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Radiocesium Concentrations and Body Size of Freshwater Fish in Lake Hayama 1 Year After the Fukushima Dai-Ichi Nuclear Power Plant Accident

, Abstract We measured radiocesium ( 134 Cs + 137 Cs) concentrations in ﬁ ve freshwater ﬁ sh species in Lake Hayama, Fukushima Prefecture, 1 year after the Fukushima Daiichi Nuclear Power Plant (FNPP) accident in March 2011. The ﬁ ve species included bluegill ( Lepomis macrochirus ), Carassius spp. ( Carassius auratus langsdorﬁ i and Carassius cuvieri ), Japanese dace ( Tribolodon hakonensis ), largemouth bass ( Micropterus salmoides ), and smallmouth bass ( Micropterus dolomieu ). We observed a “positive size effect” for radiocesium concentrations in ﬁ sh muscle, but the coefﬁ cient of determination was low for bluegill, Carassius spp., and Japanese dace. In contrast, the coefﬁ cient of determination was high for the exponential relationship between body size and radiocesium concentrations in largemouth and smallmouth bass. The geometric mean radiocesium concentration in each body size class was generally higher for carnivorous ﬁ sh than for omnivorous and herbivorous ﬁ sh.


Introduction
The Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident released a large concentration of nuclides, including 131 I, 134 Cs, and 137 Cs, into the atmosphere (Butler 2011 ;Chino et al. 2011 ). The Tokyo Electric Power Co. ( 2012 ) estimated the total amount of 131 I, 134 Cs, and 137 Cs released during March 2011 to be approximately 500 PBq, approximately 10 PBq, and approximately 10 PBq, respectively. Because the half-life of 137 Cs is relatively long (30.2 years), contamination of the ecosystem is expected to be long lasting. Following the Chernobyl nuclear power plant accident, research showed that the chemical composition of the water (e.g., potassium levels) and the rate of circulation or turnover of water in freshwater systems affects the bioaccumulation of radiocesium in fi sh (Elliot et al. 1992 ;Saxén and Koskelainen 1992 ;Rask et al. 2012 ). In addition to these environmental factors, fi sh body size is often correlated with radiocesium concentrations in fi sh (Elliot et al. 1992 ;Koulikov and Ryabov 1992 ;Smith et al. 2002 ). Fish body size may be a proxy for age and life stage, with the latter being associated with differences in traits such as feeding ecology and metabolism. The excretion rates for radiocesium are higher in younger age groups than in older age classes. Furthermore, the decrease in radiocesium concentrations in water over time also results in lower radiocesium levels in younger fi sh (Kryshev and Ryabov 2000 ). Under these conditions, it is likely that radiocesium levels in fi sh will be a positive function of size.
As described in Chapter 15 , the Fisheries Research Agency has conducted radiocesium monitoring of freshwater fi sh, lake water, sediment, and plankton in three lakes (Lake Akimoto, Lake Tagokura, and Lake Hayama) in Fukushima Prefecture since 2012. Lake Hayama ( Fig. 16.1 ), the lake nearest to the FNPP among the three lakes, is a small artifi cially dammed lake (~60 m maximum depth , 36.2 × 106 m 3 gross capacity of reservoir) in the Mano River system. This lake is located within a 30-50 km radius of the FNPP. The lake is also located in the area that was subject to high levels of radiocesium deposition (~300-600 kBq/m 2 ) in the period to 28 June 2012 (Ministry of Environment 2012a ) as it was in the pathway of the radioactive plume from the FNPP. Indeed, Lake Hayama received the highest deposition of radiocesium among the lakes that are locally important for recreational fi shing.
The concentration of radiocesium decreased in the water of Lake Hayama between the accident and 2012 (Chap. 15 ). Thus, we hypothesized that there would be a positive relationship between radiocesium concentrations in fi sh and fi sh body size in Lake Hayama. To test this, we measured radiocesium concentrations in individuals from the fi ve dominant species in Lake Hayama in 2012, including bluegill ( Lepomis macrochirus ), Carassius spp. ( Carassius auratus langsdorfi i and Carassius cuvieri ), Japanese dace ( Tribolodon hakonensis ), largemouth bass ( Micropterus salmoides ), and smallmouth bass ( Micropterus dolomieu ).

Fish Species and Lake Water
The fi ve dominant fi sh species in Lake Hayama (bluegill, Carassius spp., Japanese dace, largemouth bass, and smallmouth bass) were collected by gillnet during 2012 (see Chapter 15 ). Bluegill, largemouth bass, and smallmouth bass are invasive species. These three species have been observed in lakes and rivers in Fukushima Prefecture since the 1990s. Smallmouth bass were the most dominant species in our surveys in 2012. Largemouth bass and smallmouth bass are carnivorous whereas bluegill, Carassius spp., and Japanese dace are omnivorous, and Carassius spp. is also herbivorous. Although there are few biological data for Lake Hayama, the fi ve species we collected typically live for several years, so it is likely that some of the fi sh we collected were exposed to the fallout at the time of the accident in 2011.
The environmental characteristics of Lake Hayama are described in Chapter 15 . The concentration of radiocesium in the surface water of Lake Hayama was 89 mBq/l from September to November 2012 (Table 15.2 ). According to the Ministry of Environment ( 2011 ), 134 Cs and 137 Cs levels had declined to less than 1 Bq/l by September 2011 in the surface water of Lake Hayama whereas levels at the bottom of the lake were 10 and 12 Bq/l, respectively, at this time. From August to November 2012, levels of 134 Cs and 137 Cs decreased to less than 2 Bq/l and less than 3 Bq/l, respectively, in the water immediately above the lake bed (Ministry of Environment 2012b , 2013a ). Thus, radiocesium concentrations decreased rapidly in the water of Lake Hayama during the fi rst year after the fallout.

"Positive Size Effect" on Radiocesium Concentrations in Five Freshwater Fish Species
The total length (TL) distribution for the fi ve fi sh species is shown in Fig. 16.2 . The TL of bluegill, Carassius spp., and Japanese dace ranged from 86 to 163 mm, 217 to 461 mm, and 220 to 374 mm, respectively ( Fig. 16.2 ). Both largemouth and smallmouth bass had a wider range of TL, 80-545 mm and 79-457 mm, respectively ( Fig. 16.2 ). Because we used gill nets to capture fi sh, it is likely that small Carassius spp. and Japanese dace (TL < 200 mm) were not captured. Conversely, small bluegill, smallmouth bass, and largemouth bass have a high body height so are more susceptible to capture in our gill nets. The small-sized Carassius spp. and Japanese dace represent younger fi sh including age 0 and 1 (Suzuki and Kimura 1977 ;Liu et al. 1986 ;Ishizaki et al. 2009 ). Judging from our data and the information of age and growth for largemouth and smallmouth bass (Yodo and Kimura 1996 ;Nakamura et al. 2004 ), we assume that the samples of these two species included age 0 and older fi sh. The bluegill we captured were likely older than age 0, although their growth varies considerably with population size structure (Drake et al. 1997 ;Belk 1995 ). Taken together, these observations suggest that we obtained both age 0 and older fi sh only for largemouth and smallmouth bass.

Infl uence of Diet on Radiocesium Concentrations in Freshwater Fish
Both younger and older fi sh are needed to detect the positive size effect described by Kryshev and Ryabov ( 2000 ). We found evidence for a positive size effect in carnivorous bass, the only species for which we were able to obtain both young and old individuals. We compared the radiocesium levels in fi sh from different trophic positions, although we only collected older individuals from omnivorous and herbivorous species.
The geometric mean radiocesium concentrations by body size class (interval of 100 mm TL) for each species are given in Table 16.1 . The geometric mean radiocesium concentration in each size class ( n > 2) was higher for carnivorous fi sh than for omnivorous or herbivorous fi sh, suggesting that trophic position is an important determinant of species-specifi c concentrations. Only two exceptions to this pattern were observed, in bluegill in the 100 mm < TL ≤ 200 mm size class, and in Japanese dace in the 200 mm < TL ≤ 300 mm size class. Such exceptions may be a function of different life stages; adult (older) omnivorous and herbivorous fi sh have higher levels than younger carnivorous fi sh.
We speculate that the larger largemouth and smallmouth bass individuals, which had relatively high radiocesium concentrations, were adults at the time the FNPP accident occurred. These individuals have likely preyed continuously upon radiocesium-contaminated insects and fi shes since the time of the accident. Because of their low rate of metabolism, much of the radiocesium was retained within their body during the year following the fallout. In contrast, smaller bass (≤200 mm TL) were likely juveniles (1 year old or younger), larvae, eggs, or did not exist at the time of the FNPP accident. Even if these younger individuals consumed highly contaminated prey items after the fallout from the FNPP, they would still likely have lower radiocesium concentrations than older fi sh because of their high metabolic rate and dilution resulting from tissue growth.
The radiocesium concentrations in fi sh were variable, but generally high in the diet items of omnivorous and herbivorous fi sh, such as bluegill, Carassius spp., and Japanese dace in 2012. Radiocesium concentrations in Spirogyra and aquatic insects fl uctuated from 94 to 1,870 Bq/kg wet weight and from 92 to 1,100 Bq/kg wet weight, respectively (Ministry of Environment 2012c, 2013b. Thus, the concentration of radiocesium in Spirogyra was as high as in small fi sh (≤200 mm TL) in our study (Table 16.1 ). Given this, even herbivorous Carassius spp. are susceptible to radiocesium. Lake Hayama was located in the zone of high radiocesium deposition, so fi sh are likely exposed to radiocesium from the surrounding forest ecosystem. Compared with European forests, the forests in Japan experience a warmer climate with higher mean annual precipitation. These differences make it likely that Japanese forests will circulate radiocesium deposited by the FNPP accident more rapidly than did the European forests following the Chernobyl accident (Hashimoto et al. 2013 ). Indeed, the levels of radiocesium in trees dropped rapidly during the fi rst 2 years after the fallout, but radiocesium in the soil surface organic layer and soil surface layer (0-5 cm) components kept the same level during 2012-2013 (Forestry Agency 2014 ). During this period, fi sh in Lake Hayama were likely exposed to radiocesium from the organic components of the surrounding forest through the food web. Further monitoring of radiocesium concentrations in fi sh (including information on body size and age) is needed to predict the long-term dynamics of radiocesium concentrations in fi sh.