Radiocesium Contamination of Aquatic Organisms in the Estuary of the Abukuma River ﬂowing Through Fukushima

FISHERIES OCEANOGRAPHY Fish. Oceanogr. 26:2, 208–220, 2017

Radiocesium contamination of aquatic organisms in the estuary of the Abukuma River ﬂowing through Fukushima

YUYA SHIGENOBU,1* DAISUKE AMBE,1 seabream, which the radiocesium concentrations were TSUNEO ONO,1,2 KEN FUJIMOTO,1,3 about several times or more higher than the Japanese TAKAMI MORITA,1 standard limit, were similar to those of other individu- TADAFUMI ICHIKAWA1,3,4 AND als collected from the same sampling site. Therefore, TOMOWO WATANABE4,5 the difference in the radiocesium level between the 1National Research Institute of Fisheries Science, Japan Fisheries three heavily contaminated individuals and the less- Research and Education Agency, 2-12-4, Fukuura, Kanazawa- contaminated individuals of blackhead seabream was ward, Yokohama, Kanagawa 236-8648, Japan not because of a recent feeding habit in the Abukuma 2National Research Institute of Far Seas Fisheries, Japan Fish- River estuary. Environmental conditions in the Abu- eries Research and Education Agency, 2-12-4, Fukuura, Kana- kuma River estuary in the summer of 2013 would not zawa-ward, Yokohama, Kanagawa 236-8648, Japan have had the potential to increase radiocesium con- 3 Fisheries Agency, Ministry of Agriculture, Forestry and Fish- centrations in the muscle tissues of fish inhabiting the eries, 1-2-1, Kasumigaseki, Chiyoda-ward, Tokyo 100-8907, estuary to levels greater than 100 Bq kgÀ1 w.w. Japan 4Tohoku National Fisheries Research Institute, Japan Fisheries Key words: Abukuma River estuary, aquatic Research and Education Agency, 3-27-5, Shinhama, Shiogama, organisms, euryhaline fish, radiocesium, stable isotope Miyagi 985-0001, Japan 5Head Office of Japan Fisheries Research and Education Agency, 15F Queen’s Tower B, 2-3-3, Minato-Mirai, Nishi-ward, INTRODUCTION Yokoyama, Kanagawa 220-6115, Japan The accident at the Fukushima Dai-ichi Nuclear Power Plant (FNPP) in March 2011 released a large ABSTRACT amount of radiocesium (134Cs and 137Cs), which have In the summer of 2013, we measured the radiocesium relatively long half-lives (2.07 and 30.1 yr, respec- (134Cs and 137Cs) concentrations in aquatic organisms tively), into the environment in the form of atmo- 137 inhabiting the estuary of the Abukuma River, which spheric fallout. Estimates of the total amount of Cs flows through the Fukushima and Miyagi Prefectures. released into the atmosphere by the FNPP accident 15 Radiocesium concentrations in four muscle-tissue sam- range from 7 PBq (1 PBq = 10 Bq) (Chino et al., ples of blackhead seabream (Acanthopagrus schlegeli) 2011) to 37 PBq (Stohl et al., 2012). Moreover, Tsu- [1240, 914, 202 and 106 Bq kgÀ1 wet weight (w.w.)] mune et al. (2012) estimated that 3.5 Æ 0.7 PBq of 137 and two whole-body samples deriving from multiple Cs was released directly into the ocean between 26 individuals of flathead grey mullet (Mugil cephalus) March 2011 and the end of May 2011. The federal (129 and 110 Bq kgÀ1 w.w.) exceeded the Japanese government of Japan implemented extensive monitor- standard limit for radiocesium levels in foods ing of radiocesium levels in marine organisms immedi- (100 Bq kgÀ1 w.w.). However, radiocesium concen- ately after the accident because of the importance of trations in the other fish samples were lower than the these organisms as food resources (Fisheries Agency, Japanese standard limit. In addition, radiocesium con- 2016). Based on the monitoring data for marine fish centrations in crustaceans, major prey items of omniv- species collected off the coast of the Fukushima Prefec- orous and carnivorous fish species in the Abukuma ture (Fisheries Agency, 2016) from 1 April 2011 to River estuary, were generally low (0.444–15.1 Bq kgÀ1 the end of March 2012, 83 of 318 (26.1%) samples of w.w.). Stable isotope analysis indicated that the feed- pelagic fish and 901 of 2259 (39.9%) samples of dem- ing habit of the three heavily contaminated blackhead ersal fish exceeded the Japanese standard limit of 100 Bq kgÀ1 wet weight (w.w.) for radiocesium in *Correspondence. e-mail: [email protected] foods (Fig. 1). However, a rapid decrease in the radio- Received 30 January 2016 cesium concentration in seawater (Aoyama et al., Revised version accepted 14 November 2016 2016) would be expected to result in reduced 208 doi:10.1111/fog.12209 © 2017 The Authors. Fisheries Oceanography Published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. Radiocesium contamination in the Abukuma River 209

Figure 1. Temporal trend of radiocesium (134Cs + 137Cs) contamination levels in pelagic and demersal fish samples collected off the coast of Fukushima Prefec- ture, based on data published by the Fisheries Agency (2016). The numbers in parentheses indicate the excess ratio of the Japanese standard limit for radiocesium in food (number of samples greater than 100 Bq kgÀ1 wet weight/total number of samples). contamination levels in marine organisms, especially radiocesium concentrations of five muscle-tissue sam- pelagic fish species (Buesseler, 2012; Wada et al., ples of blackhead seabream (Acanthopagrus schlegeli) 2013). The radiocesium concentrations in marine fish (3300, 860, 850, 730 and 510 Bq kgÀ1 w.w.) and one species off the coast of Fukushima Prefecture have muscle-tissue sample of Japanese seabass (Lateolabrax decreased significantly, whereas time-series trends of japonicas) (570 Bq kgÀ1 w.w.) collected off the coast radiocesium concentration have been shown to differ of Miyagi Prefecture greatly exceeded the Japanese among taxa, habitats and spatial distributions (Wada standard limit (Fisheries Agency, 2016). Off the coast et al., 2013). of Miyagi Prefecture, radiocesium concentrations in Off the coast of Miyagi Prefecture, to the immedi- Japanese seabass and blackhead seabream are compara- ate north of Fukushima Prefecture (Fig. 2), only 7 of tively higher than concentrations observed in other 300 (2.33%) samples of marine fish species exceeded marine fish species (Fig. 3). Both Japanese seabass and the Japanese standard limit over the period of 1 April blackhead seabream are euryhaline fish that rely on 2011 to the end of March 2012 (Fig. 3; Fisheries the richness of prey congregating in estuaries during Agency, 2016). However, from May to August 2012, certain times of the year. An experimental study

Figure 2. Sampling locations of aquatic organisms included in our analyses.

Figure 3. Temporal trend of radiocesium concentration (134Cs + 137Cs) in Japa- nese seabass, blackhead seabream, and other marine fish species collected off the coast of the Miyagi Prefecture, based on data published by the Fisheries Agency (2016). Marine fish species include both of pelagic fish and demersal fish species. Invertebrate samples were excluded from the datasets. Values below the detection limit of radiocesium were excluded. revealed that the rate of removal of 137Cs from muscle effects of the recent states of the Abukuma River estu- tissues of Japanese seabass was lower under fewer saline ary on the radiocesium contamination of aquatic conditions (Ishikawa et al., 2003). Therefore, it was organisms inhabiting it is required. suspected that the heavily contaminated euryhaline In the present study, we measured radiocesium con- fish samples, which the radiocesium concentrations centrations in several types of aquatic organisms col- were about several times or more higher than the Japa- lected in the Abukuma River estuary in July and nese standard limit, collected from Sendai Bay in 2012 August 2013. Furthermore, to examine the relation- had absorbed much radiocesium under fewer saline ship between radiocesium contamination and the feed- conditions in the estuaries of rivers flowing through ing habit of euryhaline fish species, we conducted a Fukushima Prefecture, as large amounts of radiocesium stable isotope analysis of Japanese seabass, blackhead were deposited in these catchment areas (Mikami seabream and flathead (Platycephalus sp.) collected in et al., 2015; Saito et al., 2015). the estuary. Finally, we discussed whether the environ- The Abukuma River runs through Fukushima and mental conditions in the Abukuma River estuary in Miyagi prefectures and flows into the southwestern the summer of 2013 increased radiocesium concentra- part of Sendai Bay (Fig. 2). Yamashiki et al. (2014) tions in aquatic organisms inhabiting there to levels calculated the total quantity of 137Cs that was trans- greater than the Japanese standard limit (100 Bq kgÀ1 ported into the ocean by the Abukuma River during w.w.). the period of 10 August 2011 to 10 May 2012 to be 5.34 TBq, which is roughly equivalent to the esti- MATERIAL AND METHODS mated amount (8.58 TBq) of direct leakage from the FNPP to the ocean during the period of June 2011 to Sampling and measurement of radiocesium August 2011 (Kanda, 2013). Moreover, it was esti- Aquatic organisms in the Abukuma River estuary were mated in August 2013 that approximately caught by fishery workers in Miyagi Prefecture using 5600 Bq kgÀ1 dry weight of radiocesium had been various types of fishing gear from July to August 2013 deposited in sediments around the estuary of the Abu- (Fig. 2). Sampling information (date, location and kuma River (Ono et al., 2015). Kakehi et al. (2016) fishing gear) was provided by the fishery workers. reported that the concentrations of bioavailable dis- Organisms were identified to the species level, except solved radiocesium in the Abukuma River estuary Crangon spp. (Table 1). increased under lower salinity conditions owing to the Fresh samples were minced with a knife and packed desorption of riverine particulate radiocesium. How- tightly into two types of plastic cylindrical containers ever, radiocesium contamination levels in several (Type-A: diameter = 55 mm, height = 64 mm; Type- types of aquatic organisms (e.g., marine fish, freshwater B: diameter = 94 mm, height = 57 mm). We pre- fish, euryhaline fish and crustacea) inhabiting the pared three categories of samples, consisting of muscle Abukuma River estuary is unclear. Assessing the tissues, internal organs and whole-body (Table 1),

07TeAuthors. The 2017 Table 1. Radiocesium concentrations (Bq kg wet weight) in 21 aquatic organisms collected from the Abukuma River estuary in July and August 2013.

134 Cs concentrations 137 Cs concentrations Common name Sampling Sampling Number of Geometric Geometric (Species name) method/area1 Date Tissue samples Max. Min.mean Max Min. mean

Fish Japanese seabass Set net/St.6 2013/7/18 Muscle 152 12.3 4.05 6.56 25.8 8.61 14.4 ihre Oceanography Fisheries (Lateolabrax japonicus) Set net/St.6 2013/7/28 Muscle 142 10.3 3.07 5.50 24.6 7.17 12.6 Cast net/St.1 2013/8/27 Muscle 22 19.4 18.1 18.83 41.9 37.6 39.83 Blackhead seabream Sledge net/St.5 2013/8/3 Muscle 12 7.57 – 17.4 – (Acanthopagrus schlegeli) Set net/St.4 2013/7/8 Muscle 182 394. 1.56 10.1 842 3.98 22.1 Cast net/St.3 2013/8/27 Muscle 12 8.37 – 19.4 – Flathead Sledge net/St.5 2013/8/3 Muscle 22 N.D. (<2.83 and – 6.65 N.D. (<4.32) – (Platycephalus sp.) 2.69) Sledge net/St.7 2013/8/3 Muscle 42 6.13 N.D. (<3.55 4.71 12.8 5.76 7.62 ulse yJh ie osLtd., Sons & Wiley John by Published and 1.99) Set net/St.6 2013/8/4 Muscle 152 4.29 1.56 2.99 12.2 3.51 6.68 Red tonguesole Sledge net/St.5 2013/8/3 Muscle 1 1.89 – 3.58 – (Cynoglossus joyneri) Sledge net/St.7 2013/8/3 Muscle 1 1.71 – 3.60 – Purple puffer Sledge net/St.7 2013/8/3 Muscle 1 N.D. (<2.15) – N.D. (<2.76) – (Takifugu porphyreus) Needleﬁsh (Strongylura Drift net/St.3 2013/8/27 Muscle 1 1.66 – 3.41 – anastomella)

Black cow-tongue Sledge net/St.7 2013/8/3 Muscle 1 2.36 – 4.86 – River Abukuma the in contamination Radiocesium (Paraplagusia japonica) Dotted gizzard shad Cast net/St.3 2013/8/27 Muscle 1 N.D. (<0.565) – 1.89 – (Konosirus punctatus) Cast net/St.3 2013/8/27 Internal organ 1 19.9 – 40.3 – Silver croaker Sledge net/St.5 2013/8/3 Muscle 1 N.D. (<1.14) – N.D. (<1.73) – ih Oceanogr. Fish. (Pennahia argentata) Sledge net/St.7 2013/8/3 Muscle 1 N.D. (<2.20) – N.D. (<2.76) – Honnibe croaker Sledge net/St.5 2013/8/3 Muscle 1 1.60 – 4.21 – (Nibea mitsukurii) Sledge net/St.7 2013/8/3 Muscle 1 N.D. (<1.03) – 1.75 – Flathead grey mullet Drift net/St.3 2013/8/27 Muscle 1 N.D. (<2.93) – 5.39 – (Mugil cephalus) Cast net/St.2 2013/8/27 Whole-body 1 38.6 – 90.7 –

, Cast net/St.1 2013/8/27 Whole-body 1 32.5 – 77.5 – 26:2, Japanese barbel Drift net/St.3 2013/8/27 Muscle 52 4.91 2.19 3.23 9.67 6.49 7.95 (Hemibarbus barbus) Drift net/St.3 2013/8/27 Internal organ 52 7.05 2.32 4.64 15.8 4.40 10.0 208–220. Silver crucian carp Cast net/St.2 2013/8/27 Whole-body 1 10.5 – 34.5 – (Carassius auratus langsdorﬁi) Drift net/St.3 2013/8/27 Muscle 1 3.00 – 7.16 – 211 212 © .Shigenobu Y. 07TeAuthors. The 2017

Table 1. (Continued) tal. et 134 Cs concentrations 137 Cs concentrations Common name Sampling Sampling Number of Geometric Geometric (Species name) method/area1 Date Tissue samples Max. Min.mean Max Min. mean ihre Oceanography Fisheries Paciﬁc redﬁn Drift net/St.2 2013/8/27 Muscle 1 8.69 – 18.9 – (Tribolodon brandtii) Crustacea Sand shrimp Sledge net/St.7 2013/8/3 Whole-body 1 1.17 – 2.94 – (Crangon spp.) Velvet shrimp Sledge net/St.7 2013/8/3 Whole-body 1 0.802 – 1.50 –

ulse yJh ie osLtd., Sons & Wiley John by Published (Metapenaeopsis dalei) Southern rough shrimp Sledge net/St.5 2013/8/3 Whole-body 1 0.368 – 0.788 – (Trachysalambria Sledge net/St.7 2013/8/3 Whole-body 1 1.69 – 3.21 – curvirostris) Swimming crab Sledge net/St.5 2013/8/3 Muscle 1 0.591 – 1.22 – (Portunus trituberculatus) Sledge net/St.7 2013/8/3 Muscle 3 0.384 0.186 0.256 1.14 0.258 0.517 Samehada-heikegani Sledge net/St.5 2013/8/3 Whole-body 1 5.01 – 10.1 – (Japanese) (Paradorippe granulate) Hira-kobushi (Japanese) Sledge net/St.5 2013/8/3 Whole-body 1 0.767 – 1.70 – (Philyra syndactyla) Three-spot swimming crab Sledge net/St.7 2013/8/3 Muscle 1 0.342 – 0.472 – (Ovalipes punctatus)

ih Oceanogr. Fish. N.D. represents the not detected. 1For sampling area, see Figure 1. 2Samples were prepared for each individual. 3Arithmetic mean. , 26:2, 208–220. Radiocesium contamination in the Abukuma River 213 with sample weights ranging from 7.0 to 320 g. Skin individuals were collected at station 1 (St. 1) and bones were removed from the muscle-tissue sam- (Table 1, Fig. 2). Muscle tissues were freeze-dried and ples, and reproductive glands were excluded from the ground into a fine powder. To eliminate the effect of internal organ samples; however, all internal organ lipids on d13C measurements, powdered samples were and whole-body samples included digestive tract con- defatted by adding 2 : 1 chloroform–methanol solu- tents. In four fish species of Japanese seabass, black- tion (v/v) and then centrifuged; defatted samples were head seabream, flathead and Japanese barbel oven-dried and sealed in a tin container until used in (Hemibarbus barbus), samples of muscle tissues and the analyses. Carbon (d13C) and nitrogen (d15N) iso- internal organs were taken from individual fish tope ratios were analysed using an isotope ratio mass (Table 2). spectrometer (Mat 252, Thermo Finnigan MAT The measurement time for each sample differed, GmbH, Bremen, Germany) coupled to an elemental ranging from 3600 to 57027.9 s, depending on analyser (FlashEA-1112, Thermo Electron Co., Bre- gamma-ray intensity in the sample, which the weights men, Germany) via a ConFlo II split interface and sizes were different in each. Specific gamma rays (Thermo Finnigan MAT GmbH, Bremen, Germany). of 134Cs (605 and 796 keV) and 137Cs (662 keV) Results are expressed in d notation relative to Vienna were measured using a high-purity germanium PeeDee Belemnite and atmospheric N2 for d13C and (HPGe) semiconductor detector (GEM30-70-LB-C, d15N, respectively, according to the equation dX 1.85 KeV/1.33 MeV of resolution, ORTEC, Tennes- (&) = [(Rsample/Rstandard) À 1] 9 1000, where X rep- see, USA) with a multichannel analyzer. The energy- resents either 13Cor15N and R represents the corre- dependent efficiency calibration for the detector was sponding isotope ratios 13C/12Cor15N/14N. performed using activity standard gamma volume Measurement precision for both d13C and d15Nwas sources made with the same measuring containers <0.2& at replicate measurements of internal labora- (Type-A: MX033U8PP; Type-B: MX033SPS; Japan tory standards (Toyokawa, 2001). Radioisotope Association, Tokyo, Japan) with differ- 134 ent heights. Coincidence summing effects of Cs RESULTS were corrected using 134Cs standard solutions (CZ005; Japan Radioisotope Association). Uncertain- Radiocesium concentrations in aquatic organisms ties in the measurements were assigned 1-sigma of We measured radiocesium concentrations in 110 sam- counting errors, and a 3-sigma of counting error was ples taken from 21 different species of fish and crus- defined as the detection limit concentration. The tacea collected in the Abukuma River estuary in July range of the detection limit for samples in which and August 2013 (Tables 1 and 2). Radiocesium con- radiocesium was not detected was 1.14–2.69 Bq kgÀ1 centrations in crustaceans, one of the main prey items w.w. for 134Cs and 1.73–4.32 Bq kgÀ1 w.w. for 137Cs. for omnivorous and carnivorous fish species in the Variations in detection limits were the result of differ- Abukuma River estuary, were generally low (0.444– ences in measurement time and/or sample volumes. 15.1 Bq kgÀ1 w.w.) (Table 1). In contrast, radioce- The concentrations of 134Cs and 137Cs were corrected sium concentrations were highly variable in fish sam- for decay from the sampling date. Statistical analyses ples (not detected À1240 Bq kgÀ1 w.w.); four were performed with Excel Statcel 3 software (OMS individual samples of blackhead seabream muscle tis- Publishing Inc., Saitama, Japan). Values below the sue (1240, 914, 202 and 106 Bq kgÀ1 w.w.) and two detection limit of radiocesium were excluded from whole-body samples of flathead grey mullet (Mugil statistical analysis to generate more conservative cephalus, 129 and 110 Bq kgÀ1 w.w.) were found to estimates. exceed the Japanese standard limit. For the samples of dotted gizzard shad (Konosirus Stable isotope analyses punctatus) and Japanese barbel, we measured radioce- Stable isotope analyses were conducted for lateral mus- sium concentrations in muscle tissues and internal cle tissues collected from three euryhaline fish species organs, including digestive tract contents (Tables 1 – Japanese seabass (n = 5), flathead (n = 5) and black- and 2). The concentrations in the internal organs were head seabream (n = 5) – and included the three heav- higher than those of muscle tissue, except sample JB- ily contaminated blackhead seabream (radiocesium 02. Although the radiocesium concentrations in the concentrations of 1240, 914 and 202 Bq kgÀ1 w.w. in two whole-body samples of flathead grey mullet muscle-tissue samples). The lateral muscle tissues were exceeded the Japanese standard limit, the concentra- excised from each fish before the analysis of radioce- tion in the muscle-tissue sample of this species col- sium measurement. Two of the five Japanese seabass lected at St. 1 was 7.72 Bq kgÀ1 w.w. (Table 1).

Table 2. Radiocesium concentrations (Bq kgÀ1 wet weight) in individual samples of Japanese seabass, blackhead seabream, ﬂat- head and Japanese barbel.

Standard Body Sampling Sampling Sample name length (mm) weight (g) area1 date 134Cs concentrations 137Cs concentrations

Japanese seabass Muscle-tissue only JS-01 515 1836 St.6 2013/7/18 4.05 8.85 JS-02 558 2713 St.6 2013/7/18 8.74 20.5 JS-03 480 1721 St.6 2013/7/18 4.97 9.07 JS-04 514 2244 St.6 2013/7/18 10.2 18.5 JS-05 494 1798 St.6 2013/7/18 4.06 8.61 JS-06 492 1902 St.6 2013/7/18 6.83 14.1 JS-07 494 1703 St.6 2013/7/18 4.12 11.8 JS-08 545 2424 St.6 2013/7/18 11.8 24.5 JS-09 533 2298 St.6 2013/7/18 7.79 18.2 JS-10 508 2191 St.6 2013/7/18 5.36 12.6 JS-11 490 1921 St.6 2013/7/18 9.41 21.0 JS-12 500 2179 St.6 2013/7/18 4.64 11.2 JS-13 508 1946 St.6 2013/7/18 5.28 11.0 JS-14 487 1878 St.6 2013/7/18 6.19 14.0 JS-15 513 2012 St.6 2013/7/18 12.3 25.8 JS-16 448 1333 St.1 2013/8/27 19.4 41.9 JS-17 328 557 St.1 2013/8/27 18.1 37.6 JS-18 554 2571 St.6 2013/7/28 9.94 20.8 JS-19 464 1705 St.6 2013/7/28 3.34 7.73 JS-20 523 2305 St.6 2013/7/28 10.3 24.6 JS-21 528 2444 St.6 2013/7/28 4.38 12.1 JS-22 543 2428 St.6 2013/7/28 7.22 17.9 JS-23 500 1918 St.6 2013/7/28 6.93 15.6 JS-24 595 3194 St.6 2013/7/28 3.93 7.93 JS-25 478 1561 St.6 2013/7/28 4.58 9.68 JS-26 483 1654 St.6 2013/7/28 4.52 8.87 JS-27 535 2627 St.6 2013/7/28 7.05 15.2 JS-28 505 2296 St.6 2013/7/28 3.07 9.71 JS-29 465 1722 St.6 2013/7/28 6.93 16.2 JS-30 466 1554 St.6 2013/7/28 7.02 16.6 JS-31 568 2864 St.6 2013/7/28 3.63 7.17 Blackhead seabream Muscle-tissue only BS-01 363 1257 St.4 2013/7/8 2.17 5.42 BS-02 397 1496 St.4 2013/7/8 11.7 27.2 BS-03 361 1228 St.4 2013/7/8 1.91 3.98 BS-04 315 807 St.4 2013/7/8 9.03 18.5 BS-05 256 511 St.4 2013/7/8 1.56 5.27 BS-06 322 984 St.4 2013/7/8 34.3 71.8 BS-07 285 564 St.4 2013/7/8 3.13 7.91 BS-08 333 1031 St.4 2013/7/8 3.02 7.05 BS-09 353 1233 St.4 2013/7/8 14.4 29.4 BS-10 400 1927 St.4 2013/7/8 63.5 138 BS-11 349 1364 St.4 2013/7/8 293 621 BS-12 371 1494 St.4 2013/7/8 8.25 16.4 BS-13 342 1038 St.4 2013/7/8 394 842 BS-14 348 1276 St.4 2013/7/8 5.92 13.1 BS-15 372 1369 St.4 2013/7/8 2.01 4.00 BS-16 336 1098 St.4 2013/7/8 25.1 49.9

Table 2. (Continued)

Standard Body Sampling Sampling Sample name length (mm) weight (g) area1 date 134Cs concentrations 137Cs concentrations

BS-17 363 1172 St.4 2013/7/8 2.62 4.00 BS-18 319 860 St.4 2013/7/8 7.90 18.6 BS-19 330 1215 St.5 2013/8/3 7.57 17.4 BS-20 430 2189 St.3 2013/8/27 8.37 19.4 Flathead Muscle-tissue only FH-01 364 436 St.7 2013/8/3 6.13 12.8 FH-02 400 613 St.7 2013/8/3 3.29 6.50 FH-03 287 235 St.7 2013/8/3 N.D. (<1.99) 7.03 FH-04 209 84 St.7 2013/8/3 N.D. (<3.55) 5.76 FH-05 239 127 St.5 2013/8/3 N.D. (<2.69) N.D. (<4.32) FH-06 157 33 St.5 2013/8/3 N.D. (<2.83) 6.65 FH-07 457 908 St.6 2013/8/4 3.43 6.72 FH-08 434 957 St.6 2013/8/4 2.97 8.92 FH-09 499 976 St.6 2013/8/4 3.93 7.21 FH-10 376 533 St.6 2013/8/4 2.04 6.86 FH-11 384 536 St.6 2013/8/4 3.31 5.92 FH-12 381 504 St.6 2013/8/4 2.33 5.14 FH-13 421 727 St.6 2013/8/4 3.32 6.73 FH-14 416 756 St.6 2013/8/4 1.56 3.51 FH-15 430 791 St.6 2013/8/4 3.93 9.19 FH-16 435 742 St.6 2013/8/4 2.53 7.66 FH-17 362 524 St.6 2013/8/4 3.07 7.46 FH-18 401 746 St.6 2013/8/4 3.27 5.70 FH-19 370 463 St.6 2013/8/4 2.40 6.41 FH-20 460 895 St.6 2013/8/4 4.29 12.2 FH-21 385 558 St.6 2013/8/4 4.17 4.67 Japanese barbel JB-01 (Muscle) 445 1446 St.3 2013/8/27 4.52 9.67 JB-01 (Internal organ) 7.05 15.8 JB-02 (Muscle) 457 1549 St.3 2013/8/27 2.87 6.80 JB-02 (Internal organ) 2.32 4.40 JB-03 (Muscle) 467 1593 St.3 2013/8/27 4.91 9.56 JB-03 (Internal organ) 5.20 12.3 JB-04 (Muscle) 481 1763 St.3 2013/8/27 2.51 7.80 JB-04 (Internal organ) 4.70 11.9 JB-05 (Muscle) 455 1525 St.3 2013/8/27 2.19 6.49 JB-05 (Internal organ) 5.39 9.81

N.D. represents the not detected. 1For sampling area, see Figure 1.

We compared 137Cs concentrations in muscle-tis- coast of Miyagi and from the Abukuma River estuary sue samples of fish species collected off the coast of were almost equivalent. The 137Cs concentrations in Fukushima, Miyagi (Fisheries Agency, 2016), and in both Japanese seabass and blackhead seabream were the Abukuma River estuary (this study) in July and higher than those in other fish species, as shown in the August 2013 (Table 3). Concentrations of 137Cs in Figure 3. In Japanese seabass, concentrations of 137Cs fish samples collected off the coast of Fukushima were in samples collected off the coast of Fukushima higher than those in samples collected off the coast of (n = 6) were significantly higher than those in samples Miyagi and from the Abukuma River estuary, whereas collected off the coast of Miyagi (n = 34) and from contamination levels in fish samples collected off the the Abukuma River estuary (n = 31) (Steel–Dwass

Table 3. Comparison of 137Cs concentrations (Bq kgÀ1 wet weight) in muscle-tissue samples of marine ﬁsh species collected off Fukushima, Miyagi (Fisheries Agency, 2016) and in the Abukuma River estuary (this study) in July and August 2013.

Abukuma River Off Fukushima Off Miyagi1 estuary (this study)

Geometric Geometric Geometric Sample name Max. Min. n mean Max. Min. n mean Max. Min. n mean

Japanese seabass 388 17.2 6 47.8 27.2 5.11 34 12.2 41.9 7.17 31 14.5 Blackhead 42.7 N.D. 6 (1) 31.2 21.0 18.9 2 20.02 842 3.98 20 21.7 seabream Flathead 69.6 N.D. 9 (1) 32.8 7.29 N.D. 4 (3) – 12.8 N.D. 21 (1) 6.85 Red tonguesole 37.3 13.9 2 25.6 2 3.92 N.D. 2 (1) – 3.60 3.58 2 3.592 Purple puffer No data No data N.D. 1 – Needlefish No data No data 3.41 1 – Black cow- 64.5 N.D. 3 (1) 37.62 No data 4.86 1 – tongue Dotted gizzard No data 0.508 N.D. 4 (3) – 1.89 1 – shad Silver croaker 13.9 N.D. 7 (4) 11.8 2.76 N.D. 3 (2) – N.D. 2 (2) – Honnibe croaker 21.3 N.D. 7 (2) 12.6 5.62 N.D. 9 (2) 4.30 4.21 1.75 2 2.982 Flathead grey No data No data 5.39 1 – mullet n represents the number of measured samples. N.D. represents the not detected. The numbers in parentheses indicate the numbers of not detected samples. 1We excluded the samples collected in the Abukuma River estuary from the dataset of Fisheries Agency (2016). 2Arithmetic mean. test, P < 0.05). Regarding the other fish species, a sig- seabream and flathead converged, however, with val- nificant difference in 137Cs concentrations between ues ranging from À16.1 to À15.3 and 12.7 to 14.5, the three sampling localities was not detected owing respectively, for blackhead seabream, and from À17.4 to the small sample size. to À16.5 and 13.0 to 14.1, respectively, for flathead Pearson’s correlation coefficients (r) between radio- (Fig. 5). The d13C and d15N values in the three heav- cesium concentration in the muscle tissues and stan- ily contaminated blackhead seabream (radiocesium dard length (SL) of the three euryhaline fish species concentrations of 1240 and 914, and 202 Bq kgÀ1 Japanese seabass, blackhead seabream and flathead w.w. in muscle-tissue samples) fell within the range of were 0.194 (not significant, P > 0.1), 0.0173 (not sig- those of the other individuals (Fig. 5b, c). nificant, P > 0.1) and 0.448 (significant, P < 0.05), respectively (Table 2, Fig. 4). Because the samples of DISCUSSION Japanese seabass collected at two different stations (St. 1 and St. 6) clearly live under different environmental Analysis of the Pearson’s correlation coefficients conditions, we excluded the data for the two individu- between radiocesium concentrations in muscle tissues als collected at St. 1 from the analysis of Pearson’s cor- and the SL of the three euryhaline fish species revealed relation coefficients. species-specific ecological traits (Fig. 4); a significant positive correlation (r = 0.448, P < 0.05) was Stable isotope analysis detected for radiocesium concentrations in muscle-tis- The d13C and d15N values for the two individual Japa- sue samples and the SL of flathead, a sedentary demer- nese seabass collected at St. 1 ranged from À19.7 to sal fish species (Hamada and Tokuda, 1995), for À19.0 and 16.4 to 17.2, respectively. These values instance (Fig. 4c). Radiocesium concentrations were clearly differed from those of Japanese seabass col- generally higher in old and larger individuals than in lected at St. 6 (Fig. 5), for which the d13C and d15N young and small individuals, most likely owing to dif- values ranged from À17.1 to À16.9 and 14.2 to 14.4, ferences in metabolic and growth rates, as documented respectively. The d13C and d15N values for blackhead by Doi et al. (2012). The positive correlation between

Figure 4. Relationship between radiocesium concentration Figure 5. Results of stable isotope analysis for Japanese sea- (134Cs + 137Cs) and standard length (SL) in (a) Japanese bass (n = 5), ﬂathead (n = 5) and blackhead seabream seabass, (b) blackhead seabream, and (c) ﬂathead. (n = 5). (a) Relationship between d13C and d15N. (b) Rela- tionship between d13C and radiocesium concentrations. (c) Relationship between d15N and radiocesium concentrations.

radiocesium concentrations in muscle-tissue samples and the SL of flatheads suggested that the flatheads included in this study must have inhabited the same area for a certain period; moreover, the d13C and d15N muscle-tissue samples of all flathead individuals were values also indicated that these flathead fed mainly on below the Japanese standard limit, suggesting that the same prey items in the Abukuma River estuary sedentary demersal fish species in the Abukuma River over periods lasting several weeks to months (Fig. 5a), estuary have not absorbed much radiocesium since the because the low turnover rate of fish muscle tissue FNPP accident. reflects the isotopic composition of food assimilated The non-significant Pearson’s coefficient for Japa- over similar periods (Herzka, 2005). The SL of most nese seabass collected at St. 6 (r = 0.194, P > 0.1) flathead individuals included in this study was in reflected the various mechanisms of radiocesium con- excess of 300 mm (Table 2, Fig. 4c); flathead typically tamination within this species (Fig. 4a). The coexis- grow to 300 mm in total length at 3 yr of age tence of individuals with various migration patterns (Hamada and Tokuda, 1997; Morikawa et al., 2002). within a population (Ota, 2002) might be a factor for Therefore, most flathead individuals included in our explaining the highly variable contamination levels analysis would have been born before the FNPP acci- observed in this species. The radiocesium concentra- dent in 2011. However, radiocesium concentrations in tions of the two individuals collected at St. 1 (55.7

© 2017 The Authors. Fisheries Oceanography Published by John Wiley & Sons Ltd., Fish. Oceanogr., 26:2, 208–220. 218 Y. Shigenobu et al. and 61.3 Bq kgÀ1 w.w.) were slightly higher than and the less-contaminated individuals was not those of fish (10.8–36.3 Bq kgÀ1 w.w.) collected at caused by recent feeding habit, a view that was fur- St. 6, and all concentrations were below the Japanese ther supported by the relatively low contamination standard limit (Table 2, Fig. 4a). Because of their levels in prey items; for instance, radiocesium con- low d13C values, the two individuals collected at St. centrations in crustacean samples ranged from 0.444 1 fed primarily in the downstream basin of the Abu- to 15.1 Bq kgÀ1 w.w. (Table 1). Based on data col- kuma River over a period of several weeks to months lected prior to the FNPP accident, radiocesium con- (Fig. 5a). We thought that the higher concentrations centrations in marine predator fish were only in the two individuals collected at St. 1 were as a slightly higher than those in the prey items (Kasa- result of feeding on contaminated freshwater fish spe- matsu and Ishikawa, 1997). cies under fewer saline conditions. While we have The low levels of radiocesium contamination in not found heavily contaminated prey freshwater fish the muscle-tissue samples of fish species, excluding species for Japanese seabass (Table 1), the radio- the four individuals of blackhead seabream, col- cesium concentrations of freshwater fish species collected from the Abukuma River estuary in the sum- lected from the Abukuma River were comparatively mer of 2013 (Tables 1–3) suggest that the heavily higher than those of marine fish species collected in contaminated blackhead seabream and Japanese sea- Sendai Bay (Wada et al., 2016). In Sendai Bay, Japa- bass found in Sendai Bay in 2012 (Fisheries nese seabass mainly feed on pelagic fish species, such Agency, 2016) and 2013 (Table 1) did not absorb as Japanese anchovy (Engraulis japonicus) and Japa- much radiocesium while in the Abukuma River nese sand lance (Ammodytes personatus) (Kosaka, estuary. However, it is unclear where the heavily 1969). The radiocesium concentrations of Japanese contaminated blackhead seabream and Japanese sea- anchovy and Japanese sand lance collected off Miyagi bass found in Sendai Bay had absorbed much radio- and Fukushima Prefectures in 2013 ranged from cesium. Off the coast of Fukushima Prefecture, undetected to 1.7 Bq kgÀ1 w.w. and undetected to samples of fat greenling (Hexagrammos otakii) caught 15 Bq kgÀ1 w.w., respectively (Fisheries Agency, on 1 August 2012 and 8 May 2013, for which 2016). Environmental conditions at St. 1 (less saline, radiocesium concentrations of 25800 Bq kgÀ1 w.w. higher radiocesium concentrations in prey items) and 1700 Bq kgÀ1 w.w., respectively, were detected facilitated radiocesium uptake by aquatic organisms, in their muscle tissues (Tokyo Electric Power Cor- especially by ichthyophagous fish species. Neverthe- poration, 2012). Shigenobu et al. (2014) estimated less, radiocesium concentrations of the two individu- that the heavily contaminated individuals of fat als of Japanese seabass collected at St. 1 were lower greenling had absorbed much radiocesium within or than 100 Bq kgÀ1 w.w.. Environmental conditions in close to the FNPP port over a certain period imme- the Abukuma River estuary in the summer of 2013 diately after the accident before moving offshore. In would not have had the potential increase radioce- addition, on 17 November 2013, 12400 Bq kgÀ1 sium concentrations in muscle tissues of euryhaline w.w. of radiocesium was detected in the muscle-tis- fish inhabiting the estuary to levels greater than sue sample of a blackhead seabream collected 100 Bq kgÀ1 w.w. approximately 30 km south of the FNPP (Fisheries Pearson’s coefficients for blackhead seabream Research Agency, 2014). Blackhead seabream and (r = 0.0173, P > 0.1) indicated that the mechanism Japanese seabass are distributed widely along the of radiocesium contamination in this species dif- coast of Fukushima and Miyagi prefectures. There- fered among individuals (Fig. 4b). At the same fore, the heavily contaminated blackhead seabream time, the d13C and d15N values of blackhead seab- and Japanese seabass found in Sendai Bay may have ream suggested that the individuals included in our absorbed much radiocesium within or close to the analysis fed mainly on the same prey items in the FNPP port and then migrate north. Further studies Abukuma River estuary over a period of several are needed to elucidate where the heavily contami- weeks to months (Fig. 5a). The d13C and d15N val- nated blackhead seabream and Japanese seabass ues in the three heavily contaminated blackhead found in Sendai Bay had absorbed much seabream (radiocesium concentrations of 1240 and radiocesium. 914, and 202 Bq kgÀ1 w.w. in muscle-tissue sam- Several studies reported that radiocesium was being ples) also fell within the range of those of the transported from contaminated terrestrial sediments to other individuals (Fig. 5b, c), an indication that rivers and subsequently to the Pacific Ocean (Evrard the difference in radiocesium concentrations et al., 2014, 2015). Pratama et al. (2015), for instance, between the three heavily contaminated individuals calculated that the flux of radiocesium from the

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