Radioactive impacts on nekton species in the Northwest Pacific and humans more than one year after the Fukushima nuclear accident

Ecotoxicology and Environmental Safety 144 (2017) 601–610

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Radioactive impacts on nekton species in the Northwest Pacific and humans more than one year after the Fukushima nuclear accident

MARK

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Wu Men , Fangfang Deng, Jianhua He, Wen Yu, Fenfen Wang, Yiliang Li, Feng Lin, Jing Lin, Longshan Lin, Yusheng Zhang, Xingguang Yu Laboratory of Marine Isotopic Technology and Environmental Risk Assessment, Third Institute of Oceanography, State Oceanic Administration, 184 Daxue Road, Xiamen 361005, China

A R T I C L E I N F O

A B S T R A C T

Keywords: Dose assessment Fukushima Nuclear Accident Human Nekton species

This study investigated the radioactive impacts on 10 nekton species in the Northwest Pacific more than one year after the Fukushima Nuclear Accident (FNA) from the two perspectives of contamination and harm. Squids were especially used for the spatial and temporal comparisons to demonstrate the impacts from the FNA. The radiation doses to nekton species and humans were assessed to link this radioactivity contamination to possible harm. The total dose rates to nektons were lower than the ERICA ecosystem screening benchmark of 10 μGy/h. Further dose-contribution analysis showed that the internal doses from the naturally occurring nuclide 210Po were the main dose contributor. The dose rates from 134Cs, 137Cs, 90Sr and 110mAg were approximately three or four orders of magnitude lower than those from naturally occurring radionuclides. The 210Po-derived dose was also the main contributor of the total human dose from immersion in the seawater and the ingestion of nekton species. The human doses from anthropogenic radionuclides were ~ 100 to ~ 10,000 times lower than the doses from naturally occurring radionuclides. A morbidity assessment was performed based on the Linear No Threshold assumptions of exposure and showed 7 additional cancer cases per 100,000,000 similarly exposed people. Taken together, there is no need for concern regarding the radioactive harm in the open ocean area of the Northwest Pacific.

1. Introduction The Fukushima Nuclear Power Plant was damaged by the tsunami that resulted from the 9.0 magnitude Tohoku earthquake on March 11, 2011. This incident caused the largest nuclear accident since the Chernobyl disaster and the worst nuclear accident in terms of the contamination of the marine environment by radioactivity (Buesseler, 2014; Lin et al., 2016). Large amounts of radioactive contaminants, including 134Cs (t1/2 = 2.07 y), 137Cs (t1/2 30.07 y), 90Sr (t1/2 = 28.6 y), and 110mAg (t1/2 = 250 d) were released into the Northwest Pacific. The amount of radionuclides that were released into the atmosphere and ocean was estimated to be 520 PBq, approximately 10–15% of that associated with the Chernobyl Nuclear Accident, which released 5200 PBq of radioactive materials (Livingston et al., 2000; Steinhauser et al., 2014). The radioactivity that was released by the Fukushima Nuclear Accident (FNA) was dispersed over Japanese land, the ocean, and other continents, at relative percentages approximately of 19%, 80%, and 1%, respectively (Christoudias et al., 2013; Yoshida and Kanda, 2012). Although the ocean has a great capacity to dilute

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Corresponding author. E-mail address: [email protected] (W. Men).

http://dx.doi.org/10.1016/j.ecoenv.2017.06.042 Received 31 March 2017; Received in revised form 13 June 2017; Accepted 15 June 2017 0147-6513/ © 2017 Elsevier Inc. All rights reserved.

and disperse radioactive materials because of its large volume and complex current systems, radionuclides with long half-lives will remain in the marine environment for long periods. Seawater and marine organisms may be affected by radioactive contamination. Different levels of contamination in the surface water and the ocean interior have been reported (Yu et al., 2015; Men et al., 2015; Aoyama et al., 2013; Honda et al., 2012; Kaeriyama et al., 2013, 2014; Kameník et al., 2013; Buesseler et al., 2011; Kumamoto et al., 2014, 2015; Povinec et al., 2013). These data revealed that the Fukushima-derived radiocesium that was released into the Northwest Pacific Ocean has been transported eastward by surface currents and southward across the Kuroshio Extension current in subsurface layers. This radioactive contamination has already spread to most regions of the North Pacific Ocean. There is concern over the contamination of marine organisms because the radiation doses might harm marine organisms and because seafood might contain radiotoxicity due to the biological concentration and transmission of anthropogenic radionuclides in the marine food chain. How should we assess the impacts of FNA on marine organisms or humans? This paper assesses these impacts from two perspectives:

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contamination or pollution, and harm or effects. Contamination or pollution is not always “harmful” because organisms have some tolerance to these radionuclides. Only a certain degree of contamination or pollution can induce harm or other effects. Thus, we ought to assess the impacts of FNA in terms of both the activity concentrations in the marine biota and the radiation dose to the species itself and humans. 12 monitoring cruises were performed during the period 2011–2016 (one cruise every half year) to assess the impacts of the released radioactive contaminations in the Northwest Pacific. The third monitoring cruise occurred during May-June 2012. In addition to seawater samples, 10 nekton species were sampled during this cruise. The seawater monitoring results were published in January 2015 (Men et al., 2015). As a supplement to the seawater monitoring results, this paper focused on the results of nekton monitoring and the FNA-derived radiation doses to nekton species and human beings. In this work, the main Fukushima-derived radionuclides in nekton species were measured, the radiation doses to the nekton species itself and humans were computed and their corresponding dose rates were assessed. 2. Materials and methods 2.1. Sampling Nekton species samples were collected between May and June in 2012, such as squid (Ommastrephes bartramii), snake mackerel (Gempylus serpens), pelagic stingray (Pteroplatytrygon violacea), rough triggerfish (Canthidermis maculatus), Japanese amberjack (Seriolina nigrofasciata), flying fish (Cheilopogon pinnatibarbatus), grouper (Epinephelus awoara), pufferfish (Takifugu reticularis), bream (Scolopsis vosmeri) and wrasse (Choerodon azurio). Except for rough triggerfish, Japanese amberjack and flying fish, which were collected with a net, the nekton species were sampled by angling. The sampling stations were shown in Fig. 1. The nekton species that were sampled in the open ocean of the Northwest Pacific included squid, snake mackerel, pelagic stingray, flying fish, rough triggerfish and Japanese amberjack. The species that were sampled in the Taiwan Bank Fishing Ground included grouper, pufferfish, bream and wrasse. Photo of these nekton species was shown in Fig. 2. To establish background data, we searched for marine organism samples that were collected in the Northwest Pacific before the FNA

Fig. 2. Photo of the studied nekton species.

Fig. 1. Map of the sampling stations.

602

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Assessment and Management) assessment tool provides an integrated approach to scientific, managerial and societal issues that involve the environmental effects of contaminants that emit ionizing radiation with an emphasis on biota and ecosystems (Beresford et al., 2007; Brown et al., 2008; Brown et al., 2016). This tool allows the user to customize the organism model, which was used to perform a radiation dose-estimate risk assessment in this study. The studied isotopes were 134Cs, 137 Cs, 110mAg, 90Sr, 238U, 226Ra, 210Po and 40K (60Co, 58Co and 54Mn were not studied because they were not detected in either the seawater or the marine organisms). The biological characteristics of the nekton samples, including length, weight, median length and median weight, which can be used to build dose models for radiation dose estimation, were determined. The median lengths and weights are the basic parameters for constructing the radiation geometric model of each nekton species. To consider the worst-case scenario, the highest activities of each nuclide for each species were used to estimate the internal dose rate. It should be noted that the internal dose rate was calculated based on a whole-organism basis. Similarly, the measured highest activities of 134 Cs, 137Cs, 110mAg and 90Sr in the seawater from the study area (Men et al., 2015) were used to estimate the external dose rate. The data for the naturally occurring nuclides 238U, 226Ra and 210Po in the seawater were obtained from previous studies (Miyake et al., 1966; Nozaki et al., 1976; Chung and Craig, 1980). The activity of 40K in the seawater in this study was the typical ocean value of 12 kBq/m3 (Buesseler et al., 2011). We did not measure the activities of 210Po in the nekton species, rather, we inversely calculated the activities from the concentration factors as recommended by the IAEA (IAEA Technical Reports No.422, 2004) and the activities in the seawater. Due to no enough sample for measurement, we had no way to know the exactly activities of 134Cs and 137Cs in flying fishes and Japanese amberjacks. Therefore, they were also calculated in the same manner as those of 210Po. The occupancy factors (the fraction of time that an organism spends at a specified location in its habitat, which must be weighted according to the fraction of time that is spent within each of these locations, namely, air, water, or sediment, to ensure that the total occupancies of the three separate calculation runs do not exceed one) were set to “1” under the water in this study. It meant that the radiation from sediment were neglected (depth of water > 4000 m). The low beta, beta/gamma and alpha weighting factors were set to 3, 1 and 20, respectively. The other parameters were set to their default values.

and determined the radioactivity data. Squid samples that were captured before the FNA were obtained from a refrigerator of a pelagic fishery company. 2.2. Measurements The activities of 134Cs, 137Cs, 110mAg, 60Co, 58Co, 238U, 226Ra, 54Mn and 40K were measured using the γ spectrometry method and following the Technical Specification for Marine Radioactivity Monitoring (State Oceanic Administration of China, 2011). The pretreatment methods were conducted in accordance with the approved guidelines of the Technical Specification for Marine Radioactivity Monitoring as issued by the Division of Marine Environmental Protection, State Oceanic Administration of China. (No. 10 [2011] Haihuanzi). All of the experimental protocols were approved by the Third Institute of Oceanography, State Oceanic Administration of China. First, the samples were washed clean and air dried by airing. Then, the body lengths and wet masses were recorded, and the samples were dried at 105 °C. Next, approximately 2–7 kg of fresh samples (entire body) were carbonized in heated stainless woks, placed into crucibles, transferred into a muffle, and ashed at 450 °C for 24–40 h. After cooling, the ashes were weighed and ground. One hundred grams of ashes were deposited into measuring boxes and sealed for more than 20 days. The ashes were then measured for more than 24 h using HpGe γ spectrometers. The activities of 134Cs, 137Cs, 110mAg, 58Co, 238U, 54Mn and 40K were determined using γ-ray peaks of 604.9 keV (97.6%), 661.6 keV (85%), 657.7 keV (60%), 811 keV (99.4%), 63.2 keV (3.862%), 834 keV (100%) and 1460.5 keV (10.67%), respectively. 226Ra activity was determined using γ-ray peaks of 295.2 keV (19.20%), 351.9 keV (37.09%), 609.3 keV (46.1%) and 1120.3 keV (15%). 60Co activity was determined usingγ-ray peaks of 1173.2 keV (99.9%) and 1332.5 keV (100%). All of the activities of the nekton samples were corrected into units of Bq/kgfresh weight. 90 Sr was detected using the di(2-ethylhexyl) phosphoric acid (HDEHP) extraction-β counting method following the Technical Specification for Marine Radioactivity Monitoring (State Oceanic Administration of China, 2011) with some modifications. Specifically, ten grams of sample ash was transferred to a 150-ml glass beaker, and 0.5 ml of 20 mg/ml Bi2+(Bi(NO3)2), 2 ml of 100 mg/ml Sr2+ (Sr (NO3)2), 2 ml of 20 mg/ml Y3+(Y(NO3)3), 20 ml of concentrated HNO3 and 5 ml of 30% H2O2 were subsequently added. Then, the ash sample was digested on an electric stove. After cooling the solution to room temperature, the pH was adjusted to 8 by 10 M NaOH solution or concentrated NH3H2O. The precipitation of SrCO3 was induced by adding 50 ml of saturated Na2CO3 solution. After suction filtration, the precipitation was dissolved in 20 ml of 6 M HNO3. The pH was adjusted to 1 using concentrated NH3H2O. The solution was extracted twice using 50 ml of 10% di(2-ethylhexyl) phosphoric acid (HDEHP) solution. After rinsing with by 30 ml of 0.5 M HNO3, the organic phase was then re-extracted twice using 20 ml of 6 M HNO3. Next, the pH of the solution was adjusted to 2–3 using NH3H2O. The precipitation of Bi2S3 was induced by adding 1 ml of 0.3 M Na2S solution. The precipitate was separated by suction filtration. Concentrated NH3H2O was added to the filtrate to adjust the pH to 8 and dissolved, forming Y(OH)3 precipitate. After separation by suction filtration, the precipitate was dissolved in 2 M HNO3. The precipitation of Y2(C2O4)3 was induced by adding 5 ml of saturated H2C2O4 solution, and the pH was adjusted to 1 by adding NH3H2O. After suction filtration, drying and weighing for chemical recovery calculation, Y2(C2O4)3 was placed into an α/β counter to determine the 90Y activity. 1.2 g of 90Sr-90Y standard solution (6.58 ± 0.12 Bq/g) was converted into Y2(C2O4)3 for the calibration of the α/β counter. Finally, 90Sr activity was calculated from the 90Y data according to a specific formula.

2.4. Radiation dose to humans With respect to dose effects on humans, the external dose rate was estimated by assuming that humans were immersed or swam in the ocean, and the internal dose rate was estimated by assuming that the adult human consumed squids or other nekton species. For the external dose estimation, we used a self-defined simple ellipsoid human model of 1.70 × 0.35 × 0.25 m. Monte Carlo simulations were used to estimate the external dose coefficient. For comparison purposes, the external doses for an entire year, representing highly conservative scenario of the immersion or swimming of a human in the contaminated seawater for one year, were calculated by multiplying the radioactivity of the radionuclide by the external dose coefficient and the time of one year. No exact ingestion rates of squids or of the other corresponding nekton species that are consumed by humans were available for the internal dose estimation, so we assumed the worst-case scenario. We assumed that all of the fish that was consumed by the human was contaminated squids or one of the other corresponding nekton species from the Fukushima accident. The human ingestion rates were reported on a per capita basis, i.e., the total consumption is averaged over the general public population. Here, we considered the mean per capita consumption rate in China of 34.88 kg/y in 2012 to estimate the committed effective dose (FAOSTAT, 2012). The committed effective dose is a measure of the total effective dose over a lifetime (70 years for

2.3. Radiation dose to the nekton species The ERICA (Environmental Risk from Ionizing Contaminants: 603

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with values of 2.29 ± 0.16 Bq/kgfresh weight, 1.63 ± 0.12 Bq/kgfresh and 1.31 ± 0.09 Bq/kgfresh weight, which were much higher than values of the other anthropogenic radionuclides. 134Cs and 137Cs were found together only in two squid samples, with 137Cs activities almost two times higher than those of 134Cs. 137Cs was also detected in the pelagic stingray sample and the snake mackerel sample. 90Sr activities were very low and comparable with the published data of background level in the references (Miki et al., 2016; Fujimoto et al., 2015). Among the naturally occurring radionuclides, 40K had the highest activities, ranging from 39.26 ± 2.65 to 262.93 ± 17.49 Bq/kgfresh weight. The activities of 238U and 226Ra were nd-5.42 ± 0.44 Bq/kgfresh weight and nd-0.55 ± 0.09 Bq/kgfresh weight, respectively.

infants, 50 years for adults) from the intake of radioactive material into the human body, which is the sum of the products of the committed organ or tissue-equivalent doses and the appropriate tissue weighting factors (Glossary of the Nucleonica Wiki; ICRP, 2007). A person irradiated by gamma radiation outside the body will receive a dose only during the period of irradiation. However, following an intake by ingestion or inhalation, some radionuclides persist in the body and irradiate the various tissues for many years. The resulting total effective dose delivered over a lifetime (70 years for infants, 50 y for adults) is called the committed effective dose. The name arises from the fact that once a radionuclide has been taken up into the body, the person is “committed” to receiving the dose. The committed effective dose that is received by a human per unit intake (1 Bq) of a radionuclide is given as a radionuclide-specific dose coefficient (DC) for ingestion (ICRP, 2012; Fisher et al., 2013). The DC incorporates sophisticated calculations that incorporate aspects of human physiology, radiation physics and the temporal/spatial deposition of energy that is absorbed from consuming radionuclide-contaminated food stuffs, as developed and tabulated by the International Commission on Radiation Protection (Fisher et al., 2013; ICRP, 2012), which converts the energy emitted from the ingested radioactivity into a radionuclide-specific, committed effective dose to adult humans, with units of Sieverts (Sv). The committed effective doses of ingesting the nekton species were calculated by multiplying the radionuclide activity in the nekton (Bq/kgfresh weight) by the ingested mass (kg) and the DC (Sv/Bq) (ICRP, 2012).

weight

3.2. Doses to the nekton species The biological characteristics of the nekton samples that were captured in the Northwest Pacific are shown in Table 2, including length, weight, median length, median weight and habitat which can be used to build dose models for radiation dose estimation. The median lengths and weights are the basic parameters for constructing the radiation geometric model of the each nekton species. The dose rates to the six nekton species captured in the Northwest Pacific were shown in Table 2. For comparison, the anthropogenic dose rates from 134Cs, 137 Cs, 110mAg and 90Sr, the natural dose rates from 238U, 226Ra, 210Po and 40K; the ratio of the natural and anthropogenic dose rates, and the total dose rates were listed. As shown in Table 2, the ranges of the anthropogenic dose rates and natural dose rates were 0.04–0.56 nGy/h and 0.26–2.26 µGy/h, respectively. The ratio of natural dose rates to anthropogenic dose rates ranged from 839 to 6672, which suggested that the anthropogenic radionuclides contributed almost negligible dose rates, and that the naturally occurring radionuclides account for the overwhelming majority. Among the six nekton species, squids had the highest total dose rate, 2.26 µGy/h. The total dose rates of the other five nekton species differed little from one to another, ranging from 0.26 µGy/h to 0.38 µGy/h. Actually, the actual total dose rates to squid and fish will be slightly higher than what was reported here due to additional dose rates from Pu, Am, and 235U and other radionuclides which are ubiquitous in world oceans and provide background dose

3. Results 3.1. Radioactive levels of the nekton species The activities of 134Cs, 137Cs, 110mAg, 90Sr, 60Co, 58Co, 238U, 226Ra, Mn and 40K in squids and the other sampled nekton species are listed in Table 1. For all the samples, the ranges of the anthropogenic nuclides, 134Cs, 137Cs, 110mAg and 90Sr were nd~0.12 Bq/kgfresh weight, nd ~ 0.22 Bq/kgfresh weight, nd ~ 2.29 Bq/kgfresh weight and nd ~ 0.17 Bq/kgfresh weight, respectively. The anthropogenic radionuclides 60 Co, 58Co and 54Mn were not detected in the samples. Of the anthropogenic radionuclides, 110mAg was found in all of the squid samples, 54

Table 1 Radioactive levels of the nekton species in the Northwest Pacific. Nekton species

Squid 1 Squid 2 Squid 3 Squid 4 Squid 5 Squid 6 Squid 7 Squid 8 Squid 9 Squid 10 Squid 11 Squid 12 Squid 13 Squid 14 Pelagic stingray Snake mackerel Wrasse Rough triggerfish Bream Grouper Flying fish Pufferfish Japanese amberjack

Latitude °N

Longitude °E

90 Sr Bq/kgfresh

226

22.72 23.37 28.48 37.49 24.80 24.11 23.41 39.33 30.01 30.03 40.76 35.00 28.48 41.03 22.72 24.11 22.92 24.80 22.92 22.92 35.00 22.92 39.33

136.77 137.76 150.69 147.01 146.48 144.85 137.93 147.05 147.00 151.01 148.51 145.01 114.28 148.93 136.77 144.85 118.77 146.41 118.77 118.77 145.01 118.77 147.05

– 0.052 ± 0.018 – – 0.016 ± 0.010 0.022 ± 0.007 – –

Ra

40

K

137

134

0.12 ± 0.02 nd nd 0.22 ± 0.02 nd nd nd nd nd nd 0.21 ± 0.02 / / / 0.12 ± 0.01 0.05 ± 0.01 nd nd nd nd / / /

nd nd nd 0.08 ± 0.01 nd nd nd nd nd nd 0.12 ± 0.02 / / / nd nd nd nd nd nd / / /

Cs

Cs

60

Co

58

Co

238

U

54

Mn

110m

Ag

weight

0.020 ± 0.012 0.020 ± 0.006 nd – – 0.010 ± 0.007 nd 0.055 ± 0.023 0.055 ± 0.023 0.067 ± 0.023 0.186 0.042 – – –

0.21 ± 0.05 nd nd nd nd 0.11 ± 0.04 nd 0.13 ± 0.02 0.18 ± 0.02 0.12 ± 0.02 0.07 ± 0.01 / / / 0.13 ± 0.02 0.11 0.02 0.55 ± 0.09 0.32 ± 0.03 0.44 ± 0.05 0.35 ± 0.08 / / /

76.71 ± 5.26 67.17 ± 4.51 85.60 ± 5.79 73.18 ± 4.88 66.25 ± 4.46 68.22 ± 4.67 67.60 ± 4.54 64.77 ± 4.35 64.93 ± 4.36 75.84 ± 5.10 262.93 ± 17.49 / / / 39.26 ± 2.65 75.40 ± 5.06 88.60 ± 6.01 61.94 ± 4.25 72.61 ± 5.03 43.14 ± 2.95 / / /

“/” indicates samples were too small of mass for detection (too few ash samples for the γ spectrometer analysis). “nd” indicated undetected, and “-” indicates “no data”.

604

nd nd nd nd nd nd nd nd nd nd nd / / / nd nd nd nd nd nd / / /

nd nd nd nd nd nd nd nd nd nd nd / / / nd nd nd nd nd nd / / /

2.53 ± 0.50 1.20 ± 0.17 2.78 ± 0.46 0.89 ± 0.13 1.83 ± 0.22 1.68 ± 0.42 1.13 ± 0.18 0.54 ± 0.15 nd 0.45 ± 0.18 5.42 ± 0.44 / / / 1.68 ± 0.18 0.74 ± 0.16 2.29 ± 0.51 0.90 ± 0.37 1.71 ± 0.58 0.58 ± 0.15 / / /

nd nd nd nd nd nd nd nd nd nd nd / / / nd nd nd nd nd nd / / /

nd 0.18 ± 0.02 0.26 ± 0.03 2.29 ± 0.16 0.33 ± 0.03 0.39 ± 0.04 0.13 ± 0.01 0.52 ± 0.04 1.63 ± 0.12 0.31 ± 0.03 1.31 ± 0.09 / / / nd 0.13 ± 0.01 nd nd nd nd / / /

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4009 6434 5981 6672 839 906 2.26 0.26 0.27 0.29 0.38 0.38 0.13 0.02 0.04 0.02 0.13 0.13 0.03 0.02 0.02 0.04 0.02 0.02 0.08 0.02 0.01 0.02 0.03 0.03

K Po

4. Discussion 4.1. Indications of radioactive contamination in marine organisms

2.02 0.20 0.20 0.20 0.20 0.20

sum U Ra

238 226 40

Natural dose rate (µGy/h)

210

0.56 0.04 0.05 0.04 0.46 0.42 0.02 / 0.01 0.03 / / 0.04 0.01 0.03 0.01 0.30 0.29 0.03 0.01 0.01 0.01 0.16 0.14

Cs Ag

Cs, 137Cs, 90Sr and 110 mAg were the main monitored anthropogenic radionuclides. Before the FNA, 137Cs and 90Sr were detectable in marine samples; however, neither 134Cs nor 110 mAg were detectable. Therefore, the activities of 134Cs and 110 mAg and the extents to which 137 Cs and 90Sr exceeded their background levels indicated FNA radioactive contamination in marine organisms. The activity of 137Cs in squid samples that were captured before the FNA, which were obtained from a refrigerator at a pelagic fishery company, was 0.020 ± 0.003 Bq/kgfresh weight. Neither 134Cs nor 110 mAg were detected in these samples. These data were used as background data for comparison and to indicate radioactive contamination in the nekton species. The activities of the four nuclides in the squid samples and the locations were shown in Fig. 3. A comparison of the monitoring data with the background data suggested that all of the squid samples were contaminated by the radioactivity in the study area. Because of their high mobility, squids can bring radioactive contamination to a broad region over a short time scale. According to the area in which we sampled the squids, the contaminated area of marine organisms is suggested contamination from the FNA was measured in the area east to 151°E, south to 22.72°N, west to 137.76°E and north to 41°N more than one year after the FNA. Because we did not monitor other areas, we did not know the levels of contamination in other areas. The contaminated area is likely much larger than the aforementioned range. Among the four anthropogenic radionuclides, 110mAg was found in almost all of the squid samples. However, 110mAg could not be detected in the seawater of Northwest Pacific (Men et al., 2015). This suggested that squids have a very strong ability to accumulate 110mAg. Therefore, squids could be used as a bioindicator of 110mAg contamination. In this study, the range of 90Sr in the squid samples was nd ~ 0.052 Bq/kgfresh weight. Squids are cephalopods. Due to the lack of data on the background levels of 90Sr in cephalopods of the Northwest Pacific, we could not ascertain whether the squid samples were contaminated by FNAderived 90Sr. The variation in 134Cs, 137Cs and 110mAg in squids from June 2011 to June 2012 was shown in Table 4. The first and second monitoring cruises were conducted in June and December of 2011. The activities of 134 Cs, 137Cs and 110mAg were obviously higher for all three cruises than before the FNA. Some limitations in the comparability of these data were present because they present different life stages, individuals, locations and durations in which the squids stayed in contaminated water. However, the general trend was that the activities of the three anthropogenic radionuclides in the squids had increased (compared to pre-accident values) by the first two cruises and decreased by the third.

94–2800 400–1000 4000 640 110–250 10–59 277 820 380 270 233 100 149–448 675–945 380 273 215–256 65–149 Squid Snake mackerel Pelagic stingray Rough triggerfish Flying fish Japanese amberjack

(g) (g) (mm) (mm)

508.4 865 4000 640 179 37

mesopelagic mesopelagic epipelagic epipelagic epipelagic epipelagic

0.46 0.02 / / / /

sum Sr Cs

90 137 134

Anthropogenic dose rate (nGy/h)

110m

Habitat Median weight Weight range Median length Length range Nekton species

Cs.

The external dose from being immersed or swimming in seawater and the committed effective dose from ingesting nekton were shown in Table 3. For comparison, both the external doses from each radionuclide in seawater for a time scale of one year and the committed effective dose from different species and different radionuclides were listed. The sum of the external doses was 6.27 µSv. Among the radionuclides, 40K contributed over 98% of the external doses. The committed effective dose from ingesting squid (annual consumption) was 2830.37 µSv. This dose was almost ten times that from ingesting other nektons, which ranged from 288.71 to 310.66 µSv. The 210Po-driven committed effective dose accounted for most of the total committed effective dose (88.9–97.6%). 40K was the second-largest contributor, with the remaining radionuclides contributing very little to the total committed effect dose.

134

Table 2 Dose rates to marine nekton species from anthropogenic radionuclides (nGy/h) and naturally occurring radionuclides (µGy/h).

137

3.3. Doses to humans 2.26 0.26 0.27 0.29 0.38 0.38

(µGy/h)

rates to fish that typically exceed that of

Natural：anthropogenic

Total dose rate

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Table 3 External doses and committed effective doses from ingesting nekton to humans. Radionuclide

110m

Ag Cs Cs 90 Sr 210 Po 226 Ra 238 U 40 K Sum 134 137

External dosea

Committed effective dose to humans from ingesting nekton (annual consumption)b (μSv)

nSv

DCc nSv/Bq

Squid

Snake mackerel

Pelagic Stingray

Rough triggerfish

Flying fish

Japanese amberjack

/ 43.44 29.13 0.18 0.0001 7.60 0.01 6188.38 6268.74

2.80 19.00 13.00 28.00 1200.00 280.00 45.00 6.20

0.22 0.08 0.10 0.05 2762.50 2.05 8.51 56.86 2830.37

0.01 0.00 0.02 / 276.25 1.07 1.16 16.31 294.83

/ / 0.05 0.01 276.25 1.27 2.64 8.49 288.71

/ / / 0.05 276.25 3.13 1.41 13.39 294.23

/ 0.64 0.82 / 276.25 1.37 8.51 23.07 310.66

/ 0.64 0.82 / 276.25 1.37 8.51 23.07 310.66

/ No data because the corresponding radionuclides were lower than the detection limit. / Lack of data. a The external doses for an entire year. b The annual per capita consumption rates of Chinese people (34.88 kg/y) are for all types of seafood combined, whereas the dose calculations conservatively assumed the entire consumption consisted solely of each nekton species. Assumed exposure time is 50 y for adults. c DC radionuclide–specific committed effective dose coefficients for adult human ingestion (ICRP, 2012).

4.2. Radioactive levels in other nekton species

4.3. Possible sources of radionuclides in nekton

As shown in Table 1, 134Cs was not detected in any of the fishes. Sr, 137Cs and 110mAg were detected in snake mackerel, which suggested that snake mackerel was contaminated with FNA-derived radionuclides. 90Sr and 137Cs were also found in pelagic stingray samples, with activities of 0.01 Bq/kgfresh weight and 0.12 Bq/kgfresh weight, respectively. These activities fell within in the background ranges of 90 Sr(< 0.046 Bq/kgfresh weight)and 137Cs (0.10 ± 0.045 Bq/kgfresh weight) of marine fishes in the Northwest Pacific Ocean off Japan before FNA (Miki et al., 2016; Fujimoto et al., 2015), which indicated that the pelagic stingrays were not contaminated due to the FNA. 90Sr was also found in rough triggerfishes, with an activity of 0.055 Bq/kgfresh weight. This value exceeded the background range of 90Sr, which demonstrated that the rough triggerfish samples were contaminated by FNA-derived 90 Sr. Grouper, pufferfish, bream and wrasse were captured in the Taiwan Bank Fishing Ground. 134Cs, 137Cs and 110mAg were not detected in these samples, suggesting that the fishes in the Taiwan Bank Fishing Ground were not contaminated by FNA-derived radionuclides more than one year after the FNA. The 90Sr activities in Grouper, bream and wrasse (Table 1) were slightly higher than those of the other nekton species of Northwest Pacific. But they were in the range of background level of Chinese coastal area (unpublished data). A potential explanation for this finding was that grouper, bream and wrasse lived in the bottom waters of coastal areas and therefore accumulate more 90Sr from sediment than did the other nekton species. As shown in Table 1, 40K had the highest value among the naturally occurring radionuclides (measured in this study). However, a high concentration does not imply a high accumulation ability. The ability of an organism to accumulate an element is often expressed through the use of a concentration factor(CR), which in this study was, the ratio of the activity concentration in whole organism (Bq/kgfresh weight) to the activity concentration in seawater (Bq/L) (Howard et al., 2013; Buesseler et al., 2017). CRs have broad ranges because of differences among species and individuals. For research convenience, the IAEA offered a series of recommended values for some types of marine organisms, including fish, crustaceans, mollusks, macroalgae, zooplankton, phytoplankton, cephalopods and mammals (IAEA Technical Reports Series No. 422, 2004). CRs based on the data (whole organism to seawater) from this study and the IAEA's recommended values for the corresponding marine species were listed in Table 5. CR data are scarce compared with the huge range of marine organisms. The data in this study can provide some new references for the IAEA database.

The sources of radionuclides in nekton primarily include ingested food and water; in some cases, radionuclides are absorbed through the skin or respiratory systems (Buesseler et al., 2017). Due to the accumulation abilities of marine organisms, transport of radionuclides through the food web might be a common way for nekton to become contaminated. The level of radioactive contamination in a marine organism depends on three main factors: the duration of contact with the contaminated seawater, the organism's concentration ability and the organism's maturity. We could not evaluate the influences of the first two factors because of the mobility and inter-individual differences of the nekton and because of the lack of some CR data. Thus, determining the mechanisms underlying the contamination levels in various nekton species is difficult. Generally, squid and snake mackerel are largely mesopelagic, whereas flying fish and pelagic stingray are largely epipelagic. These species are all open water organisms and occupy different habitats form those of bottom dwelling/coastal species near Fukushima, which have shown the highest and most persistent concentrations of FNA-derived radiocesium (Johansen et al., 2015; Wada et al., 2016).

90

4.4. Radiation dose assessment for marine biota Radioactive impacts should be considered not only from the perspective of contamination but also from the viewpoint of potential harm. Contaminations do not always result harms. Radiological dose assessment is one way to understand the radioactive impacts from the perspective of potential harm. Radiation dose assessments for nonhuman species have gained increased developments during the past few decades (Valentin, 2004). Moreover, the ERICA tools for radiation assessment are freely available, which were used by many authors (Garnier-Laplace et al., 2011; Johansen et al., 2015; Buesseler, et al., 2017). The 210Po data were inversely calculated from the concentration factors that were recommended by the IAEA (IAEA Technical Reports Series No. 422, 2004) and the activities in the seawater (Nozaki et al., 1976). The recommended CR values are very representative and were derived from extensive field observations and literature investigations (IAEA Technical Reports Series No. 422, 2004). The calculated 210Po activity for the squids in this work was 66 Bq/kgfresh weight, which is an intermediate value compared with the previously published activity range of 1–100 Bq/kgfresh weight (Scott, 2011; Waska et al., 2008; Štrok and Smodiš, 2011; Heyraud et al., 1994; Cherry and Heyraud, 1979; Khan and Wesley, 2011; Yamamoto et al., 1994; Desideri et al., 2010). 606

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Fig. 3. Distributions of the four radionuclides in the squid samples.

The calculated 210Po activity for the fishes was 6.6 Bq/kgfresh weight, which is also an intermediate value compared with the previously published activity range of 0.4–28.1 Bq/kgfresh weight(Cherry and Heyraud, 1979; Khan and Wesley, 2011; Yamamoto et al., 1994; Desideri et al., 2010; Jackson, 1983; Jorge et al., 2012; Aarkrog et al., 1997; Musthafa and Krishnamoorthy, 2012). Thus, calculating values based on the IAEA's recommended values is recommended when lacking data for 210Po or other radionuclides. In this work, the radiation dose assessments for the six nekton species captured in the open ocean of the Northwest Pacific showed that the dose rates for Fukushima-derived radionuclides ranged from 0.04 nGy/h to 0.56 nGy/h, with those from naturally occurring radionuclides being three orders of magnitude greater than those of anthropogenic radionuclides (Table 2). The total dose rates (including

Table 4 Activity variations of anthropogenic radionuclides in the sampled squids. Nuclide

Before FNAa Cruise 1a Activity (Bq/kgfresh weight)

Cruise 2

Cruise 3

137

0.02

0.06

134

nd

0.07

nd

1.70

Range: 0.08–0.43 average: 0.24 range: 0.05–0.29 average: 0.18 range: 0.79–6.88 average: 3.23

range: nd ~ 0.22 average: 0.18 range: nd ~ 0.12 average: 0.10 range: 0.2–7.70 average: 1.76

Cs Cs

110m

a

Ag

Too few samples, no range of each nuclide.

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Table 5 CRs based on this study (whole organism-to-seawater) and the IAEA's recommended values. Marine organism

110m Ag L/kg

134

137

Squid Snake mackerel Pelagic stingray Rough triggerfish Flying fish Japanese amberjack Cephalopodsa Fisha

/ / / / / / / 10,000

66–100 / / / / / 9 100

35–65 15 35 / / / 9 100

Cs

90

Cs

210

Sr

4–19 <3 3 15–49 / / 2 3

Po

/ / / / / / 20,000 2000

226

238

Ra

50–150 79 93 229 / / / 100

U

11–128 17 40 21 / / / 1

40

K

5–22 6 3 5 / / / /

/ no data because the corresponding radionuclides were lower than the detection limit or were not measured. / lack of data in the database of IAEA recommended values. a IAEA recommended value (IAEA Technical Reports Series No. 422, 2004).

external doses and internal doses) that were absorbed by fishes following the release of Fukushima-derived and naturally occurring radionuclides (0.26–0.38 μGy/h) were much lower than the ERICA ecosystem screening benchmark of 10 μGy/h (Beresford et al., 2007). This screening benchmark is already one to two orders of magnitude lower than the International Commission on Radiological Protection (ICRP)-derived consideration reference levels (which relate radiation effects to doses over and above their normal local background natural radiation levels) for corresponding reference animals or plants (ICRP, 2008; Fisher et al., 2013). That the total additional dose rate for any of the organisms considered here was lower than the most conservative safety benchmark suggested no radiation harm to the nekton (Fisher et al., 2013). The fishes in the Fukushima coastal area were assessed by Johansen et al. (2015). The range of the total dose rate for fishes in the port harbor of Fukushima nuclear power plant (FNPP) during 12/20123/2014 was 0.83–179.17 μGy/h with the average rate of 45.8 μGy/h, which is much higher than that observed for the open area of the Northwest Pacific in this work. The range of the dose rate for greenling 3 km east off the FNPP was 0.08–1.83 μGy/h with an average of 0.54 μGy/h, which was comparable with that of coastal species of greenling size before FNA with the range of 0.05–1.50 μGy/h as well as an average of 0.42 μGy/h and slightly higher than that observed for the open area of Northwest Pacific in this work (Johansen et al., 2015). The dose-contribution analysis showed that 110mAg and 137Cs were the main dose contributors among the four anthropogenic radionuclides and that 210Po was the main dose contributor (52.4–89.3%) among the naturally occurring radionuclides (Table 6, Fig. 4). Further dose-contribution analysis of the external and internal doses for each nuclide showed that the internal doses were much larger than the external

doses (Table 6). The internal dose from 210Po was the greatest source because of its alpha emissions. 238U and 226Ra were also main contributors, which produced intermediate internal doses because of alpha emissions. Although 40K had high activity in both seawater (12 kBq/ m3) and nekton (~ 39 – ~ 260 Bq/kgfresh weight) and exhibited highenergy r-rays (1460 keV), it produced very low external doses (< 1%) and an intermediate internal dose (< 10%), as compared with 134Cs (< 0.041%), 137Cs (< 0.08%) and 110 mAg (< 0.02%). Taken together, these results suggested that Fukushima-derived radiation effects on nekton species in the open area of the Northwest was negligible when considering internal and external exposure pathways during 2011–2012.

4.5. Radiation dose assessment for humans In this study, we used a simple ellipsoidal geometric model. This model is the simplest radiation dose model that is used for external exposure during the initial stage of radiation dose assessment (ICRP, 1959; Liu, 2013). We obtained an approximate estimation by constructing the simplest radiation dose model. First, we assumed that the human was immersed or swam in the ocean for an entire year, which is a worst-case scenario, to drive the external doses from contaminated seawater of the Northwestern Pacific. However, this assumption is not realistic and is used here as a highly conservative over-estimate. Second, the external doses were always much lower than the committed effective doses. Thus, we did not need to perform precise estimations with more complicated mathematical models or voxel models. However, for other situations, mathematical models or voxel models should be considered first.

Table 6 Dose contributions of each radionuclide. Nekton species

Squid Snake mackerel Pelagic stingray Rough triggerfish Flying fish Japanese amberjack Nekton species Squid Snake mackerel Pelagic Stingray Rough triggerfish Flying fish Japanese amberjack

110m

134

Ag

137

Cs

90

Cs

Sr

External

Internal

External

Internal

External

Internal

External

Internal

/ / / / / /

0.020% 0.007% / / / /

0.0010% / / / 0.0385% 0.0334%

0.000005% 0.000116% 0.000025% 0.000035% 0.000039% 0.000056% 238 U External 0.0000002% 0.0000030% 0.0000011% 0.0000018% 0.0000021% 0.0000028%

0.0014% / 0.0023% 0.0119% / /

Internal 89.33% 78.32% 73.75% 70.11% 52.39% 52.48%

0.0002% 0.0022% 0.0018% 0.0018% 0.0014% 0.0015% 226 Ra External 0.00006% 0.00055% 0.00045% 0.00046% 0.00036% 0.00037%

0.0017% 0.0031% 0.0086% / 0.0771% 0.0732%

210 Po External 0.000000001% 0.000000006% 0.000000005% 0.000000005% 0.000000004% 0.000000004%

0.0003% 0.0032% 0.0027% 0.0027% 0.0021% 0.0022% 40 K External 0.05% 0.51% 0.36% 0.38% 0.31% 0.33%

Internal 3.50% 8.29% 4.43% 6.49% 8.17% 7.96%

608

Internal 1.29% 5.93% 6.60% 15.44% 5.05% 5.05%

Internal 5.80% 6.94% 14.84% 7.56% 34.01% 34.07%

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Fig. 4. Dose contributions of each radionuclide.

threshold, and the sum of several very small exposures is considered to have the same effect as one larger exposure. No matter how low the dose, exposure results in some projected incidents of cancer given a large enough population. LNT risks at such low doses are, of course, completely assumed. At present, inferring risks to health from such low doses encompasses large uncertainties. Statistically significant elevations in cancer risk are observed at doses > 100 mSv, and epidemiological studies cannot identify significant elevations in risk well below these levels (UNSCEAR, 2011). The Health Physics Society, the US scientific organization specialized in radiation safety, “recommends against quantitative estimation of health risks below an individual dose of 0.05 Sv in one year” (Health Physics Society, 2004; Fisher et al., 2013). (Note that the dose received by the hypothetical humans in this study was four orders of magnitude lower than the 0.05 Sv referred to by the Health Physics Society.)

A person who was immersed or swam in the seawater of the Northwest Pacific for an entire year would absorb an external dose of 6.3μSv (Table 3), which is three orders of magnitude lower than the natural radiation background (2–6 mSv/a, with an average of 2.4 mSv/a). Their dose would be at least a factor of 10 lower if they were on a ship above the seawater and not in direct contact with it (Buesseler et al., 2011). 40K contributed 98.7% of the external dose. The external dose from the four anthropogenic radionuclides was only 0.07 μSv, which is less than the dose that is acquired from eating one uncontaminated banana and absorbing its naturally occurring 40K (Munroe, 2012; Fisher et al., 2013). The internal doses from ingesting the nekton were also assessed. The assumed annual per capita consumption rate for this study was 34.88 kg/y (based on average Chinese consumption rate of 2012) for all types of seafood combined (FAOSTAT, 2012); assuming that the entire consumption in one year was solely of the nekton species in this study, the committed effective doses from the ingestion of squids were ~ 2.8 mSv, with those from other species being approximately one order of magnitude lower. The doses from naturally occurring 210Po, which comprise from ~ 81% to ~ 98% of the internal doses, were ~ 200 to ~ 9000 times greater than those from anthropogenic radionuclides (Table 3). In addition to 210Po, 40K was another main contributor. As shown in Table 3, the dose rate to humans from consumption of nekton species of ~ 0.05 and ~ 1.46 μSv are less than one-fourth of the background dose that is received by an average person in one normal day (~ 10 μSv), less than half of the dose from one dental X-ray (~ 5.0 μSv), less than one-tenth of the dose from one chest X-ray (~ 20 μSv) and less that one-twentieth of the dose from cosmic rays (~ 40 μSv) during a transcontinental flight from Los Angeles to New York (Munroe, 2012). For adult humans, the excess risk of fatal cancer is 4.1–4.8% per Sv of radiation dose (ICRP, 2007). Even if humans consumed only the nekton species in this study instead of other seafood for an entire year, the greatest increase in the probability of fatal cancer from anthropogenic radionuclides would be 0.000007% (i.e., 7 additional cancer cases per 100,000,000 similarly exposed people). Indeed, the number of extra cancer cases due to radioactive contamination is very minute. This result is based on the Linear No Threshold (LNT) assumptions. LNT states that radiation is always considered harmful with no safety

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