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Fallout volume and litter type affect 137Cs concentration difference in litter between forest and stream environments
Journal of Environmental Radioactivity 164 (2016) 169e173
Contents lists available at ScienceDirect
Journal of Environmental Radioactivity journal homepage: www.elsevier.com/locate/jenvrad
Short communication
Fallout volume and litter type affect 137Cs concentration difference in litter between forest and stream environments Masaru Sakai a, *, Takashi Gomi b, Junjiro N. Negishi c a
Faculty of Science and Engineering, Chuo University, 1-13-27 Kasuga, Bunkyo-ku, Tokyo, 112-8551, Japan Institute of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo, 183-8509, Japan c Faculty of Environmental Earth Science, Hokkaido University, N10, W5, Kita-ku, Sapporo, Hokkaido, 060-0860, Japan b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 May 2016 Received in revised form 19 July 2016 Accepted 22 July 2016
It is important to understand the changes in the 137Cs concentration in litter through leaching when considering that 137Cs is transferred from basal food resources to animals in forested streams. We found that the difference of 137Cs activity concentration in litter between forest and stream was associated with both litter type and 137Cs fallout volume around Fukushima, Japan. The 137Cs activity concentrations in the litter of evergreen conifers tended to be greater than those in the litter of broad-leaved deciduous trees because of the absence of deciduous leaves during the fallout period in March 2011. Moreover, 137Cs activity concentrations in forest litter were greater with respect to the 137Cs fallout volume. The 137Cs activity concentrations in stream litter were much lower than those in forest litter when those in forest litter were higher. The 137Cs leaching patterns indicated that the differences in 137Cs activity concentration between forest and stream litter could change with changes in both fallout volume and litter type. Because litter is an important basal food resource in the food webs of both forests and streams, the 137Cs concentration gradient reflects to possible 137Cs transfer from lower to higher trophic animals. Our findings will improve our understanding of the spatial heterogeneity and variability of 137Cs concentrations in animals resident to the contaminated landscape. © 2016 Elsevier Ltd. All rights reserved.
Keywords: Basal food resource Forest ecosystem Leaching Radiocesium Stream ecosystem
1. Introduction Cesium-137 fallout due to the Fukushima Daiichi Nuclear Power Plant (FDNPP) accident in March 2011 resulted in extensive contamination of the forest landscape of Fukushima and the surrounding regions (Yasunari et al., 2011; Hashimoto et al., 2012). Approximately 70% of the land area of Japan is covered by forest, and evergreen coniferous plantations and deciduous secondary forests are the most dominant forest types in Japan (Kuroda et al., 2013). In evergreen coniferous forest, a large amount of atmospherically supplied 137Cs was attached to the canopy, including foliated branches, while 137Cs fallout was deposited mostly on the forest floor in deciduous forest because of the absence of leaves in early March (Kato et al., 2012). Cesium-137 contamination deposited on forest ecosystems has further circulated within the ecosystems (e.g., Steiner et al., 2002). Hence, the movement of 137Cs
* Corresponding author. E-mail addresses: [email protected] (M. Sakai), [email protected] (T. Gomi), [email protected] (J.N. Negishi). http://dx.doi.org/10.1016/j.jenvrad.2016.07.030 0265-931X/© 2016 Elsevier Ltd. All rights reserved.
may differ depending on the differences in 137Cs attachment to leaves between evergreen coniferous and broad-leaved deciduous forests (Kato et al., in press). In forest environments, terrestrial and aquatic food webs are often structured by detrital food chains that originate from litter because of the limited light conditions under the canopies (Vannote et al., 1980; Sakai et al., 2016). Therefore, 137Cs transported with litterfall can generate bottom-up 137Cs transfers to higher trophic levels in such forest ecosystems (Sakai et al., 2016). Recent studies demonstrated that the 137Cs concentration in litter is lower in streams than in adjacent forest environments (Sakai et al., 2015). Such differences further reflect the contamination levels of animal communities in the food webs of forests and streams (Sakai et al., 2016). The findings of the previous studies indicated that 137Cs leaching from contaminated litter is the primary process influencing the dynamics of contaminants in stream ecosystems. Cesium-137 transported with litterfall to streams can differ depending on the dominant forest types in riparian zones, because the canopies of evergreen coniferous forests were more contaminated than those of broad-leaved deciduous forests following the FDNPP accident (Kato et al., in press). Such differences in the 137Cs
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concentration between coniferous and deciduous litter may further reflect the leaching patterns in streams, because the leaching pattern may depend on the concentration gradient (Hefter and Tomkins, 2003; Sakai et al., 2016). Changes in the 137Cs concentration in litter due to leaching in streams can be high in evergreen coniferous litter because of the high initial contamination level compared with broad-leaved deciduous litter. In addition to the litter type, the 137Cs concentrations in litter are also associated with the 137Cs fallout volume in forests. The 137Cs fallout was spatially heterogeneous from one watershed to another (Kinoshita et al., 2011). Such distribution patterns are also related to the 137Cs concentration in particulate matter in streams (Yoshimura et al., 2015). Therefore, the different 137Cs concentrations in litter due to variations in fallout volume might lead to differences in the loss of 137Cs once the litter enters stream channels in riparian zones. Thus, we hypothesized that both litter types (evergreen coniferous and broad-leaved deciduous litters) and 137Cs fallout volumes were the primary factors responsible for differences in the 137Cs concentration between forests and streams. This hypothesis was tested by investigating the 137Cs activity concentrations in litter in both forests and streams with different contamination levels. 2. Materials and methods 2.1. Study site and sampling This study was conducted in seven stream reaches, with riparian forest affected by different levels of contamination in Fukushima (six sites) and Gunma (one site) Prefectures (Table 1, Fig. 1). The seven study sites had different amounts of 137Cs fallout, ranging from the lowest with 30e60 kBq/m2 to the highest with 1000e3000 kBq/m2, with all values determined by the governmental airborne monitoring in June 2012 (MEXT, 2012). Detailed methodology of the airborne monitoring can be found at: http:// ramap.jmc.or.jp/map/eng/about.html. We classified the contamination levels into nine categories to enable a statistical analysis (see Section 2.3). Contamination classes 1 to 9 corresponded to the following respective fallout volumes (ranges of volume); 10, 10e30, 30e60, 60e100, 100e300, 300e600, 600e1000, 1000e3000, and >3000 kBq/m2. Site IDs A to G corresponded to a range from high (class 8) to low (class 3) contamination (Table 1). Most of the riparian forests of our study sites were mixed forests, containing evergreen conifers and broad-leaved deciduous trees, with the exception of site B, which was covered only by an evergreen coniferous plantation. The evergreen conifer species was Japanese cedar (Cryptomeria japonica) in all sites, whereas the
dominant deciduous tree species of the sites belonged to several families such as Fagaceae, Ulmaceae, and Sapindaceae. For sampling forest and stream litter, we selected a 50-m channel reach, with a 20 m-wide riparian zone on both sides. Three samples of both evergreen coniferous and broad-leaved deciduous litters were collected randomly from the riparian zone and in-channel region. In the monoculture riparian forest site (site B), we only collected evergreen coniferous litter. Samples of broadleaved deciduous litter comprised a range of families that were dominant within the sites. We selected a similar quality of litter, all with an intact shape and from the early stage of conditioning before starting physical and biological decomposition (Webster and Benfield, 1986; Sakai et al., 2016). All litter sampled from the forest floor was not attached to the mineral soil horizon. Samples in the stream were removed from submerged litter patches on the streambed. When sediment was attached to litter surfaces in streams, we gently rinsed and removed the sedimentary materials. Litter sampling from all sites (except site G) was completed in June 2014. Samples were also collected in May 2013 at sites F and G. Although duration of water soak can affect amount of 137Cs leaching from litter (Sakai et al., 2015), we assumed that the sampling criteria that control decomposition status of the litter samples aligned durations of water soak and enabled us to conduct fair comparisons of the difference in 137Cs concentrations in litter between forest and stream among the study sites. 2.2. Laboratory analysis All litter samples were dried at 60 C for 1 week and then pulverized using an electrical mill (FM-1; Osaka Chemical Co., Ltd., Osaka, Japan) for accurate 137Cs measurements (Sakai et al., 2015). Processed litter samples were packed into 100-mL plastic containers, and their dry weights and densities were measured. The activity concentration of 137Cs in the samples was determined by gamma-ray spectroscopy. Gamma-ray emissions at energies of 661.6 keV were counted using a high-purity germanium coaxial detector system coupled to a multi-channel analyzer (GCW2022 coupled to DSA1000, Canberra, Meriden, CT, USA; Ortec GEM20-70 coupled to DSPEC jr. 2.0, Ametek-AMT, Beijing, PRC). The energy and efficiency calibrations for this detector were performed using standard and blank (background) samples. For the analysis of radionuclide activity, each sample was measured for <10% of the error counts per net area counts. The geometry was held constant when counting all samples for 137Cs activity concentrations. All activities were corrected for decay according to the final sampling date (June 6, 2014) prior to statistical analysis. Our detector systems
Table 1 Location, site identification (ID), latitude, longitude, altitude, distance from the Fukushima Daiichi Nuclear Power Plant (FDNPP), 137Cs fallout volume, contamination class, and forest type at the study sites. The 137Cs fallout volumes at each site are taken from the governmental airborne monitoring data (MEXT, 2012), and the number of each contamination class was assigned with respect to each 137Cs deposition range shown in MEXT (2012). Place (Prefecture)
Site ID
Latitude ( )
Longitude ( )
Altitude (m)
Distance from the FDNPP
137
Cs fallout volume (kBq/ m2)
Contamination class
Forest type
Iitate village (Fukushima)
A
37.63N
140.78E
510
34 km northwest
1000e3000
8
Iitate village (Fukushima) Iitate village (Fukushima)
B C
37.68N 37.64N
140.80E 140.67E
470 630
37 km northwest 43 km northwest
600e1000 600e1000
7 7
Iitate village (Fukushima)
D
37.72N
140.79E
370
44 km northwest
300e600
6
Iitate village (Fukushima)
E
37.74N
140.69E
530
50 km northwest
300e600
6
Nihonmatsu city (Fukushima) Midori city (Gunma)
F
37.60N
140.61E
550
45 km west
100e300
5
G
36.55N
139.35E
620
180 km southwest
30e60
3
coniferous deciduous coniferous coniferous deciduous coniferous deciduous coniferous deciduous coniferous deciduous coniferous deciduous
and
and and and and and
M. Sakai et al. / Journal of Environmental Radioactivity 164 (2016) 169e173
171
Fig. 1. Map showing the location of the sample sites used in this study. (a) The location of Fukushima and Gunma Prefectures. (b) 137Cs fallout volume around Fukushima Prefecture. (c) The locations and respective 137Cs fallout volumes of the sample sites in Fukushima Prefecture.
were tested for proficiency according to the test provided by the International Atomic Energy Agency. 2.3. Statistical analysis We developed a simple linear relationship between 137Cs activity concentrations in litter and contamination classes, which was expressed as follows:
ð137 Cs activity concentration in litterÞ ¼ a ðcontamination classÞ þ b; where a and b are constants. This linear model was applied separately for forest and stream coniferous litter and forest and stream deciduous litter. A total of four regression models were developed. The statistical significance for the model constants were set at p ¼ 0.01. The statistical procedure for the regression models was performed using the lm function in R 3.1.2 (R Development Core Team, 2015). 3. Results and discussion The
137
Cs activity concentrations in both evergreen coniferous
and broad-leaved deciduous litter in both forests and streams were higher at the higher contamination classes (Fig. 2). This suggests that the 137Cs activity concentrations of litter in both the forest and stream environment were positively correlated with the amount of 137 Cs fallout regardless of the litter type. Previous studies in Fukushima have also identified a similar relationship between the 137 Cs fallout volume and soils, plants, and animals in forested environments (Kuroda et al., 2013; Hasegawa et al., 2013; Ayabe et al., 2014). Our studies have also confirmed positive relationships between fallout volume and 137Cs activity concentrations in litter, not only in forests, but also in stream environments. However, it should be noted that the horizontal axes in this study (Fig. 2) are categorical and each category has different ranges. Because broad-leaved deciduous trees were defoliated at the time of the FDNPP accident, the amount of 137Cs attached to the canopy layer in broad-leaved deciduous forests tended to be lower than the amount attached in evergreen coniferous forests (Endo et al., 2015; Komatsu et al., 2016; Kato et al., in press). For example, based on a detailed investigation in areas with contamination levels of 300e600 kBq/m2 (class 6 of our category), 70% of the 137Cs fallout was intercepted in the coniferous canopy, while only 23% of 137Cs fallout was intercepted by broad-leaved deciduous forest (Kato et al., in press). Differing amounts of intercepted
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M. Sakai et al. / Journal of Environmental Radioactivity 164 (2016) 169e173
Fig. 2. Regression lines for the 137Cs concentration in litter (upper panel: coniferous needle litter, lower panel: broad-leaved deciduous litter) and 137Cs contamination class. The black plots and line show forest litter, whereas the gray plots and line show stream litter. The bold values for the slopes and intercepts indicate statistical significance (P < 0.01).
137 Cs were also reported by Melin et al. (1994), with 90% interception in coniferous spruce forest, but only 35% in broad-leaved forest. Therefore, though immediately after the FDNPP accident, litter provided from forest floor to stream might be more contaminated in broad-leaved deciduous forest than in evergreen coniferous forest, the 137Cs activity concentrations in evergreen coniferous litter were consistently higher at our sampling periods (two to three years after the accident). Such difference of 137Cs activity concentrations in litter was also reported from 6 months after the FDNPP accident, and the 137Cs activity concentrations in Japanese cedar needle and broad-leaved deciduous litter were 6300 and 270 Bq/kg, respectively, at a site that had received 62 kBq/ m2 fallout (class 4 of our category) (Komatsu et al., 2016). Differences in the 137Cs activity concentration in litter were also associated with differences in the litterfall phenology between the two forest types. Because most of our samples were collected in 2014, the broad-leaved deciduous forests had experienced three foliation-defoliation cycles after the contamination event. Thus, although the translocation of 137Cs from root systems (or other parts of the tree) to the leaves may have occurred (Komatsu et al., 2016), the 137Cs activity concentrations in leaves in broad-leaved stands were consistently low. In evergreen coniferous forest with Japanese cedar, litterfall occurs during the autumn period and is a major process in the transfer of 137Cs from the forest canopy to the
floor (Teramage et al., 2014; Endo et al., 2015). However, a period of approximately 5 years is required to exchange all the needles on a particular tree (Cannel, 1982), which is much longer than that for broad-leaved deciduous trees (1 year). Therefore, broad-leaved deciduous forests supply less contaminated litter to forest and stream channels than do evergreen coniferous forests. We found apparent differences in the 137Cs activity concentration between forest and stream litter (Fig. 2). These differences were consistent for all sites and litter types. The lower 137Cs activity concentration in stream litter than forest litter was associated with 137 Cs leaching in the water column (Fig. 2). Litter in streams was affected by leaching through the abiotic removal of soluble substances preceding microbial colonization and invertebrate feeding (Webster and Benfield, 1986; Gessner et al., 1999). Based on a laboratory experiment, Sakai et al. (2015) demonstrated that the leaching process was important for reducing 137Cs activity concentrations in contaminated litter. In general, leaching from dried €rlocher, leaves tends to be greater than that from wet leaves (Ba 1992), and defoliated leaves are possibly affected more efficiently by leaching processes than are the fresh leaves that replace them. Our findings also revealed that the differences in the 137Cs activity concentration between forest and stream litters became greater in sites with high contamination levels, based on the different values of the slope constant (a) of the regressions (Fig. 2). The greater difference in the 137Cs activity concentration in highly contaminated sites was associated with efficient 137Cs leaching from the litter in streams (Sakai et al., 2016). Sheppard and Evenden (1990) reported that relative rate of radiocesium leaching from decaying litter is consistent among different initial concentrations in the litter, and indicated that the absolute loss of radiocesium is greater in highly contaminated litter. Our results were in accordance with the previous study. Because 137Cs activity concentration in stream water is possibly negligible in all our study sites (Ueda et al., 2013; Iwagami et al., in press), relative difference of 137Cs concentration in between litter and stream water could be largely determined by the concentration in litter. The difference in the 137Cs activity concentration between forest and stream litter was greater in evergreen coniferous litter than in broad-leaved deciduous litter. Because 137Cs leaching can be accelerated more when the 137Cs activity concentration in litter is higher, relatively high 137Cs activity concentration in evergreen coniferous litter compared with broad-leaved deciduous litter induced much more 137Cs detachment from litter by leaching. The results associated with both 137Cs fallout volume and litter type suggest that a spatially heterogeneous distribution of 137Cs in litter can be found in forest and stream ecosystems in the contaminated forest regions. Our result also showed that ratio of the slope constants (forest litter/stream litter) was similar between coniferous and deciduous litters (coniferous: 2.4; deciduous: 2.7). This result suggests that our sampling criteria (see Section 2.1) enable us to collect coniferous and deciduous litters with similar relative rate of 137Cs leaching. However, differences of morphology, persistence and litterfall phenology between the litter types are expected to intricately influence 137Cs leaching patterns in streams. Thus, further tests for examining effects of litter types on 137Cs leaching need to include information on initial 137Cs concentrations in litter and durations of water soak (e.g., Sheppard and Evenden, 1990; Sakai et al., 2015). The difference in the 137Cs activity concentration between forest and stream litter can reflect the contamination levels of animals in forests and streams (Sakai et al., 2016), because litter is the major basal food resource in not only forests, but also in streams covered by forest (Vannote et al., 1980; Gomi et al., 2002). For example, based on a stable isotope analysis, Sakai et al. (2016) reported that
M. Sakai et al. / Journal of Environmental Radioactivity 164 (2016) 169e173
the dominant basal food resource was litter in the Japanese cedar forest, and their study revealed the importance of the detrital food chains in transferring 137Cs from contaminated litter to higher trophic animals, such as arthropods in both riparian zones and streams, and fish in streams. Consequently, a low 137Cs activity concentration in litter, which is the result of leaching, propagates to relatively low 137Cs activity concentrations in stream animals compared with forest animals with similar trophic levels (Sakai et al., 2016). Therefore, fallout volume and litter type, which affected the relative differences in the 137Cs activity concentration between forest and stream litter, may further reflect the different 137 Cs activity concentrations in animals. 4. Conclusions This study showed that the differences in 137Cs activity concentrations between forest and stream litter tended to be greater with respect to the fallout volume and in evergreen coniferous forest than in broad-leaved deciduous forest. Because the 137Cs loss through leaching was greater when the concentration gradient between litter and stream water was higher, the high concentration gradient in highly contaminated sites and in evergreen coniferous litter induced efficient leaching and lowered the 137Cs activity concentrations in stream litter. Many studies have been conducted to investigate 137Cs activity contamination in animals. Most of these studies have only focused on the contamination of animals and their habitat (e.g., Sakai et al., 2014; Ayabe et al., 2014). However, our findings suggested that the differences in contamination levels, even among neighboring environments in forests and streams, were an important indicator for identifying the variability of 137Cs distributions. Such heterogeneity of 137Cs in the basal food resources of the ecosystems can also be important for developing ecosystem-based models of 137Cs transfer for long-term projections of contaminant movement in ecosystems. Acknowledgements We thank the members of the Watershed Hydrology and Ecosystem Management Laboratory at Tokyo University of Agriculture and Technology and the Watershed Conservation and Management Laboratory at Hokkaido University for sample preparation. Invaluable comment for the improvement of this manuscript was provided by Editor-in-Chief S. C. Sheppard, and the anonymous reviewers. A portion of this study was supported by the Environmental Research Fund (ZD-1202) of the Ministry of the Environment, Japan, and the Japan Society for the Promotion of Science (JSPS) KAKENHI program, Grant Number 24248058. References Ayabe, Y., Kanasashi, T., Hijii, N., Takenaka, C., 2014. Radiocesium contamination of the web spider Nephila clavata (Nephilidae: Arachnida) 1.5 year after the Fukushima Dai-ichi nuclear power plant accident. J. Environ. Radioact. 127, 105e110. €rlocher, F., 1992. Effects of drying and freezing autumn leaves on leaching and Ba colonization by aquatic hyphomycetes. Freshw. Biol. 28, 1e7. Cannel, M.G.R., 1982. World Forest Biomass and Primary Production. Academic Press, London. Endo, I., Ohte, N., Iseda, K., Tanoi, K., Hirose, A., Kobayashi, N.I., Murakami, M., Tokuchi, N., Ohashi, M., 2015. Estimation of radioactive 137-cesium transportation by litterfall, stemflow and throughfall in the forests of Fukushima. J. Environ. Radioact. 149, 176e185.
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Contents lists available at ScienceDirect
Journal of Environmental Radioactivity journal homepage: www.elsevier.com/locate/jenvrad
Short communication
Fallout volume and litter type affect 137Cs concentration difference in litter between forest and stream environments Masaru Sakai a, *, Takashi Gomi b, Junjiro N. Negishi c a
Faculty of Science and Engineering, Chuo University, 1-13-27 Kasuga, Bunkyo-ku, Tokyo, 112-8551, Japan Institute of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo, 183-8509, Japan c Faculty of Environmental Earth Science, Hokkaido University, N10, W5, Kita-ku, Sapporo, Hokkaido, 060-0860, Japan b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 May 2016 Received in revised form 19 July 2016 Accepted 22 July 2016
It is important to understand the changes in the 137Cs concentration in litter through leaching when considering that 137Cs is transferred from basal food resources to animals in forested streams. We found that the difference of 137Cs activity concentration in litter between forest and stream was associated with both litter type and 137Cs fallout volume around Fukushima, Japan. The 137Cs activity concentrations in the litter of evergreen conifers tended to be greater than those in the litter of broad-leaved deciduous trees because of the absence of deciduous leaves during the fallout period in March 2011. Moreover, 137Cs activity concentrations in forest litter were greater with respect to the 137Cs fallout volume. The 137Cs activity concentrations in stream litter were much lower than those in forest litter when those in forest litter were higher. The 137Cs leaching patterns indicated that the differences in 137Cs activity concentration between forest and stream litter could change with changes in both fallout volume and litter type. Because litter is an important basal food resource in the food webs of both forests and streams, the 137Cs concentration gradient reflects to possible 137Cs transfer from lower to higher trophic animals. Our findings will improve our understanding of the spatial heterogeneity and variability of 137Cs concentrations in animals resident to the contaminated landscape. © 2016 Elsevier Ltd. All rights reserved.
Keywords: Basal food resource Forest ecosystem Leaching Radiocesium Stream ecosystem
1. Introduction Cesium-137 fallout due to the Fukushima Daiichi Nuclear Power Plant (FDNPP) accident in March 2011 resulted in extensive contamination of the forest landscape of Fukushima and the surrounding regions (Yasunari et al., 2011; Hashimoto et al., 2012). Approximately 70% of the land area of Japan is covered by forest, and evergreen coniferous plantations and deciduous secondary forests are the most dominant forest types in Japan (Kuroda et al., 2013). In evergreen coniferous forest, a large amount of atmospherically supplied 137Cs was attached to the canopy, including foliated branches, while 137Cs fallout was deposited mostly on the forest floor in deciduous forest because of the absence of leaves in early March (Kato et al., 2012). Cesium-137 contamination deposited on forest ecosystems has further circulated within the ecosystems (e.g., Steiner et al., 2002). Hence, the movement of 137Cs
* Corresponding author. E-mail addresses: [email protected] (M. Sakai), [email protected] (T. Gomi), [email protected] (J.N. Negishi). http://dx.doi.org/10.1016/j.jenvrad.2016.07.030 0265-931X/© 2016 Elsevier Ltd. All rights reserved.
may differ depending on the differences in 137Cs attachment to leaves between evergreen coniferous and broad-leaved deciduous forests (Kato et al., in press). In forest environments, terrestrial and aquatic food webs are often structured by detrital food chains that originate from litter because of the limited light conditions under the canopies (Vannote et al., 1980; Sakai et al., 2016). Therefore, 137Cs transported with litterfall can generate bottom-up 137Cs transfers to higher trophic levels in such forest ecosystems (Sakai et al., 2016). Recent studies demonstrated that the 137Cs concentration in litter is lower in streams than in adjacent forest environments (Sakai et al., 2015). Such differences further reflect the contamination levels of animal communities in the food webs of forests and streams (Sakai et al., 2016). The findings of the previous studies indicated that 137Cs leaching from contaminated litter is the primary process influencing the dynamics of contaminants in stream ecosystems. Cesium-137 transported with litterfall to streams can differ depending on the dominant forest types in riparian zones, because the canopies of evergreen coniferous forests were more contaminated than those of broad-leaved deciduous forests following the FDNPP accident (Kato et al., in press). Such differences in the 137Cs
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concentration between coniferous and deciduous litter may further reflect the leaching patterns in streams, because the leaching pattern may depend on the concentration gradient (Hefter and Tomkins, 2003; Sakai et al., 2016). Changes in the 137Cs concentration in litter due to leaching in streams can be high in evergreen coniferous litter because of the high initial contamination level compared with broad-leaved deciduous litter. In addition to the litter type, the 137Cs concentrations in litter are also associated with the 137Cs fallout volume in forests. The 137Cs fallout was spatially heterogeneous from one watershed to another (Kinoshita et al., 2011). Such distribution patterns are also related to the 137Cs concentration in particulate matter in streams (Yoshimura et al., 2015). Therefore, the different 137Cs concentrations in litter due to variations in fallout volume might lead to differences in the loss of 137Cs once the litter enters stream channels in riparian zones. Thus, we hypothesized that both litter types (evergreen coniferous and broad-leaved deciduous litters) and 137Cs fallout volumes were the primary factors responsible for differences in the 137Cs concentration between forests and streams. This hypothesis was tested by investigating the 137Cs activity concentrations in litter in both forests and streams with different contamination levels. 2. Materials and methods 2.1. Study site and sampling This study was conducted in seven stream reaches, with riparian forest affected by different levels of contamination in Fukushima (six sites) and Gunma (one site) Prefectures (Table 1, Fig. 1). The seven study sites had different amounts of 137Cs fallout, ranging from the lowest with 30e60 kBq/m2 to the highest with 1000e3000 kBq/m2, with all values determined by the governmental airborne monitoring in June 2012 (MEXT, 2012). Detailed methodology of the airborne monitoring can be found at: http:// ramap.jmc.or.jp/map/eng/about.html. We classified the contamination levels into nine categories to enable a statistical analysis (see Section 2.3). Contamination classes 1 to 9 corresponded to the following respective fallout volumes (ranges of volume); 10, 10e30, 30e60, 60e100, 100e300, 300e600, 600e1000, 1000e3000, and >3000 kBq/m2. Site IDs A to G corresponded to a range from high (class 8) to low (class 3) contamination (Table 1). Most of the riparian forests of our study sites were mixed forests, containing evergreen conifers and broad-leaved deciduous trees, with the exception of site B, which was covered only by an evergreen coniferous plantation. The evergreen conifer species was Japanese cedar (Cryptomeria japonica) in all sites, whereas the
dominant deciduous tree species of the sites belonged to several families such as Fagaceae, Ulmaceae, and Sapindaceae. For sampling forest and stream litter, we selected a 50-m channel reach, with a 20 m-wide riparian zone on both sides. Three samples of both evergreen coniferous and broad-leaved deciduous litters were collected randomly from the riparian zone and in-channel region. In the monoculture riparian forest site (site B), we only collected evergreen coniferous litter. Samples of broadleaved deciduous litter comprised a range of families that were dominant within the sites. We selected a similar quality of litter, all with an intact shape and from the early stage of conditioning before starting physical and biological decomposition (Webster and Benfield, 1986; Sakai et al., 2016). All litter sampled from the forest floor was not attached to the mineral soil horizon. Samples in the stream were removed from submerged litter patches on the streambed. When sediment was attached to litter surfaces in streams, we gently rinsed and removed the sedimentary materials. Litter sampling from all sites (except site G) was completed in June 2014. Samples were also collected in May 2013 at sites F and G. Although duration of water soak can affect amount of 137Cs leaching from litter (Sakai et al., 2015), we assumed that the sampling criteria that control decomposition status of the litter samples aligned durations of water soak and enabled us to conduct fair comparisons of the difference in 137Cs concentrations in litter between forest and stream among the study sites. 2.2. Laboratory analysis All litter samples were dried at 60 C for 1 week and then pulverized using an electrical mill (FM-1; Osaka Chemical Co., Ltd., Osaka, Japan) for accurate 137Cs measurements (Sakai et al., 2015). Processed litter samples were packed into 100-mL plastic containers, and their dry weights and densities were measured. The activity concentration of 137Cs in the samples was determined by gamma-ray spectroscopy. Gamma-ray emissions at energies of 661.6 keV were counted using a high-purity germanium coaxial detector system coupled to a multi-channel analyzer (GCW2022 coupled to DSA1000, Canberra, Meriden, CT, USA; Ortec GEM20-70 coupled to DSPEC jr. 2.0, Ametek-AMT, Beijing, PRC). The energy and efficiency calibrations for this detector were performed using standard and blank (background) samples. For the analysis of radionuclide activity, each sample was measured for <10% of the error counts per net area counts. The geometry was held constant when counting all samples for 137Cs activity concentrations. All activities were corrected for decay according to the final sampling date (June 6, 2014) prior to statistical analysis. Our detector systems
Table 1 Location, site identification (ID), latitude, longitude, altitude, distance from the Fukushima Daiichi Nuclear Power Plant (FDNPP), 137Cs fallout volume, contamination class, and forest type at the study sites. The 137Cs fallout volumes at each site are taken from the governmental airborne monitoring data (MEXT, 2012), and the number of each contamination class was assigned with respect to each 137Cs deposition range shown in MEXT (2012). Place (Prefecture)
Site ID
Latitude ( )
Longitude ( )
Altitude (m)
Distance from the FDNPP
137
Cs fallout volume (kBq/ m2)
Contamination class
Forest type
Iitate village (Fukushima)
A
37.63N
140.78E
510
34 km northwest
1000e3000
8
Iitate village (Fukushima) Iitate village (Fukushima)
B C
37.68N 37.64N
140.80E 140.67E
470 630
37 km northwest 43 km northwest
600e1000 600e1000
7 7
Iitate village (Fukushima)
D
37.72N
140.79E
370
44 km northwest
300e600
6
Iitate village (Fukushima)
E
37.74N
140.69E
530
50 km northwest
300e600
6
Nihonmatsu city (Fukushima) Midori city (Gunma)
F
37.60N
140.61E
550
45 km west
100e300
5
G
36.55N
139.35E
620
180 km southwest
30e60
3
coniferous deciduous coniferous coniferous deciduous coniferous deciduous coniferous deciduous coniferous deciduous coniferous deciduous
and
and and and and and
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Fig. 1. Map showing the location of the sample sites used in this study. (a) The location of Fukushima and Gunma Prefectures. (b) 137Cs fallout volume around Fukushima Prefecture. (c) The locations and respective 137Cs fallout volumes of the sample sites in Fukushima Prefecture.
were tested for proficiency according to the test provided by the International Atomic Energy Agency. 2.3. Statistical analysis We developed a simple linear relationship between 137Cs activity concentrations in litter and contamination classes, which was expressed as follows:
ð137 Cs activity concentration in litterÞ ¼ a ðcontamination classÞ þ b; where a and b are constants. This linear model was applied separately for forest and stream coniferous litter and forest and stream deciduous litter. A total of four regression models were developed. The statistical significance for the model constants were set at p ¼ 0.01. The statistical procedure for the regression models was performed using the lm function in R 3.1.2 (R Development Core Team, 2015). 3. Results and discussion The
137
Cs activity concentrations in both evergreen coniferous
and broad-leaved deciduous litter in both forests and streams were higher at the higher contamination classes (Fig. 2). This suggests that the 137Cs activity concentrations of litter in both the forest and stream environment were positively correlated with the amount of 137 Cs fallout regardless of the litter type. Previous studies in Fukushima have also identified a similar relationship between the 137 Cs fallout volume and soils, plants, and animals in forested environments (Kuroda et al., 2013; Hasegawa et al., 2013; Ayabe et al., 2014). Our studies have also confirmed positive relationships between fallout volume and 137Cs activity concentrations in litter, not only in forests, but also in stream environments. However, it should be noted that the horizontal axes in this study (Fig. 2) are categorical and each category has different ranges. Because broad-leaved deciduous trees were defoliated at the time of the FDNPP accident, the amount of 137Cs attached to the canopy layer in broad-leaved deciduous forests tended to be lower than the amount attached in evergreen coniferous forests (Endo et al., 2015; Komatsu et al., 2016; Kato et al., in press). For example, based on a detailed investigation in areas with contamination levels of 300e600 kBq/m2 (class 6 of our category), 70% of the 137Cs fallout was intercepted in the coniferous canopy, while only 23% of 137Cs fallout was intercepted by broad-leaved deciduous forest (Kato et al., in press). Differing amounts of intercepted
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Fig. 2. Regression lines for the 137Cs concentration in litter (upper panel: coniferous needle litter, lower panel: broad-leaved deciduous litter) and 137Cs contamination class. The black plots and line show forest litter, whereas the gray plots and line show stream litter. The bold values for the slopes and intercepts indicate statistical significance (P < 0.01).
137 Cs were also reported by Melin et al. (1994), with 90% interception in coniferous spruce forest, but only 35% in broad-leaved forest. Therefore, though immediately after the FDNPP accident, litter provided from forest floor to stream might be more contaminated in broad-leaved deciduous forest than in evergreen coniferous forest, the 137Cs activity concentrations in evergreen coniferous litter were consistently higher at our sampling periods (two to three years after the accident). Such difference of 137Cs activity concentrations in litter was also reported from 6 months after the FDNPP accident, and the 137Cs activity concentrations in Japanese cedar needle and broad-leaved deciduous litter were 6300 and 270 Bq/kg, respectively, at a site that had received 62 kBq/ m2 fallout (class 4 of our category) (Komatsu et al., 2016). Differences in the 137Cs activity concentration in litter were also associated with differences in the litterfall phenology between the two forest types. Because most of our samples were collected in 2014, the broad-leaved deciduous forests had experienced three foliation-defoliation cycles after the contamination event. Thus, although the translocation of 137Cs from root systems (or other parts of the tree) to the leaves may have occurred (Komatsu et al., 2016), the 137Cs activity concentrations in leaves in broad-leaved stands were consistently low. In evergreen coniferous forest with Japanese cedar, litterfall occurs during the autumn period and is a major process in the transfer of 137Cs from the forest canopy to the
floor (Teramage et al., 2014; Endo et al., 2015). However, a period of approximately 5 years is required to exchange all the needles on a particular tree (Cannel, 1982), which is much longer than that for broad-leaved deciduous trees (1 year). Therefore, broad-leaved deciduous forests supply less contaminated litter to forest and stream channels than do evergreen coniferous forests. We found apparent differences in the 137Cs activity concentration between forest and stream litter (Fig. 2). These differences were consistent for all sites and litter types. The lower 137Cs activity concentration in stream litter than forest litter was associated with 137 Cs leaching in the water column (Fig. 2). Litter in streams was affected by leaching through the abiotic removal of soluble substances preceding microbial colonization and invertebrate feeding (Webster and Benfield, 1986; Gessner et al., 1999). Based on a laboratory experiment, Sakai et al. (2015) demonstrated that the leaching process was important for reducing 137Cs activity concentrations in contaminated litter. In general, leaching from dried €rlocher, leaves tends to be greater than that from wet leaves (Ba 1992), and defoliated leaves are possibly affected more efficiently by leaching processes than are the fresh leaves that replace them. Our findings also revealed that the differences in the 137Cs activity concentration between forest and stream litters became greater in sites with high contamination levels, based on the different values of the slope constant (a) of the regressions (Fig. 2). The greater difference in the 137Cs activity concentration in highly contaminated sites was associated with efficient 137Cs leaching from the litter in streams (Sakai et al., 2016). Sheppard and Evenden (1990) reported that relative rate of radiocesium leaching from decaying litter is consistent among different initial concentrations in the litter, and indicated that the absolute loss of radiocesium is greater in highly contaminated litter. Our results were in accordance with the previous study. Because 137Cs activity concentration in stream water is possibly negligible in all our study sites (Ueda et al., 2013; Iwagami et al., in press), relative difference of 137Cs concentration in between litter and stream water could be largely determined by the concentration in litter. The difference in the 137Cs activity concentration between forest and stream litter was greater in evergreen coniferous litter than in broad-leaved deciduous litter. Because 137Cs leaching can be accelerated more when the 137Cs activity concentration in litter is higher, relatively high 137Cs activity concentration in evergreen coniferous litter compared with broad-leaved deciduous litter induced much more 137Cs detachment from litter by leaching. The results associated with both 137Cs fallout volume and litter type suggest that a spatially heterogeneous distribution of 137Cs in litter can be found in forest and stream ecosystems in the contaminated forest regions. Our result also showed that ratio of the slope constants (forest litter/stream litter) was similar between coniferous and deciduous litters (coniferous: 2.4; deciduous: 2.7). This result suggests that our sampling criteria (see Section 2.1) enable us to collect coniferous and deciduous litters with similar relative rate of 137Cs leaching. However, differences of morphology, persistence and litterfall phenology between the litter types are expected to intricately influence 137Cs leaching patterns in streams. Thus, further tests for examining effects of litter types on 137Cs leaching need to include information on initial 137Cs concentrations in litter and durations of water soak (e.g., Sheppard and Evenden, 1990; Sakai et al., 2015). The difference in the 137Cs activity concentration between forest and stream litter can reflect the contamination levels of animals in forests and streams (Sakai et al., 2016), because litter is the major basal food resource in not only forests, but also in streams covered by forest (Vannote et al., 1980; Gomi et al., 2002). For example, based on a stable isotope analysis, Sakai et al. (2016) reported that
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the dominant basal food resource was litter in the Japanese cedar forest, and their study revealed the importance of the detrital food chains in transferring 137Cs from contaminated litter to higher trophic animals, such as arthropods in both riparian zones and streams, and fish in streams. Consequently, a low 137Cs activity concentration in litter, which is the result of leaching, propagates to relatively low 137Cs activity concentrations in stream animals compared with forest animals with similar trophic levels (Sakai et al., 2016). Therefore, fallout volume and litter type, which affected the relative differences in the 137Cs activity concentration between forest and stream litter, may further reflect the different 137 Cs activity concentrations in animals. 4. Conclusions This study showed that the differences in 137Cs activity concentrations between forest and stream litter tended to be greater with respect to the fallout volume and in evergreen coniferous forest than in broad-leaved deciduous forest. Because the 137Cs loss through leaching was greater when the concentration gradient between litter and stream water was higher, the high concentration gradient in highly contaminated sites and in evergreen coniferous litter induced efficient leaching and lowered the 137Cs activity concentrations in stream litter. Many studies have been conducted to investigate 137Cs activity contamination in animals. Most of these studies have only focused on the contamination of animals and their habitat (e.g., Sakai et al., 2014; Ayabe et al., 2014). However, our findings suggested that the differences in contamination levels, even among neighboring environments in forests and streams, were an important indicator for identifying the variability of 137Cs distributions. Such heterogeneity of 137Cs in the basal food resources of the ecosystems can also be important for developing ecosystem-based models of 137Cs transfer for long-term projections of contaminant movement in ecosystems. Acknowledgements We thank the members of the Watershed Hydrology and Ecosystem Management Laboratory at Tokyo University of Agriculture and Technology and the Watershed Conservation and Management Laboratory at Hokkaido University for sample preparation. Invaluable comment for the improvement of this manuscript was provided by Editor-in-Chief S. C. Sheppard, and the anonymous reviewers. A portion of this study was supported by the Environmental Research Fund (ZD-1202) of the Ministry of the Environment, Japan, and the Japan Society for the Promotion of Science (JSPS) KAKENHI program, Grant Number 24248058. References Ayabe, Y., Kanasashi, T., Hijii, N., Takenaka, C., 2014. Radiocesium contamination of the web spider Nephila clavata (Nephilidae: Arachnida) 1.5 year after the Fukushima Dai-ichi nuclear power plant accident. J. Environ. Radioact. 127, 105e110. €rlocher, F., 1992. Effects of drying and freezing autumn leaves on leaching and Ba colonization by aquatic hyphomycetes. Freshw. Biol. 28, 1e7. Cannel, M.G.R., 1982. World Forest Biomass and Primary Production. Academic Press, London. Endo, I., Ohte, N., Iseda, K., Tanoi, K., Hirose, A., Kobayashi, N.I., Murakami, M., Tokuchi, N., Ohashi, M., 2015. Estimation of radioactive 137-cesium transportation by litterfall, stemflow and throughfall in the forests of Fukushima. J. Environ. Radioact. 149, 176e185.
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