Radioactive contamination of fishes in lake and streams impacted by the Fukushima nuclear power plant accident

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<ul><li><p>Science of the Total Environment 482483 (2014) 184192</p><p>Contents lists available at ScienceDirect</p><p>Science of the Total Environment</p><p>j ourna l homepage: www.e lsev ie r .com/ locate /sc i totenv</p><p>Radioactive contamination of fishes in lake and streams impacted by theFukushima nuclear power plant accident</p><p>Mayumi Yoshimura a,, Tetsuya Yokoduka b</p><p>a Kansai Research Center, Forestry and Forest Products Research Institute, Nagaikyuutaro 68, Momoyama, Fushimi, Kyoto 612-0855, Japanb Tochigi Prefectural Fisheries Experimental Station, Sarado 2599, Ohtawara, Tochigi 324-0404, Japan</p><p>H I G H L I G H T</p><p> Concentration of 137Cs in brown trout was higher than in rainbow trout. 137Cs concentration of brown trout in a lake was higher than in a stream. 137Cs concentration of stream charr was higher in region with higher aerial activity. Concentration of 137Cs in stream charr was higher in older fish. Difference of contamination among fishes was due to difference in diet and habitat.</p><p> Corresponding author. Tel.: +81 75 611 1201; fax: +E-mail address: yoshi887@ffpri.affrc.go.jp (M. Yoshim</p><p>http://dx.doi.org/10.1016/j.scitotenv.2014.02.1180048-9697/ 2014 Elsevier B.V. All rights reserved.</p><p>a b s t r a c t</p>a r t i c l e i n f o<p>Article history:Received 27 November 2013Received in revised form 19 February 2014Accepted 25 February 2014Available online 18 March 2014</p><p>Keywords:Brown troutCharrLakeRadioactive cesiumStomach contentsStream</p><p>The Fukushima Daiichi Nuclear Power Plant (FDNPP) accident in March 2011 emitted radioactivesubstances into the environment, contaminating a wide array of organisms including fishes. We foundhigher concentrations of radioactive cesium (137Cs) in brown trout (Salmo trutta) than in rainbowtrout (Oncorhynchus nerka), and 137Cs concentrations in brown trout were higher in a lake than in astream. Our analyses indicated that these differences were primarily due to differences in diet, but thathabitat also had an effect. Radiocesium concentrations (137Cs) in stream charr (Salvelinus leucomaenis)were higher in regions with more concentrated aerial activity and in older fish. These results were alsoattributed to dietary and habitat differences. Preserving uncontaminated areas by remediating soilsand releasing uncontaminated fish would help restore this popular fishing area but would require a sig-nificant effort, followed by a waiting period to allow activity concentrations to fall below the thresholdlimits for consumption.</p><p> 2014 Elsevier B.V. All rights reserved.</p><p>1. Introduction</p><p>A massive earthquake occurred in eastern Japan on 11 March 2011,causing a tsunami that washed over the Fukushima Daiichi NuclearPower Plant (FDNPP) on the east coast of Japan. Damage to the coolingsystem of the FDNPP resulted in several explosions, causing leakage of ra-dioactive substances. The FDNPP accident released 1.6 1017 Bq ofiodine-131 (131I), 1.8 1016 Bq of cesium-134 (134Cs) and 1.5 1016 Bqof cesium-137 (137Cs) into the surrounding environment (Oharaet al., 2011). Most of these radionuclides, including 131I, 134Cs and137Cs, were unevenly deposited over large areas of land in eastern</p><p>81 75 611 1207.ura).</p><p>Japan, reaching sites hundreds of kilometers from the FDNPP. Thedense radioactive plume spewing from the FDNPP moved north-westward, descending to ground level with precipitation and heavilycontaminating large tracts of the landscape. A smaller plume driftedto the south-west and contaminated areas such as the Oku Nikko andAshio regions in Tochigi Prefecture (Kinoshita et al., 2011; MEXT,2011). Atmospheric dose rates 0.5 m above the ground exceeded20 Sv/h in some hot spots N160 km from the FDNPP in May 2011(Tochigi, 2011).</p><p>The first phase of investigation revealed that a large portion of thedeposited 134Cs and 137Cs was trapped in the forest canopies and thesoil litter layer (Hashimoto et al., 2012). Radiocesium is easily adsorbedonto clay minerals and soil organic matter (Kruyts and Delvaux, 2002)and can be transported to streams and rivers with eroded soils(Fukuyama et al., 2005; Kato et al., 2010; Wakiyama et al., 2010).Dissolved 134Cs and 137Cs in running waters that are not adsorbed tosoil, are readily taken up by microbes, algae, plankton and plants. This</p>http://crossmark.crossref.org/dialog/?doi=10.1016/j.scitotenv.2014.02.118&amp;domain=pdfhttp://dx.doi.org/10.1016/j.scitotenv.2014.02.118mailto:yoshi887@ffpri.affrc.go.jphttp://dx.doi.org/10.1016/j.scitotenv.2014.02.118http://www.sciencedirect.com/science/journal/00489697</li><li><p>185M. Yoshimura, T. Yokoduka / Science of the Total Environment 482483 (2014) 184192</p><p>pathway of 134Cs and 137Cs transport eventually leads to uptake by fishesat higher trophic levels.</p><p>Radioactive contamination of fish should be prevented becausefishes may be taken by anglers and consumed as food. A safetythreshold of 100 Bq/kg of radioactive Cs was introduced in April2012, but activity concentrations greater than this have been detect-ed in fishes hundreds of kilometers distant from the FDNPP. There isclearly a pressing imperative to reduce radioactive Cs contaminationof food.</p><p>The Chernobyl accident released more than five million TeraBecquerel of radionuclides. Much radionuclides from the Chernobylaccident spread to Finland, Sweden and Norway, 2000 km to thenorthwest. Fish have been monitored for radioactivity vreHeimdalsvatn, a Norwegian subalpine lake (Brittain et al., 1991;Brittain and Gjerseth, 2010). Activity concentrations of 137Cs inbrown trout reached 8400 Bq/kg in 1987 and declined to 200300 Bq/kg in 2008, but the contamination level has recently beenconstant and approached an asymptotic decline (Brittain andGjerseth, 2010). The broad effects of the Chernobyl accident havebeen examined and management measures have been designed forlarge geographical areas (Report of the Chernobyl Forum ExpertGroup Environment, 2006; Yablokov et al., 2009). However, theecological consequences of radioactive contamination in fishes arepoorly understood.</p><p>To precisely describe the mechanisms of diffusion and export of137Cs deposited in freshwater fish, we measured concentrations of137Cs in the muscle tissue and stomachs of brown trout (Salmo trutta),rainbow trout (Oncorhynchus mykiss) and kokanee (Oncorhynchusnerka) from a lake, that of brown trout (Salmo trutta) from a streamand that of charr (Salvelinus leucomaenis) from four streams. Here, wereport the results of preliminary investigations 21 months after theFDNPP accident.</p><p>2. Materials and methods</p><p>2.1. Study site</p><p>The study was conducted in the Nikko area (Lake Chuzenji, OkuNikko and Ashio regions) located approximately 160 km south-west of the FDNPP. According to an aircraft radioactivity surveyreported by MEXT (2012), the air dose rate in this area was0.10.25 Sv/h on 31 May 2012. The study area is mostly forested;the dominant tree species are broadleaf and deciduous. Otherareas are forested with Japanese cedar and cypress plantationsused for timber production. The field survey was conducted inLake Chuzenji and two headwater tributaries (Toyamasawa andYanagisawa streams) of the Kinu River in the Oku Nikko regionand in two headwater tributaries (Kuzosawa and Asosawastreams) of the Watarase River in the Ashio region, which formthe upper drainage component of the Tone River system, Honshu,Japan (Fig. 1).</p><p>2.2. Sampling</p><p>Fishes were captured in Lake Chuzenji and in the four streams inNovember and December, 2012 using fishing rod in the lake andbattery-powered backpack electrofishing (Smith-Root Inc. LR-24)units operated at 300-V pulse-DC in the stream. In central LakeChuzenji, three species of fishes, brown trout (Salmo trutta),rainbow trout (Oncorhynchus mykiss) and kokanee (salmon)(Oncorhynchus nerka) were sampled. In Toyamasawa stream, twospecies of fish, brown trout (Salmo trutta) and charr (Salvelinusleucomaenis) were sampled at site B (200 m stream segments). Inother three streams, only charr (Salvelinus leucomaenis) were sam-pled at sites E, G, and I (200 m stream segments). After capture, werecorded the body size (fork length) of each fish and sampled</p><p>muscle tissue for the analysis of radioactive concentration. Wethen collected and froze the stomachs for the analysis ofradiocesium concentrations in stomach tissue and for identificationof stomach contents. The age of charr specimens was determinedfrom sagittal otoliths using the surface reading method. The ageof the other three fishes was not determined; folk length wasused as a substitute metric.</p><p>In the four streams, air dose rates at 1-m above ground weremeasured with a survey meter adjacent to the stream (NaIscintillation counter; ALOKA TCS-172). Electrical conductivities(EC) of the streams were measured with a portable compacttwin conductivity meter (B-173; Horiba); pH was measuredwith a portable compact twin pH meter (B-212; Horiba). Wettedstream widths (SW) were measured with a measuring tape;stream velocities were measured with a portable meter (V-303,VC-301, KENEK). All of these environmental parameters weremeasured in stream riffles at each site along Toyamasawa stream(sites A, B, and C), Yanagisawa stream (sites D, E, and F),Kuzosawa stream (sites G and H) and Asosawa stream (site I)in December, 2012.</p><p>2.3. Radiocesium analysis and identification</p><p>Samples of fish stomach andmuscle tissuewere directly packed into100-ml polystyrene containers (U-8). The radioactive levels of 137Cs(662 keV) were measured with an HPGe coaxial detector system(GEM40P4-76, GEM20-70, Seiko EG&amp;G, Tokyo, Japan; GC4020, Canberra,Japan) for 36,000 s63,000 s depending on the sample weight.Gamma-ray peaks of 622 keV were used to determine 137Cs. Themeasurement system was calibrated using a standard gamma-raysource (MX033U8PP, Japan Radioisotope Association, Tokyo,Japan), and a standard soil sample (IAEA-444) was used to check ac-curacy. Fine adjustments to the measurements were made to corre-spond to the radiocesium concentration value for 1 December2012. The radioactivity of lake and stream water was not measuredbecause 137Cs concentrations in several lakes and streams were re-ported to be below the detection level (1 Bq/l) (MOE 2013, TochigiPrefecture, 2013).</p><p>The inner contents of the frozen stomach for the analysis ofstomach contents were removed and identified under a 50 mi-croscope (SMZ-U; Nikon). We identified specimens to the familylevel or higher following Merritt and Cummins (1996) and Kawai(1985).</p><p>2.4. Statistical analysis</p><p>KruskalWallis tests or MannWhitney U-tests were used to com-pare the 137Cs concentrations. The Kendall test was used to clarify therelationship between folk length and 137Cs concentration. We conduct-ed principal component analysis (PCA) on the presence or absence ofeach fish stomach content for three species in Lake Chuzenji, forbrown trout in Lake Chuzenji and Toyamasawa stream, and for charrin the four streams. We examined the PCA axes among the three fishspecies and among the four streams using a KruskalWallis multiplecomparison test and between lake and stream habitats using a MannWhitney U-test.</p><p>It would be useful to compare samples of the same species or thesame age at all sampling locations. However, the fishes sampled inthis study differed between the stream and lake and it was notpractical to collect specimens of equal size. Statistical analysis wasperformed using SYSTAT version 10 (SPSS Inc. 2000). Radiocesiumconcentrations that were below the detection level because of insuf-ficient weight for radiocesium analysis were excluded from thestatistical analysis.</p></li><li><p>Fig. 1. Study site of Lake Chuzenji and four streams in the Oku Nikko and Ashio areas, Tochigi Prefecture, Japan. AI: stream water sampling sites, B, E, G, I: fish sampling sites.</p><p>186 M. Yoshimura, T. Yokoduka / Science of the Total Environment 482483 (2014) 184192</p><p>3. Results</p><p>Aerial radioactivity was higher in the Ashio region than in theOku Nikko region (z = 2.33, n = 9, P b 0.05, MannWhitney U-test;Table 1), as was radiocesium deposition. These two regions did not dif-fer in air orwater temperature, pH, streamwidth or stream velocity, butEC differed between the regions (Table 1; Yoshimura andAkama, 2014).</p><p>137Cs concentrations in fish stomachs were highest in browntrout (Salmo trutta), lowest in rainbow trout (Oncorhynchusmykiss) and intermediate in kokanee (salmon) (Oncorhynchusnerka) (H = 11.1, n = 14, P b 0.005, KruskalWallis test; Fig. 2).137Cs concentrations in fish muscle showed the same patternamong species (H = 590.5, n = 69, P b 0.0001, KruskalWallis</p><p>Table 1The dose rate at 1 m above the ground, air temperature, water temperature, pH, electric conduc</p><p>Oku Nikko</p><p>Toyamasawa Yanagisaw</p><p>A B C D</p><p>Dose rate (Sv/h) 0.08 0.10 0.12 0.09Air temperature (C) 0.8 1.7 0.7 0.1Water temperature (C) 7.2 6.8 7.3 8.1pH 6.9 7.0 7.1 6.7Electric conductivity (s/cm) 61 50 49 53Stream velocity (cm/s) 30 63 32 48Stream widths (m) 7.6 5.7 4.8 17.1Altitude (m) 1270 1300 1450 1270</p><p>*: P b 0.05.</p><p>test; Fig. 2). Radioactive Cs concentrations in stomach and muscletissues did not differ significantly among the three species. Therewas no relationship between 137Cs concentrations in fish muscleand fork length in three species (brown trout: = 0.27, n = 23,n.s.; kokanee: = 0.02, n = 24, n.s.; rainbow trout: = 0.17, n = 22,n.s.; Kendall test).</p><p>Stomach contents varied significantly among the three speciesof fish (Appendix A). Brown trout stomachs primarily containedfish and unknown digested foods. Kokanee primarily contained un-known foods and rainbow trout stomachs contained a wide varietyof fish and invertebrates. The first PCA axis explained 52% of thevariation in the stomach contents (mainly the number of speciesconsumed) but was not correlated with muscle concentration of</p><p>tivity, stream velocity and streamwidth at 9 sites onDecember 2012with statistical result.</p><p>Ashio</p><p>a Kuzosawa Asosawa U-test</p><p>E F G H I z</p><p>0.10 0.11 0.26 0.21 0.27 2.33*6.4 6.7 1.3 1.7 1.9 0.654.9 2.6 4.0 4.2 1.6 1.816.4 6.9 6.5 6.3 6.8 1.56</p><p>33 51 73 59 64 2.07*35 58 70 68 57 1.815.8 8.1 3.0 3.5 5.8 2.69</p><p>1320 1380 810 950 790 2.33*</p></li><li><p>0</p><p>50</p><p>100</p><p>150</p><p>200</p><p>0 100 200 300 400 500 600</p><p>137 C</p><p>s (B</p><p>q/k</p><p>g)</p><p>Fork length (mm)Brown trout (stomach) Kokanee (stomach) Rainbow trout (stomach)</p><p>b</p><p>0</p><p>50</p><p>100</p><p>150</p><p>200</p><p>0 200 400 600 800</p><p>137 C</p><p>s (B</p><p>q/k</p><p>g)</p><p>Fork length (mm)</p><p>Brown trout Kokanee Rainbow trout</p><p>a</p><p>Fig. 2. Relationship between body length and 137Cs concentration of three species in LakeChuzenji. (a) Muscle; (b) stomach.</p><p>0</p><p>50</p><p>100</p><p>150</p><p>200</p><p>0 100 200 300 400 500 600</p><p>Fork length (mm)Chuzenji Lake Toyamasawa</p><p>a</p><p>0</p><p>50</p><p>100</p><p>150</p><p>200</p><p>0 100 200 300 400 500 600</p><p>Fork length (mm)Chuzenji Lake (stomach) Toyamasawa (stomach)</p><p>b</p><p>137 C</p><p>s (B</p><p>q/k</p><p>g)</p><p>137 C</p><p>s (B</p><p>q/k</p><p>g)</p><p>Fig. 4. Relationship between body length and 137Cs concentration in brown trout fromLake Chuzenji and Toyamasawa stream. (a) Muscle; (b) stomach.</p><p>0.8</p><p>Lake</p><p>187M. Yoshimura, T. Yokoduka / Science of the Total Environment 482483 (2014) 184192</p><p>137Cs ( = 0.37, n = 15, n.s., Kendall test). The second PCA axis ex-plained 13% of the stomach content data (the lower part of the di-agram shows higher f...</p></li></ul>

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