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Stemflow-induced spatial heterogeneity of radiocesium concentrations and stocks in the soil of a broadleaved deciduous forest
Science of the Total Environment 599–600 (2017) 1013–1021
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Stemflow-induced spatial heterogeneity of radiocesium concentrations and stocks in the soil of a broadleaved deciduous forest Naohiro Imamura a,⁎, Delphis F. Levia b,c, Jumpei Toriyama d, Masahiro Kobayashi a, Kazuki Nanko e a
Center for Forest Restoration and Radioecology, Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan Department of Geography, University of Delaware, Newark, DE 19716-2541, USA Departments of Plant and Soil Sciences, University of Delaware, Newark, DE 19716-1303, USA d Kyushu Research Center, Forestry and Forest Products Research Institute, 4-11-16 Kurokami, Chuo-ku, Kumamoto 860-0862, Japan e Department of Disaster Prevention, Meteorology and Hydrology, Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan b c
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Inputs of Fukushima-derived Cs were examined in the soil of a contaminated forest. • Cs concentrations were higher in the soils of the proximal than distal stem area. • Spatiality of Cs stocks is partly governed by preferential flowpaths of stemflow. • Cs soil stocks were higher under trees with larger canopy projection areas. • Soil sampling schema must account for Cs circumferential variation near tree stems.
a r t i c l e
i n f o
Article history: Received 23 January 2017 Received in revised form 13 April 2017 Accepted 2 May 2017 Available online xxxx Editor: D. Barcelo Keywords: Stemflow Konara oak Proximal area Double funneling Forest soils
a b s t r a c t The transport of radiocesium from the canopy and quantification of the spatial distribution of radiocesium in the soil of konara oak forests are important to better understand the variability of 137Cs stocks in the soil between proximal and distal stem areas as well as fine-scale variations around the tree trunk. Moreover, a better understanding of finescale spatial variabilities of 137Cs concentrations and stocks will provide insights for optimizing soil sampling strategies to provide a more robust estimation of contamination at the stand scale. This study aims to elucidate the transport of 137Cs by stemflow in a radioactively contaminated konara oak forest in Tsukuba, Japan by describing and quantifying the fine-scale spatial distribution of 137Cs in the soil and preferential flowpaths of stemflow on the tree stem by a dye tracing experiment. 137Cs concentrations and stocks were higher in the soils of the proximal stem area than distal stem area when they corresponded with the preferential flowpaths of stemflow. There was a significant relationship between canopy projection area of individual trees and average soil 137Cs concentrations and stocks, even though canopies of the trees overlapped. Our results demonstrate that the spatiality of 137Cs concentrations and stocks in the soil of the proximal stem area are governed (at least partially) by the preferential flowpaths of stemflow along the tree trunk. In addition, higher 137Cs concentrations and stocks in the near-trunk soils of trees with larger crown areas might be caused by an enhanced ability to capture dry deposition. © 2017 Elsevier B.V. All rights reserved.
⁎ Corresponding author. E-mail address: [email protected] (N. Imamura).
http://dx.doi.org/10.1016/j.scitotenv.2017.05.017 0048-9697/© 2017 Elsevier B.V. All rights reserved.
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1. Introduction
2. Materials and methods
The Fukushima Dai-ichi Nuclear Power Plant (FDNPP) accident released large quantities of radioactive substances into the surrounding environment. Cesium (Cs) levels of 134Cs and 137Cs, for instance, exceeded 1,000,000 Bq m−2 in areas close to the FDNPP which subsequently spread to cover a forest area of 428 km2, thereby representing roughly twothirds of the Fukushima prefecture (Hashimoto et al., 2012). Within the first year of the accident, radiocesium was primarily trapped by the forest canopy, the litter layer, and the surface mineral soil layer (Komatsu et al., 2016). Five years after the accident, the levels of radiocesium in the forest canopy and litter layer were decreasing from dilution via rainfall and defoliation, leading to an accumulation of radiocesium in the surface mineral soil layer (0–5 cm) of the forest (Imamura et al., preparation). There remains, however, much to learn about the cycling of radiocesium in forest, especially with respect to its redistribution by stemflow in localized areas around individual tree trunks. Previous studies have documented that radiocesium is intercepted by the forest canopy and transported to the soil by throughfall and stemflow (Bunzl et al., 1989a; Bonnett and Anderson, 1993; Pröhl et al., 2006; Kato et al., 2012; Endo et al., 2015; Kato et al., 2017) and litterfall (Bonnett and Anderson, 1993; Teramage et al., 2014; Endo et al., 2015; Kato et al., 2017). Compared to stemflow, large proportions of the annual radiocesium flux was found in throughfall and litterfall (Rafferty et al., 2000; Kato et al., 2012; Teramage et al., 2014). Kato et al. (2017) reported that contribution of throughfall, stemflow, and litterfall to the total flux was 31.3%, 4.7%, and 64.0%, respectively, in a deciduous mixed forest in Fukushima prefecture, although the actual input via stemflow calculated per unit basal area would be much higher. Even though the total annual flux of 137Cs by stemflow is relatively low, it is likely of importance to the spatiality of 137Cs in the forest soils for some tree species because stemflow is subject to preferential flow in the rhizosphere (Johnson and Lehmann, 2006). Förster and Schimmack (1992) concluded that the horizontal and vertical distribution of 137Cs in the soil of a beech stand was caused by the non-uniform nature of stemflow inputs. In addition, Takenaka et al. (1998) reported that the variable concentrations of 137Cs in the surface soil around a red pine tree was attributable to the transport pathway of 137Cs from the canopy to the soil and/or the uptake of 137Cs by the trees. These effects of stemflow on the spatial variation in 137Cs concentration in the surface soil may depend on the presence of preferential flow and its volume. While the studies cited above have increased our understanding of radiocesium cycling in forests, our specific focus is somewhat different. Prior work has considered the tree trunk as a whole and examined horizontal and vertical differences in 137Cs concentrations (Förster and Schimmack, 1992). We aim to expand this research by explicitly linking stemflow of konara oak (Quercus serrata Murray), a prevalent species in the deciduous forests in the Fukushima Prefecture, to the fine-scale circumferential spatial variabilities of radiocesium concentrations and stocks in the surface soil around specific trees. Konara oak stand produces relatively high stemflow volumes (Shoga et al., 1993). Therefore, it is probable that the observation and quantification of preferential flow of stemflow would aid in the prediction of the spatial distribution of 137Cs concentrations in the soil in the proximal area around konara oak trees. This is the first known study to specifically examine fine-scale circumferential differences in 137Cs concentrations and stocks in the soil of the proximal area of individual trees. Accordingly, this study aims to elucidate: (1) the radiocesium transport process by stemflow in a konara oak forest; and (2) describe and quantify the finescale spatial distribution of 137Cs in the soil in the proximal area of the stem of konara oak trees. A detailed examination of fine-scale spatial heterogeneities of 137Cs concentrations and stocks in the surface soils of the proximal areas of konara oak trees is of critical importance for the optimization of soil sampling strategies and the consequent robust estimations of soil contamination at stand scale in forests subjected to radioactive fallout.
2.1. Study site The study site was established in a konara oak dominated experimental forest at the Forestry and Forest Products Research Institute (FFPRI), Tsukuba city in Japan, which is located 170 km southwest of FDNPP (36°00′32″N, 140°07′36″E, Fig. 1). The mean 5-year annual air temperature and precipitation between 2011 and 2015 was 14.4 °C and 1280 mm, respectively, as measured at a meteorological station at FFPRI (Fig. 2). Wind speed and wind direction also were observed at meteorological station. The total deposition of 137Cs and 134Cs was 40,000 Bq m−2 as of May 31, 2012 (Extension Site of Distribution Map of Radiation Dose, etc.,/GSI Maps). In Tsukuba, a high concentration plume (N10 Bq m−3) was observed between March 14 and 15, 2011 under clear sky conditions and between March 20 and 22, 2011 under rainy conditions as observed from aerosol samples on quartz fiber filters (Adachi et al., 2013). The first rainfall event (28.0 mm and 0.64 mm h−1) after the nuclear accident occurred between March 21, 8:00 and March 23, 3:00, 2011 at FFPRI. The konara oak forest studied was 37 years old (as of 2015) with stand density of 1700 trees ha−1 (Migita et al., 2007), mean tree height of 19.1 m, and a mean diameter at breast height (dbh) of 22.4 cm. The forest is situated on level terrain over an andisol formed on a loamy soil layer. The thickness of the organic layer (Oi, Oe, and Oa), composed of thinning and decaying leaves, was approximately 2 cm in the summer. Summer soil moisture content was approximately 4%. 2.2. Stemflow dye experiment To determine the spatiality of stemflow into the forest soil, a stemflow dye experiment was performed in mid March of 2016, which was the same season as the FDNPP accident and first rainfall event after the accident. All trees were defoliated. The morphological
Fig. 1. Location of study site with respect to the Fukushima Dai-ichi Nuclear Power Plant. The deposition densities of total 137Cs and 134Cs (Bq m−2) on May 31, 2012 are based on aircraft monitoring (Extension Site of Distribution Map of Radiation Dose, etc.,/GSI Maps).
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Fig. 3. Canopy projection areas and location of the five konara oak trees studied within the experimental plot.
Fig. 2. Mean monthly temperature and rainfall amounts observed at FFPRI. Mean monthly air temperature from January 2011 to December 2015 (top) and the 5-year average monthly rainfall (solid grey bars) with standard errors bars from 2011 to 2015 (bottom).
characteristics of the five sample trees are shown in Table 1. The dbh of the sample trees ranged from 17.7–35.1 cm (Table 1). The trunk lean of tree E was about 20° from north to south, while other trees exhibited very little to no trunk lean. The canopy projection areas of each tree (Fig. 3) were calculated using the branch length in eight azimuthal directions. The canopy projection area was the largest for tree D (48 m2) and the smallest for tree C (5.5 m2). Water containing Brilliant Blue FCF colored dye was sprayed on five individual tree stems (trees A, B, C, D, and E) in the rainfall event on March 22, 2016. The dye was sprayed uniformly in a wide band along the whole circumference of the tree stem. Thus, stemflow flowpaths were identified as those areas where the dye was removed as stemflow was channelized down the tree stem (Fig. 4); the areas that remained covered with dye did not experience stemflow. To confirm the repeatability of stemflow patterning on the stem, an additional exploratory stemflow dye experiment was performed on September 13, 2016. The two sampled events differed with respect to rainfall intensity and are broadly representative of rain events in the area. Moreover, since stemflow channelization is largely controlled by canopy structure in these forests, we are confident that we can provide useful insights into the spatial variation of radiocesium in these forest surface soils. The direction and extent of stemflow dispersion on each stem was estimated using a tape measure. Discrimination between the area of the tree trunks that were and were not conducting stemflow was obvious from the presence or absence of the dye on the tree stems.
trunk areas (n = 8, i.e., proximal stem area) and the surrounding area (n = 16, i.e., distal stem area) (Fig. 5). The radiocesium concentration of all soil samples were decay-corrected to July 1, 2015 to standardize soil sample collection. Given the low levels of 137Cs in the organic layer at the time of this study (Fig. A1, Table A1, please see the web link in Appendix A for Supplementary Data), it was removed before coring for soil samples. After removal of the organic layer, one soil sample was collected in the center of each square (as depicted in Fig. 5) using a 475-mL cylinder (95 cm2 cross-sectional area × 5 cm depth). We assumed that the core sample (per 95 cm2) within each grid square was representative of the grid square (per 625 cm2) as a whole.
2.3. Soil sampling The soil sampling plot was established as a 125 × 125-cm quadrat around the center of each tree stem (Fig. 5). Chang and Matzner (2000) defined the ‘proximal stem area’ as 1 m2 (56.4 cm distance from center of stem) around the tree trunks, and ‘distal stem area’ as further away. In this study, the 24-cell grid was divided into adjacent
Table 1 Tree height, height of the lowest live branch (HB), diameter at breast height (dbh @ 1.37 m), and canopy projection area of the study trees. Tree
A
B
C
D
E
Tree height (m) HB (m) dbh (cm) Canopy projection area (m2)
22.5 9.1 28.5 15.1
25.0 6.0 29.1 23.1
15.9 7.8 17.7 5.5
25.8 10.6 35.1 48.0
23.1 6.9 21.0 8.9
Fig. 4. Brilliant blue dye on the stem of a konara oak tree. Dye was uniformly applied around the circumference of the whole tree in the rainfall event. The preferential flowpaths of stemflow, as it is channeled down the trunk, are depicted as the areas where there is an absence of dye as it was washed off by stemflow. Thus, these areas void of dye, where the tree trunk intersects with the forest floor, represent the locations where stemflow is input into the forest soil. The marked spatial heterogeneity of stemflow inputs in the proximal area is readily apparent.
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Fig. 5. Soil sampling area (n = 24). “P” denotes the proximal stem area (n = 8) and “D” denotes the distal stem area (n = 16).
2.4. Chemical analysis and calculations of radiocesium soil stocks The soil samples were air-dried and then oven-dried for 24 h at 105 °C. The concentration of 137Cs for all samples was determined using HPGe coaxial and P-type reverse detector systems (GEM20-70, GEM40P4-76, GEM-FX7025P4-ST, and GWL-120-15-LB-AWT, ORTEC, Oak Ridge, USA). The measurement times were 1800–4000 s, which normally obtain 137Cs concentration values with relative errors b 10%. The radiocesium stock (Bq m−2) of 137Cs for all samples was calculated by multiplying the radiocecium concentration per dry mass (Bq kg−1) by the dry mass per unit area (kg m−2).
Fig. 6. Locations around the tree trunk where stemflow was input to the forest soil (blue line) or void of stemflow (black line) during the rainfall events on March 22 and September 13, 2016. Please note the spatial heterogeneity of the stemflow inputs to the forest soils as well as the similarities for a given tree between the two rainfall events. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
3.2. 137Cs concentrations and stocks in the surface soil 2.5. Statistical analysis To determine the spatial variation of radiocesium inputs to the forest soil via stemflow, we compared 137Cs concentration in both the soils of the proximal stem (n = 8) and distal stem areas (n = 16) using the Wilcoxon rank sum test. Since stemflow often infiltrates the soil in a non-uniform manner as a result of preferential flowpaths (Johnson and Lehmann, 2006; Levia and Germer, 2015), we compared the 137Cs concentrations and stocks in the proximal stem area between stemflow-influenced and non-influenced points, as determined from the results of the dye experiment. The soil 137Cs concentration of stemflow and no stemflow input points were also compared using Wilcoxon rank sum test. Furthermore, to explain the distribution of radiocesium by the effect of tree size, we examined the relationship between canopy projection area and the average soil concentration and stock. 3. Results
The 137Cs concentrations in the soil of the proximal stem area (n = 8) were higher than those of the distal stem areas (n = 16) for all trees (Table 2). Median 137Cs concentrations were 20–135% larger in the proximal stem area than in distal stem area for the five trees. These differences were statistically significant for trees A, B, and D (Wilcoxon rank sum test; p b 0.05). In addition, the median 137Cs stock was 24–136% larger in the proximal stem area than distal stem area for the five trees. The average concentration of 137Cs in the soil (n = 24) for both the proximal and distal stem areas was different for each tree (Table 2), being the highest for tree D (2910 ± 1540 Bq kg−1) and the lowest for tree C (1240 ± 955 Bq kg−1). The average concentration of 137Cs was 134% higher for tree D than tree C. 137 Cs concentrations in the soils around the tree trunk exhibited a wide variability, ranging from 514 to 5520 Bq kg− 1 for tree A, 633–6965 Bq kg− 1 for tree B, 505–5323 Bq kg− 1 for tree C, 1200–5988 Bq kg−1 for tree D, and 386–6448 Bq kg−1 for tree E, respectively. In the proximal stem area, the distribution of 137Cs concentrations in the soil was different for each tree (Fig. 7). The coefficient of variation (CV) of 137Cs concentrations in the soil within the proximal
3.1. Stemflow dye experiment The first dye experiment was performed in a rainfall event with the following characteristics: rain intensity of 1.75 mm h−1, mean wind direction from the north-northeast, and mean wind speed of 3.3 m s−1. The second dye experiment was performed in a rainfall event with a rain intensity of 7.7 mm h−1, mean wind direction from the northeast, and mean wind speed of 1.9 m s−1. The spatial patterning of stemflow inputs to the soils was different for each tree (Fig. 6), although it was quite similar for both stemflow dye experiments, despite the fact that the wind and rainfall conditions were different. This underscores the fact that canopy structural characteristics exerted a strong control on stemflow channelization along the trunks of these particular trees.
Table 2 Mean (±1SD) 137Cs concentrations (Bq kg−1) in the soil of the proximal stem area of the tree trunk (n = 8), distal stem area (n = 16), and average concentration for both areas (n = 24). Median values are shown in parentheses. Tree Proximal stem area Distal stem area Average stem area
A
B
C
D
E
2,460 ± 1,710
3,490 ± 2,130
1,730 ± 1,500
4,340 ± 1,690
1,690 ± 1,960
(1,660)
(3,020)
(1,090)
(4,580)
(1,180)
1,240 ± 545
1,280 ± 387
995 ± 403
2,190 ± 798
1,030 ± 551
(1,080)
(1,360)
(912)
(1,950)
(882)
1,650 ± 1,200
2,020 ± 1,620
1,240 ± 955
2,910 ± 1,540
1,250 ± 1,210
(1,270) (1,530) (955) (2,300) (1,050) Bold values denote significance at the 0.01 level. Grey values denote significance at the 0.05 level.
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Fig. 7. The spatial distribution of 137Cs concentrations (Bq kg−1) in the surface soil in relation to the locations around the tree trunk where stemflow is input to the soil (blue line). The black line depicts area around the tree trunk that did not receive any stemflow inputs. The light grey area depicts the stem area at the surface soil. The darker grey area shows the stem area approximately 40 cm above the ground. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
stem area ranged from 0.39–1.16, and the CV was largest for tree E. The distribution of 137Cs stocks in the soil was similar to that of 137Cs concentrations in the soil (Figs. 7 and 8). The CV of 137Cs stocks in the soil within the proximal stem area ranged from 0.36–1.22. The 137Cs concentrations and stocks in the soil were higher for areas which received stemflow (Figs. 7 and 8) than those that did not, with these differences being statistically significant (Wilcoxon rank sum test; p b 0.001; Fig. 9). From the relationship between canopy projection area and average soil concentration, a significant positive correlation was found between average 137Cs concentration in the soil and canopy projection area (p b 0.01; Fig. 10). A similarly significant relationship was also found between 137Cs stock in the soil and canopy projection area (p b 0.01). 4. Concluding discussion 4.1. 137Cs concentrations and stocks in the soils of proximal and distal stem areas Our result that the concentrations and stocks of 137Cs in the soil was highest in the proximal stem area is consistent with previous work of others (e.g., Bunzl et al., 1989b; Förster and Schimmack, 1992; Table 3). Bunzl et al. (1989b) reported that 137Cs stock was 12% higher for spruce at a distance of 0–0.5 m than 3 m from the tree trunk. Likewise, Förster and Schimmack (1992) also observed that 137Cs stocks in the soil under beech trees were 130–831% higher in the area adjacent to the tree than 4 m from the stem. Similar to 137Cs, concentrations and stocks of NO3\\N in the soils near the tree trunk were N40% higher than those further away from the stem for bigleaf maple (Hamdan and Schmidt, 2012). Chang and Matzner (2000) reported 162% higher concentrations of K+ in soils near the trunk in European beech stands. These results indicate that the concentrations and stocks of elements
in the soil are higher near the tree trunk, especially for deciduous forests. These phenomena could, as suggested by numerous others, be affected by the occurrence of stemflow (Förster and Schimmack, 1992; Chang and Matzner, 2000; Hamdan and Schmidt, 2012; Fantozzi et al., 2013). Our results build upon previous studies by demonstrating the marked fine-scale circumferential spatial variation of 137Cs concentrations and stocks in the soils of the proximal area (as detailed in the next section). 4.2. Preferential flowpaths of stemflow: a control on soil 137Cs concentrations and stocks within proximal stem area Johnson and Lehmann (2006) explained the double-funneling of nutrient fluxes by trees, whereby the spatial and vertical distributions of nutrients are concentrated both above- and belowground by stemflow. In support of the double-funneling concept of Johnson and Lehmann (2006), we opined that the stocks of 137Cs in the soil would be higher for areas connected to the tree trunk via the preferential flowpaths of stemflow than the other locations within the proximal stem area. Our experimental observations substantiated this claim. In fact, the preferential flowpaths of stemflow, as identified by the areas where the previously applied dye tracer was removed by stemflow (Fig. 4), corresponded to the precise areas where stemflow transported radiocesium from the canopy to the soil. This shows that the aboveground funneling of stemflow along preferential flowpaths is a key control affecting the variable circumferential spatial patterning of 137Cs into the soil around tree trunks. However, since we did not examine the funneling of cesium along the roots in the subsurface, we cannot confirm whether 137Cs is also funneled belowground in accord with the double-funneling concept. Because prior work has found that radiocesium concentrations were not decreasing over the observation
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Fig. 8. The spatial distribution of 137Cs stocks (Bq m−2) in the surface soil in relation to the locations around the tree trunk where stemflow is input to the soil (blue line). The black line depicts area around the tree trunk that did not receive any stemflow inputs. The light grey area depicts the stem area at the surface soil. The darker grey area shows the stem area approximately 40 cm above the ground. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
period (Endo et al., 2015; Sasaki et al., 2016; Kato et al., 2017), it gives further credence to our argument that the higher concentrations of radiocesium in the proximal stem area could be the result of stemflow-supplied 137Cs. Because our site is in the forest interior on level ground, it is most likely that the fine-scale circumferential variations in 137Cs concentrations and stocks were the result of preferential inputs via stemflow. However, it is worth noting that the spatial variation of 137Cs in the soil could be attributed to phenomena and factors other than stemflow, such as a tree's location to the forest edge and topography (Ould-Dada et al., 2002; Atarashi-Andoh et al., 2015), litterfall leachate inputs
(Koarashi et al., 2016), and the horizontal and vertical migration of radiocesium (Förster and Schimmack, 1992). At our site, there was no clear pattern in the distribution of 137Cs concentrations in the organic layer (Fig. A1, Table A1, please see the web link in Appendix A for Supplementary Data). It is possible that the geometric orientation of the tree stem might influence the concentrations and stocks of 137Cs in the soil of proximal area since the orientation of tree trunks has been documented to influence stemflow volume (Levia et al., 2015). Similarly, we identified a preferential flowpath on the underside of trunk for tree E, which has a trunk lean of 20°, that resulted in a high 137Cs concentration and stock
Fig. 9. A box-and-whisker plot of 137Cs concentrations and stocks in the surface soils with and without stemflow inputs. The median values are denoted by horizontal bold lines within the boxes, while the upper and lower quartiles are represented by the boundaries of the boxes. The maximum and minimum values are denoted by the whiskers. Outliers are denoted by a circle. Stemflow input was defined by the area of color dye (blue line) when it was larger than the area of no color dye (black line) in each stem area (separated in eight azimuth directions) (grey area) in Figs. 7 and 8.
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Fig. 10. The relationship between the canopy projection area of the experimental trees and the average 137Cs concentration in the soil (n = 24) for both the proximal and distal stem areas.
in the soil along this side of the tree, which also accounted for the largest variation of 137Cs concentrations within the proximal stem area (Figs. 7 and 8). Although the variations of 137Cs concentrations in the soil within proximal stem areas of the other four trees were lower than that of tree E, we still witnessed the presence of preferential flowpaths on the stems of these trees (despite minimal trunk lean) which corresponded with the high concentrations and stocks of 137Cs in the soils of the proximal areas (Figs. 7 and 8). These preferential flows (trees A, B, C, and D) could be affected by the presence of flow path obstructions (Crockford and Richardson, 2000) and bark morphology (Levia and Herwitz, 2005). This is because bark morphology is a key control on both the generation and volume of stemflow as well as its channelization on the tree stem (Levia and Herwitz, 2005). Our findings indicate that the spatiality of 137Cs concentrations and stocks in the soils near konara oak trees is heterogeneous and that the preferential flowpaths on tree trunks is one cause of the larger 137Cs inputs in the proximal stem areas as compared to the distal stem areas. 4.3. Relationship between tree size and soil 137Cs concentration and stock To explain differences in soil 137Cs concentrations and stocks between individual trees, the effect of tree size is an important consideration. André et al. (2008) reported that the product of trunk circumference and tree height explained the inter-individual variability in stemflow chemistry. Hofhansl et al. (2012) found that dbh, tree height, and plant area index influenced stemflow chemistry in a tropical rainforest. Similarly, we found that the concentration of 137Cs in the soil (134%) was larger for the largest tree (tree D) than the tree with the smallest canopy projection area (tree C). Therefore, a significant positive correlation between average 137Cs concentration in the soil and canopy projection area (Fig. 10) could be found by the difference of tree size in this oak forest. In addition, stemflow yield was affected by tree height, basal diameter, and canopy projection area (Ford and Deans, 1978; Martinez-Meza and Whitford, 1996; Crockford and Richardson, 2000; Garcia-Estringana et al., 2010; Levia et al., 2015). As such, differential stemflow yield likely affects the relationship between average 137Cs stock in the soil.
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It must be noted that the canopies of the konara oak trees were defoliated in May 2011, soon after the FDNPP accident. Previous studies have reported that leafless canopies can capture notable quantities of dry deposition (e.g., Beckett et al., 2000; Freer-Smith et al., 2004). Therefore, it is probable that the leafless crowns of the large konara oak trees was able to effectively scavenge the dry deposition of 137Cs by the first plume after the accident onto its branches and stem surfaces. This suggests that these phenomena could lead to the significant relationship between canopy projection area and average soil concentration of 137 Cs (Figs. 3 and 10). We developed a conceptual model to describe the linkages between tree morphology, stemflow yield, and radiocesium in the soil (Fig. 11). Of course, meteorological conditions also will influence stemflow amounts (Levia and Frost, 2003), but the point of this conceptual model is to highlight the interrelationships among tree morphology, stemflow production, and consequent transport of 137Cs from the tree crown to the forest soil. The model underscores the interactions among tree trunk orientation, tree size, and bark morphology with the formation of preferential channelization along the tree trunk and the consequent spatial localization of 137Cs in the forest soil within the proximal area of tree trunks. As reported by studies already cited (e.g., Levia and Herwitz, 2005; André et al., 2008; Levia and Germer, 2015; Levia et al., 2015), the generation and volume of stemflow is affected by interactions among a host of biotic and abiotic factors that lead to differences in stemflow generation and production that ultimately result in the spatial heterogeneities of radiocesium in the proximal stem area. Our results have showed that stemflow has a detectable and important influence on 137Cs stocks in the surface soil. Our results also have demonstrated that 137Cs concentrations and stocks in the soil were higher in the proximal stem area than distal stem area because of stemflow generated by konara oak trees. Based on data from Kato et al. (2017), which showed that 4.7% of the total deposit was transferred to the soil via stemflow, this would correspond to approximately 1800 Bq m−2 over the 40,000 Bq m−2 in the present study, equating to about 36,000 Bq m−2 in the proximal areas of the tree stem (based on assumption that these areas constitute 1/20 of the total area), or about 30% of the enrichment. Thus, expressed per unit proximal area, stemflow inputs are substantial. Recognition of this fact and the finescale circumferential spatial variations of radiocesium inputs into forest soils via stemflow is of critical importance in the development and optimization of soil sampling schema that must provide a more robust estimation of contamination at the stand scale. One simply cannot assume homogeneity of 137Cs surface soil stocks across a forest stand. The heterogeneous nature of proximal area soils must be taken into account. Acknowledgments We thank Dr. Akio Akama for assistance with the field observations. Furthermore, we thank Dr. Ryuichi Tabuchi, Ms. Shukushin Endo, Dr. Koichi Yamamoto, and Dr. Mitsutoshi Tsunoda for their valuable assistance with analyzing concentrations of cesium in the soil. This work was supported by JSPS KAKENHI [grant number JP15H04522] as well as by a JSPS invitation fellowship [grant number: S16088] to both Kazuki Nanko and Delphis Levia.
Table 3 \N in the proximal and distal stem areas as reported in previous studies. Soil concentrations and stocks of 137Cs, K+, and NO3\ Forest type
Element
Depth
Proximal stem area
Distal stem area
Increase ratio
References
Norway spruce European beech European beech Bigleaf maple
Cs (Bq m−2) 137 Cs (Bq dm−2) K+ (mg l−1) \N (mg kg−1) NO3\ \N (kg ha−1) NO3\ 137 Cs (Bq kg−1) 137 Cs (Bq m−2)
0–47 (cm) 0–60 (cm) 40 (cm) Surface Surface 0–5 (cm) 0–5 (cm)
3290 ± 390 600–2700 4.64 70.89 0.43 1690 ± 2010 34,490 ± 36,520
2930 ± 240 260–290 1.77 45.60 0.30 1220 ± 700 23,640 ± 11,600
12% 130–831% 162% 55% 43% 20–135% 24–136%
Bunzl et al. (1989b) Förster and Schimmack (1992) Chang and Matzner (2000) Hamdan and Schmidt (2012)
Konara oak
137
This study
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Fig. 11. A conceptual model of the linkages among tree trunk orientation, tree size, and bark morphology with the formation of preferential channelization of stemflow along the tree trunk and the consequent spatial localization of 137Cs in the forest soil within the proximal area of konara oak tree trunks.
Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2017.05.017. Readers interested in raw concentration data may contact the corresponding author. References Adachi, K., Kajino, M., Zaizen, Y., Igarashi, Y., 2013. Emission of spherical cesium-bearing particles from an early stage of the Fukushima nuclear accident. Sci. Rep. 3:2554. http://dx.doi.org/10.1038/srep02554. André, F., Jonard, M., Ponette, Q., 2008. Spatial and temporal patterns of throughfall chemistry within a temperate mixed oak-beech stand. Sci. Total Environ. 397:215–228. http://dx.doi.org/10.1016/j.scitotenv.2008.02.043. Atarashi-Andoh, M., Koarashi, J., Takeuchi, E., Tsuduki, K., Nishimura, S., Matsunaga, T., 2015. Catchment-scale distribution of radiocesium air dose rate in a mountainous deciduous forest and its relation to topography. J. Environ. Radioact. 147:1–7. http://dx. doi.org/10.1016/j.jenvrad.2015.05.004. Beckett, K.P., Freer-Smith, P.H., Taylor, G., 2000. Particulate pollution capture by urban trees: effect of species and windspeed. Glob. Chang. Biol. 6:995–1003. http://dx.doi. org/10.1046/j.1365-2486.2000.00376.x. Bonnett, P.J.P., Anderson, M.A., 1993. Radiocaesium dynamics in a coniferous forest canopy: a mid-Wales case study. Sci. Total Environ. 136:259–277. http://dx.doi.org/10. 1016/0048-9697(93)90314-V. Bunzl, K., Schimmack, W., Kreutzer, K., Schierl, R., 1989a. Interception and retention of Chernobyl-derived 134Cs, 137Cs and 106Ru in a spruce stand. Sci. Total Environ. 78: 77–87. http://dx.doi.org/10.1016/0048-9697(89)90023-5. Bunzl, K., Schimmack, W., Kreutzer, K., Schierl, R., 1989b. The migration of fallout 134Cs, 137 Cs and 106Ru from Chernobyl and of 137Cs from weapons testing in a forest soil. J. Plant Nutr. Soil Sci. 152:39–44. http://dx.doi.org/10.1002/jpln.19891520108. Chang, S.-C., Matzner, E., 2000. The effect of beech stemflow on spatial patterns of soil solution chemistry and seepage fluxes in a mixed beech/oak stand. Hydrol. Process. 14: 135–144. http://dx.doi.org/10.1002/(SICI)1099-1085(200001)14:1b135::AIDHYP915N3.0.CO;2-R. Crockford, R.H., Richardson, D.P., 2000. Partitioning of rainfall into throughfall, stemflow and interception: effect of forest type, ground cover and climate. Hydrol. Process. 14:2903–2920. http://dx.doi.org/10.1002/1099-1085(200011/12)14:16/17b2903:: AID-HYP126N3.0.CO;2-6. 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: 176–185. http://dx.doi.org/10.1016/j.jenvrad.2015.07.027. Extension Site of Distribution Map of Radiation Dose, d. etc.,/GSI Maps. (Accessed 16.09.30). http://ramap.jmc.or.jp/map/eng/. Fantozzi, F., Monaci, F., Blanusa, T., Bargagli, R., 2013. Holm Oak (Quercus ilex L.) canopy as interceptor of airborne trace elements and their accumulation in the litter and topsoil. Environ. Pollut. 183:89–95. http://dx.doi.org/10.1016/j.envpol.2012.11.037. Ford, E.D., Deans, J.D., 1978. The effects of canopy structure on stemflow, throughfall and interception loss in a young Sitka spruce plantation. J. Appl. Ecol. 15:905–917. http:// dx.doi.org/10.2307/2402786. Förster, H., Schimmack, W., 1992. Influence of the stemflow on the depth distribution of radiocesium in the soil under a beech stand. Naturwissenschaften 79:23–24. http:// dx.doi.org/10.1007/BF01132274. Freer-Smith, P.H., El-Khatib, A.A., Taylor, G., 2004. Capture of particulate pollution by trees: a comparison of species typical of semi-arid areas (Ficus nitida and Eucalyptus
globulus) with European and North American species. Water Air Soil Pollut. 155: 173–187. http://dx.doi.org/10.1023/B:WATE.0000026521.99552.fd. Garcia-Estringana, P., Alonso-Blázquez, N., Alegre, J., 2010. Water storage capacity, stemflow and water funneling in Mediterranean shrubs. J. Hydrol. 389:363–372. http://dx.doi.org/10.1016/j.jhydrol.2010.06.017. Hamdan, K., Schmidt, M., 2012. The influence of bigleaf maple on chemical properties of throughfall, stemflow, and forest floor in coniferous forest in the Pacific Northwest. Can. J. For. Res. 42:868–878. http://dx.doi.org/10.1139/x2012-042. Hashimoto, S., Ugawa, S., Nanko, K., Shichi, K., 2012. The total amounts of radioactively contaminated materials in forests in Fukushima, Japan. Sci. Rep. 2:416. http://dx. doi.org/10.1038/srep00416. Hofhansl, F., Wanek, W., Drage, S., Huber, W., Weissenhofer, A., Richter, A., 2012. Controls of hydrochemical fluxes via stemflow in tropical lowland rainforests: effects of meteorology and vegetation characteristics. J. Hydrol. 452−453:247–258. http://dx.doi. org/10.1016/j.jhydrol.2012.05.057. Johnson, M.S., Lehmann, J., 2006. Double-funneling of trees: stemflow and root-induced preferential flow. Écoscience 13:324–333. http://dx.doi.org/10.2980/i1195-6860-133-324.1. Kato, H., Onda, Y., Gomi, T., 2012. Interception of the Fukushima reactor accident-derived 137 Cs, 134Cs and 131I by coniferous forest canopies. Geophys. Res. Lett. 39, L20403. http://dx.doi.org/10.1029/2012GL052928. Kato, H., Onda, Y., Hisadome, K., Loffredo, N., Kawamori, A., 2017. Temporal changes in radiocesium deposition in various forest stands following the Fukushima Dai-ichi Nuclear Power Plant accident. J. Environ. Radioact. 166:449–457. http://dx.doi.org/10. 1016/j.jenvrad.2015.04.016. Koarashi, J., Nishimura, S., Nakanishi, T., Atarashi-Andoh, M., Takeuchi, E., Muto, K., 2016. Post-deposition early-phase migration and retention behavior of radiocesium in a litter–mineral soil system in a Japanese deciduous forest affected by the Fukushima nuclear accident. Chemosphere 165:335–341. http://dx.doi.org/10.1016/j. chemosphere.2016.09.043. Komatsu, M., Kaneko, S., Ohashi, S., Kuroda, K., Sano, T., Ikeda, S., Saito, S., Kiyono, Y., Tonosaki, M., Miura, S., Akama, A., Kajimoto, T., Takahashi, M., 2016. Characteristics of initial deposition and behavior of radiocesium in forest ecosystems of different locations and species affected by the Fukushima Daiichi Nuclear Power Plant accident. J. Environ. Radioact. 161:2–10. http://dx.doi.org/10.1016/j. jenvrad.2015.09.016. Levia, D.F., Frost, E.E., 2003. A review and evaluation of stemflow literature in the hydrologic and biogeochemical cycles of forested and agricultural ecosystems. J. Hydrol. 274:1–29. http://dx.doi.org/10.1016/S0022-1694(02)00399-2. Levia, D.F., Germer, S., 2015. A review of stemflow generation dynamics and stemflowenvironment interactions in forests and shrublands. Rev. Geophys. 53:673–714. http://dx.doi.org/10.1002/2015RG000479. Levia, D.F., Herwitz, S.R., 2005. Interspecific variation of bark water storage capacity of three deciduous tree species in relation to stemflow yield and solute flux to forest soils. Catena 64:117–137. http://dx.doi.org/10.1016/j.catena.2005.08.001. Levia, D.F., Michalzik, B., Näthe, K., Bischoff, S., Richter, S., Legates, D.R., 2015. Differential stemflow yield from European beech saplings: the role of individual canopy structure metrics. Hydrol. Process. 29:43–51. http://dx.doi.org/10.1002/hyp.10124. Martinez-Meza, E., Whitford, W.G., 1996. Stemflow, throughfall and channelization of stemflow by roots in three Chihuahuan desert shrubs. J. Arid Environ. 32:271–287. http://dx.doi.org/10.1006/jare.1996.0023. Migita, C., Chiba, Y., Tange, T., 2007. Seasonal and spatial variations in leaf nitrogen content and resorption in a Quercus serrata canopy. Tree Physiol. 27:63–70. http://dx. doi.org/10.1093/treephys/27.1.63. Ould-Dada, Z., Copplestone, D., Toal, M., Shaw, G., 2002. Effect of forest edges on deposition of radioactive aerosols. Atmos. Environ. 36:5595–5606. http://dx.doi.org/10. 1016/S1352-2310(02)00699-4.
N. Imamura et al. / Science of the Total Environment 599–600 (2017) 1013–1021 Pröhl, G., Ehlken, S., Fiedler, I., Kirchner, G., Klemt, E., Zibold, G., 2006. Ecological half-lives of 90Sr and 137Cs in terrestrial and aquatic ecosystems. J. Environ. Radioact. 91:41–72. http://dx.doi.org/10.1016/j.jenvrad.2006.08.004. Rafferty, B., Brennan, M., Dawson, D., Dowding, D., 2000. Mechanisms of 137Cs migration in coniferous forest soils. J. Environ. Radioact. 48:131–143. http://dx.doi.org/10. 1016/S0265-931X(99)00027-2. Sasaki, Y., Abe, H., Mitachi, K., Watanabe, T., Ishii, Y., Niizato, T., 2016. The transfer of radiocesium from the bark to the stemflow of chestnut trees (Castanea crenata) contaminated by radionuclides from the Fukushima Dai-ichi nuclear power plant accident. J. Environ. Radioact. 161:58–65. http://dx.doi.org/10.1016/j.jenvrad.2015.12.001.
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Shoga, M., Hiraki, T., Tamaki, M., Nakagawa, Y., Kobayashi, T., 1993. Characteristics and relationship of rainfall, throughfall, and stemflow. Report of Hyogo Prefect. Inst. Environ. Sci. 25, 45–50. Takenaka, C., Onda, Y., Hamajima, Y., 1998. Distribution of cesium-137 in Japanese forest soils: correlation with the contents of organic carbon. Sci. Total Environ. 222: 193–199. http://dx.doi.org/10.1016/S0048-9697(98)00305-2. Teramage, M.T., Onda, Y., Kato, H., Gomi, T., 2014. The role of litterfall in transferring Fukushima-derived radiocesium to a coniferous forest floor. Sci. Total Environ. 490: 435–439. http://dx.doi.org/10.1016/j.scitotenv.2014.05.034.
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Stemflow-induced spatial heterogeneity of radiocesium concentrations and stocks in the soil of a broadleaved deciduous forest Naohiro Imamura a,⁎, Delphis F. Levia b,c, Jumpei Toriyama d, Masahiro Kobayashi a, Kazuki Nanko e a
Center for Forest Restoration and Radioecology, Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan Department of Geography, University of Delaware, Newark, DE 19716-2541, USA Departments of Plant and Soil Sciences, University of Delaware, Newark, DE 19716-1303, USA d Kyushu Research Center, Forestry and Forest Products Research Institute, 4-11-16 Kurokami, Chuo-ku, Kumamoto 860-0862, Japan e Department of Disaster Prevention, Meteorology and Hydrology, Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan b c
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Inputs of Fukushima-derived Cs were examined in the soil of a contaminated forest. • Cs concentrations were higher in the soils of the proximal than distal stem area. • Spatiality of Cs stocks is partly governed by preferential flowpaths of stemflow. • Cs soil stocks were higher under trees with larger canopy projection areas. • Soil sampling schema must account for Cs circumferential variation near tree stems.
a r t i c l e
i n f o
Article history: Received 23 January 2017 Received in revised form 13 April 2017 Accepted 2 May 2017 Available online xxxx Editor: D. Barcelo Keywords: Stemflow Konara oak Proximal area Double funneling Forest soils
a b s t r a c t The transport of radiocesium from the canopy and quantification of the spatial distribution of radiocesium in the soil of konara oak forests are important to better understand the variability of 137Cs stocks in the soil between proximal and distal stem areas as well as fine-scale variations around the tree trunk. Moreover, a better understanding of finescale spatial variabilities of 137Cs concentrations and stocks will provide insights for optimizing soil sampling strategies to provide a more robust estimation of contamination at the stand scale. This study aims to elucidate the transport of 137Cs by stemflow in a radioactively contaminated konara oak forest in Tsukuba, Japan by describing and quantifying the fine-scale spatial distribution of 137Cs in the soil and preferential flowpaths of stemflow on the tree stem by a dye tracing experiment. 137Cs concentrations and stocks were higher in the soils of the proximal stem area than distal stem area when they corresponded with the preferential flowpaths of stemflow. There was a significant relationship between canopy projection area of individual trees and average soil 137Cs concentrations and stocks, even though canopies of the trees overlapped. Our results demonstrate that the spatiality of 137Cs concentrations and stocks in the soil of the proximal stem area are governed (at least partially) by the preferential flowpaths of stemflow along the tree trunk. In addition, higher 137Cs concentrations and stocks in the near-trunk soils of trees with larger crown areas might be caused by an enhanced ability to capture dry deposition. © 2017 Elsevier B.V. All rights reserved.
⁎ Corresponding author. E-mail address: [email protected] (N. Imamura).
http://dx.doi.org/10.1016/j.scitotenv.2017.05.017 0048-9697/© 2017 Elsevier B.V. All rights reserved.
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1. Introduction
2. Materials and methods
The Fukushima Dai-ichi Nuclear Power Plant (FDNPP) accident released large quantities of radioactive substances into the surrounding environment. Cesium (Cs) levels of 134Cs and 137Cs, for instance, exceeded 1,000,000 Bq m−2 in areas close to the FDNPP which subsequently spread to cover a forest area of 428 km2, thereby representing roughly twothirds of the Fukushima prefecture (Hashimoto et al., 2012). Within the first year of the accident, radiocesium was primarily trapped by the forest canopy, the litter layer, and the surface mineral soil layer (Komatsu et al., 2016). Five years after the accident, the levels of radiocesium in the forest canopy and litter layer were decreasing from dilution via rainfall and defoliation, leading to an accumulation of radiocesium in the surface mineral soil layer (0–5 cm) of the forest (Imamura et al., preparation). There remains, however, much to learn about the cycling of radiocesium in forest, especially with respect to its redistribution by stemflow in localized areas around individual tree trunks. Previous studies have documented that radiocesium is intercepted by the forest canopy and transported to the soil by throughfall and stemflow (Bunzl et al., 1989a; Bonnett and Anderson, 1993; Pröhl et al., 2006; Kato et al., 2012; Endo et al., 2015; Kato et al., 2017) and litterfall (Bonnett and Anderson, 1993; Teramage et al., 2014; Endo et al., 2015; Kato et al., 2017). Compared to stemflow, large proportions of the annual radiocesium flux was found in throughfall and litterfall (Rafferty et al., 2000; Kato et al., 2012; Teramage et al., 2014). Kato et al. (2017) reported that contribution of throughfall, stemflow, and litterfall to the total flux was 31.3%, 4.7%, and 64.0%, respectively, in a deciduous mixed forest in Fukushima prefecture, although the actual input via stemflow calculated per unit basal area would be much higher. Even though the total annual flux of 137Cs by stemflow is relatively low, it is likely of importance to the spatiality of 137Cs in the forest soils for some tree species because stemflow is subject to preferential flow in the rhizosphere (Johnson and Lehmann, 2006). Förster and Schimmack (1992) concluded that the horizontal and vertical distribution of 137Cs in the soil of a beech stand was caused by the non-uniform nature of stemflow inputs. In addition, Takenaka et al. (1998) reported that the variable concentrations of 137Cs in the surface soil around a red pine tree was attributable to the transport pathway of 137Cs from the canopy to the soil and/or the uptake of 137Cs by the trees. These effects of stemflow on the spatial variation in 137Cs concentration in the surface soil may depend on the presence of preferential flow and its volume. While the studies cited above have increased our understanding of radiocesium cycling in forests, our specific focus is somewhat different. Prior work has considered the tree trunk as a whole and examined horizontal and vertical differences in 137Cs concentrations (Förster and Schimmack, 1992). We aim to expand this research by explicitly linking stemflow of konara oak (Quercus serrata Murray), a prevalent species in the deciduous forests in the Fukushima Prefecture, to the fine-scale circumferential spatial variabilities of radiocesium concentrations and stocks in the surface soil around specific trees. Konara oak stand produces relatively high stemflow volumes (Shoga et al., 1993). Therefore, it is probable that the observation and quantification of preferential flow of stemflow would aid in the prediction of the spatial distribution of 137Cs concentrations in the soil in the proximal area around konara oak trees. This is the first known study to specifically examine fine-scale circumferential differences in 137Cs concentrations and stocks in the soil of the proximal area of individual trees. Accordingly, this study aims to elucidate: (1) the radiocesium transport process by stemflow in a konara oak forest; and (2) describe and quantify the finescale spatial distribution of 137Cs in the soil in the proximal area of the stem of konara oak trees. A detailed examination of fine-scale spatial heterogeneities of 137Cs concentrations and stocks in the surface soils of the proximal areas of konara oak trees is of critical importance for the optimization of soil sampling strategies and the consequent robust estimations of soil contamination at stand scale in forests subjected to radioactive fallout.
2.1. Study site The study site was established in a konara oak dominated experimental forest at the Forestry and Forest Products Research Institute (FFPRI), Tsukuba city in Japan, which is located 170 km southwest of FDNPP (36°00′32″N, 140°07′36″E, Fig. 1). The mean 5-year annual air temperature and precipitation between 2011 and 2015 was 14.4 °C and 1280 mm, respectively, as measured at a meteorological station at FFPRI (Fig. 2). Wind speed and wind direction also were observed at meteorological station. The total deposition of 137Cs and 134Cs was 40,000 Bq m−2 as of May 31, 2012 (Extension Site of Distribution Map of Radiation Dose, etc.,/GSI Maps). In Tsukuba, a high concentration plume (N10 Bq m−3) was observed between March 14 and 15, 2011 under clear sky conditions and between March 20 and 22, 2011 under rainy conditions as observed from aerosol samples on quartz fiber filters (Adachi et al., 2013). The first rainfall event (28.0 mm and 0.64 mm h−1) after the nuclear accident occurred between March 21, 8:00 and March 23, 3:00, 2011 at FFPRI. The konara oak forest studied was 37 years old (as of 2015) with stand density of 1700 trees ha−1 (Migita et al., 2007), mean tree height of 19.1 m, and a mean diameter at breast height (dbh) of 22.4 cm. The forest is situated on level terrain over an andisol formed on a loamy soil layer. The thickness of the organic layer (Oi, Oe, and Oa), composed of thinning and decaying leaves, was approximately 2 cm in the summer. Summer soil moisture content was approximately 4%. 2.2. Stemflow dye experiment To determine the spatiality of stemflow into the forest soil, a stemflow dye experiment was performed in mid March of 2016, which was the same season as the FDNPP accident and first rainfall event after the accident. All trees were defoliated. The morphological
Fig. 1. Location of study site with respect to the Fukushima Dai-ichi Nuclear Power Plant. The deposition densities of total 137Cs and 134Cs (Bq m−2) on May 31, 2012 are based on aircraft monitoring (Extension Site of Distribution Map of Radiation Dose, etc.,/GSI Maps).
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Fig. 3. Canopy projection areas and location of the five konara oak trees studied within the experimental plot.
Fig. 2. Mean monthly temperature and rainfall amounts observed at FFPRI. Mean monthly air temperature from January 2011 to December 2015 (top) and the 5-year average monthly rainfall (solid grey bars) with standard errors bars from 2011 to 2015 (bottom).
characteristics of the five sample trees are shown in Table 1. The dbh of the sample trees ranged from 17.7–35.1 cm (Table 1). The trunk lean of tree E was about 20° from north to south, while other trees exhibited very little to no trunk lean. The canopy projection areas of each tree (Fig. 3) were calculated using the branch length in eight azimuthal directions. The canopy projection area was the largest for tree D (48 m2) and the smallest for tree C (5.5 m2). Water containing Brilliant Blue FCF colored dye was sprayed on five individual tree stems (trees A, B, C, D, and E) in the rainfall event on March 22, 2016. The dye was sprayed uniformly in a wide band along the whole circumference of the tree stem. Thus, stemflow flowpaths were identified as those areas where the dye was removed as stemflow was channelized down the tree stem (Fig. 4); the areas that remained covered with dye did not experience stemflow. To confirm the repeatability of stemflow patterning on the stem, an additional exploratory stemflow dye experiment was performed on September 13, 2016. The two sampled events differed with respect to rainfall intensity and are broadly representative of rain events in the area. Moreover, since stemflow channelization is largely controlled by canopy structure in these forests, we are confident that we can provide useful insights into the spatial variation of radiocesium in these forest surface soils. The direction and extent of stemflow dispersion on each stem was estimated using a tape measure. Discrimination between the area of the tree trunks that were and were not conducting stemflow was obvious from the presence or absence of the dye on the tree stems.
trunk areas (n = 8, i.e., proximal stem area) and the surrounding area (n = 16, i.e., distal stem area) (Fig. 5). The radiocesium concentration of all soil samples were decay-corrected to July 1, 2015 to standardize soil sample collection. Given the low levels of 137Cs in the organic layer at the time of this study (Fig. A1, Table A1, please see the web link in Appendix A for Supplementary Data), it was removed before coring for soil samples. After removal of the organic layer, one soil sample was collected in the center of each square (as depicted in Fig. 5) using a 475-mL cylinder (95 cm2 cross-sectional area × 5 cm depth). We assumed that the core sample (per 95 cm2) within each grid square was representative of the grid square (per 625 cm2) as a whole.
2.3. Soil sampling The soil sampling plot was established as a 125 × 125-cm quadrat around the center of each tree stem (Fig. 5). Chang and Matzner (2000) defined the ‘proximal stem area’ as 1 m2 (56.4 cm distance from center of stem) around the tree trunks, and ‘distal stem area’ as further away. In this study, the 24-cell grid was divided into adjacent
Table 1 Tree height, height of the lowest live branch (HB), diameter at breast height (dbh @ 1.37 m), and canopy projection area of the study trees. Tree
A
B
C
D
E
Tree height (m) HB (m) dbh (cm) Canopy projection area (m2)
22.5 9.1 28.5 15.1
25.0 6.0 29.1 23.1
15.9 7.8 17.7 5.5
25.8 10.6 35.1 48.0
23.1 6.9 21.0 8.9
Fig. 4. Brilliant blue dye on the stem of a konara oak tree. Dye was uniformly applied around the circumference of the whole tree in the rainfall event. The preferential flowpaths of stemflow, as it is channeled down the trunk, are depicted as the areas where there is an absence of dye as it was washed off by stemflow. Thus, these areas void of dye, where the tree trunk intersects with the forest floor, represent the locations where stemflow is input into the forest soil. The marked spatial heterogeneity of stemflow inputs in the proximal area is readily apparent.
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Fig. 5. Soil sampling area (n = 24). “P” denotes the proximal stem area (n = 8) and “D” denotes the distal stem area (n = 16).
2.4. Chemical analysis and calculations of radiocesium soil stocks The soil samples were air-dried and then oven-dried for 24 h at 105 °C. The concentration of 137Cs for all samples was determined using HPGe coaxial and P-type reverse detector systems (GEM20-70, GEM40P4-76, GEM-FX7025P4-ST, and GWL-120-15-LB-AWT, ORTEC, Oak Ridge, USA). The measurement times were 1800–4000 s, which normally obtain 137Cs concentration values with relative errors b 10%. The radiocesium stock (Bq m−2) of 137Cs for all samples was calculated by multiplying the radiocecium concentration per dry mass (Bq kg−1) by the dry mass per unit area (kg m−2).
Fig. 6. Locations around the tree trunk where stemflow was input to the forest soil (blue line) or void of stemflow (black line) during the rainfall events on March 22 and September 13, 2016. Please note the spatial heterogeneity of the stemflow inputs to the forest soils as well as the similarities for a given tree between the two rainfall events. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
3.2. 137Cs concentrations and stocks in the surface soil 2.5. Statistical analysis To determine the spatial variation of radiocesium inputs to the forest soil via stemflow, we compared 137Cs concentration in both the soils of the proximal stem (n = 8) and distal stem areas (n = 16) using the Wilcoxon rank sum test. Since stemflow often infiltrates the soil in a non-uniform manner as a result of preferential flowpaths (Johnson and Lehmann, 2006; Levia and Germer, 2015), we compared the 137Cs concentrations and stocks in the proximal stem area between stemflow-influenced and non-influenced points, as determined from the results of the dye experiment. The soil 137Cs concentration of stemflow and no stemflow input points were also compared using Wilcoxon rank sum test. Furthermore, to explain the distribution of radiocesium by the effect of tree size, we examined the relationship between canopy projection area and the average soil concentration and stock. 3. Results
The 137Cs concentrations in the soil of the proximal stem area (n = 8) were higher than those of the distal stem areas (n = 16) for all trees (Table 2). Median 137Cs concentrations were 20–135% larger in the proximal stem area than in distal stem area for the five trees. These differences were statistically significant for trees A, B, and D (Wilcoxon rank sum test; p b 0.05). In addition, the median 137Cs stock was 24–136% larger in the proximal stem area than distal stem area for the five trees. The average concentration of 137Cs in the soil (n = 24) for both the proximal and distal stem areas was different for each tree (Table 2), being the highest for tree D (2910 ± 1540 Bq kg−1) and the lowest for tree C (1240 ± 955 Bq kg−1). The average concentration of 137Cs was 134% higher for tree D than tree C. 137 Cs concentrations in the soils around the tree trunk exhibited a wide variability, ranging from 514 to 5520 Bq kg− 1 for tree A, 633–6965 Bq kg− 1 for tree B, 505–5323 Bq kg− 1 for tree C, 1200–5988 Bq kg−1 for tree D, and 386–6448 Bq kg−1 for tree E, respectively. In the proximal stem area, the distribution of 137Cs concentrations in the soil was different for each tree (Fig. 7). The coefficient of variation (CV) of 137Cs concentrations in the soil within the proximal
3.1. Stemflow dye experiment The first dye experiment was performed in a rainfall event with the following characteristics: rain intensity of 1.75 mm h−1, mean wind direction from the north-northeast, and mean wind speed of 3.3 m s−1. The second dye experiment was performed in a rainfall event with a rain intensity of 7.7 mm h−1, mean wind direction from the northeast, and mean wind speed of 1.9 m s−1. The spatial patterning of stemflow inputs to the soils was different for each tree (Fig. 6), although it was quite similar for both stemflow dye experiments, despite the fact that the wind and rainfall conditions were different. This underscores the fact that canopy structural characteristics exerted a strong control on stemflow channelization along the trunks of these particular trees.
Table 2 Mean (±1SD) 137Cs concentrations (Bq kg−1) in the soil of the proximal stem area of the tree trunk (n = 8), distal stem area (n = 16), and average concentration for both areas (n = 24). Median values are shown in parentheses. Tree Proximal stem area Distal stem area Average stem area
A
B
C
D
E
2,460 ± 1,710
3,490 ± 2,130
1,730 ± 1,500
4,340 ± 1,690
1,690 ± 1,960
(1,660)
(3,020)
(1,090)
(4,580)
(1,180)
1,240 ± 545
1,280 ± 387
995 ± 403
2,190 ± 798
1,030 ± 551
(1,080)
(1,360)
(912)
(1,950)
(882)
1,650 ± 1,200
2,020 ± 1,620
1,240 ± 955
2,910 ± 1,540
1,250 ± 1,210
(1,270) (1,530) (955) (2,300) (1,050) Bold values denote significance at the 0.01 level. Grey values denote significance at the 0.05 level.
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Fig. 7. The spatial distribution of 137Cs concentrations (Bq kg−1) in the surface soil in relation to the locations around the tree trunk where stemflow is input to the soil (blue line). The black line depicts area around the tree trunk that did not receive any stemflow inputs. The light grey area depicts the stem area at the surface soil. The darker grey area shows the stem area approximately 40 cm above the ground. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
stem area ranged from 0.39–1.16, and the CV was largest for tree E. The distribution of 137Cs stocks in the soil was similar to that of 137Cs concentrations in the soil (Figs. 7 and 8). The CV of 137Cs stocks in the soil within the proximal stem area ranged from 0.36–1.22. The 137Cs concentrations and stocks in the soil were higher for areas which received stemflow (Figs. 7 and 8) than those that did not, with these differences being statistically significant (Wilcoxon rank sum test; p b 0.001; Fig. 9). From the relationship between canopy projection area and average soil concentration, a significant positive correlation was found between average 137Cs concentration in the soil and canopy projection area (p b 0.01; Fig. 10). A similarly significant relationship was also found between 137Cs stock in the soil and canopy projection area (p b 0.01). 4. Concluding discussion 4.1. 137Cs concentrations and stocks in the soils of proximal and distal stem areas Our result that the concentrations and stocks of 137Cs in the soil was highest in the proximal stem area is consistent with previous work of others (e.g., Bunzl et al., 1989b; Förster and Schimmack, 1992; Table 3). Bunzl et al. (1989b) reported that 137Cs stock was 12% higher for spruce at a distance of 0–0.5 m than 3 m from the tree trunk. Likewise, Förster and Schimmack (1992) also observed that 137Cs stocks in the soil under beech trees were 130–831% higher in the area adjacent to the tree than 4 m from the stem. Similar to 137Cs, concentrations and stocks of NO3\\N in the soils near the tree trunk were N40% higher than those further away from the stem for bigleaf maple (Hamdan and Schmidt, 2012). Chang and Matzner (2000) reported 162% higher concentrations of K+ in soils near the trunk in European beech stands. These results indicate that the concentrations and stocks of elements
in the soil are higher near the tree trunk, especially for deciduous forests. These phenomena could, as suggested by numerous others, be affected by the occurrence of stemflow (Förster and Schimmack, 1992; Chang and Matzner, 2000; Hamdan and Schmidt, 2012; Fantozzi et al., 2013). Our results build upon previous studies by demonstrating the marked fine-scale circumferential spatial variation of 137Cs concentrations and stocks in the soils of the proximal area (as detailed in the next section). 4.2. Preferential flowpaths of stemflow: a control on soil 137Cs concentrations and stocks within proximal stem area Johnson and Lehmann (2006) explained the double-funneling of nutrient fluxes by trees, whereby the spatial and vertical distributions of nutrients are concentrated both above- and belowground by stemflow. In support of the double-funneling concept of Johnson and Lehmann (2006), we opined that the stocks of 137Cs in the soil would be higher for areas connected to the tree trunk via the preferential flowpaths of stemflow than the other locations within the proximal stem area. Our experimental observations substantiated this claim. In fact, the preferential flowpaths of stemflow, as identified by the areas where the previously applied dye tracer was removed by stemflow (Fig. 4), corresponded to the precise areas where stemflow transported radiocesium from the canopy to the soil. This shows that the aboveground funneling of stemflow along preferential flowpaths is a key control affecting the variable circumferential spatial patterning of 137Cs into the soil around tree trunks. However, since we did not examine the funneling of cesium along the roots in the subsurface, we cannot confirm whether 137Cs is also funneled belowground in accord with the double-funneling concept. Because prior work has found that radiocesium concentrations were not decreasing over the observation
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Fig. 8. The spatial distribution of 137Cs stocks (Bq m−2) in the surface soil in relation to the locations around the tree trunk where stemflow is input to the soil (blue line). The black line depicts area around the tree trunk that did not receive any stemflow inputs. The light grey area depicts the stem area at the surface soil. The darker grey area shows the stem area approximately 40 cm above the ground. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
period (Endo et al., 2015; Sasaki et al., 2016; Kato et al., 2017), it gives further credence to our argument that the higher concentrations of radiocesium in the proximal stem area could be the result of stemflow-supplied 137Cs. Because our site is in the forest interior on level ground, it is most likely that the fine-scale circumferential variations in 137Cs concentrations and stocks were the result of preferential inputs via stemflow. However, it is worth noting that the spatial variation of 137Cs in the soil could be attributed to phenomena and factors other than stemflow, such as a tree's location to the forest edge and topography (Ould-Dada et al., 2002; Atarashi-Andoh et al., 2015), litterfall leachate inputs
(Koarashi et al., 2016), and the horizontal and vertical migration of radiocesium (Förster and Schimmack, 1992). At our site, there was no clear pattern in the distribution of 137Cs concentrations in the organic layer (Fig. A1, Table A1, please see the web link in Appendix A for Supplementary Data). It is possible that the geometric orientation of the tree stem might influence the concentrations and stocks of 137Cs in the soil of proximal area since the orientation of tree trunks has been documented to influence stemflow volume (Levia et al., 2015). Similarly, we identified a preferential flowpath on the underside of trunk for tree E, which has a trunk lean of 20°, that resulted in a high 137Cs concentration and stock
Fig. 9. A box-and-whisker plot of 137Cs concentrations and stocks in the surface soils with and without stemflow inputs. The median values are denoted by horizontal bold lines within the boxes, while the upper and lower quartiles are represented by the boundaries of the boxes. The maximum and minimum values are denoted by the whiskers. Outliers are denoted by a circle. Stemflow input was defined by the area of color dye (blue line) when it was larger than the area of no color dye (black line) in each stem area (separated in eight azimuth directions) (grey area) in Figs. 7 and 8.
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Fig. 10. The relationship between the canopy projection area of the experimental trees and the average 137Cs concentration in the soil (n = 24) for both the proximal and distal stem areas.
in the soil along this side of the tree, which also accounted for the largest variation of 137Cs concentrations within the proximal stem area (Figs. 7 and 8). Although the variations of 137Cs concentrations in the soil within proximal stem areas of the other four trees were lower than that of tree E, we still witnessed the presence of preferential flowpaths on the stems of these trees (despite minimal trunk lean) which corresponded with the high concentrations and stocks of 137Cs in the soils of the proximal areas (Figs. 7 and 8). These preferential flows (trees A, B, C, and D) could be affected by the presence of flow path obstructions (Crockford and Richardson, 2000) and bark morphology (Levia and Herwitz, 2005). This is because bark morphology is a key control on both the generation and volume of stemflow as well as its channelization on the tree stem (Levia and Herwitz, 2005). Our findings indicate that the spatiality of 137Cs concentrations and stocks in the soils near konara oak trees is heterogeneous and that the preferential flowpaths on tree trunks is one cause of the larger 137Cs inputs in the proximal stem areas as compared to the distal stem areas. 4.3. Relationship between tree size and soil 137Cs concentration and stock To explain differences in soil 137Cs concentrations and stocks between individual trees, the effect of tree size is an important consideration. André et al. (2008) reported that the product of trunk circumference and tree height explained the inter-individual variability in stemflow chemistry. Hofhansl et al. (2012) found that dbh, tree height, and plant area index influenced stemflow chemistry in a tropical rainforest. Similarly, we found that the concentration of 137Cs in the soil (134%) was larger for the largest tree (tree D) than the tree with the smallest canopy projection area (tree C). Therefore, a significant positive correlation between average 137Cs concentration in the soil and canopy projection area (Fig. 10) could be found by the difference of tree size in this oak forest. In addition, stemflow yield was affected by tree height, basal diameter, and canopy projection area (Ford and Deans, 1978; Martinez-Meza and Whitford, 1996; Crockford and Richardson, 2000; Garcia-Estringana et al., 2010; Levia et al., 2015). As such, differential stemflow yield likely affects the relationship between average 137Cs stock in the soil.
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It must be noted that the canopies of the konara oak trees were defoliated in May 2011, soon after the FDNPP accident. Previous studies have reported that leafless canopies can capture notable quantities of dry deposition (e.g., Beckett et al., 2000; Freer-Smith et al., 2004). Therefore, it is probable that the leafless crowns of the large konara oak trees was able to effectively scavenge the dry deposition of 137Cs by the first plume after the accident onto its branches and stem surfaces. This suggests that these phenomena could lead to the significant relationship between canopy projection area and average soil concentration of 137 Cs (Figs. 3 and 10). We developed a conceptual model to describe the linkages between tree morphology, stemflow yield, and radiocesium in the soil (Fig. 11). Of course, meteorological conditions also will influence stemflow amounts (Levia and Frost, 2003), but the point of this conceptual model is to highlight the interrelationships among tree morphology, stemflow production, and consequent transport of 137Cs from the tree crown to the forest soil. The model underscores the interactions among tree trunk orientation, tree size, and bark morphology with the formation of preferential channelization along the tree trunk and the consequent spatial localization of 137Cs in the forest soil within the proximal area of tree trunks. As reported by studies already cited (e.g., Levia and Herwitz, 2005; André et al., 2008; Levia and Germer, 2015; Levia et al., 2015), the generation and volume of stemflow is affected by interactions among a host of biotic and abiotic factors that lead to differences in stemflow generation and production that ultimately result in the spatial heterogeneities of radiocesium in the proximal stem area. Our results have showed that stemflow has a detectable and important influence on 137Cs stocks in the surface soil. Our results also have demonstrated that 137Cs concentrations and stocks in the soil were higher in the proximal stem area than distal stem area because of stemflow generated by konara oak trees. Based on data from Kato et al. (2017), which showed that 4.7% of the total deposit was transferred to the soil via stemflow, this would correspond to approximately 1800 Bq m−2 over the 40,000 Bq m−2 in the present study, equating to about 36,000 Bq m−2 in the proximal areas of the tree stem (based on assumption that these areas constitute 1/20 of the total area), or about 30% of the enrichment. Thus, expressed per unit proximal area, stemflow inputs are substantial. Recognition of this fact and the finescale circumferential spatial variations of radiocesium inputs into forest soils via stemflow is of critical importance in the development and optimization of soil sampling schema that must provide a more robust estimation of contamination at the stand scale. One simply cannot assume homogeneity of 137Cs surface soil stocks across a forest stand. The heterogeneous nature of proximal area soils must be taken into account. Acknowledgments We thank Dr. Akio Akama for assistance with the field observations. Furthermore, we thank Dr. Ryuichi Tabuchi, Ms. Shukushin Endo, Dr. Koichi Yamamoto, and Dr. Mitsutoshi Tsunoda for their valuable assistance with analyzing concentrations of cesium in the soil. This work was supported by JSPS KAKENHI [grant number JP15H04522] as well as by a JSPS invitation fellowship [grant number: S16088] to both Kazuki Nanko and Delphis Levia.
Table 3 \N in the proximal and distal stem areas as reported in previous studies. Soil concentrations and stocks of 137Cs, K+, and NO3\ Forest type
Element
Depth
Proximal stem area
Distal stem area
Increase ratio
References
Norway spruce European beech European beech Bigleaf maple
Cs (Bq m−2) 137 Cs (Bq dm−2) K+ (mg l−1) \N (mg kg−1) NO3\ \N (kg ha−1) NO3\ 137 Cs (Bq kg−1) 137 Cs (Bq m−2)
0–47 (cm) 0–60 (cm) 40 (cm) Surface Surface 0–5 (cm) 0–5 (cm)
3290 ± 390 600–2700 4.64 70.89 0.43 1690 ± 2010 34,490 ± 36,520
2930 ± 240 260–290 1.77 45.60 0.30 1220 ± 700 23,640 ± 11,600
12% 130–831% 162% 55% 43% 20–135% 24–136%
Bunzl et al. (1989b) Förster and Schimmack (1992) Chang and Matzner (2000) Hamdan and Schmidt (2012)
Konara oak
137
This study
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Fig. 11. A conceptual model of the linkages among tree trunk orientation, tree size, and bark morphology with the formation of preferential channelization of stemflow along the tree trunk and the consequent spatial localization of 137Cs in the forest soil within the proximal area of konara oak tree trunks.
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