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Radiation Protection Dosimetry (2015), Vol. 163, No. 2, pp. 238 – 250 Advance Access publication 14 May 2014

doi:10.1093/rpd/ncu158

FUKUSHIMA NUCLEAR ACCIDENT: PRELIMINARY ASSESSMENT OF THE RISKS TO NON-HUMAN BIOTA Abubakar Sadiq Aliyu1,2,*, Ahmad Termizi Ramli1, Nuraddeen Nasiru Garba1, Muneer Aziz Saleh1, Hamman Tukur Gabdo1 and Muhammad Sanusi Liman2 1 Department of Physics, Universiti Teknologi Malaysia, UTM, 81310 Skudai, Johor, Malaysia 2 Department of Physics, Nasarawa State University, Keffi, Nigeria *Corresponding author: [email protected] or [email protected]

This study assesses the ‘radio-ecological’ impacts of Fukushima nuclear accident on non-human biota using the ERICA Tool, which adopts an internationally verified methodology. The paper estimates the impacts of the accident on terrestrial and marine biota based on the environmental data reported in literature for Japan, China, South Korea and the USA. Discernible impacts have been detected in the marine biota around Fukushima Daiichi nuclear power plant. This study confirms that the Fukushima accident had caused heavier damage to marine bionts compared with terrestrial flora and fauna, in Japan.

INTRODUCTION On 11 March 2011, a 9.0 Richter scale earthquake and subsequent tsunami occurred in Tohoku, Japan. The 14-m-high tsunamis overrun the Fukushima Nuclear Power Plant (FNPP) in the northeast of Japan causing the release of radioactive materials into the environment. This was as a result of the reactor rod meltdown and multiple explosions of hydrogen gas in the reactors after the backup cooling system failed. The accident led to the atmospheric and oceanic dispersion of fission products around Japan and other parts of the World. This paper estimates the impacts of the accident to nonhuman biota in Japan and other countries (namely, USA, China and South Korea). This preliminary assessment is based on the measurement data reported in literature for the study countries. The radio-ecological impact assessment was based on the D-ERICA-integrated approach to the assessment and management of environmental risks from ionising radiation. Because of the significant number of nuclear power plants (NPPs) and their potential to increase in the future, a radio-ecological impact assessment of Fukushima nuclear accident is important. Several studies have tracked the atmospheric transport patterns and deposition of radionuclides from Fukushima(1 – 10). However, only a few of the known published studies considered the impacts of the accidents on non-human biota(7, 8, 11 – 15). Kim et al.(7) concluded that the accident does not have any significant impact on environmental radioactivity (hence to ecology) in Korea. Buck(8) reported that the radiation in the ocean will be diluted within Japanese coast; however, exposed marine organism and contaminated tsunami debris plume will likely reach the USA. Wu et al.(11) examine the impact of the accident on marine environment in China Sea and reported that 137Cs ranged from 0.75 + 0.07 to

1.43 + 0.08 Bq m23. Wada et al.(13) assessed the impact of the accident on marine product in Fukushima and concluded that the total activity concentrations of Cs in the marine products have decreased significantly. However, higher activity concentrations have been observed in shallower waters south of the Fukushima nuclear plant. Wada et al.(13) emphasised that long-term monitoring of marine biota off Fukushima, especially around the nuclear plant, will be necessary to restart the coastal fishery. Chen(14) measured the level of radioactivity in fish products from the adjacent prefectures and reported that the activity concentrations of 134Cs, varied from 0.1 to 338 Bq kg21 (average: 11 Bq kg21); for 137Cs the activity concentrations varied from 0.1 to 699 Bq kg21 (average: 18 Bq kg21). The International Commission on Radiological Protection (ICRP) Task Group 84(16), which was saddled with the responsibility of compiling the lessons learned from the Fukushima accident with respect to the ICRP system of radiological protection, suggests that studies are needed to evaluate the marine environmental impact of the accident on marine biota, as most of the radioactivity released was deposited into the oceans. A recently published study(13) assessed the impacts of the accident on marine biota in Japan. Thus, a preliminary estimation of the dose to terrestrial and both marine and freshwater biota using the ICRP recommendations for reference animals and plants(17, 18) is timely and relevant. A preliminary estimation of the source terms of radioactive caesium (137Cs) and iodine (131I) was first reported by Chino et al.(2) They adopted the use of atmospheric dispersion modelling and reverse estimation method to compute the source terms. Their results were comparable with that of the Ministry of Education, Culture, Sports, Science and Technology,

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Received 8 March 2014; revised 14 April 2014; accepted 16 April 2014

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Japan (MEXT). They(2) verified the validity of the techniques adopted in later studies(4, 10), which compares the air sampling data with the atmospheric dispersion calculations. The results obtained by the three studies were quite comparable. Other studies(1, 6 – 8, 11, 12, 19, 20) present the radiotoxicity and risk assessments of detected fission products in Japan and other countries. MATERIALS AND METHODS

Description of the ERICA Tool Environmental Risks from Ionizing Contaminants: Assessment and Management (ERICA) project (which produced ERICA Tool, a software program with supporting databases, which guides users through the assessment process) was co-funded by the European Union and fifteen organisations in seven European Countries, between 2004 and 2007. The aim of this project was to develop an approach whereby the environmental impacts of ionising radiation could be quantified and to ensure that decisions on environmental issues give appropriate weight to the exposure, effects and risks from ionising radiation. Incorporated in the modelling system are databases on transfer, dose conversion coefficients and radiation effects on nonhuman biota that have been developed specifically for the purpose of the integrated Approach(21). The aims are to conduct species sensitivity to radiation, on the basis of a universal screening dose rate criterion of 10 mGy h21. There are three elements of the ERICA Integrated Approach, which are to aid decision-making related to the environmental effects of ionising radiation; the elements have been combined with the ERICA Integrated Approach. These are assessment of environmental exposure and effects using the ERICA Tool, risk characterisation and management of environmental risks(22, 23). Tier 1 is designed to be simple and conservative, requiring a minimum of input data and enabling the user to exit the process and exempt the situation from further evaluation, provided the assessment meets a predefined screening criterion. Here, the predefined screening dose is used to calculate the environmental media concentration limits (EMCLs) for all reference organism/radionuclide combinations. The risk quotient (RQ) is then obtained by comparing the input media concentrations with the most restrictive EMCL for each radionuclide. These are defined by the following equation:

ACn EMCLn

ð1Þ

where AC is the measured activity concentration in the medium for a specific radionuclide n. If RQ , 1, then the probability of exceeding the benchmark is acceptably low (,5 %) and this serves as the justification of terminating the risk calculations at this stage. In a situation where RQ . 1, there is .5 % probability that the benchmark has been exceeded and further assessment is recommended (Tier 2). Tier 2: this allows the modeller to be more interactive, to change the default parameters (screening dose rate and radionuclides) and to select specific reference organisms. The evaluation is performed directly against the screening dose rate, with the dose rate and RQs generated for each reference organism selected for assessment. A ‘traffic light’ system is used to indicate whether the situation can be considered: (1) Green: of negligible concern (with a high degree of confidence); (2) Yellow: of potential concern, where more qualified judgments may need to be made and/or a refined assessment at Tier 2 or an in-depth assessment in Tier 3 performed and (3) Red: of concern, where the user is recommended to continue the assessment, either at Tier 2 if refined input data can be obtained or at Tier 3. Decisions to exit an assessment given outcomes (2) and (3) should be justified, for example by using information from FREDERICA provided in the Tool as ‘look-up effects tables’ for different wildlife groups. The basic equations for Tier 2 assessment are presented in Equations (2) and (3): X j _j ¼ Ci  DCCjint; j ð2Þ D int i

where Cij is the average concentration radionuclide i in the reference organism j (Bq kg21 fresh weight); DCCjint; i is the radionuclide-specific dose conversion coefficient for internal exposure (mG h21 per Bq Kg21 fresh weight). X X _j ¼ vz Cziref  DCCjext; zi ð3Þ D ext z

i

where v is the occupancy factor of the organism j at location z; C ziref is the average concentration of radionuclide i in the reference media in a given location z and is dose conversion coefficient for external exposure. _ J is assessed by summing The total dose rate D Tot Equations (2) and (3). Two RQs [expected (RQexp) and conservative (RQcons)] are obtained at the end of this assessment. If RQexp  1, the screening dose rate has been exceeded and assessment should continue to Tier 3; If

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Source term activity concentrations in air, soil and sea water in Japan, China, South Korea and the USA have been adopted in the assessment. ERICA Tool is employed due to its robustness in environmental radiological impact assessment.

RQn ¼

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RQcons  1 or RQexp , 1, there is substantial probability that the screening dose rate has been exceeded the assessment needs to be reviewed. If RQcons ,1, there is low probability that the screening dos rate has been exceeded. In this case, the environmental risk is arguably negligible and the assessment is terminated at this stage. Since the aim of Tier 2 is to outline situations where there is a very low probability that the dose to any selected organism exceeds the adopted screening dose rate, the screening test is implemented as follows:

In Tier 2, the total RQ is calculated as in the following equation: X

RQ ¼

DTot Dlim

ð4Þ

where DTot is the total dose rate and Dlim is the screening dose rate.

Figure 1. Underlying approach to Environment Impact Assessment in ERICA(24).

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(1) An expected value of the RQ (RQexp) is calculated using expected (or best estimate) values for the input data and the parameters; (2) The 95th or 99th percentile of the RQ is estimated by multiplying the expected value of the RQ by an uncertainty factor (UF) of 3 or 5, respectively, and it is reported as the conservative RQ (RQcons). The UF is defined as the ratio between the 95th or 99th percentile and the expected value of the probability distribution of the dose rate (and RQ).

Tier 3 is a probabilistic risk assessment in which uncertainties within the results may be determined using sensitivity analysis. The assessor can also access up-to-date scientific literature (which may not be available at Tier 2) on the biological effects of exposure to ionising radiation in a number of different species. Together, these allow the user to estimate the probability (or incidence) and magnitude (or severity) of the environmental effects likely to occur and, by discussion and agreement with stakeholders, to determine the acceptability of the risk to non- human species. Situations, which give rise to a Tier 3 assessment, are likely to be complex and unique, and it is therefore not possible to provide detailed or specific guidance on how the Tier 3 assessment should be conducted. Furthermore, a Tier 3 assessment does not provide a simple yes/no answer nor is the ERICAderived incremental screening dose rate of 10 mGy h21 appropriate with respect to the assessment endpoint. The requirement to consider aspects such as the biological effects data within the FREDERICA database, or to undertake ecological survey work, is not straightforward and requires an experienced, knowledgeable assessor or consultation with an appropriate expert (22). A pictorial representation of the ERICA Integrated Approach is shown in Figure 1. It is important to note that in the ERICA Tool, the user can choose between three different screening values (the ERICA dose rate screening value (10 mG h21), the UNSCEAR value and a value defined by the user).

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Detailed descriptions of the ERICA Tool and the integrated approach for environmental impact assessment have been presented in literatures(21 – 23, 25, 26). RESULTS AND DISCUSSION

Terrestrial assessments Discussion for terrestrial assessment in Japan The total dose rate for the selected terrestrial organisms in Japan is presented in Figure 2. The organisms with highest dose rates are deer, rat and reptile whereas the minimum dose rates were those of bird egg and tree. The conservative RQs for deer, rat and reptile were more than unity (Figure 3), and these were the organisms with highest dose rates in Japan. This shows that for other terrestrial animals, there is no substantial probability that the screening dose rate was exceeded. It is important to mention that a dose rate of 10 mGy h21 to mammals (e.g. Otter) will result in 10 % reduction in body weight with no significant effect on hair density and a dose rate of 16 mGy h21 to mice will result in significant increase in the life span (1.3 times the control value).

Figure 2. Total dose rate for terrestrial organism based on the top soil activity concentration of 137Cs closer to the NPP.

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For Clarity, the results are presented in two subsections: terrestrial and marine assessments (subsections a and b, respectively). Within the terrestrial subsection, the authors present the impact for Japan, Korea and the USA. For the marine environment, the authors also present the impacts in the study countries.

This information has been incorporated into the FREDERICA (database of the ERICA Tool). Near the Fukushima NPP, the dose rate to the terrestrial organisms ranges from 2.5 to 21 mGy h21. The reference organisms that received the low dose rates are bird egg, flying insects and gastropod. The organisms that received high dose rates are deer, rat, reptile and shrub. This preliminary assessment indicates that, based on the report of Yasunari et al.(9), the reference terrestrial organisms and plants that received dose rates higher than the screening dose rates (10 mGy h21) are deer, rat and reptile and these corresponding RQs are higher than unity, indicating that there is a substantial probability that the screening dose has been exceeded. Also Lichen and bryophytes and shrub receive dose rates higher than the screening value. The assessments result for radiological dose and risk of terrestrial organisms due to 137Cs deposition away from the NPP indicates that there is low probability that the screening dose has been exceeded and hence the environmental risk is insignificant (Figures 4 and 5). The dose rates range from 0.6 to 6 mGy h21. The reference organisms with the higher dose rates are deer, rat, reptile and shrub. Bird egg, flying insects and tree received lower dose rates. Of paramount importance are the risks to grasses and herbs as well as trees away from the Fukushima nuclear plant (Figure 5), which are almost no existence and these organisms might be considered to be reference organisms of agricultural produce and other plantations. Although the estimates of the top soil deposition by Yasunari et al.(9) were conservative (compared with

A. S. ALIYU ET AL.

Figure 4. Total dose rate for terrestrial organism based on the top soil activity concentration of 137Cs away from the NPP.

data provided when compared with the MEXT’s), the risks to the terrestrial biota were not significant. It is however important to mention that 137Cs was not the only radionuclide that has been deposited on the top soil in Japan; other nuclides were also deposited. Therefore, computing the risk based on only 137 Cs deposition reported by Yasunari et al.(9) may not give a good representative of the risk to terrestrial bionts in Japan. However, the isotope’s long half-life

could serve as argument for its relevance in the accident’s dosimetry. Discussion for terrestrial assessment in Korea Two areas were reported to have high activity concentrations of 131I, 134Cs and 137C in the southern parts of Korea (i.e. Gusan and Busan). For worst impact assessment, this study assumes that the activity

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Figure 3. Risk quotient for each terrestrial organism at close distance to the NPP due to 137Cs top soil activity concentration.

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Table 1. Values used in the ERICA terrestrial assessment. Location, country Whole Japan South Korea USA

Radionuclide, activity concentrations and reference used 137

Cs: 20, 575 Bq kg21 closer to the NPP and 5969 Bq kg21 away from the NPP(9) 3.12`  1023 Bq m23 for 131I, 1.19`  1023 Bq m23 for 134Cs and 1.25`  1023 Bq m23 for 137Cs(9) 1.11 Bq`  1023 m23 for 134Cs, 1.18`  1023 Bq m23 for 137Cs and 3.85`  1023 Bq m23 for 131I(6)

Figure 6. Total dose rate for organism for reference organisms in Korea.

ERICA tier used

Screening value used (m Gy h21)

Figure(s) showing result

2

10

Figures 2 –5

2

10

Figure 6

2

10

Figure 8

concentrations of the source terms in these areas were uniform. The values used for the assessment are presented in Table 1. Figures 6 and 7 present the total dose rate for organism and RQs of terrestrial organisms due to Fukushima accident in Korea. The dose rate was received by bird egg, and no discernible radiological risks were found in Korea due to Fukushima nuclear accident. The dose rates of terrestrial organisms in Korea range from 8.84 `  1027 to 6.07 `  1025 mGy h21. The reference organisms that received higher dose rates in Korea are bird, bird egg and detritivorous invertebrate. The dose rates are not significant compared with the screening dose rate.

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Figure 5. Risk quotient for terrestrial organism away from the NPP due to 137Cs top soil activity concentration.

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Discussion of terrestrial assessment in the USA Studies have indicated that the most radionuclides released during the Fukushima nuclear accident were transported by wind over the ocean, towards the west coast of the USA(1, 6, 8). Figure 8 is a representative of the atmospheric dispersion pattern of fission products at different heights of the PBL during the first 10 d of the Fukushima nuclear accident using single-particle trajectory calculation method in National Oceanic and Atmospheric Administration HYSPLIT model. The start time of release of the particle is 12 March 2011 from the FNPP. The lower trajectories [100 and 500 m AGL (above ground level)] have their path along the eastern coast of Japan towards northern part of the country. The particle in higher trajectories (1 and 1.5 km AGL) was transported across the Pacific Ocean to the west coast of the USA. An earlier investigation(6) has shown that 19 % of total airborne fallout from the Fukushima nuclear accident was deposited in Japan, and only 2 % made it to other land areas in Asia and North America; the bulk was absorbed by the Pacific Ocean. The RQs and dose to the terrestrial organisms in the USA were computed based on the data reported by Thakur et al.(6) ( presented in Table 1). The highest dose rates were received by mammals, reptile and shrub (Figure 9). Based on the values of the RQs, there are no discernible impacts detected in the USA due to Fukushima. The dose rate for reference terrestrial organism in the USA ranges from 6.2`  1027 to 2.2`  1025 mGy

h21. The RQs are far less than unity and in all cases, indicating that no reference organisms have been exposed to a dose rate that is more than the screening dose rate. Marine assessments Discussion of marine assessment in Japan The activity concentrations of fission products (131I, 134 Cs and 137Cs) in water samples collected near the plant during the early stage of the accident have been adopted (Table 2). Figure 10 presents the dose rates for reference marine organism near the FNPP, at the early stage of the accident. It shows that the majority of the organisms received dose rates that are more than three orders of magnitude than the ERICA screening dose rates (10 mGy h 21 ). The reference organisms with higher dose rates were polychaete worm, vascular plant and macroalgae. The lower dose rates were received by pelagic fish and phytoplankton. All the dose rates are more than the screening dose rate considered by the current study. For instance, the dose rate for polycheate worm is 1.6 5 21 ` 10 mGy h . A dose rate of 5000–10 000 mGy h21 results in an increase in mortality in Benthic fish (Medaka), pathological deterioration of eyesight in Grass carp, 2-fold increase in the incidence of vertebral malformations in Medaka among other effects. A dose rate of 2 mGy h21 to zooplankton results in one-halffold increase in fertility rate and that of 5000–1000

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Figure 7. RQs of terrestrial organisms due to Fukushima accident in Korea for the maximum measured activity concentrations.

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mGy h21 leads to 1.5-fold increase in the interval between moultings in zooplankton. The RQs for the marine organism in the FNPP cooling waters are presented in Figure 11. For all organisms, with the exception of phytoplankton, the RQ values are greater than unity, indicating that there is a substantial probability that the screening dose rate has been exceeded; hence, high risks of radiation induced detriment for the marine organism. This provides the justification to continue to a Tier 3 assessment of ERICA. The data available for this preliminary study could not provide a robust Tier 3 ERICA assessment. Future studies may be considered on this issue. A dose rate of about ,2.45 mGy h21 results in 1.2fold stimulating effect on growth of vascular plant, and the effects at higher dose rates are not yet available in FREDERICA. In Tilapia mossambica ( pelagic fish), a dose rate of 1250 mGy h21 results in 39 % reduction in life time and complete suppression of reproduction. A field-based assessment of the impacts of the accident to the marine organisms is

needed, especially now that there are reported cases of leakages from the large storage tanks containing radioactive waters in FNPP site(27). Figure 12 presents the total dose rate for marine organism 37 km away from the FNPP due to activity concentrations of 131I and 137Cs. The highest dose rates were received by macroalgae (15.2 mGy h21) and polychaete worm (15.1 mGy h21). A dose rate of 14 mGy h21 results in a moderate increase in cytogenetic damage in somatic cells like Dero obtusa (polychaete worm). The dose rates (for macroalgae and polychaete worm) are greater than the screening dose rate. The RQs (Figure 13) are less than unity indicating that there is low probability that the screening dose rate value is exceeded away from the FNPP.

Discussion of marine assessment in East China Sea Homogeneous distribution of 137Cs and the upper bound values reported by Wu et al.(11) were adopted

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Figure 8. Single-particle forward trajectories at different height above ground levels (first 10 d) of Fukushima accident.

A. S. ALIYU ET AL.

Table 2. Values used in the ERICA marine assessment. Location, country

Radionuclide, activity concentrations and reference used

ERICA tier used

Screening value used (m Gy h21)

Figure(s) showing result

Japan

(1) The activity concentrations of fission products (131I, 134 Cs and 137Cs) in water samples collected near the plant during the early stage of the accident were 13`  104 Bq l21 for 131I, 32`  103 Bq l21 for 137Cs and 31` 103 Bq l21 for 134Cs(8) (2) At a distance of 37 km from Fukushima Daiichi, the concentrations at offshore sampling locations decreased: 5 –18 Bq l21 for 131I and 1– 11 Bq l21 for 137 Cs. The upper bounds of these measurements were considered for the risk assessment by this study(8) 137 Cs in the ECS was 1.43 + 0.08 Bq m23(11)

2

10

Figures 9– 12

2

10

Figure 13

ECS

for the marine assessment in East China Sea (ECS). The result of the assessment is shown in Figure 14. Though traceable amount of radionuclides were detected, the RQ values for marine organisms in the ECS (Figure 13) are far less than unity, indicating that there is low probability that the screening dose rate has been exceeded. The reference organisms that received the highest dose rate were polychaete worm, sea anemones-polyp and macroalgae: 2.03, 1.08 and 1.05 mGy h21, respectively. In paramecium aurelia (polychaete worm), a dose rate of 0.83 mGy h21 results in a moderate increase

in cell proliferation at radiation levels below normal background levels. This assessment process complements Wu et al.’s(11) argument that 137Cs concentration in ECS due to the Fukushima nuclear accident does not have any significant impact on the marine organisms in the ECS.

CONCLUSION The Fukushima nuclear accident resulted in the release of radioactive fission products to the

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Figure 9. Total dose rates and RQs for terrestrial organisms due to Fukushima accident in the USA.

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Figure 11. Risk quotients of marine organisms near the FNPP (natural log scale).

environment. The impact assessment on the terrestrial and marine biota indicated that the impacts in Japan (near the FNPP) were high especially for marine organisms in the cooling water of the NPP, and this is in agreement with the results of Wada et al.(13). These impacts could lead to fertility and morbidity issues in some of the organisms. However, no discernible

impacts were detected on marine and terrestrial biota in China, Korea and the USA. The impacts on the terrestrial non-human biota in Japan and the USA show that the reference organisms that received the higher dose rate were deer, whereas in Korea, bird eggs received the higher dose rates. It is important to stress that despites deer and bird egg

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Figure 10. Total dose rate per marine organism near the FNPP at the early stage of the accident.

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Figure 13. Risk quotients of marine organisms 37 km from the FNPP.

received the high dose rates in the later countries, the risks were insignificant. This was because the dose rates were less than the dose rate screening value (10 mGy h21) adopted by this work. The preliminary assessment of the impact to marine biota in both Japan and ECS indicated that

the organism that received higher dose rates were polychaete worm and macroalgae. However, the risks and impacts in ECS were not discernible. This study confirms that the Fukushima accident had caused heavier damage to marine bionts compared with terrestrial flora and fauna, in Japan.

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Figure 12. Total dose rate for marine organism 37 km away from FNPP.

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FUNDING This work was supported by the Malaysian Ministry of Higher Education and the Universiti Teknologi Malaysia (UTM) Grant [Q.J130000.2526.03H67], under Prof Dr Ahmad Termizi Ramli and partly supported by the Research Management Center of UTM.

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Figure 14. Total dose rate for selected organisms and RQs due to measured activity concentration of 137Cs in ECS.

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