation-on-populations-and-ecosystems.
Johansen, M.P., Ruedig, E., Tagami, K., Uchida, S., Higley, K., Beresford, N.A., 2015.
Radiological dose rates to marine fish from the Fukushima Daiichi accident: the
first three years across the North Pacific. Environ. Sci. Technol. 49 (3),
1277e1285.
Kryshev, I.I., Sazykina, T.G., Beresford, N.A., 2005. Effects on wildlife. In: Smith, J.T.,
Beresford, N.A. (Eds.), Chernobyl d Catastrophe and Consequences. Springer
Praxis Books, Chichester, UK, pp. 267e287.
Kubota, Y., Takahashi, H., Watanabe, Y., Fuma, S., Kawaguchi, I., Aoki, M., Kubota, M.,
Furuhata, Y., Shigemura, Y., Yamada, F., Ishikawa, T., Obara, S., Yoshida, S., 2015a.
Estimation of absorbed radiation dose rates in wild rodents inhabiting a site
severely contaminated by the Fukushima Dai-ichi nuclear power plant accident.
J. Environ. Radioact. 142, 124e131.
Kubota, Y., Tsuji, H., Kawagoshi, T., Shiomi, N., Takahashi, H., Watanabe, Y., Fuma, S.,
Doi, K., Kawaguchi, I., Aoki, M., Kubota, M., Furuhata, Y., Shigemura, Y.,
Mizoguchi, M., Yamada, F., Tomozawa, M., Sakamoto, S.H., Yoshida, S., 2015b.
Chromosomal aberrations in wild mice captured in areas differentially
contaminated by the Fukushima Dai-ichi nuclear power plant accident. Environ.
Sci. Technol. 49 (16), 10074e10083.
Kuroda, K., Kagawa, A., Tonosaki, M., 2013. Radiocesium concentrations in the bark,
sapwood and heartwood of three tree species collected at Fukushima forests
half a year after the Fukushima Dai-ichi nuclear accident. J. Environ. Radioact.
122, 37e42.
Landis, W.G., Sofield, R.M., Yu, M., 2011. Introduction to Environmental Toxicology:
Molecular Substructures to Ecological Landscapes, fourth ed. CRC Press.
Larsson, C.M., 2008. An overview of the ERICA integrated approach to the assess-
ment and management of environmental risks from ionising contaminants.
J. Environ. Radioact. 99, 1364e1370.
Linkov, I., Burmistrov, D., 2003. Model uncertainty and choices made by modelers:
lessons learned from the international atomic energy agency model in-
tercomparisons. Risk Anal. 23 (6), 1297e1308.
Matsui, S., Kasahara, S., Morimoto, G., Mikami, O.K., Watanabe, M., Ueda, K., 2015.
Radioactive contamination of nest materials of the Eurasian tree sparrow Passer
montanus due to the Fukushima nuclear accident: the significance in the first
year. Environ. Pollut. 206, 159e162.
Matsushima, N., Ihara, S., Takase, M., Horiguchi, T., 2015. Assessment of radiocesium
contamination in frogs 18 months after the Fukushima Daiichi nuclear disaster.
Sci. Rep. 5, 9712.
Millennium Ecosystem Assessment, 2003. Ecosystems and Human Well-being: a
Framework for Assessment. http://www.maweb.org/en/Framework.aspx.
Mizuno, T., Kubo, H., 2013. Overview of active cesium contamination of freshwater
fish in Fukushima and Eastern Japan. Sci. Rep. 3, 1742.
Møller, A.P., Hagiwara, A., Matsui, S., Kasahara, S., Kawatsu, K., Nishiumi, I.,
Suzuki, H., Ueda, K., Mousseau, T.A., 2012. Abundance of birds in Fukushima as
judged from Chernobyl. Environ. Pollut. 164, 36e39.
Møller, A.P., Nishiumi, I., Suzuki, H., Ueda, K., Mousseau, T.A., 2013. Differences in
effects of radiation on abundance of animals in Fukushima and Chernobyl. Ecol.
Indic. 24, 75e81.
Møller, A.P., Mousseau, T.A., Nishiumi, I., et al., 2015a. Ecological differences in
response of bird species to radioactivity from Chernobyl and Fukushima.
J. Ornithol. 156 (S1), 287e296.
Møller, A.P., Nishiumi, I., Mousseau, T.A., 2015b. Cumulative effects of radioactivity
from Fukushima on the abundance and biodiversity of birds. J. Ornithol. 156
(S1), 297e305.
Mousseau, T.A., Møller, A.P., 2012b. Entomological studies in Chernobyl and
Fukushima. Am. Entomologist 58 (3), 148e150.
Mousseau, T.A., Møller, A.P., 2014. Genetic and ecological studies of animals in
Chernobyl and Fukushima. J. Hered. 105 (5), 704e709.
Mousseau, Møller, 2012a. Reply to response regarding “Abundance of birds in
Fukushima as judged from Chernobyl” by Møller, et al. (2012). Environ. Pollut.
169, 141e142.
MRIJ, 2007. Meterological Research Institute of Japan, a 50-Year History of Artificial
Radionuclides in the Environment: Fallout Containing Strontium-90. Caesium-
137 and Plutonium (2007) (in Japanese). http://www.mri-jma.go.jp/Dep/ap/
ap4lab/recent/ge_report/2007Artifi_Radio_report/Chapter5.htm.
Murase, K., Murase, J., Horie, R., Endo, K., 2015. Effects of the Fukushima Daiichi
nuclear accident on goshawk reproduction. Sci. Rep. 5, 9405.
Nohara, C., Hiyama, A., Taira, W., Otaki, J.M., 2014. The biological impacts of ingested
radioactive materials on the pale grass blue butterfly. Sci. Rep. 4, 4946. http://
dx.doi.org/10.1038/srep04946.
Ochiai, K., Hayama, S., Nakiri, S., Nakanishi, S., Ishii, N., Uno, T., Kato, T., Konno, F.,
Kawamoto, Y., Tsuchida, S., Omi, T., 2014. Low blood cell counts in wild Japanese
monkeys after the Fukushima Daiichi nuclear disaster. Sci. Rep. 4, 5793.
Oguri, K., Kawamura, K., Sakaguchi, A., Toyofuku, T., Kasaya, T., Murayama, M.,
Fujikura, K., Glud, R.N., Kitazato, H., 2013. Hadal disturbance in the Japan trench
induced by the 2011 TohokueOki earthquake. Sci. Rep. 3, 1915.
Ohtsuka, Y., Takaku, Y., Hisamatsu, S., 2015. Background internal dose rates of
earthworm and arthropod species in the forests of Aomori. Jpn. J. Radioanal.
Nucl. Chem. 303, 1441e1445.
 P. Strand et al. / Journal of Environmental Radioactivity 169-170 (2017) 159e173
Okano, T., Ishiniwa, H., Onuma, M., Shindo, J., Yokohata, Y., Tamaoki, M., 2016. Ef-
fects of Environmental Radiation on Testes and Spermatogenesis in Wild Large
Japanese Field Mice (Apodemus Speciosus) from Fukushima. Scientific Reports 6,
23601.
Olive, P.L., 2009. Impact of the comet assay in radiobiology. Mutat. Res. 681, 13e23.
Real, A., Sundell-Bergman, S., Knowles, J.F., Woodhead, D.S., Zinger, I., 2004. Effects
of ionising radiation exposure on plants, fish and mammals: relevant data for
environmental radiation protection. J. Radiol. Prot. 24, A123eA137.
Rose, K.S.B., 1992. Lower limits of radiosensitivity in organisms, excluding man.
J. Environ. Radioact. 15, 113e133.
Sazykina, T.G., 2000. ECOMOD: an ecological approach to radioecological modelling.
J. Environ. Radioact. 50 (3), 207e220.
Shigenobu, Y., Fujimoto, K., Ambe, D., Kaeriyama, H., Ono, T., Morinaga, K.,
Nakata, K., Morita, T., Watanabe, T., 2014. Radiocesium contamination of
greenlings (Hexagrammos otakii) off the coast of Fukushima. Sci. Rep. 4, 6851.
Smith, J.T., 2008. Is Chernobyl radiation really causing negative individual and
population-level effects on barn swallows? Biol. Lett. 4, 63e64.
Sohtome, T., Wada, T., Mizuno, T., Nemoto, Y., Igarashi, S., Nishimune, A., Aono, T.,
Ito, Y., Kanda, J., Ishimaru, T., 2014. Radiological impact of TEPCO's Fukushima
Dai-ichi nuclear power plant accident on invertebrates in the coastal benthic
food web. J. Environ. Radioact. 138, 106e115.
Strand, P., Larsson, C.M., 2001. Delivering a framework for the protection of the
environment from ionising radiation. In: Bre chignac, F., Howard, B.J. (Eds.),
Radioactive Pollutants Impact on the Environment. EDP Sciences: Les Ulis.
Strand, P., Brown, J.E., Woodhead, D.S., Larsson, C.-M., 2000. Delivering a system and
framework for the protection of the environment from ionising radiation. Proc.
Tenth Int. Congr. IRPA 14e19. May. Hiroshima, Japan: IRPA, 2000: P-2a-116, 5 pp.
Strand, P., Aono, T., Brown, J.E., Hosseini, A., Garnier-Laplace, Sazykina, T.,
Steenhuisen, F., Vives I Batlle, J., 2014. Assessment of Fukushima-derived radi-
ation doses and effects on wildlife in Japan. Environ. Sci. Technol. Viewp. 2014
(1), 198e203.
Suzuki, Y., 2015. Influences of radiation on carp from farm ponds in Fukushima.
J. Radiat. Res. 56 (Suppl. 1), i19ei23.
Svensson, L., Mullarney, K., Zetterstrom, D., Grant, P.J., 2009. Collins bird Guide: the
Most Complete Field Guide to the Birds of Britain and Europe. Harper Collins
Publishers, London, 2009 second edition.
Taira, W., Nohara, C., Hiyama, A., Otaki, J.M., 2014. Fukushima's biological impacts:
the case of the pale grass blue butterfly. J. Hered. 105 (5), 710e722.
Taira, W., Iwasaki, M., Otaki, J.M., 2015. Body size distributions of the pale grass blue
butterfly in Japan: size rules and the status of the Fukushima population. Sci.
Rep. 5, 12351.
Tazoe, H., Hosoda, M., Sorimachi, A., Nakata, A., Yoshida, M.A., Tokonami, S.,
Yamada, M., 2012. Radioactive pollution from Fukushima Daiichi nuclear power
plant in the terrestrial environment. Radiat. Prot. Dosim. 152 (1e3), 198e203.
Tsuboi, J., Abe, S., Fujimoto, K., Kaeriyama, H., Ambe, D., Matsuda, K., Enomoto, M.,
Tomiya, A., Morita, T., Ono, T., Yamamoto, S., Iguchi, K., 2015. Exposure of a
herbivorous fish to 134Cs and 137Cs from the riverbed following the Fukushima
disaster. J. Environ. Radioact. 141, 32e37.
173
UNSCEAR, 1996. United Nations Scientific Committee on the Effects of Atomic Ra-
diation. Sources and Effects of Ionizing Radiation. United Nations Scientific
Committee on the Effects of Atomic Radiation, 1996 Report to the General As-
sembly, with scientific annexes. Scientific Annex: Effects.
UNSCEAR, 2000. United Nations Scientific Committee on the Effects of Atomic
Radiation UNSCEAR 2000 Report to the General Assembly, with Scientific An-
nexes, vol. II (EFFECTS; ANNEX J; Exposures and effects of the Chernobyl
accident).
UNSCEAR, 2008. UNITED NATIONS, Effects of Ionizing Radiation (Report to the
General Assembly) UNSCEAR 2006 Report, vol. 1. Scientific Annexes A and B,
Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) UN, New
York, 2008.
UNSCEAR, 2011. United Nations Scientific Committee on the Effects of Atomic Ra-
diation. Sources and Effects of Ionizing radiation, 2008 Report to the General
Assembly, with scientific annexes; Annex E: Effects of ionizing radiation on
non-human biota; United Nations: New York, 2011.
UNSCEAR, 2014. UNSCEAR 2013 Report. UNITED NATIONS, Sources, Effects and
Risks of Ionizing Radiation (Report to the General Assembly), vol. I. Scientific
Annex A: Levels and Effects of Radiation Exposure Due to the Nuclear Accident
after the 2011 Great East-Japan Earthquake and Tsunami, Scientific Committee
on the Effects of Atomic Radiation (UNSCEAR), UN, New York (2014).
UNSCEAR, 2015. Developments since the 2013 UNSCEAR Report on the Levels and
Effects of Radiation Exposure Due to the Nuclear Accident Following the Great
East-Japan Earthquake and Tsunami. A 2015 White Paper to Guide the Scientific
Committee's Future Programme of Work. United Nations Scientific Committee
on the Effects of Atomic Radiation, United Nations, New York, 2015.
Vives i Batlle, J., Balonov, M., Beaugelin-Seiller, K., Beresford, N.A., Brown, J.,
Cheng, J.-J., Copplestone, D., Doi, M., Filistovic, V., Golikov, V., Horyna, J.,
Hosseini, A., Howard, B.J., Jones, S.R., Kamboj, S., Kryshev, A., Nedveckaite, T.,
Olyslaegers, G., Pro €hl, G., Sazykina, T., Ulanovsky, A., Vives Lynch, S.,
Yankovich, T., Yu, C., 2007. Inter-comparison of absorbed dose rates for non-
human biota. Radiat. Environ. Biophysics 46, 349e373.
Vives i Batlle, J., Wilson, R.C., Watts, S.J., Jones, S.R., McDonald, P., Vives-Lynch, S.,
2008. Dynamic model for the assessment of radiological exposure to marine
biota. J. Environ. Radioact. 99 (11), 1711e1730.
Vives i Batlle, J., Aono, T., Brown, J.E., Hosseini, A., Garnier-Laplace, J., Sazykina, T.,
Steenhuisen, F., Strand, P., 2014. The impact of the Fukushima nuclear accident
on marine biota: retrospective assessment of the first year and perspectives.
Sci..Total Environ. 487, 143e153.
Wada, T., Nemoto, Y., Shimamura, S., Fujita, T., Mizuno, T., Sohtome, T.,
Kamiyama, K., Morita, T., Igarashi, S., 2013. Effects of the nuclear disaster on
marine products in Fukushima. J. Environ. Radioact. 124, 246e254.
Watanabe, Y., Ichikawa, S., Kubota, M., Hoshino, J., Kubota, Y., Maruyama, K.,
Fuma, S., Kawaguchi, I., Yoschenko, V.I., Yoshida, S., 2015. Morphological defects
in native Japanese fir trees around the Fukushima Daiichi nuclear power plant.
Sci. Rep. 5, 13232.
Yoshioka, A., Mishima, Y., Fukasawa, K., 2015. Pollinators and other flying insects
inside and outside the Fukushima evacuation zone. PLoS One 10 (11), e0140957.