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Accueil Tous les numéros Volume 58 / Numéro 3 (July - September 2023) Radioprotection, 58 3 (2023) 181-195 Full HTML
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Numéro
Radioprotection
Volume 58, Numéro 3, July - September 2023
Page(s) 181 - 195
DOI https://doi.org/10.1051/radiopro/2023017
Publié en ligne 14 septembre 2023

© The Authors, published by EDP Sciences 2023

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

1 Introduction

The accident at the Fukushima Daiichi Nuclear Power Plant (FDNPP) in March 2011 led to the release of radioactive materials into the environment and exposure to ionizing radiation of humans and environment. Interest in environmental radiological protection has been growing recently, and the latest general recommendations by the International Commission on Radiological Protection (ICRP) highlight the importance of environmental protection (ICRP, 2007). Environmental radiological protection applies to all exposure situations, including emergency and post-accident situations, such as the FDNPP event.

The focus of environmental radiological protection is often on populations at the species or higher levels, although protection objectives depend on specific scenarios. In ICRP Publication 124 (2014), the protection objectives are species conservation, maintenance of biological diversity, and sustaining ecosystem health. Accordingly, the most relevant biological endpoints are those that could lead to changes in population size or structure. The ICRP (2008) introduced a practical approach to environmental radiological protection with its reference animals and plants (RAPs) and derived consideration reference levels (DCRLs). The RAPs are 12 animals and plants that are representative of the major taxonomic families inhabiting major ecosystem (terrestrial, freshwater, marine). The biological effects and risks of RAPs are assessed with doses by comparing with the DCRLs as benchmarks. DCRLs are bands of dose rates within which there is likely to be some chance of deleterious effects of radiation to individuals RAPs. These are derived from knowledge on biological effects. DCRLs can be used as reference points to optimize environmental protection. Under emergency exposure situations, the RAPs and DCRL frameworks may be useful when communicating with stakeholders about radiological situations. Similar approaches are also used by other international organizations (International Atomic Energy Agency (IAEA), United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR)), countries, and research projects, providing a series of benchmark values. The lowest benchmark values are broadly comparable among these organizations and publications (Real and Garnier-Laplace, 2020).

The benchmark values contain uncertainties. Data were obtained in various ways: studies examined high dose rates over short periods of time, and lower dose rates over extended periods of time. Some data were obtained from field observations, others from experiments under controlled conditions. In the current DCRLs, some dose rate bands have insufficient or lacking information (ICRP, 2008). Further, as most data were from studies of small groups of individuals, the relevance of endpoints above the population level is debatable (Real and Garnier-Laplace, 2020). After the Chernobyl nuclear accident in 1986, many studies were conducted and knowledge has been summarized for acute/chronic effects, differences in effects by organism, and remaining issues (IAEA, 2006; Hinton et al., 2007; Beresford and Copplestone, 2011). The consistency of knowledge between field data and laboratory experiments has been discussed, along with data from Fukushima (Real and Garnier-Laplace, 2020). Although UNSCEAR reported that regional impacts on wildlife populations with a clear causal link to radiation exposure were unlikely (UNSCEAR, 2013, 2021), studies are continuing in Fukushima. In addition to the knowledge gained from Chernobyl, new findings from Fukushima will improve the robustness of knowledge on environmental effects and the protection system. As a first step, we present a systematic review of studies conducted in Japan on dose and radiation effects on non-human species after the FDNPP accident. Our review contributes to refining the objectives of the environmental radiological protection approach. These are to identify:

  1. target non-human species and methods of dose estimation;

  2. distributions of doses and comparisons with DCRL;

  3. observed radiation effects.

2 Materials and methods

We consulted the Web of Science database to select publications and completed a manual search. Keywords included “Fukushima,” “exposure,” and “environment or environmental or non-human biota” in varying combinations. We limited results to original articles published in 2011 or later. All references cited in the chapters of “assessment of doses and effects for non-human biota” in Scientific Annexes of the UNSCEAR 2013 and 2020/2021 reports, and in Appendix F of the 2013 report were included. A rater used the following screening criteria:

  • survey was conducted in Japan;

  • target(s) were non-human species;

  • data included dose, not air dose rate or radioactivity;

  • data were obtained in the field, not a laboratory.

After screening titles and abstracts, 51 studies were identified (Web of Science 31: UNSCEAR, 2013, 2: UNSCEAR, 2020/2021, 18). We excluded articles in languages other than English, book chapters, and sources that did not include a dose determination. After removing duplicates, the full text of 46 articles was evaluated against the eligibility criteria, and 27 articles remained (Tab. 1). The detailed study characteristics and main findings of the 27 articles are summarized in the Appendix A.

For each article, we summarized methods of dose estimation, study sites, and data collection periods. Estimated doses were compiled and compared with DCRLs according to RAPs. Finally, we summarized radiation effects, if provided, and estimated doses. We included data evaluated by the UNSCEAR (2013) report’s Appendix F.

Table 1

Properties of the 27 eligible articles.

3 Results

3.1 Characteristics of the articles included in the review

In all, 94 data points were included in the 27 eligible articles and UNSCEAR (2013) report. Figure 1a shows the number of data for each category of non-human species, (i.e., RAPs) and organisms other than RAPs. When several species or different life stages of a species were evaluated in an article, we considered them as different data. If several sampling points were contained in an article, we considered it as one data. Accordingly, the total data number does not correspond to the number of eligible articles. To sort data into RAPs, we used the following procedures. When scientific names were identified and matched RAPs at the “family” level, as defined in ICRP, we assigned them to the corresponding RAP. When the targeted species did not match RAPs at the family level, but were close to the intent of the RAP definitions, we assigned them to the corresponding RAP. For example, data for “pelagic fish” in a freshwater lake were assigned to “trout (freshwater fish).” If author(s) compared the data to RAPs in the article, we applied the correspondence.

Among data about RAPs, the largest number corresponded to flatfish (marine fish) and frogs (amphibians), with 12 and 11 reported, respectively, about 12–13% of the total (Fig. 1a). The next-most frequent data were deer (large terrestrial mammals), rats (small terrestrial mammals), and crabs (marine crustaceans), each with 7 data (7%). Following them, brown seaweed (seaweed), wild grass (small terrestrial plant), and ducks (aquatic birds) accounted for 5 or 6 data, 5–6% of the total. Data for pine trees (large terrestrial plants), bees (terrestrial insects), earthworms (terrestrial annelids), and trout were the least common, with 3 or 4 data (3–4%) each. We noted 22 data reported that did not belong to any RAP, about 22% of the total. These included terrestrial reptiles and marine mollusks.

Figure 1b shows the data by period for data collection from 2011–2019. If a study for one species provided several data obtained in different years, we counted as data for each year. About 30% of data were obtained in 2011. Data gathered by 2012 accounted for about half of the total. The numbers of data tend to decrease with time, with the last collected in 2019. One from the UNSCEAR (2013) report did not identify the collection period; it was omitted from Figure 1b, we expect it was from 2011, 2012, or 2013.

Figure 1c shows each study’s location. All data were taken in Fukushima Prefecture and along the coast. We divided them into four categories: Hamadori, Nakadori, and Aizu (terrestrial areas), and the coast (Fig. 1d). The three terrestrial regions are divided by two mountain ranges, stretching from north to south. They feature topographical, natural, and cultural differences. As shown in Figure 1c, 63% of the data were obtained in Hamadori; 90% were from Hamadori and Nakadori. All marine data were obtained from the port of FDNPP and several kilometers offshore.

thumbnail Fig. 1

Number of data (a) per RAP category and non-assimilated organisms (others), (b) per year in the period 2011–2019 and (c) per studied areas, as spatially distributed in the vicinity of the FDNPP (d).

3.2 Dose estimation

Dose determination methods were mainly classified into equilibrium or dynamic models based on direct measurements of environmental media (Appendix A). Of the eligible 27 articles, except for data from the UNSCEAR (2013) report, 21 used equilibrium models, 5 used dynamic models, and 1 applied electron spin resonance tooth enamel dosimetry. The highest doses were estimated using dynamic models under non-equilibrium conditions immediately after the accident, and in many cases corresponded to data from the marine environment.

Cs-134 and 137Cs were targeted radionuclides for all articles; 16 focused on radiocesium only, but 8 articles also targeted 131I. Four covered other trace radionuclides, such as 110mAg, 3H, and 90Sr. Twenty-six of the 27 articles provided figures of the estimated doses in the manuscripts, and 22 introduce the concept of dose rate (e.g., μGy/h, mGy/h, μGy/d, mGy/d). Nine articles provided accumulated doses in Gy or mGy. Five used both units.

3.3 Distribution of dose rates and comparison with DCRLs

Estimated dose rates corresponding to each RAP are summarized in Figure 2 (articles for each value are in the Appendix A). Data of the 9 articles providing only accumulated doses were not included in Figure 2. For each RAP, estimated dose rates on the left side are those of the immediate aftermath of the accident.

Estimated dose rates for bee and earthworm were below the lower limit of DCRLs. Several dose rates for trout and frog were located within the DCRL bands. The other eight organisms showed estimated doses above the upper limit of DCRLs. Most data correspond to 2011, but two data for rats are from 2012 and later assessments (Appendix A). Although most data above DCRLs were about one order of magnitude higher, one for marine birds (ducks) and several for flatfish, crabs, and brown seaweed in the marine environment exceeded the upper limit of the DCRL band by more than two orders of magnitude.

thumbnail Fig. 2

Comparison between estimated dose rates and DCRLs by RAP types. Estimated dose rates providing a range of values are represented with a bar; those providing representative values are represented by points. Asterisks (*) indicate the availability of information on radiation effects (Tab. 2 and discussed in the following section). For each RAP, estimated dose rates on the left are those of the immediate aftermath of the accident.

3.4 Radiation effects

Among the 27 eligible articles, 14 aimed at dose estimation and 13 articles also contained radiation effects assessments. There were three studies each on deer and rats; two on frogs; and one each on pine trees, wild grass, bees, ducks, and crabs. Eight of these concluded there were some impacts, and five found no effects (Tab. 2).

Nine articles included assessments of radiation effects focused on those at a subcellular level, such as chromosomal aberrations. Three examined individual impacts: Hancock et al. (2019) reported that morphological abnormality and mortality rates for pale grass blue butterflies (Zizeeria maha) increased with accumulation external doses. Yoschenko et al. (2016) showed that canceling the apical dominance of Japanese red pine (Pinus densiflora) correlated with the dose rate. Pederson et al. (2020) did not confirm radiation’s effect on cataract prevalence in wild boars (Sus scrofa) in the difficult-to-return zone. Garnier-Laplace et al. (2015) noted effects at above population levels; they revealed that abundance and species diversity for birds decreased with increasing total doses.

Table 2

Summaries of articles examining dose and radiation effects.

4 Discussion

4.1 Characteristics of data and methods

RAPs are generalized to the family level (ICRP, 2008), but few data in the present articles matched this. Some studies provided integrated results by general characteristics of a category, such as marine fish (e.g., Keum et al., 2014). Assignment according to RAP descriptions, such as deer as large terrestrial mammals, or matching at the class or higher taxonomic levels allowed for more data to be assigned to RAPs. If DCRLs were generalized at a higher taxonomic level than family (e.g., order or class), it would be easier to apply for assessment, especially in such emergency situations.

Dose estimation methods were mostly classified into equilibrium or dynamic models. The equilibrium model assumes an equilibrium environment and is therefore suitable for situations after a certain period from a release. The dynamic model can be used to evaluate the situation immediately after the accident, in an emergency exposure situation. Comprehensive understanding of exposure circumstances and radiation effects after the accident spatiotemporally requires a holistic view of the results from these methods.

4.2 Radiation effect

Some studies assessed radiation effects and dose estimation, and a few identified impacts, but most were at a subcellular level, such as genetic abnormalities (Tab. 2). However, impacts at a subcellular level on the population level are still not well understood (ICRP, 2014; Real and Garnier-Laplace, 2020). Therefore, the effects at the subcellular level in the present review cannot conclude inducing immediate serious effects on population maintenance, one of the main objectives for environmental radiological protection. Further research needs to be developed on the relationship between radiation effects below the individual level and population dynamics of non-human species. Garnier-Laplace et al. (2015) showed that bird abundance in Fukushima decreased with increasing total doses, and the relationship was directly consistent with exposure levels to induce physiological effects in birds. The observed effects corresponding to the estimated doses in the present review agreed with knowledge leading to DCRLs (and other benchmark values).

Some studies gave necessary information by adding additional assessments to existing studies. Garnier-Laplace et al. (2015) examined the relationship between bird abundance and total doses using bird census data (Møller et al., 2015) and air dose information. Hancock et al. (2019) focused on impacts on pale grass blue butterflies (Zizeeria maha) with accumulated dose, using butterfly data from Hiyama et al. (2012).

There were several studies on impact assessment without dose estimation except for the present eligible articles. Watanabe et al. (2015) founded that Japanese fir populations near the FDNPP showed a significantly increased number of morphological defects. Yoshioka et al. (2015) reported that the number of individuals of Apidae species Xylocopa appendiculata was low inside the evacuation zone. The response of non-human species to the Chernobyl accident was a complex interaction among radiation and indirect effects (Hinton et al., 2007). The same would be true for Fukushima. Indeed, Yoshioka et al. (2015) noted that decreases in Xylocopa appendiculata may have been affected not by radiation but by the cessation of anthropogenic activities and the resulting disturbances due to evacuation. As obtaining data retroactively is impossible, examining relations with doses and effects by combining other published data would provide important findings.

4.3 Strengths and limitations

The present study reviewed studies performed in Fukushima after the accident focusing on dose estimation and the potential radiation effects, and we observed that most exposures of non-human species following the Fukushima accident are below the DCRLs (and other benchmarks) adopted for environmental protection. Only a few values were observed above the upper limit of DCRLs, but they were for a limited period. This suggests that there would be no significant impacts on species’ biodiversity and reproduction. In the future, we should continue the surveillance or observation to confirm these results and consolidate the scientific knowledge used to derive DCRLs. The elements collected by our review contribute to refining the objective of an environmental radiological protection approach.

This review has some limitations. Some articles did not include dose rates and provided only cumulative doses, and thus these results were not included in the discussion of agreement with DCRLs. Hancock et al. (2019) showed increased mortality rates in Pale grass blue butterfly and Sproull et al. (2021) detected effects at a subcellular level on Japanese field mice. It should be noted that these studies only provided cumulative doses and thus excluded them from comparison with DCRLs. The dose assessment period was shortly after the accident through 2019, but we did not identify whether exposures were acute or chronic. The present review is limited to field studies, but there are some studies on dose estimation and impact assessment under controlled environments replicating the FDNPP accident (e.g., Fujiwara et al., 2015). Studies on radiation effects without dose estimation were excluded from review; as these studies often have information on air dose rates, it may be possible to reconstruct doses in the future studies.

5 Conclusion

This review provides a summary of current findings on doses to non-human species and the related effects after the FDNPP accident by categorizing RAPs and comparing them with DCRL under the ICRP’s environmental protection system. Most data were collected soon after the accident and close to FDNPP, which was largely affected by the accident. Two main methods for dose estimation were equilibrium or dynamic models based on direct measurements of environmental media. A majority of estimated dose rates were within or below DCRL bands, but several values largely exceeded the DCRLs. Half of the articles estimated dose only, while the other half also contained radiation effects assessments. Eight of these concluded there were some impacts. The observed effects were at the subcellular level, such as chromosomal aberrations, and at the individual or higher level, in the form of morphological abnormalities and declining populations. The observed effects corresponding to estimated dose rates were in agreement with DCRLs. This review will contribute to robust knowledge of the effects on non-human species and improve the environmental radiological protection system.

Conflict of interest

The authors declare that they have no conflicts of interest in relation to this article.

Funding

This work was supported by Environment Research and Technology Development Fund (JPMEERF22S20900) of the Environmental Restoration and Conservation Agency Provided by the Ministry of Environment of Japan.

Ethical approval

No ethical approval was required.

Informed consent

No informed consent was required.

Authors’ contributions

M. Takada: Conceptualization, methodology, investigation, writing original draft. T. Schneider: Conceptualization, supervision, writing, reviewing, editing.

Acknowledgements

We thank Speedtensaku.com (https://www.speedtensaku.com/) for editing a draft of this manuscript.

Appendix A Study characteristics and main findings of the 27 eligible articles.

Reference Animals and plants Focus Study site Period for data collection Targeted radionuclides Method for dosimetry Estimated dose Effect Memo
Anderson et al. (2021) Wild rodents (Apodemus argenteus, Apodemus speciosus) Absorbed dose Namie town 2012, 2014, 2016 134Cs, 137Cs Used actual measured values with the ERICA tool. Evaluated exposure at the time of the survey. 1.3–33 μGy/h N/A Rodent radiocesium data was from Ishiniwa et al. (2019)
Anderson et al. (2022) Wild boar (Sus scrofa) Absorbed dose and germ line mutations Evacuation zone and in nearby areas 2016, 2017, 2018, 2019 134Cs, 137Cs Internal exposure from actual measured values with the ERICA tool and external exposure from air dose rates. Evaluated exposure at the time of the survey. 0.02–36 μGy/h
Lifetime doses: < 0.1–700 mGy		 Did not cause elevated mutation rates in loci.  
de With et al. (2021) Non-piscivorous fish, piscivorous fish, invertebrates, demersal fish, bottom predators, coastal predators Absorbed dose Coastal area located at the discharge area of the Fukushima Dai-ichi NPP and the surrounding regional area 2011, 2012, 2013 3H, 90Sr, 131I, 134Cs, 137Cs Dynamic model to estimate exposure at the accident retrospectively. Non-piscivorous fish: 0.7–6066.3 μGy/d
Piscivorous fish: 3.1–410.1 μGy/d
Invertebrates: 2.7–277 μGy/d
Demersal fish: 2.9–132 μGy/d
Bottom predators: 3.9–207 μGy/d
Coastal predators: 2.7–212 μGy/d		 N/A  
Fuller et al. (2022) Japanese mitten crab (Eriocheir japonica) Absorbed dose and fluctuating asymmetry 4–44 km in distance from the FDNPS 2017 134Cs, 137Cs Used actual measured values with the ERICA tool. Evaluated exposure at the time of the survey. 0.016–37.7 μGy/h No significant relationship between radiocaesium accumulation and fluctuating asymmetry  
Fuma et al. (2015) Tohoku hynobiid salamander (Hynobius lichenatus) Absorbed dose Namie town, Minami-soma city, Otama village, Shimogo town, Showa village 2011, 2012, 2013 134Cs, 137Cs Used actual measured values with the ERICA tool. Evaluated exposure at the time of the survey. Adults: 0.2–47 μGy/h
Overwintering larvae: 0.2–11 μGy/h
Embryos: 6.3–24 μGy/h		 N/A  
Fuma et al. (2017) Mosses, fungi, herbaceous plants, ferns, amphibians, reptiles, bivalves, insects, earthworms Absorbed dose Minami-soma city, Date city, Iitate village, Namie town, Katsurao village, Nihonmatsu city 2011, 2012 134Cs, 137Cs Used actual measured values with the ERICA tool. Evaluated exposure at the time of the survey. Mosses: 9.5–160 μGy/h
Fungi: 4.4–39 μGy/h
Herbaceous plants: 2.4–13 μGy/h
Ferns: 2.6–44 μGy/h
Amphibians: 3.4–76 μGy/h
Bivalves: 4.6–8.5 μGy/h
Insects: 1.9–23 μGy/h
Earthworms: 26–40 μGy/h		 N/A  
Fuma et al. (2019) Amphibians, birds, pelagic fish, phytoplankton, zooplankton, benthic fish, crustaceans, insect larvae, mollusks-bivalves, mollusks-gastropods, reptiles, vascular plants Absorbed dose Exclusion zone 2013, 2014, 2015, 2016, 2017 134Cs, 137Cs Used actual measured values with the ERICA tool. Evaluated exposure at the time of the survey. Amphibians: 0.5–2.9 μGy/h
Birds: 0.9–5.0 μGy/h
Pelagic fish: 1.3–7.1 μGy/h
Phytoplankton: 0.02–0.10 μGy/h
Zooplankton: 0.01–0.08 μGy/h
Benthic fish: 1.4–55 μGy/h
Crustaceans: 0.3–66 μGy/h
Insect larvae: 0.4–132 μGy/h
Mollusks-bivalves: 0.06–57 μGy/h
Mollusks-gastropods: 0.06–60 μGy/h
Reptiles: 1.6–56 μGy/h
Vascular plants: 0.09–66 μGy/h		 N/A  
Garnier-Laplace et al. (2011) Plants, birds, soil invertebrates, forest rodents, marine birds, macroalgae, benthic biota (fish, mollusks, crustaceans) Absorbed dose Iitate village, coastal area located at the Fukushima Dai-ichi NPP 2011 134Cs, 137Cs, 131I ERICA tool. Plants: 1 mGy/d
Birds: 1.5 mGy/d
Soil invertebrates: 2.3 mGy/d
Forest rodents: 3.9 mGy/d
Marine birds: 210 mGy/d
Macroalgae: 4600 mGy/d
Benthic biota (fish, mollusks, crustaceans): 2600 mGy/d		 N/A  
Garnier-Laplace et al. (2015) Birds Absorbed dose, abundance and species diversity 50 km northwest area 2011–2014 134Cs, 137Cs, 131I Estimated exposure at the time of the survey based on actual measured data of soil radioactivity and air dose rate. 0.3–97 μGy/h Abundance and species diversity decreased with increasing total doses. Re-analysed a data subset described in Møller et al. (2015)
Giraudeau et al. (2018) Japanese tree frogs (Hyla japonica) Absorbed dose and carotenoid distribution Kawamata town, Iitate village, Namie town, Nihonmatsu city 2012 134Cs, 137Cs, 110mAg Evaluated exposure at the time of the survey from actual measured samples. 0.18–34.20 μGy/h No effects on tissue carotenoid levels  
Gombeau et al. (2020) Japanese tree frogs (Dryophytes japonicus) Absorbed dose, global genomic DNA methylation level and mitochondrial DNA damages 50 km area around the FDNPP 2013 134Cs, 137Cs Evaluated exposure at the time of the survey from actual measured samples. 0.3–7.7 μGy/h Increase of DNA methylation and mitochondrial DNA damage  
Hancock et al. (2019) Pale grass blue butterflies (Zizeeria maha) Absorbed dose, mortality/abnormality Within a 596-km radius of the Fukushima Dai-ichi
NPP		 2011 134Cs, 137Cs Dynamic model to estimate exposure at the accident retrospectively. Only external exposure is considered. 0.0037–0.10 Gy Genomic instability, morphological abnormality, and mortality rates Data from Hiyama et al. (2012) on the morphological abnormality frequencies. Only external exposure considered.
Horemans et al. (2018) Shepherd’s purse (Capsella bursa-pastoris) Absorbed dose, genome-wide DNA methylation changes Aizu, Nakadori, Hamadori 2016 134Cs, 137Cs Actual measured values with the ERICA tool. Evaluated exposure at the time of the survey. 0.027–38 μGy/h No change in genome-wide methylation levels  
Johansen et al. (2015) Marine fish, greenlings (Hexagrammos otakii) Absorbed dose FDNPP Port, 3 km east of FDNPP 2011, 2012, 2013, 2014 134Cs, 137Cs, 3H, 90Sr, 110mAg, 99Tc, 235U, 239Pu, 240Pu, 241Am, 40K, 210Po, 226Ra, 228Ra, 228Th, 238U Used actual measured values with the ERICA tool. Evaluated exposure at the time of the survey. Marine Fish: 2.0E-02–4.3E+00 mGy/d
Greenlings (Hexagrammos otakii): 2.1E-03–4.4E-02 mGy/d		 N/A  
Kawagoshi et al. (2017) Wild rodents (Apodemus argenteus) Absorbed dose and chromosomal aberrations Iwaki city, Namie town, Okuma town 2012, 2013 134Cs, 137Cs Internal exposure from actual measured values with the ERICA tool. External exposure from air dose rate. Evaluated exposure at the time of the survey. 0.008–3.67 mGy/d
Cumulative dose: 1.3–1387 mGy		 Chromosomal aberrations in the splenic lymphocytes increase with the estimated dose rates and accumulated doses  
Keum et al. (2014) Pelagic fish, benthic fish (flat fish), mollusks, crustaceans (crabs), macroalgae (brown seaweed), polychaete worms (benthic worms) Absorbed dose 30 m north, 330 m south, 15 km offshore 2011 134Cs, 137Cs, 131I Equilibrium model with the measured seawater activity concentrations. Maximum value
Pelagic fish: 4.8E+04 μGy/d
Crustaceans (crabs): 3.6E+06 μGy/d
Benthic fish (flat fish): 3.8E+06 μGy/d
Macroalgae (brown seaweed): 5.2E+06 μGy/d
Mollusks: 6.6E+06 μGy/d
Polychaete worms (benthic worms): 8.0E+06 μGy/d		 N/A  
Keum et al. (2015) Benthic fish, mollusks, crustaceans, macroalgae Absorbed dose In the port of the Fukushima Daiichi Nuclear Power Station About 2.5 years from the accident 134Cs, 137Cs, 131I Dynamic model to estimate exposure at the accident retrospectively. 10−1.0E+06 μGy/d (Read from graph)
Accumulated dose for the initial 3 months
Benthic fish: ca 4.2 Gy
Crustaceans: ca 4.0 Gy
Mollusks: ca 4.4 Gy
Macroalgae: ca 4.5 Gy		 N/A  
Kryshev et al. (2012) Fish, mollusks, algae Absorbed dose 30 km from the NPP and coastal zone near the NPP 2011 134Cs, 137Cs, 131I Dynamic model to estimate exposure at the accident retrospectively. Fish: 11.2–52.3 μGy/h
Mollusks: 12.2–57.6 μGy/h
Algae: 14.2–714.9 μGy/h		 N/A  
Kubota et al. (2015a) Wild rodents (Apodemus argenteus, Apodemus speciosus, Microtus montebelli) Absorbed dose Okuma town 2013 134Cs, 137Cs Internal exposure; actual measured values with the ERICA tool. External exposure; from air dose rate. Evaluated exposure at the time of the survey. 41.3–88.8 μGy/h N/A  
Kubota et al. (2015b) Wild rodents (Apodemus argenteus, Mus musculus) Absorbed dose and chromosomal aberrations Iwaki city, Namie town, Okuma town 2012 134Cs, 137Cs Used actual measured values with the ERICA tool. Evaluated exposure at the time of the survey and cumulative dose with age in days. 0.02–3.5 mGy/d
Cumulative dose: 2.1–1050 mGy		 Chromosomal aberrations increase with dose rate  
Pederson et al. (2020) Wild boars (Sus scrofa) Absorbed dose and cataract prevalence Exclusion zone, Minami-soma city, Fukushima city 2017 134Cs, 137Cs Internal exposure; actual measured values with the ERICA tool. External exposure from air dose rate. Evaluated exposure at the time of the survey and lifetime exposure retrospectively. Upper-bound, lifetime radiation dose: 1–1596 mGy No effect on cataract prevalence  
Sproull et al. (2021) Japanese field mice (Apodemus speciosus) Absorbed dose and changes in proteomic biomarker expression Namie town 2018 134Cs, 137Cs Internal exposure from the radioactivity concentration and external exposure from the air dose rate. Evaluated exposure at the time of the survey. Lifetime dose: 0.01–0.64 Gy Changes in expression of proteomic biomarkers in the serum  
Tagami et al. (2018) Montane Brown (Rana ornativentris), Wrinkled (Glandirana rugosa) Absorbed dose Inawashiro town/Kita-shiobara village, Soma city 2012, 2013, 2015, 2016 134Cs, 137Cs Actual measured values with the ERICA tool. Evaluated exposure at the time of the survey. Frogspawn: 8.3E-08–2.9E-03 μGy/h
Tadpoles: 1.0E-01–5.0E-01 μGy/h
Adults: 1.1E-01–9.7E-01 μGy/h		 N/A  
Toyoda et al. (2019) Cattle Absorbed dose Okuma town, Namie town 2016, 2017 – Electron spin resonance (ESR) tooth enamel dosimetry Cumulative dose: 80–1210 mGy N/A  
Urushihara et al. (2016) Cattle Absorbed dose, plasma protein concentrations, and enzyme activities Within a 20-km radius of FNPP 2011, 2012 134Cs, 137Cs Internal exposure from the radioactivity concentration and external exposure from the air dose rate. Evaluated exposure at the time of the survey. 9.1–155.1 μGy/d
Cumulative dose: 3.5–85.5 mGy		 Modified plasma protein and enzyme levels  
Vives i Batlle et al. (2014) Fish, crustaceans, macroalgae, mollusks Absorbed dose – 2011, 2012 134Cs, 137Cs, 131I Dynamic model to estimate exposure at the accident retrospectively. No values available in the text. Only graphs. N/A As part of an overall assessment for the terrestrial and aquatic ecosystems of Fukushima (Strand et al., 2014: UNSCEAR, 2014)

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Cite this article as: Takada M, Schneider T. 2023. Radiation doses to non-human species after the Fukushima accident and comparison with ICRP’s DCRLs: A systematic qualitative review. Radioprotection 58(3): 181–195

All Tables

Table 1

Properties of the 27 eligible articles.

In the text
Table 2

Summaries of articles examining dose and radiation effects.

In the text

All Figures

thumbnail Fig. 1

Number of data (a) per RAP category and non-assimilated organisms (others), (b) per year in the period 2011–2019 and (c) per studied areas, as spatially distributed in the vicinity of the FDNPP (d).
In the text
thumbnail Fig. 2

Comparison between estimated dose rates and DCRLs by RAP types. Estimated dose rates providing a range of values are represented with a bar; those providing representative values are represented by points. Asterisks (*) indicate the availability of information on radiation effects (Tab. 2 and discussed in the following section). For each RAP, estimated dose rates on the left are those of the immediate aftermath of the accident.
In the text

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