Science of the Total Environment 482–483 (2014) 184–192
Contents lists available at ScienceDirect
Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Radioactive contamination of fishes in lake and streams impacted by the Fukushima nuclear power plant accident Mayumi Yoshimura a,⁎, Tetsuya Yokoduka b a b
Kansai Research Center, Forestry and Forest Products Research Institute, Nagaikyuutaro 68, Momoyama, Fushimi, Kyoto 612-0855, Japan Tochigi Prefectural Fisheries Experimental Station, Sarado 2599, Ohtawara, Tochigi 324-0404, Japan
H I G H L I G H T • 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.
a r t i c l e
i n f o
Article history: Received 27 November 2013 Received in revised form 19 February 2014 Accepted 25 February 2014 Available online 18 March 2014 Keywords: Brown trout Charr Lake Radioactive cesium Stomach contents Stream
a b s t r a c t The Fukushima Daiichi Nuclear Power Plant (FDNPP) accident in March 2011 emitted radioactive substances into the environment, contaminating a wide array of organisms including fishes. We found higher concentrations of radioactive cesium ( 137 Cs) in brown trout (Salmo trutta) than in rainbow trout (Oncorhynchus nerka), and 137 Cs concentrations in brown trout were higher in a lake than in a stream. Our analyses indicated that these differences were primarily due to differences in diet, but that habitat 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 also attributed to dietary and habitat differences. Preserving uncontaminated areas by remediating soils and releasing uncontaminated fish would help restore this popular fishing area but would require a significant effort, followed by a waiting period to allow activity concentrations to fall below the threshold limits for consumption. © 2014 Elsevier B.V. All rights reserved.
1. Introduction A massive earthquake occurred in eastern Japan on 11 March 2011, causing a tsunami that washed over the Fukushima Daiichi Nuclear Power Plant (FDNPP) on the east coast of Japan. Damage to the cooling system of the FDNPP resulted in several explosions, causing leakage of radioactive substances. The FDNPP accident released 1.6 × 1017 Bq of iodine-131 (131I), 1.8 × 1016 Bq of cesium-134 (134Cs) and 1.5 × 1016 Bq of cesium-137 ( 137 Cs) into the surrounding environment (Ohara et al., 2011). Most of these radionuclides, including 131I, 134Cs and 137 Cs, were unevenly deposited over large areas of land in eastern
⁎ Corresponding author. Tel.: +81 75 611 1201; fax: +81 75 611 1207. E-mail address: [email protected] (M. Yoshimura).
http://dx.doi.org/10.1016/j.scitotenv.2014.02.118 0048-9697/© 2014 Elsevier B.V. All rights reserved.
Japan, reaching sites hundreds of kilometers from the FDNPP. The dense radioactive plume spewing from the FDNPP moved northwestward, descending to ground level with precipitation and heavily contaminating large tracts of the landscape. A smaller plume drifted to the south-west and contaminated areas such as the Oku Nikko and Ashio regions in Tochigi Prefecture (Kinoshita et al., 2011; MEXT, 2011). Atmospheric dose rates 0.5 m above the ground exceeded 20 μSv/h in some hot spots N 160 km from the FDNPP in May 2011 (Tochigi, 2011). The first phase of investigation revealed that a large portion of the deposited 134Cs and 137Cs was trapped in the forest canopies and the soil litter layer (Hashimoto et al., 2012). Radiocesium is easily adsorbed onto 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 to soil, are readily taken up by microbes, algae, plankton and plants. This
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
pathway of 134Cs and 137Cs transport eventually leads to uptake by fishes at higher trophic levels. Radioactive contamination of fish should be prevented because fishes may be taken by anglers and consumed as food. A safety threshold of 100 Bq/kg of radioactive Cs was introduced in April 2012, but activity concentrations greater than this have been detected in fishes hundreds of kilometers distant from the FDNPP. There is clearly a pressing imperative to reduce radioactive Cs contamination of food. The Chernobyl accident released more than five million Tera Becquerel of radionuclides. Much radionuclides from the Chernobyl accident spread to Finland, Sweden and Norway, 2000 km to the northwest. Fish have been monitored for radioactivity Øvre Heimdalsvatn, a Norwegian subalpine lake (Brittain et al., 1991; Brittain and Gjerseth, 2010). Activity concentrations of 137Cs in brown trout reached 8400 Bq/kg in 1987 and declined to 200– 300 Bq/kg in 2008, but the contamination level has recently been constant and approached an asymptotic decline (Brittain and Gjerseth, 2010). The broad effects of the Chernobyl accident have been examined and management measures have been designed for large geographical areas (Report of the Chernobyl Forum Expert Group ‘Environment’, 2006; Yablokov et al., 2009). However, the ecological consequences of radioactive contamination in fishes are poorly understood. To precisely describe the mechanisms of diffusion and export of 137 Cs deposited in freshwater fish, we measured concentrations of 137 Cs in the muscle tissue and stomachs of brown trout (Salmo trutta), rainbow trout (Oncorhynchus mykiss) and kokanee (Oncorhynchus nerka) from a lake, that of brown trout (Salmo trutta) from a stream and that of charr (Salvelinus leucomaenis) from four streams. Here, we report the results of preliminary investigations 21 months after the FDNPP accident. 2. Materials and methods 2.1. Study site The study was conducted in the Nikko area (Lake Chuzenji, Oku Nikko and Ashio regions) located approximately 160 km southwest of the FDNPP. According to an aircraft radioactivity survey reported by MEXT (2012), the air dose rate in this area was 0.1–0.25 μSv/h on 31 May 2012. The study area is mostly forested; the dominant tree species are broadleaf and deciduous. Other areas are forested with Japanese cedar and cypress plantations used for timber production. The field survey was conducted in Lake Chuzenji and two headwater tributaries (Toyamasawa and Yanagisawa streams) of the Kinu River in the Oku Nikko region and in two headwater tributaries (Kuzosawa and Asosawa streams) of the Watarase River in the Ashio region, which form the upper drainage component of the Tone River system, Honshu, Japan (Fig. 1). 2.2. Sampling Fishes were captured in Lake Chuzenji and in the four streams in November and December, 2012 using fishing rod in the lake and battery-powered backpack electrofishing (Smith-Root Inc. LR-24) units operated at 300-V pulse-DC in the stream. In central Lake Chuzenji, three species of fishes, brown trout (Salmo trutta), rainbow trout (Oncorhynchus mykiss) and kokanee (salmon) (Oncorhynchus nerka) were sampled. In Toyamasawa stream, two species of fish, brown trout (Salmo trutta) and charr (Salvelinus leucomaenis) were sampled at site B (200 m stream segments). In other three streams, only charr (Salvelinus leucomaenis) were sampled at sites E, G, and I (200 m stream segments). After capture, we recorded the body size (fork length) of each fish and sampled
185
muscle tissue for the analysis of radioactive concentration. We then collected and froze the stomachs for the analysis of radiocesium concentrations in stomach tissue and for identification of stomach contents. The age of charr specimens was determined from sagittal otoliths using the surface reading method. The age of the other three fishes was not determined; folk length was used as a substitute metric. In the four streams, air dose rates at 1-m above ground were measured with a γ survey meter adjacent to the stream (NaI scintillation counter; ALOKA TCS-172). Electrical conductivities (EC) of the streams were measured with a portable compact twin conductivity meter (B-173; Horiba); pH was measured with a portable compact twin pH meter (B-212; Horiba). Wetted stream 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 were measured 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.
2.3. Radiocesium analysis and identification Samples of fish stomach and muscle tissue were directly packed into 100-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&G, Tokyo, Japan; GC4020, Canberra, Japan) for 36,000 s–63,000 s depending on the sample weight. Gamma-ray peaks of 622 keV were used to determine 137 Cs. The measurement system was calibrated using a standard gamma-ray source (MX033U8PP, Japan Radioisotope Association, Tokyo, Japan), and a standard soil sample (IAEA-444) was used to check accuracy. Fine adjustments to the measurements were made to correspond to the radiocesium concentration value for 1 December 2012. The radioactivity of lake and stream water was not measured because 137Cs concentrations in several lakes and streams were reported to be below the detection level (1 Bq/l) (MOE 2013, Tochigi Prefecture, 2013). The inner contents of the frozen stomach for the analysis of stomach contents were removed and identified under a 50 × microscope (SMZ-U; Nikon). We identified specimens to the family level or higher following Merritt and Cummins (1996) and Kawai (1985).
2.4. Statistical analysis Kruskal–Wallis tests or Mann–Whitney U-tests were used to compare the 137Cs concentrations. The Kendall test was used to clarify the relationship between folk length and 137Cs concentration. We conducted principal component analysis (PCA) on the presence or absence of each fish stomach content for three species in Lake Chuzenji, for brown trout in Lake Chuzenji and Toyamasawa stream, and for charr in the four streams. We examined the PCA axes among the three fish species and among the four streams using a Kruskal–Wallis multiple comparison test and between lake and stream habitats using a Mann– Whitney U-test. It would be useful to compare samples of the same species or the same age at all sampling locations. However, the fishes sampled in this study differed between the stream and lake and it was not practical to collect specimens of equal size. Statistical analysis was performed using SYSTAT version 10 (SPSS Inc. 2000). Radiocesium concentrations that were below the detection level because of insufficient weight for radiocesium analysis were excluded from the statistical analysis.
186
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
Fig. 1. Study site of Lake Chuzenji and four streams in the Oku Nikko and Ashio areas, Tochigi Prefecture, Japan. ● A–I: stream water sampling sites, □ B, E, G, I: fish sampling sites.
3. Results Aerial radioactivity was higher in the Ashio region than in the Oku Nikko region (z = 2.33, n = 9, P b 0.05, Mann–Whitney U-test; Table 1), as was radiocesium deposition. These two regions did not differ in air or water temperature, pH, stream width or stream velocity, but EC differed between the regions (Table 1; Yoshimura and Akama, 2014). 137 Cs concentrations in fish stomachs were highest in brown trout (Salmo trutta), lowest in rainbow trout (Oncorhynchus mykiss) and intermediate in kokanee (salmon) (Oncorhynchus nerka) (H = 11.1, n = 14, P b 0.005, Kruskal–Wallis test; Fig. 2). 137 Cs concentrations in fish muscle showed the same pattern among species (H = 590.5, n = 69, P b 0.0001, Kruskal–Wallis
test; Fig. 2). Radioactive Cs concentrations in stomach and muscle tissues did not differ significantly among the three species. There was no relationship between 137 Cs concentrations in fish muscle and fork length in three species (brown trout: τ = 0.27, n = 23, n.s.; kokanee: τ = 0.02, n = 24, n.s.; rainbow trout: τ = 0.17, n = 22, n.s.; Kendall test). Stomach contents varied significantly among the three species of fish (Appendix A). Brown trout stomachs primarily contained fish and unknown digested foods. Kokanee primarily contained unknown foods and rainbow trout stomachs contained a wide variety of fish and invertebrates. The first PCA axis explained 52% of the variation in the stomach contents (mainly the number of species consumed) but was not correlated with muscle concentration of
Table 1 The dose rate at 1 m above the ground, air temperature, water temperature, pH, electric conductivity, stream velocity and stream width at 9 sites on December 2012 with statistical result. Oku Nikko
Ashio
Toyamasawa
Dose rate (μSv/h) Air temperature (°C) Water temperature (°C) pH Electric conductivity (μs/cm) Stream velocity (cm/s) Stream widths (m) Altitude (m) *: P b 0.05.
Asosawa
U-test
A
B
C
Yanagisawa D
E
F
G
Kuzosawa H
I
z
0.08 −0.8 7.2 6.9 61 30 7.6 1270
0.10 1.7 6.8 7.0 50 63 5.7 1300
0.12 0.7 7.3 7.1 49 32 4.8 1450
0.09 0.1 8.1 6.7 53 48 17.1 1270
0.10 6.4 4.9 6.4 33 35 5.8 1320
0.11 6.7 2.6 6.9 51 58 8.1 1380
0.26 1.3 4.0 6.5 73 70 3.0 810
0.21 1.7 4.2 6.3 59 68 3.5 950
0.27 −1.9 1.6 6.8 64 57 5.8 790
2.33* 0.65 1.81 1.56 2.07* 1.81 2.69 2.33*
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
a
a
(Bq/kg)
200
150 100
137Cs
137Cs
(Bq/kg)
200
50
150 100 50 0
0 0
200
400
600
0
800
100
200
Brown trout
400
Chuzenji Lake
Rainbow trout
b
137Cs
150 100
500
600
Toyamasawa
b
200
(Bq/kg)
200
(Bq/kg)
Kokanee
300
Fork length (mm)
Fork length (mm)
137Cs
187
150 100 50
50 0 0
0 0
100
200
300
400
500
Kokanee (stomach)
Chuzenji Lake (stomach)
137
Cs (τ = 0.37, n = 15, n.s., Kendall test). The second PCA axis explained 13% of the stomach content data (the lower part of the diagram shows higher fish contents and the upper part of diagram shows higher insects contents) and was correlated with muscle concentrations of 137 Cs (τ = − 0.56, n = 15, P b 0.005, Kendall test). The PCA also showed that stomach contents of the three species were statistically different based on the first axis (H = 9.1, n = 15,
500
600
Toyamasawa (stomach)
P b 0.05, Kruskal–Wallis test; Fig. 3) and the second axis (H = 6.2, n = 15, P b 0.05, Kruskal–Wallis test; Fig. 3). No significant correlation was observed between the PCA axes and 137Cs concentration in any of the three fish species (Kendall test; Fig. 3). 0.8
Lake Stream
0.4
Brown trout Kokanee Rainbow trout Axis 2 (20%)
0.2
0.4
Axis 2 (13%)
400
Fig. 4. Relationship between body length and 137Cs concentration in brown trout from Lake Chuzenji and Toyamasawa stream. (a) Muscle; (b) stomach.
0.6
0.6
300
Rainbow trout (stomach)
Fig. 2. Relationship between body length and 137Cs concentration of three species in Lake Chuzenji. (a) Muscle; (b) stomach.
0.8
200
Fork length (mm)
Fork length (mm) Brown trout (stomach)
100
600
0.2
0
-0.2
0 -0.4 -0.2 -0.6 -0.4 -0.8
-0.6 -0.8
-1 0
0.2
0.4
0.6
0.8
1
1.2
Axis 1 (52%) Fig. 3. Scatter diagram of the principal components analysis (PCA) of stomach contents of three fishes from Lake Chuzenji. Bubble size indicates the concentrations of 137Cs in muscle tissue of each fish.
0
0.2
0.4
0.6
0.8
1
Axis 1 (33%) Fig. 5. Scatter diagram of stomach contents in the principal components analysis (PCA) of each brown trout in Lake Chuzenji and Toyamasawa stream. Bubble size indicates the concentration of 137Cs in the muscle tissue of each fish.
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
Concentrations of 137 Cs in the stomach contents of brown trout were higher in Lake Chuzenji than in the streams (z = 2.7, n = 11, P b 0.01, Mann–Whitney U-test; Fig. 4), and so were 137 Cs concentrations in muscle tissue (z = 6.0, n = 50, P b 0.0001, Mann–Whitney U-test; Fig. 4). No significant difference in 137Cs concentration was observed between stomach and muscle tissues. There was significant relationship between 137Cs concentrations in fish muscle and fork length in brown trout from streams (τ = 0.51, n = 29, P b 0.001; Kendall test). Stomach contents of brown trout differed between Lake Chuzenji and Toyamasawa stream (Appendix A). In streams, the brown trout stomach contents were mainly insects. The first PCA axis explained 33% of the variation in stomach content (mainly the number of species consumed) and was not correlated with 137Cs concentrations in muscle tissue (τ = 0.01, n = 14, n.s., Kendall test). The second PCA axis explained 20% of the variation in stomach content data (the lower part of the diagram shows higher fish content and the upper part of the diagram shows higher insect content) and was correlated with 137 Cs concentrations in muscle tissue (τ = − 0.40, n = 14, P b 0.05, Kendall test). Stomach contents were statistically different between lake and stream fish based on PCA axis 2 (z = 3.0, n = 14, P b 0.005, Mann–Whitney U-test; Fig. 5), but not on axis 1 (z = 0.2, n = 14, n.s., Mann–Whitney U-test; Fig. 5). No significant correlation was detected between these two axes and 137Cs concentrations of fish in each habitat (Kendall test; Fig. 5). Concentrations of 137Cs in the stomach tissue of charr did not differ among the four streams (H = 4.6, n = 18, n.s., Kruskal–Wallis test), but muscle activity concentrations did differ among the streams (H = 16.2, n = 88, P b 0.001, Kruskal–Wallis test). Older fish had higher muscle concentrations of 137Cs (Toyamasawa: H = 7.8, n = 35, P b 0.052; Yanagisawa: H = 8.6, n = 19, P b 0.05; Kuzosawa: H = 22.5, n = 33, P b 0.0001, Kruskal–Wallis test; Fig. 6), but no difference was observed in the concentrations of 137Cs in stomach tissues among age. The stomach contents of charr consisted primary of insections in all four streams (Appendix B). Axis 1 of the PCA explained 30% of the variation in stomach contents (the right side of the diagram shows higher aquatic insect content and the left side of diagram shows higher terrestrial insects content) and was correlated with concentrations of 137Cs in muscle tissue (τ = 0.31, n = 26, P b 0.05, Kendall test). Axis 2 of the PCA explained 9% of the variation in stomach contents (the lower part of the diagram shows higher Bryophyta content) and was also correlated with 137Cs levels in muscle (τ = − 0.30, n = 26, P b 0.05, Kendall test). Stomach contents among the four streams differed statistically along PCA axis 1 (H = 22.2, n = 40, P b 0.001, Kruskal–Wallis test; Fig. 7), especially between fish in Toyamasawa and the other streams. Stomach contents also differed among the four streams based on PCA axis 2 (H = 22.9, n = 40, P b 0.001, Kruskal–Wallis test; Fig. 7), especially between fish in the Ashio region and the Oku Nikko region. No
100
60 40 20
0.2 0 -0.2 -0.4 -0.6 -0.8 -0.4
0+
1+
2+
Fish age
3+
-0.2
0
0.2
0.4
0.6
0.8
1
Axis 1 (30%) Fig. 7. Scatter diagram of the principal components analysis (PCA) for stomach contents of each charr from the four streams. Bubble size indicates the concentrations of 137Cs in muscle tissue of each fish.
significant correlation was observed between these two axes and Cs concentrations of fish in each of the four streams, except the relationship between PCA axis 2 and 137Cs concentration in muscle tissue of fish from the Kuzosawa stream (τ = −0.73, n = 11, P b 0.005, Kendall test; Fig. 7). 137
4. Discussion Fishes were contaminated with radioactive substances even where dose rates in the atmosphere were relatively lower (160 km distance from the FDNPP). In Lake Chuzenji, concentrations of 137Cs in muscle tissues and stomach were highest in S. trutta, lowest in O. mykiss and intermediate in O. nerka. The lack of difference between stomach and muscle concentrations of 137Cs indicates that the absence of a high level of contamination in the stomach contents and suggests that and radioactive materials are transferred from food items to muscle tissues. Research after the Chernobyl accident also showed that radioactive contamination was caused by diet (Forseth et al., 1991; Ugedal et al., 1995), and dietary differences were reflected in the decay rates and ecological half-lives (Hessen et al., 2002). The primary food of brown trout in Lake Chuzenji was goby, and the 137 Cs concentration of goby in Lake Chuzenji averaged 57.4 Bq/kg (n = 20, 1 December 2012, unpublished data). There was no diet in the stomach of kokanee and they usually consume zooplankton. The 137Cs concentration of zooplankton in Lake Chuzenji is 8.3 Bq/kg (n = 1, 1 December 2012, unpublished data). Thus,
100
b
80 60 40 20 0
0
Toyamasawa Yanagisawa Kuzosawa asosawa
(Bq/kg)
(Bq/kg)
80
0.4
137Cs
a
137Cs
137Cs
(Bq/kg)
100
0.6
Axis 1 (9%)
188
c
80 60 40 20 0
0+
1+
2+
Fish age
3+
0+
1+
2+
3+
Fish age
Fig. 6. Relationship between fish age and concentration of 137Cs in stream fish. (a) Toyamasawa stream, (b) Yanagisawa stream, (c) Kuzosawa stream. ○: Concentration of 137Cs in charr muscle and ♦: concentration of 137Cs in charr stomach tissue.
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
higher 137Cs concentrations in brown trout are likely to be acquired mainly from their diet. Some rainbow trout had 137 Cs concentrations that were below the detection limit; these fishes may have been released as adults. Brown trout and kokanee are released into Lake Chuzenji only as fry, but rainbow trout are released as both fry and adult fish. Because fish released as adults spend only a short period in the contaminated lake, their muscle tissue is expected to be less contaminated. The mean 137 Cs concentrations of three families of aquatic stream insects (Perlidae, Perlodidae and Stenopsychidae) were 67.9 Bq/kg (max: 271 Bq/kg, min: 0 Bq/kg; Yoshimura and Akama, 2014). Thus, 137Cs concentrations in aquatic insects in lake are higher than those of zooplankton, but with a large variance. Activity concentrations of more than 50 Bq/kg in some lake rainbow trout, which feed primarily on insects and are released as fry, indicate that muscle contamination is a result of diet. However, concentrations of 137 Cs did not differ greatly between goby in the lake and aquatic insects in the streams. The difference in 137Cs concentrations between these two fish species may instead be a result of habitat differences. Brown trout typically reside from benthic substrate to middle strata of the lake interior, whereas rainbow trout reside from middle to upper depths close to the shoreline. Radioactive substances tend to condense more in deeper area of the lake where less water flow occurs. Higher 137 Cs concentrations in brown trout may arise from these differences in habitat preference. Stomach contents of brown trout in Lake Chuzenji differed from those in Toyamasawa stream, and radiocesium concentrations of stomach and muscle tissue also differed between the habitats, suggesting that the differences in contamination are due to habitat differences. However, 137 Cs concentrations of goby consumed by brown trout in the lake and aquatic insects consumed by brown trout in the stream did not differ. The primary environmental difference between the lake and stream is the rate of water flow. In lakes, particulate organic matter from the surrounding forest, which may be contaminated with 137Cs, settles to the bottom and releases 137 Cs by the decomposition of particle organic materials gathered. The released 137 Cs accumulates at the bottom of the lake and is not easily washed away. The lack of flow in deep portions of the lake may also result in accumulation of silt contaminated with 137Cs. Sand substrates had higher 137Cs concentrations in Lake Chuzenji (81.28 Bq/kg, n = 11, unpublished data) than in any of the four streams (26.59 Bq/kg; Yoshimura and Akama, 2014). The 137Cs value of sand in the lake seems to be higher than that in the stream (Ministry of the Environment, 2011, 2013). Aquatic insects that inhabit stream pools have higher value of 137 Cs than insects in riffles (Yoshimura and Akama, 2014); water flow rate may thus be a key factor determining the activity concentrations in fishes. Retention time would also be related to contamination level and would lead to variability in radioactive cesium concentration in fish from different lentic environments (Håkanson, 1992). Free 137Cs in stagnant water in lakes accumulates particulate organic matter associated with the substrate. Thus, fishes living near the bottoms of lakes would intake highly 137Cs contaminated materials into their bodies from dietary items settling to the bottom. Brown trout in Norwegian lake contaminated by radioactive fallout from the Chernobyl accident retain substantial radioactivity levels more than 20 years after the accident, and these levels do not appear to be declining (Brittain and Gjerseth, 2010), probably because of continuing input of radioactive substances from the catchment and remobilization of sediments in the lake. Some mechanisms of 137Cs contamination of fishes remain unknown. Removal of radioactive substances is necessary to alleviate this problem. At present, only catch-and-release fishing is permitted in Lake Chuzenji. Although restoring the lake environment would take decades, areas in which fishing and fish consumption can be safely
189
practiced must be reclaimed. Full-grown rainbow trout released to the lake had lower concentrations of 137Cs. Decontamination of soil substrates and release of non-contaminated fish in designated areas would be the most rapid way to improve fish quality and enable tourism to resume. However, continual removal of highly contaminated adult fish such as brown trout and release of uncontaminated fry may constitute a more appropriate long-term approach. Among the four streams, radioactive Cs values in the muscle tissues of charr were elevated where aerial dose rates were higher. Although no differences in 137 Cs values were observed in stomach among the four streams, fishes in the Ashio region consumed more Chlorophyta and Heterokontophyta. The 137Cs value of Chlorophyta in the Ashio region was 170 Bq/kg (n = 1, 1 December 2012, unpublished data). The higher 137 Cs value of fish in the Ashio region might be a result of consumption of these algae in addition to higher contamination from fallout. The higher 137Cs concentrations in older fish might also be caused by continuous intake of contaminated food. However, a large degree of variation in 137 Cs was detected in equal-aged fishes in a given stream. The habitat range of charr is generally larger than that of aquatic insects and always includes a small riffle and a pool. Concentrations of 137 Cs in aquatic insects differed between pools and riffles even within the same families. Habitat selection (proportion of time spent in pools and riffles) by individual fish may cause dietary variation in 137 Cs, leading to variability in 137Cs levels among fish in the same sampling area. The PCA axes for fish diet were correlated with 137 Cs concentrations of muscle tissue in all three species of fish in the lake, in brown trout in the lake and streams, and in charr in all four streams, suggesting that dietary differences are primarily responsible for the differences in radioactive Cs concentrations among these fish. However, the PCA axis for diet was not correlated with 137 Cs concentrations in muscle tissue across species, habitat or streams, which suggests that the diet menu of each individual is not always almost the same and there is substantial variation of 137 Cs concentration in individual diets. Fritsch et al. (2008) reported that 137 Cs in soil is transferred to plants, earthworms and snails, but that transfer rates of radionuclides through the food web depend on the concentration of radioactive substances, exposure period and consumption rates. Habitat variability among individual fish would also affect 137 Cs transfer. The areas where this study was conducted are extremely popular fishing locations. However, only catch-and-release fishing is currently permitted because of the elevated radioactivity levels. As long as the diet and sand substratum are contaminated, levels of radioactive Cs in fishes are expected to remain high, and continual monitoring and management of radioactivity will be necessary.
Conflict of interest The authors declare no conflicts of interests.
Acknowledgements We thank Dr. Makino in the Forestry and Forest Products Research Institute, Dr. Yamamoto in the National Research Institute of aquaculture and Dr. Yoshida in the fisheries experimental station of Tochigi Prefecture for their assistance with sampling survey. Capture of fishes was done with the permission from Tochigi Prefecture. This work was supported in part by a research grant from the Council of Science and Technology Policy in 2012.
190
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
Appendix A. Stomach contents of three species of fishes in Lake Chuzenji and of brown trout in the Toyamasawa stream Lake Chuzenji Division
Order
Family
Nematomorpha Arthropoda
Gordea Araneae Lithobiomorpha Thysanura Ephemeroptera
Gordiidae Undetermined Ethopolidae Lepismatidae Baetidae Heptageniidae Ephemerellidae Undetermined Nemouridae Chloroperlidae Perlodidae Acrididae Membracidae Psyllidae Aphididae Tettigometridae Reduviidae Lygaeidae Pentatomidae Acanthosomatidae Undetermined Arctopsychidae Philopotamidae Stenopsychidae Rhyacophilidae Brachycentridae Limnephilidae Undetermined Tipulidae Chronomidae Bibionidae Drosophilidae Undetermined Staphylinidae Undetermined Chalcidoidea Formicidae Undetermined
Plecoptera
Orthoptera Hemiptera
Trichoptera
Diptera
Coleoptera Hymenoptera
Chordata
Unknown egg Chlorophyta Bryophyta Magnoliophyta
Insect (fragments) Insect egg Perciformes Ichthyic digest Ichthyic eggs Ichthyic bone Bird feather
Brown trout (5)
Gobiidae
Toyama sawa Kokanee (5)
Rainbow trout (5)
Brown trout (9) *** ** ** * ** ** * ** *** * ** *** * *** ** ** ** ** *** ** *** ** * * **
*
* * **
*** ** **
* ** ***** **
** *** **
* *** * ** ** ** * ** ** ****
*** ** ** *** ** *** ***
**** **** ** *
** *
Ulotrichales Bryidae Hepaticopsida Hydrocharitales Sapindales
Ulotrichaceae
* **** ** *** *** **** *** *****
Hydrocharitaceae Aceraceae
Plant (fragment) Sand Unknown digest
*
**
****
****
** *** *****
Weight of each stomach content, *: b0.01, **: b0.1, ***: b1.0, ****: b10.0, *****: b100.0 (g).
Appendix B. Stomach contents of charr in four streams Division Nematoda Arthropoda
Order
Family
Opiliones Acari Araneae
Phalangiidae Spercontidae Thomisidae Undetermined Ligiidae
Isopoda Collembola Ephemeroptera
Siphlonuridae Baetidae Heptageniidae
Toyama sawa (14)
Yanagi sawa (10)
Kuzo sawa (11)
Aso sawa (5)
** **
***
**
*
* ** * ** * **
** ** **
* * *
**
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
191
Appendix (continued) B (continued) Division
Order
Plecoptera
Orthoptera Hemiptera
Neuroptera Trichoptera
Lepidoptera Diptera
Coleoptera
Hymenoptera
Chordata Unknown egg Chlorophyta Heterokontophyta Bryophyta Plant (fragment) Sand Unknown digest
Insect (fragments) Salmoniformes Ichthyic bone
Family Ephemeridae Ephemerellidae Undetermined Scopuridae Capniidae Nemouridae Taeniopterygidae Chloroperlidae Perlidae Perlodidae Acrididae Membracidae Aphrophoridae Psyllidae Aphididae Lygaeidae Pentatomidae Acanthosomatidae Undetermined Osmylidae Undetermined Arctopsychidae Hydropsychidae Philopotamidae Stenopsychidae Glossosomatidae Rhyacophilidae Limnephilidae Brachycentridae Goeridae Lepidostomatidae Uenoidae Undetermined Tipulidae Blephariceridae Chronomidae Simuliidae Empididae Bibionidae Undetermined Carabidae Staphylinidae Curculionidae Chrysomelidae Undetermined Cynipoidea Chalcidoidea Braconidae Ichneumonidae Formicidae Salmonidae
Toyama sawa (14)
Yanagi sawa (10)
Kuzo sawa (11)
Aso sawa (5)
** * ***
***
** ***
* **
* * * ** *** *** **
* * *
*** * ** ** ** ** ** ** * *** ** ** ** **
* ** * * ** ***
* *
*** *** ** **
**
** *** **
*
**
** *
*** * ** ** ** *** ** * * * *** * **** ****
*
*
**
**** ** *** * *** *
* ***
** * *** *** ** **
*** *
* **** * *
**
*** *** ** * *** **
** ** *** * **
*
*
***
***
* * *
*
*** **** *****
** *** ***
*
* ** **
* Ulotrichales Centrales Pennales Bryidae
Ulotrichaceae Melosiraceae Diatomaceae ** *** *** ****
** *** ****
*
Weight of each stomach content, *: b0.01, **: b0.1, ***: b1.0, ****: b10.0, *****: b100.0.
References Brittain JE, Gjerseth JE. Long-term trends and variation in 137Cs activity concentrations in brown trout (Salmo trutta) from Øvre Heimdalsvatn, a Norwegian subalpine lake. Hydrobiologia 2010;642:107–13. Brittain JE, Storruste A, Larsen E. Radiocesium in brown trout (Salmo-trutta) from a subalpine lake ecosystem after the Chernobyl reactor accident. J Environ Radioact 1991;14:181–91. Forseth T, Ugedal O, Jonsson B, Langeland A, Njastad O. Radiocaesium turnover in Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta) in a Norwegian lake. J Appl Ecol 1991;28:1053–67.
Fritsch C, Scheifler R, Beaugelin-Seiller K, Hubert P, Coeurdassier M, Vaufleury AD, et al. Biotic interactions modify the transfer of Cesium-137 in a soil–earthworm–plant– snail food web. Environ Toxicol Chem 2008;27:1698–707. Fukuyama T, Takenaka C, Onda Y. 137Cs loss via soil erosion from a mountainous headwater catchment in central Japan. Sci Total Environ 2005;350:238–47. Håkanson L. Radioactive cesium in fish in Swedish lakes 1986–1988—general pattern related to fallout and lake characteristics. J Environ Radioact 1992;15: 207–29. Hashimoto S, Ugawa S, Nanko K, Shichi K. The total amounts of radioactively contaminated materials in forests in Fukushima, Japan. Sci Rep 2012;2. [article number 416].
192
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
Hessen DO, Skurdal J, Hegge O, Hesthagen T. Radiocesium decay in populations of brown trout and Arctic char in the alpine Atna area, south-eastern Norway. Hydrobiologia 2002;489:55–62. Kato H, Onda Y, Tanaka Y. Using 137Cs and 210Pbex measurements to estimate soil redistribution rates on semi-arid grassland in Mongolia. Geophys J Roy Astron Soc 2010; 114:508–19. Kawai TIn: Kawai T, editor. An illustrated book of aquatic insects of Japan. Tokyo: Tokai University Press; 1985. Kinoshita N, Sueki K, Sasa K, Kitagawa J, Ikarashi S, Nishimura T, et al. Assessment of individual radionuclide distributions from the Fukushima nuclear accident covering central-east Japan. Proc Natl Acad Sci 2011;108:19526–9. Kruyts N, Delvaux B. Soil organic horizons as a major source for radiocesium biorecycling in forest ecosystems. J Environ Radioact 2002;58:175–90. Merritt RW, Cummins KW. An Introduction to the aquatic insects of North America. 3rd ed. Dubuque, IA: Kendall/Hunt; 1996. Ministry of Education, Culture, Sports, Science, Technology (MEXT). Database on the research of radioactive substances distribution. http://radioactivity.nsr.go.jp/ja/contents/5000/4930/24/1305819_0727.pdf, 2011. [10 January 2014]. Ministry of Education, Culture, Sports, Science, Technology (MEXT). Database on the research of radioactive substances distribution. http://radb.jaea.go.jp/mapdb/portals/ 101002/?prefectures=09&category_b=b1201&year=2012, 2012. [10 January 2014]. Ministry of the Environment. Database on the environmental monitoring research of radioactive substances in East Japan. http://www.env.go.jp/jishin/monitoring/result_ pw111216-2.pdf, 2011. [10 January 2014]. Ministry of the Environment. Database on the environmental monitoring research of radioactive substances in East Japan. http://www.env.go.jp/jishin/monitoring/result_ pw131108-1.pdf, 2013. [10 January 2014].
Ohara T, Morino Y, Tanaka A. Atmospheric behavior of radioactive materials from Fukushima Daiichi Nuclear Power Plant. J Natl Inst Public Health 2011;60: 292–9. Report of the Chernobyl Forum Expert Group ‘Environment’. Environmental consequences of the Chernobyl accident and their remediation: twenty years of experience. Vienna, Austria: Radiological Assessment Reports Series, IAEA; 2006. Tochigi prefecture. Data base on the dose rate in the air in Tochigi Prefecture from May 13 to May 31. http://www.pref.tochigi.lg.jp/kinkyu/documents/20110601_1400_50cm. pdf, 2011. [10 January 2014]. Tochigi prefecture. Data base on the activity concentrations in stream and lake sand in Tochigi Prefecture. http://www.pref.tochigi.lg.jp/d03/kankyosho_houshaseibusshitu. html, 2013. [10 January 2014]. Ugedal O, Forseth T, Jonsson B, Njastad O. Sources of variation in radiocaesium levels between individual fish from a Chernobyl contaminated Norwegian lake. J Appl Ecol 1995;32:352–61. Wakiyama Y, Onda Y, Mizugaki S, Asai H, Hiramatsu S. Soil erosion rates on forested mountain hillslopes estimated using 137 Cs and 210 Pb ex . Geoderma 2010;159: 39–52. Yablokov AV, Nesterenko VB, Nesterenko AV. Chernobyl, consequences of the catastrophe for people and the environment. Ann N Y Acad Sci 2009;1181. Yoshimura M, Akama A. Radioactive contamination of aquatic insects in a stream impacted by the Fukushima nuclear power plant accident. Hydrobiologia 2014; 722:19–30.
Contents lists available at ScienceDirect
Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Radioactive contamination of fishes in lake and streams impacted by the Fukushima nuclear power plant accident Mayumi Yoshimura a,⁎, Tetsuya Yokoduka b a b
Kansai Research Center, Forestry and Forest Products Research Institute, Nagaikyuutaro 68, Momoyama, Fushimi, Kyoto 612-0855, Japan Tochigi Prefectural Fisheries Experimental Station, Sarado 2599, Ohtawara, Tochigi 324-0404, Japan
H I G H L I G H T • 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.
a r t i c l e
i n f o
Article history: Received 27 November 2013 Received in revised form 19 February 2014 Accepted 25 February 2014 Available online 18 March 2014 Keywords: Brown trout Charr Lake Radioactive cesium Stomach contents Stream
a b s t r a c t The Fukushima Daiichi Nuclear Power Plant (FDNPP) accident in March 2011 emitted radioactive substances into the environment, contaminating a wide array of organisms including fishes. We found higher concentrations of radioactive cesium ( 137 Cs) in brown trout (Salmo trutta) than in rainbow trout (Oncorhynchus nerka), and 137 Cs concentrations in brown trout were higher in a lake than in a stream. Our analyses indicated that these differences were primarily due to differences in diet, but that habitat 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 also attributed to dietary and habitat differences. Preserving uncontaminated areas by remediating soils and releasing uncontaminated fish would help restore this popular fishing area but would require a significant effort, followed by a waiting period to allow activity concentrations to fall below the threshold limits for consumption. © 2014 Elsevier B.V. All rights reserved.
1. Introduction A massive earthquake occurred in eastern Japan on 11 March 2011, causing a tsunami that washed over the Fukushima Daiichi Nuclear Power Plant (FDNPP) on the east coast of Japan. Damage to the cooling system of the FDNPP resulted in several explosions, causing leakage of radioactive substances. The FDNPP accident released 1.6 × 1017 Bq of iodine-131 (131I), 1.8 × 1016 Bq of cesium-134 (134Cs) and 1.5 × 1016 Bq of cesium-137 ( 137 Cs) into the surrounding environment (Ohara et al., 2011). Most of these radionuclides, including 131I, 134Cs and 137 Cs, were unevenly deposited over large areas of land in eastern
⁎ Corresponding author. Tel.: +81 75 611 1201; fax: +81 75 611 1207. E-mail address: [email protected] (M. Yoshimura).
http://dx.doi.org/10.1016/j.scitotenv.2014.02.118 0048-9697/© 2014 Elsevier B.V. All rights reserved.
Japan, reaching sites hundreds of kilometers from the FDNPP. The dense radioactive plume spewing from the FDNPP moved northwestward, descending to ground level with precipitation and heavily contaminating large tracts of the landscape. A smaller plume drifted to the south-west and contaminated areas such as the Oku Nikko and Ashio regions in Tochigi Prefecture (Kinoshita et al., 2011; MEXT, 2011). Atmospheric dose rates 0.5 m above the ground exceeded 20 μSv/h in some hot spots N 160 km from the FDNPP in May 2011 (Tochigi, 2011). The first phase of investigation revealed that a large portion of the deposited 134Cs and 137Cs was trapped in the forest canopies and the soil litter layer (Hashimoto et al., 2012). Radiocesium is easily adsorbed onto 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 to soil, are readily taken up by microbes, algae, plankton and plants. This
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
pathway of 134Cs and 137Cs transport eventually leads to uptake by fishes at higher trophic levels. Radioactive contamination of fish should be prevented because fishes may be taken by anglers and consumed as food. A safety threshold of 100 Bq/kg of radioactive Cs was introduced in April 2012, but activity concentrations greater than this have been detected in fishes hundreds of kilometers distant from the FDNPP. There is clearly a pressing imperative to reduce radioactive Cs contamination of food. The Chernobyl accident released more than five million Tera Becquerel of radionuclides. Much radionuclides from the Chernobyl accident spread to Finland, Sweden and Norway, 2000 km to the northwest. Fish have been monitored for radioactivity Øvre Heimdalsvatn, a Norwegian subalpine lake (Brittain et al., 1991; Brittain and Gjerseth, 2010). Activity concentrations of 137Cs in brown trout reached 8400 Bq/kg in 1987 and declined to 200– 300 Bq/kg in 2008, but the contamination level has recently been constant and approached an asymptotic decline (Brittain and Gjerseth, 2010). The broad effects of the Chernobyl accident have been examined and management measures have been designed for large geographical areas (Report of the Chernobyl Forum Expert Group ‘Environment’, 2006; Yablokov et al., 2009). However, the ecological consequences of radioactive contamination in fishes are poorly understood. To precisely describe the mechanisms of diffusion and export of 137 Cs deposited in freshwater fish, we measured concentrations of 137 Cs in the muscle tissue and stomachs of brown trout (Salmo trutta), rainbow trout (Oncorhynchus mykiss) and kokanee (Oncorhynchus nerka) from a lake, that of brown trout (Salmo trutta) from a stream and that of charr (Salvelinus leucomaenis) from four streams. Here, we report the results of preliminary investigations 21 months after the FDNPP accident. 2. Materials and methods 2.1. Study site The study was conducted in the Nikko area (Lake Chuzenji, Oku Nikko and Ashio regions) located approximately 160 km southwest of the FDNPP. According to an aircraft radioactivity survey reported by MEXT (2012), the air dose rate in this area was 0.1–0.25 μSv/h on 31 May 2012. The study area is mostly forested; the dominant tree species are broadleaf and deciduous. Other areas are forested with Japanese cedar and cypress plantations used for timber production. The field survey was conducted in Lake Chuzenji and two headwater tributaries (Toyamasawa and Yanagisawa streams) of the Kinu River in the Oku Nikko region and in two headwater tributaries (Kuzosawa and Asosawa streams) of the Watarase River in the Ashio region, which form the upper drainage component of the Tone River system, Honshu, Japan (Fig. 1). 2.2. Sampling Fishes were captured in Lake Chuzenji and in the four streams in November and December, 2012 using fishing rod in the lake and battery-powered backpack electrofishing (Smith-Root Inc. LR-24) units operated at 300-V pulse-DC in the stream. In central Lake Chuzenji, three species of fishes, brown trout (Salmo trutta), rainbow trout (Oncorhynchus mykiss) and kokanee (salmon) (Oncorhynchus nerka) were sampled. In Toyamasawa stream, two species of fish, brown trout (Salmo trutta) and charr (Salvelinus leucomaenis) were sampled at site B (200 m stream segments). In other three streams, only charr (Salvelinus leucomaenis) were sampled at sites E, G, and I (200 m stream segments). After capture, we recorded the body size (fork length) of each fish and sampled
185
muscle tissue for the analysis of radioactive concentration. We then collected and froze the stomachs for the analysis of radiocesium concentrations in stomach tissue and for identification of stomach contents. The age of charr specimens was determined from sagittal otoliths using the surface reading method. The age of the other three fishes was not determined; folk length was used as a substitute metric. In the four streams, air dose rates at 1-m above ground were measured with a γ survey meter adjacent to the stream (NaI scintillation counter; ALOKA TCS-172). Electrical conductivities (EC) of the streams were measured with a portable compact twin conductivity meter (B-173; Horiba); pH was measured with a portable compact twin pH meter (B-212; Horiba). Wetted stream 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 were measured 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.
2.3. Radiocesium analysis and identification Samples of fish stomach and muscle tissue were directly packed into 100-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&G, Tokyo, Japan; GC4020, Canberra, Japan) for 36,000 s–63,000 s depending on the sample weight. Gamma-ray peaks of 622 keV were used to determine 137 Cs. The measurement system was calibrated using a standard gamma-ray source (MX033U8PP, Japan Radioisotope Association, Tokyo, Japan), and a standard soil sample (IAEA-444) was used to check accuracy. Fine adjustments to the measurements were made to correspond to the radiocesium concentration value for 1 December 2012. The radioactivity of lake and stream water was not measured because 137Cs concentrations in several lakes and streams were reported to be below the detection level (1 Bq/l) (MOE 2013, Tochigi Prefecture, 2013). The inner contents of the frozen stomach for the analysis of stomach contents were removed and identified under a 50 × microscope (SMZ-U; Nikon). We identified specimens to the family level or higher following Merritt and Cummins (1996) and Kawai (1985).
2.4. Statistical analysis Kruskal–Wallis tests or Mann–Whitney U-tests were used to compare the 137Cs concentrations. The Kendall test was used to clarify the relationship between folk length and 137Cs concentration. We conducted principal component analysis (PCA) on the presence or absence of each fish stomach content for three species in Lake Chuzenji, for brown trout in Lake Chuzenji and Toyamasawa stream, and for charr in the four streams. We examined the PCA axes among the three fish species and among the four streams using a Kruskal–Wallis multiple comparison test and between lake and stream habitats using a Mann– Whitney U-test. It would be useful to compare samples of the same species or the same age at all sampling locations. However, the fishes sampled in this study differed between the stream and lake and it was not practical to collect specimens of equal size. Statistical analysis was performed using SYSTAT version 10 (SPSS Inc. 2000). Radiocesium concentrations that were below the detection level because of insufficient weight for radiocesium analysis were excluded from the statistical analysis.
186
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
Fig. 1. Study site of Lake Chuzenji and four streams in the Oku Nikko and Ashio areas, Tochigi Prefecture, Japan. ● A–I: stream water sampling sites, □ B, E, G, I: fish sampling sites.
3. Results Aerial radioactivity was higher in the Ashio region than in the Oku Nikko region (z = 2.33, n = 9, P b 0.05, Mann–Whitney U-test; Table 1), as was radiocesium deposition. These two regions did not differ in air or water temperature, pH, stream width or stream velocity, but EC differed between the regions (Table 1; Yoshimura and Akama, 2014). 137 Cs concentrations in fish stomachs were highest in brown trout (Salmo trutta), lowest in rainbow trout (Oncorhynchus mykiss) and intermediate in kokanee (salmon) (Oncorhynchus nerka) (H = 11.1, n = 14, P b 0.005, Kruskal–Wallis test; Fig. 2). 137 Cs concentrations in fish muscle showed the same pattern among species (H = 590.5, n = 69, P b 0.0001, Kruskal–Wallis
test; Fig. 2). Radioactive Cs concentrations in stomach and muscle tissues did not differ significantly among the three species. There was no relationship between 137 Cs concentrations in fish muscle and fork length in three species (brown trout: τ = 0.27, n = 23, n.s.; kokanee: τ = 0.02, n = 24, n.s.; rainbow trout: τ = 0.17, n = 22, n.s.; Kendall test). Stomach contents varied significantly among the three species of fish (Appendix A). Brown trout stomachs primarily contained fish and unknown digested foods. Kokanee primarily contained unknown foods and rainbow trout stomachs contained a wide variety of fish and invertebrates. The first PCA axis explained 52% of the variation in the stomach contents (mainly the number of species consumed) but was not correlated with muscle concentration of
Table 1 The dose rate at 1 m above the ground, air temperature, water temperature, pH, electric conductivity, stream velocity and stream width at 9 sites on December 2012 with statistical result. Oku Nikko
Ashio
Toyamasawa
Dose rate (μSv/h) Air temperature (°C) Water temperature (°C) pH Electric conductivity (μs/cm) Stream velocity (cm/s) Stream widths (m) Altitude (m) *: P b 0.05.
Asosawa
U-test
A
B
C
Yanagisawa D
E
F
G
Kuzosawa H
I
z
0.08 −0.8 7.2 6.9 61 30 7.6 1270
0.10 1.7 6.8 7.0 50 63 5.7 1300
0.12 0.7 7.3 7.1 49 32 4.8 1450
0.09 0.1 8.1 6.7 53 48 17.1 1270
0.10 6.4 4.9 6.4 33 35 5.8 1320
0.11 6.7 2.6 6.9 51 58 8.1 1380
0.26 1.3 4.0 6.5 73 70 3.0 810
0.21 1.7 4.2 6.3 59 68 3.5 950
0.27 −1.9 1.6 6.8 64 57 5.8 790
2.33* 0.65 1.81 1.56 2.07* 1.81 2.69 2.33*
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
a
a
(Bq/kg)
200
150 100
137Cs
137Cs
(Bq/kg)
200
50
150 100 50 0
0 0
200
400
600
0
800
100
200
Brown trout
400
Chuzenji Lake
Rainbow trout
b
137Cs
150 100
500
600
Toyamasawa
b
200
(Bq/kg)
200
(Bq/kg)
Kokanee
300
Fork length (mm)
Fork length (mm)
137Cs
187
150 100 50
50 0 0
0 0
100
200
300
400
500
Kokanee (stomach)
Chuzenji Lake (stomach)
137
Cs (τ = 0.37, n = 15, n.s., Kendall test). The second PCA axis explained 13% of the stomach content data (the lower part of the diagram shows higher fish contents and the upper part of diagram shows higher insects contents) and was correlated with muscle concentrations of 137 Cs (τ = − 0.56, n = 15, P b 0.005, Kendall test). The PCA also showed that stomach contents of the three species were statistically different based on the first axis (H = 9.1, n = 15,
500
600
Toyamasawa (stomach)
P b 0.05, Kruskal–Wallis test; Fig. 3) and the second axis (H = 6.2, n = 15, P b 0.05, Kruskal–Wallis test; Fig. 3). No significant correlation was observed between the PCA axes and 137Cs concentration in any of the three fish species (Kendall test; Fig. 3). 0.8
Lake Stream
0.4
Brown trout Kokanee Rainbow trout Axis 2 (20%)
0.2
0.4
Axis 2 (13%)
400
Fig. 4. Relationship between body length and 137Cs concentration in brown trout from Lake Chuzenji and Toyamasawa stream. (a) Muscle; (b) stomach.
0.6
0.6
300
Rainbow trout (stomach)
Fig. 2. Relationship between body length and 137Cs concentration of three species in Lake Chuzenji. (a) Muscle; (b) stomach.
0.8
200
Fork length (mm)
Fork length (mm) Brown trout (stomach)
100
600
0.2
0
-0.2
0 -0.4 -0.2 -0.6 -0.4 -0.8
-0.6 -0.8
-1 0
0.2
0.4
0.6
0.8
1
1.2
Axis 1 (52%) Fig. 3. Scatter diagram of the principal components analysis (PCA) of stomach contents of three fishes from Lake Chuzenji. Bubble size indicates the concentrations of 137Cs in muscle tissue of each fish.
0
0.2
0.4
0.6
0.8
1
Axis 1 (33%) Fig. 5. Scatter diagram of stomach contents in the principal components analysis (PCA) of each brown trout in Lake Chuzenji and Toyamasawa stream. Bubble size indicates the concentration of 137Cs in the muscle tissue of each fish.
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
Concentrations of 137 Cs in the stomach contents of brown trout were higher in Lake Chuzenji than in the streams (z = 2.7, n = 11, P b 0.01, Mann–Whitney U-test; Fig. 4), and so were 137 Cs concentrations in muscle tissue (z = 6.0, n = 50, P b 0.0001, Mann–Whitney U-test; Fig. 4). No significant difference in 137Cs concentration was observed between stomach and muscle tissues. There was significant relationship between 137Cs concentrations in fish muscle and fork length in brown trout from streams (τ = 0.51, n = 29, P b 0.001; Kendall test). Stomach contents of brown trout differed between Lake Chuzenji and Toyamasawa stream (Appendix A). In streams, the brown trout stomach contents were mainly insects. The first PCA axis explained 33% of the variation in stomach content (mainly the number of species consumed) and was not correlated with 137Cs concentrations in muscle tissue (τ = 0.01, n = 14, n.s., Kendall test). The second PCA axis explained 20% of the variation in stomach content data (the lower part of the diagram shows higher fish content and the upper part of the diagram shows higher insect content) and was correlated with 137 Cs concentrations in muscle tissue (τ = − 0.40, n = 14, P b 0.05, Kendall test). Stomach contents were statistically different between lake and stream fish based on PCA axis 2 (z = 3.0, n = 14, P b 0.005, Mann–Whitney U-test; Fig. 5), but not on axis 1 (z = 0.2, n = 14, n.s., Mann–Whitney U-test; Fig. 5). No significant correlation was detected between these two axes and 137Cs concentrations of fish in each habitat (Kendall test; Fig. 5). Concentrations of 137Cs in the stomach tissue of charr did not differ among the four streams (H = 4.6, n = 18, n.s., Kruskal–Wallis test), but muscle activity concentrations did differ among the streams (H = 16.2, n = 88, P b 0.001, Kruskal–Wallis test). Older fish had higher muscle concentrations of 137Cs (Toyamasawa: H = 7.8, n = 35, P b 0.052; Yanagisawa: H = 8.6, n = 19, P b 0.05; Kuzosawa: H = 22.5, n = 33, P b 0.0001, Kruskal–Wallis test; Fig. 6), but no difference was observed in the concentrations of 137Cs in stomach tissues among age. The stomach contents of charr consisted primary of insections in all four streams (Appendix B). Axis 1 of the PCA explained 30% of the variation in stomach contents (the right side of the diagram shows higher aquatic insect content and the left side of diagram shows higher terrestrial insects content) and was correlated with concentrations of 137Cs in muscle tissue (τ = 0.31, n = 26, P b 0.05, Kendall test). Axis 2 of the PCA explained 9% of the variation in stomach contents (the lower part of the diagram shows higher Bryophyta content) and was also correlated with 137Cs levels in muscle (τ = − 0.30, n = 26, P b 0.05, Kendall test). Stomach contents among the four streams differed statistically along PCA axis 1 (H = 22.2, n = 40, P b 0.001, Kruskal–Wallis test; Fig. 7), especially between fish in Toyamasawa and the other streams. Stomach contents also differed among the four streams based on PCA axis 2 (H = 22.9, n = 40, P b 0.001, Kruskal–Wallis test; Fig. 7), especially between fish in the Ashio region and the Oku Nikko region. No
100
60 40 20
0.2 0 -0.2 -0.4 -0.6 -0.8 -0.4
0+
1+
2+
Fish age
3+
-0.2
0
0.2
0.4
0.6
0.8
1
Axis 1 (30%) Fig. 7. Scatter diagram of the principal components analysis (PCA) for stomach contents of each charr from the four streams. Bubble size indicates the concentrations of 137Cs in muscle tissue of each fish.
significant correlation was observed between these two axes and Cs concentrations of fish in each of the four streams, except the relationship between PCA axis 2 and 137Cs concentration in muscle tissue of fish from the Kuzosawa stream (τ = −0.73, n = 11, P b 0.005, Kendall test; Fig. 7). 137
4. Discussion Fishes were contaminated with radioactive substances even where dose rates in the atmosphere were relatively lower (160 km distance from the FDNPP). In Lake Chuzenji, concentrations of 137Cs in muscle tissues and stomach were highest in S. trutta, lowest in O. mykiss and intermediate in O. nerka. The lack of difference between stomach and muscle concentrations of 137Cs indicates that the absence of a high level of contamination in the stomach contents and suggests that and radioactive materials are transferred from food items to muscle tissues. Research after the Chernobyl accident also showed that radioactive contamination was caused by diet (Forseth et al., 1991; Ugedal et al., 1995), and dietary differences were reflected in the decay rates and ecological half-lives (Hessen et al., 2002). The primary food of brown trout in Lake Chuzenji was goby, and the 137 Cs concentration of goby in Lake Chuzenji averaged 57.4 Bq/kg (n = 20, 1 December 2012, unpublished data). There was no diet in the stomach of kokanee and they usually consume zooplankton. The 137Cs concentration of zooplankton in Lake Chuzenji is 8.3 Bq/kg (n = 1, 1 December 2012, unpublished data). Thus,
100
b
80 60 40 20 0
0
Toyamasawa Yanagisawa Kuzosawa asosawa
(Bq/kg)
(Bq/kg)
80
0.4
137Cs
a
137Cs
137Cs
(Bq/kg)
100
0.6
Axis 1 (9%)
188
c
80 60 40 20 0
0+
1+
2+
Fish age
3+
0+
1+
2+
3+
Fish age
Fig. 6. Relationship between fish age and concentration of 137Cs in stream fish. (a) Toyamasawa stream, (b) Yanagisawa stream, (c) Kuzosawa stream. ○: Concentration of 137Cs in charr muscle and ♦: concentration of 137Cs in charr stomach tissue.
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
higher 137Cs concentrations in brown trout are likely to be acquired mainly from their diet. Some rainbow trout had 137 Cs concentrations that were below the detection limit; these fishes may have been released as adults. Brown trout and kokanee are released into Lake Chuzenji only as fry, but rainbow trout are released as both fry and adult fish. Because fish released as adults spend only a short period in the contaminated lake, their muscle tissue is expected to be less contaminated. The mean 137 Cs concentrations of three families of aquatic stream insects (Perlidae, Perlodidae and Stenopsychidae) were 67.9 Bq/kg (max: 271 Bq/kg, min: 0 Bq/kg; Yoshimura and Akama, 2014). Thus, 137Cs concentrations in aquatic insects in lake are higher than those of zooplankton, but with a large variance. Activity concentrations of more than 50 Bq/kg in some lake rainbow trout, which feed primarily on insects and are released as fry, indicate that muscle contamination is a result of diet. However, concentrations of 137 Cs did not differ greatly between goby in the lake and aquatic insects in the streams. The difference in 137Cs concentrations between these two fish species may instead be a result of habitat differences. Brown trout typically reside from benthic substrate to middle strata of the lake interior, whereas rainbow trout reside from middle to upper depths close to the shoreline. Radioactive substances tend to condense more in deeper area of the lake where less water flow occurs. Higher 137 Cs concentrations in brown trout may arise from these differences in habitat preference. Stomach contents of brown trout in Lake Chuzenji differed from those in Toyamasawa stream, and radiocesium concentrations of stomach and muscle tissue also differed between the habitats, suggesting that the differences in contamination are due to habitat differences. However, 137 Cs concentrations of goby consumed by brown trout in the lake and aquatic insects consumed by brown trout in the stream did not differ. The primary environmental difference between the lake and stream is the rate of water flow. In lakes, particulate organic matter from the surrounding forest, which may be contaminated with 137Cs, settles to the bottom and releases 137 Cs by the decomposition of particle organic materials gathered. The released 137 Cs accumulates at the bottom of the lake and is not easily washed away. The lack of flow in deep portions of the lake may also result in accumulation of silt contaminated with 137Cs. Sand substrates had higher 137Cs concentrations in Lake Chuzenji (81.28 Bq/kg, n = 11, unpublished data) than in any of the four streams (26.59 Bq/kg; Yoshimura and Akama, 2014). The 137Cs value of sand in the lake seems to be higher than that in the stream (Ministry of the Environment, 2011, 2013). Aquatic insects that inhabit stream pools have higher value of 137 Cs than insects in riffles (Yoshimura and Akama, 2014); water flow rate may thus be a key factor determining the activity concentrations in fishes. Retention time would also be related to contamination level and would lead to variability in radioactive cesium concentration in fish from different lentic environments (Håkanson, 1992). Free 137Cs in stagnant water in lakes accumulates particulate organic matter associated with the substrate. Thus, fishes living near the bottoms of lakes would intake highly 137Cs contaminated materials into their bodies from dietary items settling to the bottom. Brown trout in Norwegian lake contaminated by radioactive fallout from the Chernobyl accident retain substantial radioactivity levels more than 20 years after the accident, and these levels do not appear to be declining (Brittain and Gjerseth, 2010), probably because of continuing input of radioactive substances from the catchment and remobilization of sediments in the lake. Some mechanisms of 137Cs contamination of fishes remain unknown. Removal of radioactive substances is necessary to alleviate this problem. At present, only catch-and-release fishing is permitted in Lake Chuzenji. Although restoring the lake environment would take decades, areas in which fishing and fish consumption can be safely
189
practiced must be reclaimed. Full-grown rainbow trout released to the lake had lower concentrations of 137Cs. Decontamination of soil substrates and release of non-contaminated fish in designated areas would be the most rapid way to improve fish quality and enable tourism to resume. However, continual removal of highly contaminated adult fish such as brown trout and release of uncontaminated fry may constitute a more appropriate long-term approach. Among the four streams, radioactive Cs values in the muscle tissues of charr were elevated where aerial dose rates were higher. Although no differences in 137 Cs values were observed in stomach among the four streams, fishes in the Ashio region consumed more Chlorophyta and Heterokontophyta. The 137Cs value of Chlorophyta in the Ashio region was 170 Bq/kg (n = 1, 1 December 2012, unpublished data). The higher 137 Cs value of fish in the Ashio region might be a result of consumption of these algae in addition to higher contamination from fallout. The higher 137Cs concentrations in older fish might also be caused by continuous intake of contaminated food. However, a large degree of variation in 137 Cs was detected in equal-aged fishes in a given stream. The habitat range of charr is generally larger than that of aquatic insects and always includes a small riffle and a pool. Concentrations of 137 Cs in aquatic insects differed between pools and riffles even within the same families. Habitat selection (proportion of time spent in pools and riffles) by individual fish may cause dietary variation in 137 Cs, leading to variability in 137Cs levels among fish in the same sampling area. The PCA axes for fish diet were correlated with 137 Cs concentrations of muscle tissue in all three species of fish in the lake, in brown trout in the lake and streams, and in charr in all four streams, suggesting that dietary differences are primarily responsible for the differences in radioactive Cs concentrations among these fish. However, the PCA axis for diet was not correlated with 137 Cs concentrations in muscle tissue across species, habitat or streams, which suggests that the diet menu of each individual is not always almost the same and there is substantial variation of 137 Cs concentration in individual diets. Fritsch et al. (2008) reported that 137 Cs in soil is transferred to plants, earthworms and snails, but that transfer rates of radionuclides through the food web depend on the concentration of radioactive substances, exposure period and consumption rates. Habitat variability among individual fish would also affect 137 Cs transfer. The areas where this study was conducted are extremely popular fishing locations. However, only catch-and-release fishing is currently permitted because of the elevated radioactivity levels. As long as the diet and sand substratum are contaminated, levels of radioactive Cs in fishes are expected to remain high, and continual monitoring and management of radioactivity will be necessary.
Conflict of interest The authors declare no conflicts of interests.
Acknowledgements We thank Dr. Makino in the Forestry and Forest Products Research Institute, Dr. Yamamoto in the National Research Institute of aquaculture and Dr. Yoshida in the fisheries experimental station of Tochigi Prefecture for their assistance with sampling survey. Capture of fishes was done with the permission from Tochigi Prefecture. This work was supported in part by a research grant from the Council of Science and Technology Policy in 2012.
190
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
Appendix A. Stomach contents of three species of fishes in Lake Chuzenji and of brown trout in the Toyamasawa stream Lake Chuzenji Division
Order
Family
Nematomorpha Arthropoda
Gordea Araneae Lithobiomorpha Thysanura Ephemeroptera
Gordiidae Undetermined Ethopolidae Lepismatidae Baetidae Heptageniidae Ephemerellidae Undetermined Nemouridae Chloroperlidae Perlodidae Acrididae Membracidae Psyllidae Aphididae Tettigometridae Reduviidae Lygaeidae Pentatomidae Acanthosomatidae Undetermined Arctopsychidae Philopotamidae Stenopsychidae Rhyacophilidae Brachycentridae Limnephilidae Undetermined Tipulidae Chronomidae Bibionidae Drosophilidae Undetermined Staphylinidae Undetermined Chalcidoidea Formicidae Undetermined
Plecoptera
Orthoptera Hemiptera
Trichoptera
Diptera
Coleoptera Hymenoptera
Chordata
Unknown egg Chlorophyta Bryophyta Magnoliophyta
Insect (fragments) Insect egg Perciformes Ichthyic digest Ichthyic eggs Ichthyic bone Bird feather
Brown trout (5)
Gobiidae
Toyama sawa Kokanee (5)
Rainbow trout (5)
Brown trout (9) *** ** ** * ** ** * ** *** * ** *** * *** ** ** ** ** *** ** *** ** * * **
*
* * **
*** ** **
* ** ***** **
** *** **
* *** * ** ** ** * ** ** ****
*** ** ** *** ** *** ***
**** **** ** *
** *
Ulotrichales Bryidae Hepaticopsida Hydrocharitales Sapindales
Ulotrichaceae
* **** ** *** *** **** *** *****
Hydrocharitaceae Aceraceae
Plant (fragment) Sand Unknown digest
*
**
****
****
** *** *****
Weight of each stomach content, *: b0.01, **: b0.1, ***: b1.0, ****: b10.0, *****: b100.0 (g).
Appendix B. Stomach contents of charr in four streams Division Nematoda Arthropoda
Order
Family
Opiliones Acari Araneae
Phalangiidae Spercontidae Thomisidae Undetermined Ligiidae
Isopoda Collembola Ephemeroptera
Siphlonuridae Baetidae Heptageniidae
Toyama sawa (14)
Yanagi sawa (10)
Kuzo sawa (11)
Aso sawa (5)
** **
***
**
*
* ** * ** * **
** ** **
* * *
**
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
191
Appendix (continued) B (continued) Division
Order
Plecoptera
Orthoptera Hemiptera
Neuroptera Trichoptera
Lepidoptera Diptera
Coleoptera
Hymenoptera
Chordata Unknown egg Chlorophyta Heterokontophyta Bryophyta Plant (fragment) Sand Unknown digest
Insect (fragments) Salmoniformes Ichthyic bone
Family Ephemeridae Ephemerellidae Undetermined Scopuridae Capniidae Nemouridae Taeniopterygidae Chloroperlidae Perlidae Perlodidae Acrididae Membracidae Aphrophoridae Psyllidae Aphididae Lygaeidae Pentatomidae Acanthosomatidae Undetermined Osmylidae Undetermined Arctopsychidae Hydropsychidae Philopotamidae Stenopsychidae Glossosomatidae Rhyacophilidae Limnephilidae Brachycentridae Goeridae Lepidostomatidae Uenoidae Undetermined Tipulidae Blephariceridae Chronomidae Simuliidae Empididae Bibionidae Undetermined Carabidae Staphylinidae Curculionidae Chrysomelidae Undetermined Cynipoidea Chalcidoidea Braconidae Ichneumonidae Formicidae Salmonidae
Toyama sawa (14)
Yanagi sawa (10)
Kuzo sawa (11)
Aso sawa (5)
** * ***
***
** ***
* **
* * * ** *** *** **
* * *
*** * ** ** ** ** ** ** * *** ** ** ** **
* ** * * ** ***
* *
*** *** ** **
**
** *** **
*
**
** *
*** * ** ** ** *** ** * * * *** * **** ****
*
*
**
**** ** *** * *** *
* ***
** * *** *** ** **
*** *
* **** * *
**
*** *** ** * *** **
** ** *** * **
*
*
***
***
* * *
*
*** **** *****
** *** ***
*
* ** **
* Ulotrichales Centrales Pennales Bryidae
Ulotrichaceae Melosiraceae Diatomaceae ** *** *** ****
** *** ****
*
Weight of each stomach content, *: b0.01, **: b0.1, ***: b1.0, ****: b10.0, *****: b100.0.
References Brittain JE, Gjerseth JE. Long-term trends and variation in 137Cs activity concentrations in brown trout (Salmo trutta) from Øvre Heimdalsvatn, a Norwegian subalpine lake. Hydrobiologia 2010;642:107–13. Brittain JE, Storruste A, Larsen E. Radiocesium in brown trout (Salmo-trutta) from a subalpine lake ecosystem after the Chernobyl reactor accident. J Environ Radioact 1991;14:181–91. Forseth T, Ugedal O, Jonsson B, Langeland A, Njastad O. Radiocaesium turnover in Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta) in a Norwegian lake. J Appl Ecol 1991;28:1053–67.
Fritsch C, Scheifler R, Beaugelin-Seiller K, Hubert P, Coeurdassier M, Vaufleury AD, et al. Biotic interactions modify the transfer of Cesium-137 in a soil–earthworm–plant– snail food web. Environ Toxicol Chem 2008;27:1698–707. Fukuyama T, Takenaka C, Onda Y. 137Cs loss via soil erosion from a mountainous headwater catchment in central Japan. Sci Total Environ 2005;350:238–47. Håkanson L. Radioactive cesium in fish in Swedish lakes 1986–1988—general pattern related to fallout and lake characteristics. J Environ Radioact 1992;15: 207–29. Hashimoto S, Ugawa S, Nanko K, Shichi K. The total amounts of radioactively contaminated materials in forests in Fukushima, Japan. Sci Rep 2012;2. [article number 416].
192
M. Yoshimura, T. Yokoduka / Science of the Total Environment 482–483 (2014) 184–192
Hessen DO, Skurdal J, Hegge O, Hesthagen T. Radiocesium decay in populations of brown trout and Arctic char in the alpine Atna area, south-eastern Norway. Hydrobiologia 2002;489:55–62. Kato H, Onda Y, Tanaka Y. Using 137Cs and 210Pbex measurements to estimate soil redistribution rates on semi-arid grassland in Mongolia. Geophys J Roy Astron Soc 2010; 114:508–19. Kawai TIn: Kawai T, editor. An illustrated book of aquatic insects of Japan. Tokyo: Tokai University Press; 1985. Kinoshita N, Sueki K, Sasa K, Kitagawa J, Ikarashi S, Nishimura T, et al. Assessment of individual radionuclide distributions from the Fukushima nuclear accident covering central-east Japan. Proc Natl Acad Sci 2011;108:19526–9. Kruyts N, Delvaux B. Soil organic horizons as a major source for radiocesium biorecycling in forest ecosystems. J Environ Radioact 2002;58:175–90. Merritt RW, Cummins KW. An Introduction to the aquatic insects of North America. 3rd ed. Dubuque, IA: Kendall/Hunt; 1996. Ministry of Education, Culture, Sports, Science, Technology (MEXT). Database on the research of radioactive substances distribution. http://radioactivity.nsr.go.jp/ja/contents/5000/4930/24/1305819_0727.pdf, 2011. [10 January 2014]. Ministry of Education, Culture, Sports, Science, Technology (MEXT). Database on the research of radioactive substances distribution. http://radb.jaea.go.jp/mapdb/portals/ 101002/?prefectures=09&category_b=b1201&year=2012, 2012. [10 January 2014]. Ministry of the Environment. Database on the environmental monitoring research of radioactive substances in East Japan. http://www.env.go.jp/jishin/monitoring/result_ pw111216-2.pdf, 2011. [10 January 2014]. Ministry of the Environment. Database on the environmental monitoring research of radioactive substances in East Japan. http://www.env.go.jp/jishin/monitoring/result_ pw131108-1.pdf, 2013. [10 January 2014].
Ohara T, Morino Y, Tanaka A. Atmospheric behavior of radioactive materials from Fukushima Daiichi Nuclear Power Plant. J Natl Inst Public Health 2011;60: 292–9. Report of the Chernobyl Forum Expert Group ‘Environment’. Environmental consequences of the Chernobyl accident and their remediation: twenty years of experience. Vienna, Austria: Radiological Assessment Reports Series, IAEA; 2006. Tochigi prefecture. Data base on the dose rate in the air in Tochigi Prefecture from May 13 to May 31. http://www.pref.tochigi.lg.jp/kinkyu/documents/20110601_1400_50cm. pdf, 2011. [10 January 2014]. Tochigi prefecture. Data base on the activity concentrations in stream and lake sand in Tochigi Prefecture. http://www.pref.tochigi.lg.jp/d03/kankyosho_houshaseibusshitu. html, 2013. [10 January 2014]. Ugedal O, Forseth T, Jonsson B, Njastad O. Sources of variation in radiocaesium levels between individual fish from a Chernobyl contaminated Norwegian lake. J Appl Ecol 1995;32:352–61. Wakiyama Y, Onda Y, Mizugaki S, Asai H, Hiramatsu S. Soil erosion rates on forested mountain hillslopes estimated using 137 Cs and 210 Pb ex . Geoderma 2010;159: 39–52. Yablokov AV, Nesterenko VB, Nesterenko AV. Chernobyl, consequences of the catastrophe for people and the environment. Ann N Y Acad Sci 2009;1181. Yoshimura M, Akama A. Radioactive contamination of aquatic insects in a stream impacted by the Fukushima nuclear power plant accident. Hydrobiologia 2014; 722:19–30.
