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Feb 14, 2014 - Impacts on wildlife have not yet been comprehensively studied, although early radiation risk estimates have signaled the potential for ...
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Assessment of Fukushima-Derived Radiation Doses and Effects on Wildlife in Japan P. Strand,† T. Aono,‡ J. E. Brown,*,† J. Garnier-Laplace,§ A. Hosseini,† T. Sazykina,∥ F. Steenhuisen,⊥ and J. Vives i Batlle@ †

Norwegian Radiation Protection Authority, Grini næringspark 13, 1332 Østerås, Norway, and Centre for Environmental Radioactivity (CERAD CoE), Norwegian University of Life Sciences, NO-1432 Ås, Norway ‡ National Institute of Radiological Sciences, 4-9-1 Anagawa, Inage-ku, Chiba 263-8555, Japan § Institute for Radioprotection and Nuclear Safety, IRSN/DEI/SECRE, Cadarache, Building 159, 13115 Saint Paul lez Durance Cedex, France ∥ State Institution Research and Production Association Typhoon, 4 Pobedy Strasse, Obninsk, Kaluga Region 249038, Russian Federation ⊥ Arctic Centre, University of Groningen, Groningen, The Netherlands @ Biosphere Impact Studies, SCK·CEN, Boeretang 200, 2400 Mol, Belgium S Supporting Information *

ABSTRACT: Following releases from the nuclear accident at the Fukushima-Daiichi Nuclear Power Station (FDNPS), contention has arisen over the potential radiological impact on wildlife. Under the auspices of the United Nations Scientific Committee on the Effects of Atomic Radiation, a suite of recently developed approaches was applied to calculate exposure and thereafter infer effects on wildlife through comparison with compiled dose−response relationships. Only macroalgae (accumulated dose of 7 Gy) substantially exceeded its corresponding benchmark. We inferred that although effects on sensitive end points in individual plants and animals might have occurred in the weeks directly following the accident in relatively contaminated areas, impacts on population integrity would have been unlikely because of the short duration of the most highly elevated exposures. The conclusions of the assessment are incongruous with recent field observations of effects on some animal species, the cause of which has been reportedly exposures from FDNPS releases.



INTRODUCTION The accident at the Fukushima-Daiichi Nuclear Power Station (FDNPS) on March 11, 2011, led to very significant releases of radioactive substances and was allocated the highest level of 7 (“Severe Accident”) on the International Nuclear Event Scale. Estimates for atmospheric releases of radionuclides varied, for example, falling in the ranges of 6.1−62.5 PBq and 65−200 PBq for 137Cs and 131I, respectively.1 The protection of human health was paramount, with an evacuation order to a radius of 20 km from the FDNPS being given on March 12, 2011. Impacts on wildlife have not yet been comprehensively studied, although early radiation risk estimates have signaled the potential for ecological consequences.2 To assess the impact of radioactive releases on the environment, monitoring data representative of the first year after the accident and compiled by the United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) were used, along with other relevant reports and published scientific papers. The data set was comprehensive, consisting of more than 2000 soil, 4700 seawater, and 4500 © 2014 American Chemical Society

biota data points. Many more data have subsequently been published following this initial compilation. The radiation exposures were considered in terms of the more dynamic, “intermediate” phase after the accident (approximately first 3 months) where short-lived radioisotopes such as 131I cannot be neglected and the “late” phase (from 3 months to 1 year after the accident) where the external exposure was largely dominated by 134Cs and 137Cs. The areas considered in detail were those of highest radioactive deposition, i.e., areas geographically constrained within the Fukushima Prefecture and any neighboring prefectures some 100 km distant from the FDNPS covering a land area of 7000 km2 and extending to 30 km off the Fukushima coast. The UNSCEAR has previously concluded3 that “chronic dose rates of less than 100 μGy h−1 to the most highly exposed Received: Revised: Accepted: Published: 198

November 15, 2013 February 14, 2014 February 14, 2014 February 14, 2014 dx.doi.org/10.1021/ez500019j | Environ. Sci. Technol. Lett. 2014, 1, 198−203

Environmental Science & Technology Letters

Letter

Figure 1. Interpolated map of total weighted absorbed dose rates for a large mammal. Calculations were based on 131I, 134Cs, and 137Cs soil deposition empirical data measured in June and July 2011 (converted to soil concentrations using density and sampling depth) and corrected for radioactive decay to mid-March 2011. Koriyama City and Okuma Town are marked on the map.

Figure 2. Exposures vs benchmarks for selected terrestrial and marine organisms in areas affected by FDNPS releases. (a) Total weighted absorbed dose rates in the late phase with respect to chronic exposure benchmarks. (b) Accumulated doses during the first 90 days after the accident with respect to acute exposure benchmarks. The availability of data allowed wild boar to be selected as representative mammals for which more detailed assessment (including grouping/clustering analyses to provide a better indication of population groups) could be performed.

individuals would be unlikely to have significant effects on most terrestrial communities” and “that maximum dose rates of 400 μGy h−1 to any individual in aquatic populations of organisms would be unlikely to have any detrimental effects at the population level”. Other benchmark dose rates have been developed, most notably the International Commission on Radiological Protection’s Derived Consideration Reference Levels (DCRLs), mainly for guiding efforts to protect the environment,4−6 which are broadly consistent with those provided by the UNSCEAR. Whereas DCRLs are dose rate bands within which there is some chance of deleterious effects occurring to individuals, the UNSCEAR benchmarks pertain to higher levels of biological organization. These benchmarks provide a means of interpreting the significance of calculated dose rates in terms of potential biological impacts. Consistency

has been introduced by comparing intermediate phase doses with acute exposure benchmarks and late phase dose rates with chronic exposure benchmarks. In this work, some highlights and important conclusions from the comprehensive analyses undertaken by the UNSCEAR have been extracted for presentation.



MATERIALS AND METHODS The ERICA Tool7 was used to calculate radiation dose rates for non-human biota. The methodology consisted of (a) selecting representative species (primarily based around ERICA reference organisms) and radionuclides, i.e., 134Cs, 137Cs, 89Sr, 90 Sr, 239Pu, 240Pu, 129mTe, 110mAg, and 131I; (b) conducting the assessment preferably using actual radionuclide concentrations in biota, measured over time and space; additionally or 199

dx.doi.org/10.1021/ez500019j | Environ. Sci. Technol. Lett. 2014, 1, 198−203

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Figure 3. Predicted dynamics of marine system exposures. Dose rates with time in the South Channel (∼1.3 km south of the unit 3-4 discharge channel of FDNPS; coordinates of {37.4153, 141.0339}) using the ECOMOD12 and CR model.

broad range of contamination levels observed in this area, were considered to be indicative of the most highly exposed individuals for the assessment based on measurements in wildlife. Dose rates were calculated from whole body and soil radionuclide concentration measurements (Figure 2a) and were approximately 1 order of magnitude greater than exposures from naturally occurring radionuclides in the environment (excluding inhalation doses from Rn and its daughters).23 Dose rates have also been calculated using the mean deposition levels, derived from the UNSCEAR database, for Okuma Town and default transfer parameters. Okuma Town was selected because it was a small and relatively contaminated area and might thus characterize an area where the most highly exposed individuals of various biota populations resided. The dose rates estimated for mid-June 2011 (Figure S1 of the Supporting Information) were 71 μGy h−1 for deer and large mammals and 26 μGy h−1 for grass (Figure 2a). Deer and large mammals were the most exposed biota for an assessment including the full suite of radionuclides specified in the methodology section. Regional dose rates for this organism group were generally substantially lower (Figure 1). Although the dose rate for mammals fell above the DCRL and at a level where minor cytogenetic effects could occur, it fell below a level considered to have significant impacts on terrestrial communities (i.e., 100 μGy h−1). Once this has been inferred, it is important to note that the dose rates pertained to averages, albeit over a relatively small, highly contaminated area, so there is a possibility that some individual organisms may have been exposed to levels higher than those calculated. Nonetheless, the comparison of these extreme values with benchmarks was deemed inappropriate as the corresponding areas were incongruent with population sustainability. Dose rates of 300 μGy h−1 were estimated using an equilibrium-based approach for soil-dwelling organisms in Okuma Town during the intermediate phase of the accident. Through application of a kinetic model, a maximal dose rate of 370 μGy h−1 (0.2 Gy accumulated over 30 days) was estimated for deer, a value slightly higher than corresponding values derived using an equilibrium-based approach, and such exposures occurred within the first week following the main

alternatively (c) conducting an equilibrium-based assessment using concentration ratios8,9 to derive radionuclide concentrations in biota from soil and water or (d) using kinetic models10−13 to calculate time-dependent concentrations in biota based on measured concentrations in media; and (e) performing dose calculations using dose conversion coefficients (DCC, in micrograys per hour per becquerel per kilogram) and making projections of dose rate as a function of time from which cumulative doses can be calculated. From this information, risks to non-human biota could be assessed through comparison with compiled effects data and benchmarks.3−6,14−17 Where direct determinations of radionuclide concentrations in terrestrial animals were available, some interpolation of deposition data among measurement points was required to predict deposition levels at locations where biota had been sampled and over their home range. Empirical Bayesian Kriging was used to construct interpolated radionuclide deposition and absorbed dose rate maps for the Fukushima area.18−20 In the dose calculations, occupancy factors (i.e., fraction of time that an organism spends at a specified position in its habitat) for organisms were selected to characterize simplified yet realistic exposures. Weighted total (i.e., sum of internal and external exposure accounting for radiation quality) absorbed dose rates (in micrograys per hour) were derived using default radiation weighting factors in line with previous analyses3 (i.e., 10 for α radiation and 1 for γ and β). The dosimetric calculations underpinning the derivation of DCCs are explained elsewhere.21,22



RESULTS AND DISCUSSION

Interpolated maps of dose rates estimated for a large mammal are shown in Figure 1. During the late phase of the accident (June 2011), 95th percentile dose rates (in a range) between 1.2 and 2.2 μGy h−1 for terrestrial mammals and birds were estimated for Koriyama City some 50−100 km west of the FDNPS. Koriyama City was selected as being a representative area for which direct determinations of radionuclide activity concentrations in biota were available. Ninety-fifth percentile dose rates, based on the 200

dx.doi.org/10.1021/ez500019j | Environ. Sci. Technol. Lett. 2014, 1, 198−203

Environmental Science & Technology Letters

Letter

unsubstantiated assumptions, such as those associated with selection of diet for mammals, the uncertainties for dynamic terrestrial modeling may be even greater than this. A substantial uncertainty is associated with exposures of the mammalian thyroid to 131I. The applied method does not account for this adequately; thus, further consideration is provided in section S4 of the Supporting Information. In contrast, where dose rates were estimated using directly measured concentrations of radionuclides in biota, uncertainties are much lower (typically less than ±35%). Where comparison between terrestrial model predictions and empirical data was possible, the indication is that the prognoses of activity concentrations in biota were reasonably robust (Figure S3 of the Supporting Information). The results from two dynamic models for marine biota, D-DAT and ECOMOD, using the same data sets corresponded closely. Furthermore, there was a degree of correspondence between modeled radionuclide concentrations in biota using D-DAT and measurements by Greenpeace26 for the period of May 3− 10, 2011, although the degree of agreement is not so strong because of incomplete overlap between sampling and modeling stations. When compared with modeled data (except for the FDNPS drainage channels and most adjacent locations), the dose rates based on measurements were generally within 1 order of magnitude. Conflicting Evidence with Field Studies. An apparent negative correlation was reported by Møller and co-workers27 between the levels of ambient radiation dose rate and the abundance of common birds in the Fukushima area. The abundances of several invertebrates and birds were determined28 at more than 1000 sites in the vicinity of the power stations at Chernobyl and Fukushima. While all taxa showed significant declines in abundance with an increasing level of ambient radiation dose in the Chernobyl case, only three of seven taxa showed such an effect for the Fukushima case. The impacts of FDNPS releases on morphological and genetic characteristics of the pale grass blue butterfly have also been studied.30 First-voltine adults were collected in the Fukushima area in May 2011. Some of these individuals showed relatively mild abnormalities. Offspring from the first-voltine females showed more severe abnormalities, which were inherited by the subsequent generation. Furthermore, adult butterflies collected in September 2011 showed abnormalities more severe than those of adult butterflies collected in May. The authors concluded that artificial radionuclides from the FDNPS caused physiological and genetic damage to this species and that the cumulative effects of exposures could have resulted in deterioration of the population. In the field studies cited above, uncertainties with regard to dosimetry and possible confounding factors (including the impact of the tsunami itself) make it difficult to substantiate firm conclusions. Some of the studies27,28 have been questioned, leading to considerable debate.29 Furthermore, the main body of scientific data does not support the appearance of such effects at the dose rates recorded. Most notably, in the butterfly study,30 a manifestation of similar effects under laboratory conditions required radiation exposures that were orders of magnitude higher than those observed in the field. The dose rates derived in the UNSCEAR’s theoretical assessment are not indicative of severe population impacts from radiation in contrast to the aforementioned field studies. Summary. The Fukushima-Daiichi nuclear accident and subsequent radioactive releases into the environment led to estimated exposures for the intermediate phase that may have

deposition event. Inclusion of the very short-lived radioisotopes 132 I and 132Te indicates that dose rates may have been as high as 1 mGy h−1 for some organisms over short periods (hours to days). An exemplified single estimate of accumulated dose incorporating these contributions nonetheless suggests that exposure levels were somewhat below corresponding acute effects benchmarks (Figure 2b). However, changes in some biomarkers may occur at such doses, especially in mammals.15 For the marine ecosystem, dose rates in the late period from May 10, 2011, to August 12, 2012, for coastal locations where biological samples were available, were low relative to effects benchmarks (Figure 2a). The highest dose rates, from compiled arithmetic means of all organism groups, were commensurate with background exposures arising from the presence of naturally occurring radionuclides in the marine environment.24 The highest dose rates for the entire marine assessment were calculated for the intermediate phase (before May 10, 2011, when biological samples were unavailable) using monitored radionuclide concentrations in seawater, via two dynamic models.10,12 The maximal dose rate for fish, using the D-DAT model,10 of approximately 140 μGy h−1 occurred within the first month in the Northern drainage channel (∼30 m north of the unit 5-6 discharge channel at the FDNPS). The accumulated dose over 1 year was approximately 0.32 Gy. Maximal calculated exposures for macroalgae (>20 mGy h−1) at the same location occurred 23 days after the accident but fell rapidly. The accumulated dose for macroalgae over 1 year was approximately 7 Gy. Reported benchmarks available for comparison3,5,17 indicate that the calculated doses, other than potentially for macroalgae very close to the discharge point, fell substantially below those at which observable effects on populations would be expected (Figure 2b). Typical outputs from dynamic model simulations for the marine environment are shown in Figure 3. Uncertainties. The assessment of the effects of the Fukushima-Daiichi nuclear accident on non-human biota is inevitably subject to a degree of uncertainty. In particular, it was difficult to account for short-lived radionuclides in the initial postaccident period. Although estimates were made for the terrestrial ecosystem, these were considered highly uncertain. Furthermore, there were limitations associated with the modeling of external doses for the marine environment because it was not practicable to include exposures from sediment in some simulations because of the mismatch between biological and sediment sampling stations and dynamic model limitations. The effect on the total dose of neglecting sediment exposure ranges from negligible in the acute phase (dynamic modeling) to a factor of