Radiological impact of the nuclear power plant accident on freshwater fish in Fukushima: An overview of monitoring results

Journal of Environmental Radioactivity 151 (2016) 144e155

Contents lists available at ScienceDirect

Journal of Environmental Radioactivity journal homepage: www.elsevier.com/locate/jenvrad

Radiological impact of the nuclear power plant accident on freshwater fish in Fukushima: An overview of monitoring results Toshihiro Wada a, *, Atsushi Tomiya b, Masahiro Enomoto b, Toshiyuki Sato b, Daigo Morishita b, Shigehiko Izumi b, Kouji Niizeki b, Shunji Suzuki b, Takami Morita c, Gyo Kawata b a b c

Institute of Environmental Radioactivity at Fukushima University, Fukushima, Fukushima 960-1296, Japan Fukushima Prefectural Inland Water Fisheries Experimental Station, Inawashiro, Fukushima 969-3283, Japan National Research Institute of Fisheries Science, Fisheries Research Agency, Yokohama, Kanagawa 236-8648, Japan

a r t i c l e i n f o

a b s t r a c t

Article history: Received 19 June 2015 Received in revised form 7 September 2015 Accepted 17 September 2015 Available online xxx

Radionuclide (131I, 134Cs, and 137Cs) concentrations of monitored freshwater fish species collected from different habitats (rivers, lakes, and culture ponds) in Fukushima Prefecture during March 2011 eDecember 2014 (total 16 species, n ¼ 2692) were analyzed to present a detailed description of radionuclide contamination after the Fukushima Dai-ichi Nuclear Power Plant (FDNPP) accident, and to elucidate species-specific spatiotemporal declining trends of 137Cs concentration for their respective habitats. Low concentrations of 131I (24 Bq kg1-wet) were detected from only 11 samples collected during MarcheJune 2011, demonstrating that 131I transferred to freshwater fish were not intense. In river and lake fishes, a more gradual decrease and higher radiocesium (134Cs, 137Cs) concentrations were observed than in culture pond fishes, which strongly implied that radiocesium in freshwater fish species was mainly bioaccumulated through the food web in the wild. During 2011e2014, percentages above the Japanese regulatory limit of 100 Bq kg1-wet for radiocesium in river and lake fish (14.0% and 39.6%, respectively) were higher than in monitored marine fish (9.9%), indicating longer-term contamination of freshwater fish species, especially in lakes. Higher radiocesium concentrations (maximum 18.7 kBq kg1wet in Oncorhynchus masou) were found in the northwestern areas from the FDNPP with higher deposition. However, radiocesium contamination levels were regarded as 1e2 orders of magnitude less than those after the Chernobyl accident. Lagged increase of 137Cs concentration and longer ecological half-lives (Teco: 1.2e2.6 y in the central part of Fukushima Prefecture) were observed in carnivorous salmonids (O. masou, Salvelinus leucomaenis), whereas a rapid increase and decrease of 137Cs concentration and shorter Teco (0.99 and 0.69 y) were found in herbivorous and planktivorous osmerids (Plecoglossus altivelis, Hypomesus nipponensis) with younger age at maturity. Comparison of Teco among salmonids, osmerids, and cyprinids suggests that, in addition to the fish feeding habits and life-cycles, hydraulic conditions in rivers and lakes (e.g., turnover time), which are expected to affect radiocesium concentration in prey items, are an important factor affecting the 137Cs decreasing rate of freshwater fish. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Fukushima Nuclear power plant accident Freshwater fish 131 I 134 Cs and 137Cs Ecological half-life

1. Introduction Some of the huge amount of radioactive fallout released after the Fukushima Dai-ichi Nuclear Power Plant (FDNPP) accident that occurred on and after 11 March 2011 (Chino et al., 2011) was deposited on land (Mikami et al., 2015; Saito et al., 2015),

* Corresponding author. E-mail address: [email protected] (T. Wada). http://dx.doi.org/10.1016/j.jenvrad.2015.09.017 0265-931X/© 2015 Elsevier Ltd. All rights reserved.

contaminating the terrestrial and aquatic ecosystems of eastern Japan (e.g., Tazoe et al., 2012; Mizuno and Kubo, 2013; Yamamoto et al., 2014a). Radionuclide contamination, especially that by radiocesium (134Cs and 137Cs), was severe in areas northwest of the FDNPP (Mikami et al., 2015), where high radioactive plume transport and deposition with snowfall occurred during mid-March 2011 (Povinec et al., 2013). Consequently, radiocesium concentrations exceeding the Japanese regulatory limit for foodstuffs (100 Bq kg1wet), which were enforced in April 2012, have often been detected from terrestrial and aquatic biota in Fukushima Prefecture and its

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155

vicinity (MAFF, 2015). From 30 March 2011, the Fukushima Prefectural Inland Water Fisheries Experimental Station began monitoring radioiodine (131I) and radiocesium concentrations in Fukushima's freshwater products at the instruction of the Fukushima Prefectural Government, as reported already for marine products taken off the coast of Fukushima Prefecture (Wada et al., 2013). The monitoring data, officially released by the Japan Ministry of Agriculture, Forestry and Fisheries (MAFF, 2015), have been used for the evaluation criteria for foodstuff shipments. As of May 2015, eight fish species (Japanese eel Anguilla japonica, Ayu Plecoglossus altivelis, white-spotted char Salvelinus leucomaenis (resident form), masu salmon Oncorhynchus masou (resident form), kokanee Oncorhynchus nerka, Japanese dace Tribolodon hakonensis, common carp Cyprinus carpio, crucian carp Carassius spp.) and one crustacean species (Japanese mitten crab Eriocheir japonica) distributed in contaminated rivers and lakes in Fukushima Prefecture are listed as restricted foodstuffs for shipment by the Japan Ministry of Health, Labour and Welfare (MHLW, 2015). Some studies using these publicly available data showed that higher radiocesium concentrations were found in freshwater fish caught in areas with high radiocesium deposition (Mizuno and Kubo, 2013; Arai, 2014). One study showed that, in 2011, significantly higher radiocesium concentrations were found in the order of carnivorous Salmonidae, omnivorous Cyprinidae, and herbivorous Plecoglossidae (Mizuno and Kubo, 2013), which implies higher bioaccumulation in higher trophic levels, as observed in the aftermath of the Chernobyl accident (Koulikov, 1996; Sundbom et al., 2003). Another study has demonstrated that radiocesium concentrations in freshwater fish decreased considerably during the threeyear period following the FDNPP accident (Arai, 2014). However, no report in the relevant literature, except for one of an ayu study in 2011 (Iguchi et al., 2013), describes inspection of the decreasing rates of radiocesium (expressed by ecological half-life, Teco; Jonsson et al., 1999) in freshwater fish living in different freshwater environments (e.g., lakes and rivers) with varying degrees of contamination in Fukushima Prefecture. Freshwater fish are well known to maintain higher plasma osmolality and consequently to have higher monovalent and divalent ion (e.g., Naþ, Kþ, Ca2þ, Mg2þ) concentrations than surrounding water environments (Hickman and Trump, 1969). For that reason, they reportedly show longer biological half-lives of radiocesium (Ugedal et al., 1992) than marine teleosts (Kasamatsu, 1999), which actively excrete Csþ (a biochemical analog of Kþ) through gill chloride cells during osmoregulation (Furukawa et al., 2012). These physiological characteristics, in association with radiocesium recycling or remobilization within a freshwater ecosystem (Comans et al., 1989) engendered long-term contamination of freshwater fish after the Chernobyl accident, especially fish living in closed lake ecosystems (Bulgakov et al., 2002). These results underscore the necessity of examining the area-specific and habitat-specific decreasing rates of radiocesium activity in freshwater fish species to predict long-term trends of radiocesium contamination and also to detect factors affecting the contamination of freshwater fish in Fukushima Prefecture. This information is expected to be useful to restart the local freshwater fisheries and recreational fishing reliably and to prevent harmful rumors in the future. This study analyzes the radionuclide concentrations (131I, 134Cs, and 137Cs) by monitoring surveys during 2011e2014 (n ¼ 2692, including unpublished 134Cs and 137Cs concentrations in 2011) to present an overview of the contamination of freshwater fish of different species collected from different areas and habitats (rivers, lakes, and culture ponds) in Fukushima Prefecture, and to show species-specific spatiotemporal declining trends of radiocesium concentrations by calculating the ecological half-lives for their

145

respective habitats. Based on the obtained results, the factors potentially affecting radiocesium concentrations in freshwater fish in Fukushima Prefecture are discussed.

2. Materials and methods 2.1. Sample collection, processing and measurement of radionuclides Freshwater fish individuals were caught weekly by fishery workers of local fishery cooperatives for each river and lake, and by owners of fish culture ponds in Fukushima Prefecture (Table S1). Samples were identified and processed at the Fukushima Prefectural Inland Water Fisheries Experimental Station. Primarily, whole bodies (Ayu, pond smelt Hypomesus nipponensis, willow gudgeon Gnathopogon caerulescens, topmouth gudgeon Pseudorasbora parva, weather loach Micropterus dolomieu) or bodies without the head and internal organs (Japanese eel, white-spotted char, masu salmon, kokanee, rainbow trout Oncorhynchus mykiss, Japanese dace, barbel steed Hemibarbus barbus, common carp, crucian carp, smallmouth bass Misgurnus anguillicaudatus) were used for radionuclide measurements, but in some cases, especially when individual weights exceeded ca. 200 g, only muscle tissues were used (Japanese eel, white-spotted char, masu salmon, kokanee, rainbow trout, Japanese dace, barbell steed, common carp, crucian carp, smallmouth bass, and cultured peled Coregonus peled). These samples were processed according to the standard method recommended by the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT, 2003). The processed samples were wrapped in plastic bags and were transported to the Fukushima Agricultural Technology Centre (total of 2586 samples during June 2011eDecember 2014). They were minced, packed tightly into plastic cylindrical containers (55 mm diameter, 64 mm height), weighed, measured for height, calculated for density, and wrapped in polyethylene bags. Gamma rays from 131I, 134Cs, and 137Cs were detected using a closed-end coaxial high-purity germanium (HPGe) detector (GC3020 with Multi Channel Analyzer Lynx system; Canberra, Meriden, U.S.A.). The counting efficiency of the HPGe semiconductor detector was calibrated using volume standard sources (MX033U8PP; Japan Radioisotope Association, Tokyo, Japan). The counting time for each sample was 2000 s. Genie 2000 software was used to analyze the respective peaks in the energy spectrum for 131I (364 keV), 134Cs (605 keV and 796 keV), and 137Cs (662 keV). The concentration of three times the standard deviation from counting statistics was defined as the detection limit concentration, resulting in respective detection limits of 131I, 134Cs, and 137Cs of 2.4e49 Bq kg1-wet, 4.2e14 kg1-wet, and 3.4e11 kg1-wet, depending on the sample quantity and density. Immediately after the FDNPP accident, some samples (106 samples in MarcheJune 2011) were measured at the Japan Chemical Analysis Center using the procedures described above. The counting efficiency of the detectors (Model GX2518; Canberra, Meriden, U.S.A.) was calibrated using volume standard sources (MX033U8PP; Japan Radioisotope Association, Tokyo, Japan). This study analyzed the original data of all monitored freshwater fish species (131I, 134Cs, and 137Cs concentrations with detection limits, Table S1). Publicly available data released by the Ministry of Agriculture, Forestry and Fisheries of Japan (MAFF, 2015) show only the total radiocesium concentrations for 2011. The activity concentrations of 134Cs and 137Cs and detection limits of 131I, 134Cs, and 137Cs were not publicized in 2011.

146

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155

2.2. Estimation of site-specific and habitat-specific ecological halflife for each species To elucidate area-specific and habitat-specific decreasing trends, radiocesium data of freshwater fish samples were first compiled for rivers and lakes, and for culture ponds: five weather loach samples from irrigation channels were treated as culture ponds for expedience. Data from rivers were divided into five geographic categories: Aga River System (AGR), northern Abukuma River System (NABR), southern Abukuma River System (SABR), rivers of the southeast area (SER, including Natsui, Same, and Kuji Rivers), and rivers of the northeast area of Fukushima Prefecture (NER, including Mano, Niida, and Ohta Rivers) (Fig. 1). Abukuma River runs south to north through Fukushima Prefecture and finally flows into Sendai Bay at Miyagi Prefecture. We separated its system into lower and upper reaches by the point of 37 280 N (Fig. 1), because significantly higher deposition were found in the northern areas than the southern in Fukushima Prefecture (Mikami et al., 2015; Saito et al., 2015). Numbers of samples for each category were, respectively, 1207 (AGR), 282 (NABR), 143 (SABR), 147 (SER), and 10 (NER). Data from lakes (nine lakes: Lake Okutadami, LOT; Tagokura, LTG; Numazawa, LNZ; Inawashiro, LIW; Hatori, LHT; Bobata, LBO; Hibara, Onogawa, Akimoto) were fundamentally analyzed for each lake (Fig. 1). However, three lakes (Lake Hibara, Onogawa, Akimoto) located at north-central Fukushima Prefecture (Ura-bandai district) were regarded as one category (Ura-bandai Lakes: LUB) because these lakes were located near one another and were connected through the channels (Chiba, 1988). Numbers of samples for the lakes were, respectively, 4 (LOT), 43 (LTG), 52 (LNZ), 28 (LIW), 3 (LHT), 1 (LBT), and 123 (LUB). Table 1 presents geographical, radiological, and hydrological information related to

lakes and rivers with a sufficient number of samples. To ascertain whether area-specific and habitat-specific (river or lake) decreasing trends were statistically significant or not, a singlecomponent exponential model fitted for 137Cs concentration in samples (excluding some data described below) was examined for each category using a software package (Ekuseru-Toukei ver. 2015; Social Survey Research Information Co. Ltd.). In this study, 137Cs data obtained before the date when the maximum value (or exceptional second maximum value for white-spotted char in NABR, Table 3) was recorded were excluded from analyses following procedures described by Elliott et al. (1992), because some reports after the Chernobyl accident described that the peak of 137Cs concentration in several freshwater fish species lagged behind that in the surrounding environments because of the gradual food chain transfer of 137Cs (Håkanson et al., 1989; Sundbom et al., 2003). Correlation between the 137Cs concentration (after conversion to natural log scale) and the number of days following the nuclear accident was tested when the number of 137 Cs data, except for those below the detection limit (BDL), amounted to five or greater for each category. The singlecomponent exponential model is expressed as

At ¼ A0 elt ; where At and A0 respectively stand for 137Cs concentration at time t (d) and 0, and where l represents the decreasing rate constant (d1) that allows the calculation of the effective ecological half-life (Teff) or ecological half-life (Teco), which are calculated respectively from observed or decay-corrected data. In addition, t denotes the number of days from the initial date of the FDNPP accident of 12 March 2011, when the first hydrogen explosion occurred at Unit 1 of the FDNPP (Wakeford, 2011). In the Teco calculations, 137Cs

Fig. 1. Map of the study area showing main rivers and lakes in Fukushima Prefecture, and their categories (dotted circles): AGR, Aga River system; NABR, northern Abukuma River system; SABR, southern Abukuma River system; SER, rivers of the southeastern area (including Natsui, Same, and Kuji rivers); NER, rivers of the northeastern area of Fukushima Prefecture (including Mano, Niida, and Ohta Rivers); LOT, Lake Okutadami; LTG, Lake Tagokura; LNZ, Lake Numazawa; LIW, Lake Inawashiro; LHT, Lake Hatori; LBO, Lake Bobata; LUB, Ura-bandai Lakes (including Lake Hibara, Onogawa, Akimoto); FDNPP, Fukushima Dai-ichi Nuclear Power Plant.

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155

147

Table 1 Geographical, radiological, and hydrological information for six studied lakes and nine rivers with abbreviated categories with a sufficient number of monitored fish samples (n  10). Lake or river namea Nearest distance from the FDNPP (km)b

Altitude Mean 137Cs concentration (Bq kg1(m)b dry) in sediments in September eOctober 2011c

Lake Inawashiro (LIW) Lake Akimoto (LUB)

514

1.2  102

85.0

736

3.2  10

2

0.21

Lake Onogawa (LUB)

87.0

797

2.7  102

0.19

Lake Hibara (LUB)

91.0

822

5.3  102

0.24

129

475

2.9  102

0.18

155

515

1.2  102

0.060

18.4 24.2 29.3 41.3 60.7 74.3 46.4

2.00 1.00 1.00 2.00 3.00 232 411

2.5 9.4 1.1 1.4 5.3 9.9 7.4

103 103 103 103 102 102 103

0.68 6.5 0.49 0.28 0.19 0.32 1.5

40.8

205

4.0  102

0.76

81.4

580

9.8  102

0.30

Lake Numazawa (LNZ) Lake Tagokura (LTG) Ohta River (NER) Niida River (NER) Mano River (NER) Natsui River (SER) Same River (SER) Kuji River (SER) Northern Abukuma River System (NABR) Southern Abukuma River System (SABR) Aga River System (AGR) a b c d

78.0

      

Lake type

0.082

Tectonic 105 3860 lake 3.90 32.8 Naturally dammed lake 1.40 11.8 Naturally dammed lake 10.8 128 Naturally dammed lake Crater lake 3.00 194 Artifical dam reservoir

Lake area (km2)

Volume Max. (106  m3) depth (m)

Mean air dose rate (mSv h1) in September eOctober 2011c

9.95

494

Turnover time (y)

95

3.7

33

0.075

21

0.046

31

0.83

96 80

20d 0.31

Abbreviations in parentheses show geographical categories. Data are those for the nearest survey point from the FDNPP, as monitored by the Japan Ministry of the Environment in 2011 (MOE, 2011). Publicly available data released by the Japan Ministry of the Environment (MOE, 2011) were used. Estimated turnover time during July 2011eDecember 2013 when pumped-storage hydroelectricity was stopped after a heavy rainfall disaster.

concentrations were corrected for physical decay from 12 March 2011. In addition, a two-component exponential model (Jonsson et al., 1999) was applied to the same dataset of 137Cs concentration for pond smelt (category LUB) and ayu (NABR), each of which showed the more rapid decrease of 137Cs during 2011e2012 than during 2013e2014, as described in the results section. The twocomponent exponential model applied for pond smelt and ayu is expressed as

At ¼ A1 el1 t þ A2 el2 t ; where A1 and A2 respectively denote the 137Cs concentration of first and second components at the time 0, and where l1 and l2 respectively represent the decreasing rate constants (d1) of first and second components that allow the calculation of the ecological half-lives of two components (Jonsson et al., 1999). The most suitable coefficients of the two-component model were decided using a least-squares method using the slover function of Excel (Microsoft Corp.). For pond smelt, the two-component model with a constraint (l2  0) was also calculated using the same methods because the l2 value showed a negative value in the best fit model. The fitness of single-component and two-component models of pond smelt and ayu was evaluated using Akaike's information criterion (AIC) (Akaike, 1987). The ecological half-life was calculated to assess the difference of decreasing rates of 137Cs from fishes in each category. It describes the decreasing which results from all contributing processes. It is strictly dependent on the location, the date, and the inputeoutput with other compartments (e.g., waters, sediments, foods). As a

consequence, it cannot be used by extrapolation in another accidental situation. However, it describes what is observed in the natural environment in the particular situation, in this case, freshwater fish after the FDNPP accident. In this study, 134Cs and 137Cs data were used as described in the section 3.1. (Fig. 2), in which total radiocesium (134Csþ137Cs) concentrations were necessary to compare the results with Japanese regulatory limit of 100 kg1-wet for radiocesium. However, only 137 Cs data were used for Teco calculation (Figs. 3 and 4), as described by Sohtome et al. (2014) because 134Cs data showed much more BDL data in the latter sampling dates as a result of the shorter physical half-life (2.07 y for 134Cs vs. 30.1 y for 137Cs). Additionally, BDL data were excluded from Teco analyses. We acknowledge that exclusion of the BDL values can cause underestimation of the decreasing rate constant (or overestimation of the calculated ecological half-life), but it leads to conservative and safe side estimation. 3. Results 3.1. Overview of radionuclide concentrations in fish from different habitats Time series trends in 131I concentration, 134Csþ137Cs concentration, and 134Cs/137Cs ratio of monitored freshwater fish species during 2011e2014 are presented in Fig. 2. Iodine-131 of 5.2e24 Bq kg1-wet, far below the Japanese regulatory limit of 2000 Bq kg1-wet for foodstuffs, was only detected from 11 samples of five species collected from SER (ayu), LUB (pond smelt), and

148

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155

Table 2 Summary of radiocesium (134Csþ137Cs) concentration of 16 freshwater fish species monitored during 2011e2014. Species

White-spotted char

Masu salmon

Japanese dace

Ayu

Common carp

Pond smelt

Rainbow trout

Crucian carp

Trophic levela

Habitat

4.4

River River River Lake Lake Lake Lake Culture pond River River River River River Lake Lake Lake Culture pond River River River River River Lake Lake Lake Lake Culture pond River River River River River Culture pond River River River Lake Lake Lake Culture pond River Lake Lake Lake Lake River Culture pond River River River River Lake Lake Lake Lake Culture pond Culture pond River River River River Lake Culture pond River

3.6

3.0

2.8

3.1

3.2

4.1

2.8

Kokanee

3.5

Peled

4.1

Japanese eel

3.6

Weather loach

3.2

Smallmouth bass

3.6

Category

2011

2012

Max. Csb (Bq kg1) AGR NABR SABR LOT LTG LUB LIW

AGR NABR SABR NER SER LTG LUB LIW

>DL %c

Max. Csb (Bq kg1)

n

>DL %c

Max. Csb (Bq kg1)

n

>DL %c

68.6 100 92.9

9.8  7.4  1.0  7.1 BDL 1.4 

294 25 19 2 3 3

58.8 100 100 50 0 100

9.3

98

2

4.4  10 4.6  102 1.1  102

85 36 21

62.4 94.4 71.4

2.3  10 BDL 1.4  102

6 2 1

16.7 0 100

4.0  102 8.4  102 3.0  102

134 19 6

70.1 100 100

9.3  10 6.0  102 1.8  102

137 22 14

2.7 3.5 9.0 3.0

   

10 102 10 10

2 2 2 64

100 100 100 9.9

1.1  10 4.5  102 BDL 3.0  10

5 3 1 105

40 100 0 3.8

BDL 2.9  102

2 2

0 100

7.3

98

1

1.7 9.9 6.2 2.1 1.9 2.2 6.7 1.7 3.5

        

102 102 102 103 102 10 102 102 10

15 5 2 1 6 1 3 1 22

80 100 100 100 100 100 100 100 22.7

2.5  102 1.4  103 3.0  102 1.87  104 2.0  102 1.9  10 3.6  102 3.9  102 2.4  10

71 23 9 3 17 3 2 2 23

63.4 100 88.9 100 100 66.7 100 50 4.3

6.4  10 5.7  102 1.3  102

66 26 21

69.7 96.2 61.9

9.6  10 9.3 2.4  102 2.3  102 BDL

41 2 2 1 20

    

2

2

109 6 5

17.4 100 100

8

100

4.9  10

17

58.8

1.3  10 5.7  102 1.9  102

3 2 1

66.7 100 100

BDL 3.9  102 1.4  102

2 2 2

BDL BDL 8.7 8.1  10 1.3  102 BDL

1 2 5 1 5 1

0 0 20 100 100 0

94.7 100 100 100 82.1 50

5.0  10 2.8  102 5.0  10

31 13 5

19.4 100 100

7.9 2.0  102 3.5  10

22 18 4

4.5 94.4 100

BDL 1.3  102 7.5  10

24 29 5

0 100 80

6.5  10 BDL

10 4

50 0

8.2  10 9.3  10

5 2

40 50

5

0

5

100

5.6  10 BDL 4.4  10

2 1 1

100 0 100

17 2 3 2 1 1 12

82.4 100 100 50 100 100 8.3

5 5 4

80 100 100

1.1  102

2

100

11

102 102 10 10 102 10 10

3.6  10 9.1  10 8.8  10

5.9  10

1.4 2.8 8.9 1.4 1.9 6.3 7.7

7.6

11

27.3

3 1 5 1 1 1 11

100 100 80 0 100 100 0

2.7  10 BDL 8.7  102

1 1 26

BDL BDL 2.4  102

1 1 28

0 0 100

BDL 7.6  10

2 18

0 94.4

BDL 4.2  10 1.7  10

1 7 3

0 100 100

1

0

BDL 3.5  10

1 14

1.1  10

25

4

1.6  10

24

7.4  10 3.1  102 4.8  10

6 2 3

100 100 100

2.7  10 9.0  10 1.4  10

5 5 1

100 100 100

BDL 2.9  102 6.9  10 1.7  102

1 6 1 15

0 100 100 100

BDL 6.1  10 8.8  10 1.5  102 BDL

1 1 3 22 1

0 100 100 100 0

BDL

11

0

BDL

12

0

2.4  10 7.6  10 1.2  10

1 2 1

100 100 100

BDL

1

0

10 103 102 103 102 10

19 21 2 4 28 4

1.6  102

AGR NABR SABR LTG LUB LIW

0 100 100

0

1.0  10 2.7  10 3.8  10

     

3.0  102

22 2

44.7 100 100

2 2 1

42 5 2

BDL

47 3 6

BDL 1.2  102 4.2  10

2.5  10 4.0  102 1.6  102

102

1.7  10 1.3  102 8.4  10

27 4 1 1 2

96.3 100 100 100 100

2

39 50 100 100 0

10 102 102

85.7 100 100

10 102 102 103 102

9.0 2.1 1.6 4.4 7.2 1.7

63.6 100 0 100

      

BDL

1.9  10

2

5.8  10

0 28.6

12

100

1

100

BDL

18

0

2

1.2  10 3.1  102

11 2

100 100

2.0  102

1

100 100 100 100

0 100 100

4 1 4

75 0 100

2.6  102 7.7  10 2.2  102

1 1 11

10

20

1.0  10

14

1.4  102

1

100

3.9  102

2

100

1.1  102

1

100

1.1  102 BDL 2.8  102

1 1 4

100 0 100

4.4  10 2.4  102

1 3

100 100

5.8  10

1

100

9.3  10

1

100

9.1  10 BDL 1.2  102

9.3

AGR

n

100 100 100

AGR NABR SABR NER SER

AGR NABR SABR SER LIW

2014

Max. Csb (Bq kg1)

13 3 1

2.1 8.8 4.3 2.5 1.6

AGR NABR SABR NER LTG LUB LIW LNZ

2013

>DL %c

2.0  102 5.9  102 2.0  102

AGR NABR SABR NER SER LOT LTG LUB LIW

AGR LTG LUB LHT LBT AGR

n

7.1

BDL

1.8  9.1  1.1  BDL 7.8  3.0  BDL

10 10 102 10 10

12.5

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155

149

Table 2 (continued ) Species

Topmouth gudgeon Barbel steed Willow gudgeon

Trophic levela

Habitat

Category

3.5 3.2

All All All

2012

Max. Csb (Bq kg1) River Lake Lake Culture pond River Culture pond River Lake Culture pond

3.1

2011 >DL %c

n

NABR LUB LIW

1.4 3.3 1.6 1.2

102 102 10 102

1 2 1 3

100 100 100 100

AGR

1.1  102 1.3  103

2 1

100 100

4.4  103 9.9  102 1.3  103

182 59 133

   

94 88.1 25.6

2013

Max. Csb (Bq kg1)

n

1.87  104 5.7  102 2.4  102

437 70 179

>DL %c

75.5 85.7 5.6

2014

Max. Csb (Bq kg1)

n

6.0  102 3.9  102 9.3  10

475 61 167

>DL %c

66.9 85.2 3.6

Max. Csb (Bq kg1)

n

7.4  102 1.5  102 1.6  10

694 65 170

>DL %c

58.5 76.9 2.9

n represents the number of samples measured. a Data are from fish base 2000 (Froese and Pauly, 2000). b Maximum radiocesium (134Csþ137Cs) concentration (Bq kg1-wet). Radiocesium concentrations are shown with two significant digits except for masu salmon in NER in 2012 (three significant digits). See details in Table S1. c >DL%, percentage of the samples with radiocesium concentration above the detection limit.

Table 3 Results of statistical tests for regression slopes of species (n  5) in each category. Species White-spotted char

Masu salmon

Japanese dace

Ayu

Common carp Pond smelt Crucian carp

Kokanee

Habitat River River River Lake River River River River Lake River River River Lake River Lake River River River River River Lake River River Lake Lake

Category AGR NABR SABR LUB AGR NABR SABR SER LUB AGR NABR SABR LIW SER LUB AGR NABR SER AGR NABR LUB AGR NABR LIW LNZ

Cs concentrations (Bq kg1-wet), and effective ecological half-life (Teff) and ecological half-life (Teco) of freshwater fish

137

Da 377 383 377 345 387 387 76 365 217 396 81 77 396 351 377 133 105 57 365 414 59 244 782 244 400

n 348 64 36 7 133 70 38 31 8 74 17 14 8 18 5 16 73 29 20 8 78 24 7 5 46

R

2

0.16 0.24 0.21 0.82 0.039 0.079 0.099 0.41 0.56 0.23 0.79 0.65 0.55 0.41 0.79 0.32 0.58 0.16 0.23 0.21 0.73 0.25 0.29 0.70 0.40

Pb <0.001 <0.001 0.0045 0.0048 0.023 0.018 0.054 <0.001 0.087 <0.001 <0.001 <0.001 0.035 0.0042 0.045 0.022 <0.001 0.034 0.033 0.26 <0.001 0.013 0.22 0.075 <0.001

A0 (Bq kg1-wet) 3.7 2.6 1.2 5.1 2.3 1.9 6.5 1.7 3.1 4.2 3.1 1.9 2.9 1.8 7.0 2.9 2.7 6.7 4.5 1.2 2.6 5.8 4.2 5.1 1.2

                        

10 102 102 102 10 102 10 102 102 10 102 102 102 102 102 10 102 10 10 102 102 10 102 10 102

leff (d1) 7.55 1.35 1.31 1.62 3.13 9.08 7.96 3.21 1.16 1.22 2.21 2.24 1.61 3.43 1.89 1.55 1.97 1.97 1.22 9.99 2.82 1.03 1.95 9.82 6.15

                        

4

10 103 103 103 104 104 104 103 103 103 103 103 103 103 103 10-3 103 103 103 104 103 103 103 104 104

Teff (y)

Teco (y)

2.5 1.4 1.5 1.2 6.1 2.1 2.4 0.59 1.6 1.6 0.86 0.85 1.2 0.55 1.0 1.2 0.96 0.96 1.7 1.9 0.67 1.8 0.98 1.9 3.1

2.7 1.5 1.5 1.2 7.6 2.2 2.6 0.60 1.7 1.6 0.88 0.87 1.2 0.56 1.0 1.3 0.99 0.99 1.8 2.0 0.69 2.0 1.0 2.1 3.4

n represents the number of analyzed samples without BDL data. a Days after the FDNPP accident when maximum 137Cs concentration was recorded, except for white-spotted char in NABR for which the day when the second maximum concentration was recorded was used for expedience. b Boldface denotes statistical significance (P < 0.05) for the decreasing trend of surveyed data.

culture ponds (white-spotted char, rainbow trout, and common carp) during 30 March e 4 June 2011 (Fig. 2a). In contrast, radiocesium concentrations of 5.6 Bq kg1-wet e 18.7 kBq kg1-wet were detected from 1494 samples (55.5%) of all 16 species during 2011e2014 (Fig. 2b). The percentages of the samples with radiocesium concentration above the detection limit (hereinafter, >DL%) differed greatly among habitats: higher >DL% was obtained in the order of lakes (83.9%), rivers (68.5%), and culture ponds (8.5%) during 2011e2014. Maximum radiocesium concentrations of fish and >DL% in each habitat and category decreased during the four year period after the nuclear accident (Table 2). However, high >DL % in rivers (87.9%) and lakes (100%) were still obtained in 2014, when samples from western areas of Fukushima Prefecture (AGR,

LOT, and LTG) were excluded. In contrast, >DL% in culture pond fish were extremely low (2.9%) in 2014. The total number of species that exceeded the Japanese regulatory limit of radiocesium (100 Bq kg1-wet) during 2011e2014 was 14, but that number differed among habitats (Table 2): 9 in rivers, 8 in lakes, and 3 in culture ponds. The exponential decreasing function of the 134Cs/137Cs ratio (Fig. 2c) was statistically significant (n ¼ 972, coefficient of determination (R2) ¼ 0.65, P < 0.0001). The leading coefficient (0.98) of the exponential decreasing function was comparable to that observed in seawater (initial 134Cs/137Cs ratio of 1.0, Buesseler et al., 2011) and marine products (0.985, Wada et al., 2013) off Fukushima after the FDNPP accident.

150

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155

in rivers (Fig. 3), and from 59 d (pond smelt in LUB) to 850 d (crucian carp in LUB) in lakes (Fig. 4). Among six fish species inhabiting rivers, only ayu reached the maximum 137Cs concentration at less than 140 d in all five geographic river categories (AGR, NABR, SABR, NER, and SER). Among six fish species inhabiting lakes, pond smelt reached the maximum concentrations at 59 d (the first sampling date) or less, whereas those of masu salmon, white-spotted char and Japanese dace in LUB, and kokanee in LNZ were at 217e400 d. The ranges of Teco calculated from statistically significant negative exponential model (P < 0.05) were from 0.56 y (Japanese dace in SER) to 7.6 y (masu salmon in AGR) in rivers, and were from 0.69 y (pond smelt in LUB) to 3.4 y (kokanee in LNZ) in lakes (Table 3). In NABR, with the highest >DL% among river categories, Teco were shorter, whereas A0 (the estimated concentration at start time of decreasing (d ¼ 0) extrapolated by the fitted single exponential function) were larger in the order of Japanese dace (0.88 y, 3.1  102 Bq kg1-wet), ayu (0.99 y, 2.7  102 Bq kg1-wet), whitespotted char (1.5 y, 2.6  102 Bq kg1-wet), and masu salmon (2.2 y, 1.9  102 Bq kg1-wet). In LUB, with the most samples analyzed in lake categories, pond smelt showed the shortest Teco (0.69 y) and smallest A0 (2.6  102 Bq kg1-wet) among four species analyzed. Among the other three species in LUB, Teco were shorter, whereas A0 were larger in the order of Japanese dace (1.0 y, 7.0  102 Bq kg1wet), white-spotted char (1.2 y, 5.1  102 Bq kg1-wet), and masu salmon (1.7 y, 3.1  102 Bq kg1-wet), which is the same order as that in rivers described above. The AIC value between single and two-component exponential models revealed that a two-component model gives better model fit in pond smelt in LUB (Fig. 4), but not in ayu in NABR (Fig. 3), although AIC values were similar between the two models in ayu, and higher coefficients of determination (R2) were found in both species (Table 4). The decreasing rate of second component (l2) in pond smelt showed a negative value. When a constraint (l2  0) was included in the model calculation, a single exponential function plus a constant term (A2 ¼ 17 Bq kg1-wet, l2 ¼ 0) was adopted as a best fit model in pond smelt (Fig. 4). In both species, Teco of the first component of the two-component model was smaller than Teco of the single-component model (Table 4). 4. Discussion 4.1. Overview of radionuclide contamination in freshwater fish species in Fukushima

Fig. 2. Comprehensive results of monitoring. (a) 131I (Bq kg1-wet) in freshwater fish species from rivers (grey diamonds), lakes (black circles), and culture ponds (open triangles). Data below the detection limit (BDL) were placed on or immediately above the x-axis. (b) Radiocesium concentration (134Csþ137Cs in Bq kg1-wet). Dotted and black horizontal lines respectively represent provisional regulatory limit (500 Bq kg1wet) and Japanese regulatory limit (100 Bq kg1-wet). (c) Ratio of 134Cs/137Cs (Bq/Bq). The black line shows the fitted formulae for the decay trend.

3.2. Area-specific and habitat-specific trend of in each species

137

Cs concentration

The species-specific 137Cs concentrations of six fish species from five river categories are presented in Fig. 3. The species-specific 137 Cs concentrations of six fish species from four lake categories are depicted in Fig. 4. Results of statistical tests for fitting the single exponential model and Teff and Teco of fishes of each habitat and category are presented in Table 3. The ranges of the days after the nuclear accident when the maximum 137Cs concentration was found were from 57 d (ayu in SER) to 782 d (crucian carp in NABR)

By analyzing the data obtained during 2011e2014, we succeeded in gaining an overview of radionuclide (131I, 134Cs, and 137Cs) contamination, and habitat-specific and area-specific decreasing rates of 137Cs in freshwater fish species in Fukushima Prefecture after the FDNPP accident. First, it is evident that 131I transferred to freshwater fish were not intense because low concentrations of 131I (24 Bq kg1-wet) were detected from only 11 samples of five species collected during 30 March e 4 June 2011 (Fig. 2a). Although 131I concentrations of freshwater fish were not measured in mid-March, when the highest atmospheric release (Chino et al., 2011) and highest 131I concentrations of unfiltered pond water (2.45 kBq L1) in Iidate Village, 35 km northwest from the FDNPP, were recorded (Povinec et al., 2013), our results strongly suggest that the effects were limited and/or that they decreased quickly immediately after the accident, probably because of the rapid decay of 131I (8.02 d). Reportedly, much higher 131I concentrations were observed in freshwater fish after the Chernobyl accident (about 6 kBq kg1-wet) (Kryshev, 1995), from which larger amounts of atmospheric release (1940 PB vs. 159 PBq in Fukushima) (Povinec et al., 2013) and higher

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155

151

Fig. 3. Species-specific 137Cs concentration (Bq kg1-wet) of six fish species in rivers. Solid lines with different colors show fitted exponential functions for 137Cs concentration of fish in each category. Data below the detection limit (BDL) were placed on the x-axis. The dotted red line in upper right panel shows the fitted two-component exponential modes for ayu in NABR. Results of the fitted exponential functions are presented in Tables 3 and 4.

concentrations of 131I (4.44 kBq L1) in the water of Pripyat River located close to the Chernobyl Nuclear Power Plant (IAEA, 2006) were recorded. In both cases, the 131I concentration in freshwater fish became insignificant within a few months after the accident. In contrast to 131I, long-term contamination and higher concentrations of radiocesium in freshwater fish species were observed, especially in river and lake habitats (Fig. 2b). In culture ponds, only four samples of three species (weather loach, willow gudgeon, and topmouth gudgeon), which probably preyed on contaminated food in the pond in the wild (mainly zooplankton, Kanou et al., 2007; Kikko et al., 2013), exceeded the Japanese regulatory limit of 100 Bq kg1-wet (Table 2). Cultured fishes (e.g., white-spotted char, masu salmon, and common carp) reared in concrete culture ponds with river/well water being fed noncontaminated artificial pellets showed lower radiocesium concentrations and lower >DL% (Table 2), especially after 2012 when low dissolved radiocesium concentrations (0.51 Bq L1) in several rivers in Fukushima Prefecture were reported (Yoshimura et al., 2015). In contrast, many samples of several fish species in rivers

and lakes remained contaminated after 2012 (Figs. 3 and 4). The highest concentrations of several species (white-spotted char, masu salmon, kokanee, common and crucian carps) were found in 2012 or later. Furthermore, the Teco of studied fish (0.56e7.6 y, Table 3) were longer than the reported biological half-lives of freshwater fish (0.27 y, Vanderploeg et al., 1975; 0.29e0.44 y under 15  C in brown trout Salmo trutta, Ugedal et al., 1992). These results suggest that the main contamination source for these freshwater fish species is contaminated food in the wild, rather than contaminated water in rivers and lakes, as shown in the rearing experiments using salmonids (Hewett and Jefferies, 1976; Yamamoto et al., 2014b). Overall radiocesium concentrations in fish in rivers and lakes have decreased gradually (Fig. 2, Table 2), probably because of the physical decay of 134Cs with short half-life (2.07 y), and decrease of radiocesium from the bodies and surrounding environments (Figs. 3 and 4, Table 3), as reported for several lake fishes (Fukushima and Arai, 2014; Matsuda et al., 2015). However, some freshwater fish samples in rivers (3.6%) and lakes (15.4%) exceeded

152

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155

Fig. 4. Species-specific 137Cs concentration (Bq kg1-wet) of six fishes in lakes. Solid lines with different colors show fitted exponential functions for the 137Cs concentration of fish in each category. Data below the detection limit (BDL) are shown on the x-axis. The dotted red line and thin black line in the upper right panel respectively show a fitted twocomponent exponential model and a single exponential model plus a constant term for pond smelt in LUB. Results of the fitted exponential functions are presented in Tables 3 and 4.

Table 4 Results of parameters for the fitted two-component exponential model of Species Ayu Pond smelt Pond smeltb a b

A1 (Bq kg

1

2

8.6  10 5.5  102 5.7  102

-wet)

1

l1 (d )

Teco1 (y) 3

8.11  10 5.63  103 6.00  103

0.24 0.34 0.32

137

Cs concentrations in ayu in NABR and pond smelt in LUB. A2 (Bq kg1-wet) 5.4  10 1.1  10 1.7  10

l2 (d1) 4

5.35  10 4.39  104 0

Teco2 (y)

AICa

R2a

4.0 3.6

150.9 (149.4) 36.4 (108.3) 39.5

0.70 (0.58) 0.85 (0.73) 0.85

Numbers in parentheses present results for single exponential model in Table 3. A constraint (l2  0) was included in the model calculation.

the Japanese regulatory limit of 100 Bq kg1-wet even in 2014, when fewer samples (1.0%) exceeded the regulatory limit in monitored marine fish (MAFF, 2015). These results indicate longerterm contamination and slower decrease of radiocesium in freshwater fish species, especially in lake fish. Results suggest that radiocesium contamination levels of the monitored freshwater fish species after the FDNPP accident were lower by 1e2 orders of magnitude than those observed after the Chernobyl accident (IAEA, 2006). The 137Cs concentration of about 100 kBq kg1-wet, much higher than the maximum 11 kBq kg1-

wet in masu salmon in this study (Table S1), was observed for several species at the Chernobyl cooling pond within a few years after the accident (Kryshev, 1995). In addition, freshwater fish with 137 Cs concentrations over 100 Bq kg1-wet were reported frequently from several countries in western Europe (e.g., Germany, Norway, Sweden, and England) several years after the Chernobyl accident (Brittain et al., 1991; Elliott et al., 1992; Håkanson et al., 1992; Zibold and Klemt, 2005), although the European Union intervention level for radiocesium concentration in fish was 1250 Bq kg1-wet (Janssens, 2013). These different contamination

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155

levels are partly attributable to the difference in radiocesium amounts released to the atmosphere from the Fukushima (134Cs, 17.5 PBq; 137Cs, 15.3 PBq) and from the Chernobyl (134Cs, 54 PBq; 137 Cs, 85 PBq) accidents (Povinec et al., 2013). As the next step for research, long-term and detailed surveys of radiocesium contamination of freshwater habitats in areas near the FDNPP (e.g., rivers, lakes, and irrigation ponds within evacuation zone) must be conducted to evaluate the precise radiological impact of the FDNPP accident on freshwater fish species. 4.2. Area-specific and habitat-specific

137

Cs trend

Within rivers, 137Cs concentrations of white-spotted char in Abukuma River System (ABR) were significantly higher than those in AGR (P < 0.001, ManneWhitney U test). The northern area of ABR (NABR) showed significantly higher concentrations than the southern area (SABR) (P < 0.001, analysis of covariance), resulting in higher A0 values in the order of NABR, SABR, and AGR (Table 3). The same tendency was found for other five species (Fig. 3). In addition, the highest 137Cs concentrations in masu salmon, Japanese dace, and ayu were observed in NER, which runs through contaminated areas northwest from the FDNPP (Yoshimura et al., 2015). Similarly, in lakes, 137Cs concentrations of all five species from UBL, 85e91 km northwest from the FDNPP, exceeded 100 Bq kg1-wet, whereas fish from LTG, 155 km west from the FDNPP, showed 137Cs concentration of 15 Bq kg1-wet or less, or BDL values. A significant and positive exponential relation (P < 0.001) between publicly available air dose rates (FPG, 2015) and 137Cs concentrations in river and lake fishes (Fig. 5) well reflects the tendency by which higher 137Cs concentrations were observed in highly contaminated areas. In both river and lake habitats, higher 137Cs concentrations within a species were found in areas with higher deposition (Figs. 3 and 4). The positive relation between 137Cs concentrations in sediments and fish in several lakes has also been reported from several studies conducted after the Chernobyl and Fukushima accidents (Håkanson et al., 1989; Jagoe et al., 1998; Fukushima and Arai, 2014; Matsuda et al., 2015). The higher 137Cs concentration in sediments, as reflected in higher air dose rates, is expected to be related to higher 137 Cs concentrations in food organisms (e.g., zooplankton, aquatic insects), resulting in the higher 137Cs concentration of fishes in areas with dense deposits. Time-series trends of 137Cs concentration of Japanese dace, a common and indicator species distributed in various river/lake habitats, showed significant and negative exponential models for

Fig. 5. Relation between air dose rates (mSv h1) at 1 m height, measured by the Fukushima Prefectural Government during MayeJune 2012 (FPG, 2015), and 137Cs concentrations of freshwater fish from rivers and lakes in 2012. A significantly positive exponential function is shown in the figure.

153

six geographical categories (AGR, NABR, SABR, SER, LIW, and LUB) (Figs. 3 and 4). A large difference in A0 values of these models (Table 3), from 42 Bq kg1-wet in AGR to 7.0  102 Bq kg1-wet in LUB, was regarded as strongly related to the initial amount of 137Cs contamination introduced around these habitats, although the A0 values themselves did not reflect the actual 137Cs concentrations immediately after the FDNPP accident. However, differences in Teco of Japanese dace are expected to reflect the differences in decreasing rate of 137Cs in water/food in each category. Except for AGR, for which overestimation of Teco should not be ignored because of the high percentages of BDL values (54.9%), Teco values were smaller in the order of SER (0.56 y), SABR (0.87 y), NABR (0.88 y), LUB (1.0 y), and LIW (1.2 y). Although the reason why decreasing rate of 137Cs in Japanese dace and masu salmon was higher in SER than in ABR has not been elucidated, the smaller size of the catchment and 137Cs contaminated areas, shorter stream lengths, and steeper stream gradients in SER compared with ABR might engender faster discharges of 137Cs in water and riverside sediments, as shown from a typhoon event (Nagao et al., 2013), thereby resulting in faster 137Cs decrease of food organisms and fishes. In contrast, in lake habitats, the hydraulic turnover time is expected to be an important factor for determining the Teco of freshwater fish, as shown in several lakes after the Chernobyl accident (Sårkkå et al., 1995; Bulgakov et al., 2002). Actually, longer Teco was found in LIW with longer turnover time compared with LUB (Table 3). Furthermore, longer Teco was observed in kokanee in LNZ, a closed crater lake with a small stream, where pumpedstorage hydroelectricity was stopped during July 2011eDecember 2013 after a heavy rainfall disaster. Therefore, a much longer turnover time than that before the accident was estimated (Table 1). 4.3. Species-specific

137

Cs trend

Many studies conducted after the Chernobyl accident have shown that the increase of radiocesium concentration was slower in predatory fish with higher trophic level, and predatory and large fish tended to have higher radiocesium concentrations than nonpredatory and small fish had (Koulikov and Ryabov, 1992; Ugedal et al., 1995; Koulikov, 1996). The same tendencies were found after the FDNPP accident. Except for ayu, a microalgae-grazing osmerid, for which effects of internal organs with gut contents showing higher radiocesium concentration than muscles (Tsuboi et al., 2015) cannot be excluded through the whole body measurement in the monitoring surveys, maximum 137Cs concentrations in NABR were higher in carnivorous salmonids (white-spotted char and masu salmon) than in omnivorous cyprinids (Japanese dace, common carp, and crucian carp). Furthermore, the increase of 137 Cs concentrations was slower and Teco was fundamentally longer in white-spotted char and masu salmon than in Japanese dace or ayu (Fig. 3, Tables 2 and 3). Additionally, it is noteworthy that more gradual 137Cs increase and higher >DL% were found in common and crucian carps. The omni-benthivorous feeding habits (GarcíaBerthou, 2001), low metabolic rate (Yamamoto et al., 1986; Yamamoto and Hirano, 1988), and greater longevity of these carps (8 y) (Suzuki and Kimura, 1977; Vilizzi and Walker, 1999) compared with other fish species (white-spotted char, kokanee, 3e6 y; masu salmon, 2e3 y; ayu, 1 y; pond smelt, 1e3 y) (Kato, 1980; Nakamura, 2012; Tamate, 2002; Tsuboi et al., 2015) might engender lower but less variable and slower increase of 137Cs concentrations. Rapid decrease of 137Cs concentrations and short Teco by alteration of generation was marked in ayu (Fig. 3), an annual fish. Additionally, large variations of 137Cs concentrations in several salmonids attributed from those in prey items (mainly aquatic insects) were reported from several studies conducted after

154

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155

the Chernobyl and Fukushima accidents (Ugedal et al., 1992; Yoshimura and Yokoduka, 2014). In this study, large variations of 137 Cs concentration were also observed in salmonids (masu salmon and white-spotted char) in rivers (Fig. 3). In LNZ, the lagged increase and longer Teco of kokanee strongly suggest their continuous radiocesium uptake from contaminated food (mainly zooplankton, Konno and Sakano, 2010) as shown in other lake in Japan (Yamamoto et al., 2014a,b). As the next step for future research, factors affecting 137Cs concentrations in salmonids and other species such as feeding habits, body size (termed “size effects”), and age (Koulikov and Ryabov, 1992; Ugedal et al., 1995), as well as physicochemical properties of water such as Kþ concentration (Rowan and Rasmussen, 1994; Smith et al., 2000) should be examined. Rapid increase and decrease of 137Cs concentrations were detected in two osmerids: ayu in NABR and pond smelt in LUB. Although they showed different feeding habits and life cycles (Iguchi and Hino, 1996; Katayama et al., 2000; Chang et al., 2005), their common points are that they have shorter longevity, and lower trophic levels than those of salmonids (Table 2). In addition to the alteration of generations, rapid 137Cs decreases in ayu and pond smelt were respectively attributable to the rapid decrease of 137 Cs concentration in algae and silt particles attached to rocks on the river floors (Iguchi et al., 2013; Tsuboi et al., 2015), and in zooplankton in the water column (Tomiya et al., 2014), both of which certainly followed the rapid 137Cs decrease in surrounding water (Tomiya et al., 2014; Iwagami et al., 2015). For pond smelt, a two-component model or a single-component model plus a constant term was adopted as a better fitting model than a singlecomponent model (Table 4). This result might reflect the fact that the 137Cs concentration in zooplankton and surrounding lake water changed from rapid decrease to a stagnant phase within a few years after the FDNPP accident. Because the increasing trend of 137Cs concentration expressed by the negative decreasing constant of second component of the two-component model is not expected to extend into the future, long-term and more detailed data are necessary to anticipate future trends precisely and to detect factors affecting 137Cs concentration in pond smelt. 5. Conclusion Radionuclide (131I, 134Cs, and 137Cs) concentrations of monitored freshwater fish species collected from different habitats (rivers, lakes, and culture ponds) in Fukushima Prefecture during March 2011eDecember 2014 (total 16 species, n ¼ 2692) were analyzed. Low concentrations of 131I were detected from only 11 samples collected during MarcheJune 2011, demonstrating that 131I transferred to freshwater fish were not intense. In river and lake fishes, a more gradual decrease and higher radiocesium (134Csþ137Cs) concentration than in culture pond fish were observed, which suggests strongly that radiocesium in freshwater fish was mainly bioaccumulated through the food web in the wild. Longer-term contamination in freshwater fish species (especially lake fish species) than in marine fishes was detected. Higher radiocesium concentrations were found in the northwestern areas from the FDNPP with higher deposition. However, radiocesium contamination levels were regarded as 1e2 orders of magnitude less than those after the Chernobyl accident. A lagged increase of 137Cs concentration and longer Teco were observed in carnivorous salmonids, whereas rapid increase and decrease of 137Cs concentration and shorter Teco were found in herbivorous and planktivorous osmerids with younger age at maturity. Comparison of Teco among salmonids, osmerids, and cyprinids suggests that, in addition to the feeding habits and life-cycles of a fish, hydraulic conditions in rivers and lakes (e.g., turnover time), which are expected to affect radiocesium

concentration in prey items, are an important factor affecting 137Cs decreasing rates of freshwater fish. Acknowledgment We are grateful to T. Iwakami, T. Kawai, T. Ishida, M. Watanabe, T. Sato, K. Konno, K. Sasaki and other staff of the Fukushima Prefectural Inland Water Fisheries Experimental Station for their help with sample processing and measurement. We thank all fishery workers in Fukushima Prefecture who caught freshwater products for monitoring surveys. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.jenvrad.2015.09.017. References Akaike, H., 1987. Factor analysis and AIC. Psychometrika 52, 317e332. Arai, T., 2014. Radioactive cesium accumulation in freshwater fishes after the Fukushima nuclear accident. SpringerPlus 3, 479. Brittain, J.E., Storruste, A., Larsen, E., 1991. Radiocesium in brown trout (Salmo trutta) from a subalpine lake ecosystem after the Chernobyl reactor accident. J. Environ. Radioact. 14, 181e191. Buesseler, K.O., Aoyama, M., Fukasawa, M., 2011. Impacts of the Fukushima Nuclear Power Plants on marine radioactivity. Environ. Sci. Technol. 45, 9931e9935. Bulgakov, A.A., Konoplev, A.V., Smith, J.T., Hilton, J., Comans, R.N.J., Laptevd, G.V., Christyukd, B.F., 2002. Modelling the long-term dynamics of radiocaesium in closed lakes. J. Environ. Radioact. 61, 41e53. Chang, K.H., Hanazato, T., Ueshima, G., Tahara, H., 2005. Feeding habit of pond smelt (Hypomesus transpacificus nipponensis) and its impact on the zooplankton community in Lake Suwa. Jpn. J. Freshw. Ecol. 20, 129e138. Chiba, S., 1988. Water quality of Lake Inawashiro and Lakes in Ura-bandai district. Chigaku Zasshi 97, 376e381 (in Japanese). Chino, M., Nakayama, H., Nagai, H., Terada, H., Katata, G., Yamazawa, H., 2011. Preliminary estimation of release amounts of 131I and 137Cs accidentally discharged from the Fukushima Daiichi Nuclear Power Plant into the atmosphere. J. Nucl. Sci. Tech. 48, 1129e1134. Comans, R.N.J., Middelburg, J.J., Zonderhula, J., Wolttiez, J.R.W., De Lange, G.J., Das, H.A., Van Der Weijden, C.H., 1989. Mobilization of radiocaesium in pore water of lake sediments. Nature 339, 367e369. Elliott, J.M., Hilton, J., Rigg, E., Tullett, P.A., Swift, D.J., Leonard, D.R.P., 1992. Sources of variation in post-Chernobyl radiocaesium in fish from two Cumbrian lakes (north-west England). J. Appl. Ecol. 29, 108e119. FPG (Fukushima Prefectural Government), 2015. Monitoring Information of Environmental Radioactivity Level. http://www.pref.fukushima.lg.jp/sec/16025d/ kukan-monitoring.html (accessed 31.05.15.). Froese, R., Pauly, D., 2000. FishBase 2000. A Global Information System on Fishes: ~ os, Laguna, Philippines. Concepts, Design and Data Sources. ICLARM, Los Ban Fukushima, T., Arai, H., 2014. Radiocesium contamination of lake sediments and fish following the Fukushima nuclear accident and their partition coefficient. Inland Waters 4, 204e214. Furukawa, F., Watanabe, S., Kaneko, T., 2012. Excretion of cesium and rubidium via the branchial potassium-transporting pathway in Mozambique tilapia. Fish. Sci. 78, 597e602. García-Berthou, E., 2001. Size- and depth-dependent variation in habitat and diet of the common carp (Cyprinus carpio). Aquat. Sci. 63, 466e476. Håkanson, L., Andersson, T., Nilsson, Å., 1989. Caesium-137 in perch in Swedish lakes after Chernobyl-present situation, relationships and trends. Environ. Poll. 58, 195e212. Håkanson, L., Andersson, T., Nilsson, Å., 1992. Radioactive caesium in fish in Swedish lakes 1986e1988-general pattern related to fallout and lake characteristics. J. Environ. Radioact. 15, 207e229. Hewett, C.J., Jefferies, D.F., 1976. The accumulation of radioactive caesium from water by the brown trout (Salmo trutta) and its comparison with plaice and rays. J. Fish. Biol. 9, 479e489. Hickman Jr., C.P., Trump, B.F., 1969. The kidney. In: Hoar, W.S., Randall, D.J. (Eds.), Fish Physiology, vol. I. Academic Press, New York, pp. 91e239. IAEA (International Atomic Energy Agency), 2006. Environmental Consequences of the Chernobyl Accident and Their Remediation: Twenty Years of Experience. Report of the Chernobyl Forum Expert Group “Environment”, Vienna. http:// www-pub.iaea.org/mtcd/publications/pdf/pub1239_web.pdf. Iguchi, K., Hino, T., 1996. Effect of competitor abundance on feeding territoriality in a grazing fish, the ayu Plecoglossus altivelis. Ecol. Res. 11, 165e173. Iguchi, K., Fujimoto, K., Kaeriyama, H., Tomiya, A., Enomoto, M., Abe, S., Ishida, T., 2013. Cesium-137 discharge into the freshwater fishery ground of grazing fish, ayu Plecoglossus altivelis after the March 2011 Fukushima nuclear accident. Fish. Sci. 79, 983e988.

T. Wada et al. / Journal of Environmental Radioactivity 151 (2016) 144e155 Iwagami, S., Tsujimura, M., Onda, Y., Nishino, M., Konuma, R., Abe, Y., Hada, M., Pun, I., Sakaguchi, A., Kondo, H., Yamamoto, M., Miyata, Y., Igarashi, Y., 2015. Temporal changes in dissolved 137Cs concentrations in groundwater and stream water in Fukushima after the Fukushima Dai-ichi Nuclear Power Plant accident. J. Environ. Radioact. (in press). Jagoe, C.H., Sallas, C.E., Chesser, R.K., Smith, M.H., Lingenfelser, S.K., Lingenfelser, J.T., Holloman, K., lomakin, M., 1998. Contamination near Chernobyl: radiocaesium, lead and mercury in fish and sediment radiocaesium from waters within the 10 km zone. Ecotoxicol 7, 201e209. Janssens A., 2013. EU basic safety standards and European response to the Fukushima accident. Radioprotection 48, S19eS26. Jonsson, B., Forseth, T., Ugedal, O., 1999. Chernobyl radioactivity persists in fish. Nature 400, 417. Kanou, K., Saito, S., Fuchigami, S., Imamura, A., Imai, H., Taki, Y., 2007. Occurrence patterns and food habits of introduced alien loach Paramisgurnus dabryanus and native loach Misgurnus anguillicaudatus at irrigation drainages around rice fields in the Watarase River System, central Honshu. Jpn. Aquac. Sci. 55, 109e114 (in Japanese with English abstract). Kasamatsu, F., 1999. Marine organisms and radionuclides with special reference to the factors affecting concentrations of 137Cs in marine fish. Radioisotopes 48, 266e282 (in Japanese). Katayama, S., Radtke, R., Omori, M., Shafer, D.J., 2000. Coexistence of anadromous and resident life history styles of pond smelt, Hypomesus nipponensis, in Lake Ogawara, Japan, as determined by analyses of otolith structure and strontium: calcium ratios. Environ. Biol. Fish. 58, 195e201. Kato, T., 1980. Relation between age at maturity and growth of kokanee, Oncorhynchus nerka, in Lake Towada. Bull. Natl. Res. Inst. Aquac. 1, 7e19 (in Japanese with English abstract). Kikko, T., Nemoto, M., Ban, S., Saegusa, J., Sawada, N., Ishizaki, D., Nakahashi, T., Teramoto, N., Fujioka, Y., 2013. Efficient rearing of larvae and juveniles of Honmoroko Gnathopogon caerulescens in paddy fields. Aquac. Sci. 61, 303e309 (in Japanese with English abstract). Konno, K., Sakano, H., 2010. Zooplankton Selectivity by Lacustrine Sockeye Salmon Oncorhynchus nerka in Lake Numazawa, Fukushima Prefecture, Japan, vol. 58, pp. 121e126 (in Japanese with English abstract). Koulikov, A.O., Ryabov, I.N., 1992. Specific cesium activity in freshwater fish and the size effect. Sci. Total Environ. 112, 125e142. Koulikov, A.O., 1996. Physiological and ecological factors influencing the radiocaesium contamination of fish species from Kiev reservoir. Sci. Total Environ. 177, 125e135. Kryshev, I.I., 1995. Radioactive contamination of aquatic ecosystems following the Chernobyl accident. J. Environ. Radioact. 27, 207e219. MAFF (Japan Ministry of Agriculture, Forestry and Fisheries), 2015. Results of the Inspection on Radioactivity Materials in Fisheries Products. http://www.jfa. maff.go.jp/j/housyanou/kekka.html (accessed 31.05.15.). Matsuda, K., Takagi, K., Tomiya, A., Enomoto, M., Tsuboi, J., Kaeriyama, H., Ambe, D., Fujimoto, K., Ono, T., Uchida, K., Morita, T., Yamamoto, S., 2015. Comparison of radioactive cesium contamination of lake water, bottom sediment, plankton, and freshwater fish among lakes of Fukushima Prefecture, Japan after the Fukushima fallout. Fish. Sci. 81, 737e747. MEXT (Ministry of Education, Culture, Sports, Science and Technology in Japan), 2003. Radioactivity Measurement Series 16. http://www.kankyo-hoshano.go. jp/series/lib/No16.pdf (accessed 31. 05. 15.). MHLW (Japan Ministry of Health, Labour and Welfare), 2015. Information on the Great East Japan Earthquake (accessed 31. 05. 15.). http://www.mhlw.go.jp/ english/topics/2011eq/index.html. Mikami, S., Maeyama, T., Hoshide, Y., Sakamoto, R., Sato, S., Okuda, N., Demongeot, S., Gurriaran, R., Uwamino, Y., Kato, H., Fujiwara, M., Sato, T., Takemiya, H., Saito, K., 2015. Spatial distributions of radionuclides deposited onto ground soil around the Fukushima Dai-ichi Nuclear Power Plant and their temporal change until December 2012. J. Environ. Radioact. 139, 320e343. Mizuno, T., Kubo, H., 2013. Overview of active cesium contamination of freshwater fish in Fukushima and eastern Japan. Sci. Rep. 3, 1742. MOE (Japan Ministry of the Environment), 2011. Results of the Inspection on Radionuclide Monitoring for Public Water Bodies in Fisheries Prefecture in September and October 2011. http://www.env.go.jp/jishin/monitoring/results_ r-pw.html (accessed 31.05.15.). Nagao, S., Kanamori, M., Ochiai, S., Tomihara, S., Fukushi, K., Yamamoto, M., 2013. Export of 134Cs and 137Cs in the Fukushima river systems at heavy rains by Typhoon Roke in September 2011. Biogeosciences 10, 6215e6223. Nakamura, T., 2012. Present status and future conservation of fluvial charr (Salvelinus spp.) and salmon (Oncorhynchus spp.) populations in Japanese mountain streams. Jpn. J. Ichthyol. 59, 163e167 (in Japanese). Povinec, P.P., Hirose, K., Aoyama, M., 2013. Fukushima Accident: Radioactivity Impact on the Environment. Elsevier, Amsterdam, pp. 1e382. Rowan, D.J., Rasmussen, J.B., 1994. Bioaccumulation of radiocesium by fish: the influence of physicochemical factors and trophic structure. Can. J. Fish. Aquat.

155

Sci. 51, 2388e2410. Saito, K., Tanihata, I., Fujiwara, M., Saito, T., Shimomura, S., Otsuka, T., Onda, Y., Hoshi, M., Ikeuchi, Y., Takahashi, F., Kinouchi, N., Saegusa, J., Seki, A., Takemiya, H., Shibata, T., 2015. Detailed deposition density maps constructed by large-scale soil sampling for gamma-ray emitting radioactive nuclides from the Fukushima Dai-ichi Nuclear Power Plant accident. J. Environ. Radioact. 139, 308e319. Sårkkå, J., Jåmså, Al, Luukko, A., 1995. Chernobyl-derived radiocaesium in fish as dependent on water quality and lake morphometry. J. Fish. Biol. 46, 227e240. Smith, J.T., Kudelsky, A.V., Ryabov, I.N., Hadderingh, R.H., 2000. Radiocaesium concentration factors of Chernobyl-contaminated fish: a study of the influence of potassium, and “blind” testing of a previously developed model. J. Environ. Radioact. 48, 359e369. Sohtome, T., Wada, T., Mizuno, T., Nemoto, Y., Igarashi, S., Nishimune, A., Aono, T., Ito, Y., Kanda, J., Ishimaru, T., 2014. Radiological impact of TEPCO's Fukushima Dai-ichi Nuclear Power Plant accident on invertebrates in the coastal benthic food web. J. Environ. Radioact. 138, 106e115. € Sundbom, M., Meili, M., Andersson, E., Ostlund, M., Broberg, A., 2003. Long-term dynamics of Chernobyl 137Cs in freshwater fish: quantifying the effects of body size and trophic level. J. Appl. Ecol. 40, 228e240. Suzuki, K., Kimura, S., 1977. Growth of the crucian carps belonging to the genus Carassius in the lower reaches of the Nagara River, central Japan. Jpn. J. Ichthol 24, 199e206 (in Japanese with English abstract). Tamate, T., 2002. Age and size at maturity of Japanese smelt (Hypomesus nipponensis) in Shumarinai Lake, northern Hokkaido, Japan. Res. Bull. Hokkaido Univ. For. 2, 99e102 (in Japanese with English abstract). Tazoe, H., Hosoda, M., Sorimachi, A., Nakata, A., Yoshida, M.A., Tokonami, S., Yamada, M., 2012. Radioactive pollution from Fukushima Daiichi Nuclear Power Plant in the terrestrial environment. Radiat. Prot. Dosim. 152, 198e203. Tomiya, A., Enomoto, M., Kawata, G., 2014. Elucidation of radionuclide transfer mechanisms in pond smelt and kokanee. Annual report of the Fukushima Prefectural Inland Water Fisheries experimental station. Fisc. Year 2013, 72e76 (in Japanese). Tsuboi, J., Abe, S., Fujimoto, K., Kaeriyama, H., Ambe, D., Matsuda, K., Enomoto, M., Tomiya, A., Morita, T., Ono, T., Yamamoto, S., Iguchi, K., 2015. Exposure of a herbivorous fish to 134Cs and 137Cs from the riverbed following the Fukushima disaster. J. Environ. Radioact. 141, 32e37.  , R., 1992. Effects of temperature and Ugedal, O., Jonsson, B., Njåstad, O., Næumann body size on radiocaesium retention in brown trout, Salmo trutta. Freshw. Biol. 28, 165e171. Ugedal, O., Forseth, T., Jonsson, B., Njåstad, O., 1995. Sources of variation in radiocaesium levels between individual fish from a Chernobyl contaminated Norwegian lake. J. Appl. Ecol. 32, 352e361. Vanderploeg, H.A., Parzyck, D.C., Wilcox, W.H., Kercher, J.R., Kaye, S.V., 1975. Bioaccumulation Factors for Radionuclides in Freshwater Biota. Report No. ORNL5002. Oak Ridge, National Laboratory, Oak Ridge, TN. Vilizzi, L., Walker, K.F., 1999. Age and growth of the common carp, Cyprinus carpio, in the River Murray, Australia: validation, consistency of age interpretation, and growth models. Environ. Biol. Fish. 54, 77e106. Wada, T., Nemoto, Y., Shimamura, S., Fujita, T., Mizuno, T., Sohtome, T., Kamiyama, K., Morita, T., Igarashi, S., 2013. Effects of the nuclear disaster on marine products in Fukushima. J. Environ. Radioact. 124, 246e254. Wakeford, R., 2011. And now, Fukushima. J. Radiol. Prot. 31, 167e176. Yamamoto, K., Hirano, O., 1988. Changes of oxygen consumption in rose bitterling, field gudgeon, common minnow, dark chub and common carp under progressive hypoxia. Aquac. Sci. 36, 45e48 (in Japanese with English abstract). Yamamoto, K., Hirano, O., Igagami, T., Nagashima, H., Raita, T., 1986. Changes of oxygen consumption in the gengorou-funa, gin-funa, largemouth bass and kamatsuka under progressive hypoxia. Aquac. Sci. 34, 179e183 (in Japanese with English abstract). Yamamoto, S., Yokoduka, T., Fujimoto, K., Takagi, K., Ono, T., 2014a. Radiocaesium concentrations in the muscle and eggs of salmonids from Lake Chuzenji, Japan, after the Fukushima fallout. J. Fish. Biol. 84, 1607e1613. Yamamoto, S., Mutou, K., Nakamura, H., Miyamoto, K., Uchida, K., Takagi, K., Fujimoto, K., Kaeriyama, H., Ono, T., 2014b. Assessment of radiocaesium accumulation by hatchery-reared salmonids after the Fukushima nuclear accident. Can. J. Fish. Aquat. Sci. 71, 1772e1775. Yoshimura, K., Onda, Y., Sakaguchi, A., Yamamoto, M., 2015. An extensive study of the concentrations of particulate/dissolved radiocaesium derived from the Fukushima Dai-ichi Nuclear Power Plant accident in various river systems and their relationship with catchment inventory. J. Environ. Radioact. 139, 370e378. Yoshimura, M., Yokoduka, T., 2014. Radioactive contamination of fishes in lake and streams impacted by the Fukushima nuclear power plant accident. Sci. Total Environ. 482e483, 184e192. Zibold, G., Klemt, E., 2005. Ecological half-times of 137Cs and 90Sr in forest and freshwater ecosystems. Radioprotection 40 (Suppl. 1), S497eS502.