https://orcid.org/0000-0001-5361-0978
Figures
Abstract
Collection and cooking of wild vegetables have provided seasonal enjoyments for Japanese local people as provisioning and cultural ecosystem services. However, the Fukushima Daiichi Nuclear Power Plant accident in March 2011 caused extensive radiocesium contamination of wild vegetables. Restrictions on commercial shipments of wild vegetables have been in place for the last 10 years. Some species, including buds of Aralia elata, are currently showing radiocesium concentrations both above and below the Japanese reference level for food (100 Bq/kg), implying that there are factors decreasing and increasing the 137Cs concentration. Here, we evaluated easy-to-measure environmental variables (dose rate at the soil surface, organic soil layer thickness, slope steepness, and presence/absence of decontamination practices) and the 137Cs concentrations of 40 A. elata buds at 38 locations in Fukushima Prefecture to provide helpful information on avoiding collecting highly contaminated buds. The 137Cs concentrations in A. elata buds ranged from 1 to 6,280 Bq/kg fresh weight and increased significantly with increases in the dose rate at the soil surface (0.10–6.50 μSv/h). Meanwhile, the 137Cs concentration in A. elata buds were not reduced by decontamination practices. These findings suggest that measuring the latest dose rate at the soil surface at the base of A. elata plants is a helpful way to avoid collecting buds with higher 137Cs concentrations and aid in the management of species in polluted regions.
Citation: Sakai M, Watanabe M, Kanao Koshikawa M, Tanaka A, Takahashi A, Takechi S, et al. (2024) Exploring simple ways to avoid collecting highly 137Cs-contaminated Aralia elata buds for the revival of local wild vegetable cultures. PLoS ONE 19(4): e0292206. https://doi.org/10.1371/journal.pone.0292206
Editor: Mohamad Syazwan Mohd Sanusi, Universiti Teknologi Malaysia, MALAYSIA
Received: September 14, 2023; Accepted: March 16, 2024; Published: April 2, 2024
Copyright: © 2024 Sakai et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript and its Supporting Information files.
Funding: This study was performed by the commissioned research fund by F-REI (grant number: JPFR23050301, website: https://www.f-rei.go.jp/) (to S.H.). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Collecting and cooking wild vegetables (sansai) provides seasonal enjoyment for Japanese people and such traditional activity promotes communication among local people through sharing of dishes and information [1]. However, the Fukushima Daiichi Nuclear Power Plant accident in March 2011 resulted in radionuclide contamination, leading to the termination of such activities [2,3]. Collecting various wild vegetables is restricted in some contaminated areas due to radiocesium concentrations exceeding the Japanese reference level (100 Bq/kg) [4,5]. Among the vegetables, the buds of Koshiabura (Eleutherococcus [Chengiopanax] sciadophylloides [Araliaceae]), which is known as the “Queen of sansai,” exhibits particularly high radiocesium concentrations compared to other wild vegetables [6–8]. Consequently, commercial shipping of this species is restricted in 113 municipalities in Japan [9].
Radiocesium concentrations in several wild vegetable species have decreased over the past decade [10] and some species are exhibiting concentrations below the reference level. For example, the reported 137Cs concentrations in wild vegetables collected in Iitate village, one of the former evacuation zones, include a substantial number of minimally contaminated species [11]. Among them, the buds of Taranoki (Aralia elata [Araliaceae]), which is one of the most popular wild vegetables in Japan known as the “King of sansai,” exhibited 137Cs concentrations that varied widely above and below the reference level according to the open data provided by Iitate village (Fig 1) [11].
The blue horizontal line indicates the Japanese reference level for foods (100 Bq/kg). Data were retrieved from Iitate village (2022) [11]. 137Cs activity concentrations below the detection limits were regarded as 5 Bq/kg. Reported ratios of 134Cs to 137Cs outside the range of 0.8–1.2 on 11 March 2011 were excluded to ensure reliability.
Aralia elata is a deciduous shrub species distributed in East Asia, including the Japanese Archipelago, the Korean Peninsula, China, and Russia. As a typical pioneer species, A. elata primarily inhabits sunlit spaces on forest edges, roadside slopes, and riparian zones. The buds of this species (Taranome) are typically collected during spring and are often cooked as tempura and ohitashi in Japan or boiled as medicine in Korea and China. Forty-three Japanese municipalities restrict commercial shipments of wild A. elata buds; only Koshiabura buds are subjected to more stringent limitations [9]. However, as mentioned above, 137Cs concentrations in A. elata buds vary widely, including values below the reference level, even within a single municipality (Fig 1). This trend suggests that potential factors lower and/or raise the 137Cs concentrations in A. elata buds. For example, the 137Cs inventory in the soil (or the dose rate at the soil surface) is a fundamental factor determining the 137Cs concentrations in various organisms, including plants that assimilate 137Cs from root systems [12–14]. Moreover, A. elata predominates in open spaces that often lie near areas of human activity, such as roadside slopes and clear-cut areas. Soils in these areas may have undergone decontamination efforts following the Fukushima accident [15]. Forested areas have rarely been decontaminated; thus, leaf abscission and circulation of 137Cs in the organic soil layer may continue to deposit bioavailable 137Cs [16]. Furthermore, the steepness of the slope can affect the 137Cs concentration in A. elata buds due to the pronounced effects of soil erosion on steeper slopes, which reduces the amount of deposited 137Cs in the soil [17].
As collecting and cooking A. elata buds have provided seasonal enjoyment for local people, proposing easy ways to avoid obtaining highly contaminated buds would be helpful. In this study, we collected A. elata buds and constructed an environmental variable dataset around the A. elata plants that can be easily obtained using commercially available equipment or public data. This investigation was performed in six municipalities of Fukushima Prefecture with a variety of 137Cs deposition levels. The environmental variable dataset included the dose rate at the soil surface, organic soil layer thickness, slope steepness, and presence/absence of a decontamination practice. We assessed which environmental variable(s) should be avoided to collect highly contaminated buds. Simply identifying these factors could help revive traditional wild vegetable collection and cooking practices, as well as aid decontamination programs. This is particularly crucial to preserve the traditional sansai culture within contaminated regions.
Methods
Study sites and bud collection
This study was conducted at 38 sampling locations in Iitate and Katsurao villages, Kawamata town, and Minamisoma, Nihonmatsu, and Tamura cities in Fukushima Prefecture, Japan. For the investigations, field access to the sampling locations did not require any permission because all the locations did not within the difficult-to-return zone. The 137Cs deposition after the Fukushima Daiichi Nuclear Power Plant accident varied widely, ranging from 41 to 1,200 kBq/m2 in the study locations [18]. The habitats of A. elata plants sampled in this study were categorized as forest, forest edge, or roadside slope, which are preferred habitats for this species. The height of the 38 sampled plants was approximately 2.0 m. Because A. elata generally grows 20–60 cm/year, we assumed that the sampled plants had not been contaminated by the 137Cs deposition on their surfaces in 2011. While A. elata generates underground stems for vegetative propagation, the plants we selected were treated as separated genets due to the significant distance between their habitats. Buds were collected from all plants from April to May in 2022 and 2023 to measure 137Cs concentrations. A total of 40 buds were collected, including four buds from two plants collected in 2022 and 2023 (one bud per plant for each year) and 36 buds from each of the remaining 36 plants in 2022 or 2023.
Environmental variables
To identify “easy-to-measure” factors that increased the 137Cs concentrations in A. elata buds, we investigated the presence/absence of decontamination practices, the dose rate at the soil surface, slope steepness, and the thickness of the organic soil layer at the base of each A. elata plant. According to information gathered from the decontamination records provided by the Ministry of the Environment, the sampling locations included 24 decontaminated and 14 abandoned habitats.
Because several years have passed since decontamination, the current soil 137Cs inventory, particularly within the decontaminated areas, could change owing to recontamination from the surrounding environment [19]. To address this concern, we measured the dose rate at the soil surface at the base of each A. elata plant to serve as a reliable indicator of the 137Cs inventory (see Aggregated transfer factors below for details). The dose rates at the soil surface were determined using a scintillation survey meter (TCS-172B; Hitachi Aloka Medical, Tokyo, Japan). The NaI(Tl) probe of the survey meter was placed at the soil surface, and thus the measured dose rates were assumed to be primarily affected by radiation from the soil, rather than that from the surrounding environment. The measured gamma dose rates were majorly contributed by 137Cs and primordial radionuclide series from the soils though the dose rate might be slightly higher than the actual soils’ gamma dose rate due to contribution from cosmic rays and instrument noise. Surface geology of all the sampling locations was homogeneously granite, and thus the measured dose rates derived from radiations other than 137Cs were substantially similar among the locations. Therefore, we assumed that difference in the measured dose rates among the locations simply reflect 137Cs accumulation levels, as dose rate on the soil surface is a good indicator for estimating 137Cs inventories in soils [22]. Dose rate can also be measured using a portable dosimeter, which is generally available to the public, and thus we included this as an easy-to-measure variable.
Slope steepness was determined using the “Measure” iPhone application (iPhone 13; Apple Inc., Cupertino, CA, USA). We assumed that slope steepness could affect the soil runoff rate, which, in turn, is related to decreasing 137Cs content in the soil [17]. The cumulative thickness of the litter, fermentation, and humus layers at the soil surface was measured using a 3-point folding scale in the vicinity of each A. elata plant because the organic soil layer possessed abundant bioavailable 137Cs that has the potential to contaminate A. elata buds [16]. The boundaries between organic and mineral soil layers at each location were confirmed by eye after digging small and shallow trenches.
Aggregated transfer factors
Estimating the potential internal radiation exposure after consuming contaminated wild vegetables is important for radiation protection [20]. This is particularly important to improve the quality of life of local people who wish to enjoy collecting and consuming wild vegetables [21]. In this regard, the aggregated transfer factor (Tag) is widely used to indicate the relationship between radionuclide concentration in wild vegetables and the soil. Tag is expressed as the radionuclide activity concentration in wild vegetables (Bq/kg) divided by the radionuclide inventory in the soil (Bq/m2). Because accumulating Tag values from spatiotemporally wide areas is helpful to understand the 137Cs dynamics in wild vegetables and predict the revival of sansai culture, this study also calculated the Tag values based on the 137Cs activity concentrations in A. elata buds and 137Cs deposition in the soil that was estimated using a previously published method [22].
We first measured the dose rate at the soil surface and collected soil samples from 78 measurement points from 2020 to 2022 before investigating the A. elata buds. The 78 locations included forests, forest edges, and roadside slopes around Fukushima Prefecture (also three locations from the A. elata investigations). The dose rate at the soil surface was determined as described above. Then, the organic layer and the soil layer at depths from 0 to 10 cm were collected at each measurement point because these layers contain most of the 137Cs derived from the disaster [23]. The 137Cs soil inventory (kBq/m2) was estimated based on soil mass per unit area and the 137Cs activity concentrations of the collected samples. The procedures for measuring 137Cs activity concentrations are detailed below. A linear model was constructed based on the loge-transformed data for the soil surface dose rates and the 137Cs inventories in the soil using R 3.6.3 [24]. It was used to transform the measured dose rate at each A. elata plant into the 137Cs inventory at each point to calculate Tag for the A. elata samples.
Radioactivity measurements
The soil samples used to estimate the 137Cs inventory were dried at 25°C for at least 1 month, sieved through 2 mm mesh, and packed into 100 mL plastic containers. The dried soil weight was calculated based on the weight loss after subsequent drying of several grams of the samples at 105°C for at least 24 h because we needed to store soils dried at 25°C for other chemical analyses. All fresh buds were gently washed with tap water, wiped, weighed, dried at 60°C for at least 2 days, and reweighed, because drying organic matter at 60°C could avoid loss of volatile organic matter compared to drying at 105°C. The dried samples were finely ground using an electrical mill and packed into 100 mL plastic containers. The dry weights and the densities of the soil and bud samples were measured before the radioactivity measurements (buds: 0.85–4.91 g, organic layer: 4.99–16.99 g, soil layer: 24.05–63.45 g). The 137Cs activity concentrations in the soil and bud samples from all A. elata plants were determined by gamma-ray spectroscopy. Gamma-ray emissions were measured at an energy of 661.6 keV using a coaxial high-purity germanium detector system (model GC 2020; Canberra Japan, Tokyo, Japan). The accuracy of 137Cs activity was within 5% (error counts/net area counts). Sample activity was corrected for radioactive decay at the time of collection. After determining the 137Cs activity concentrations based on the bud dry weights, fresh weight concentrations were calculated based on water content estimated from the initial weight measurements (mean = 87.4%). The detector system was routinely calibrated using blank (empty 100 mL plastic containers) and 137Cs standard (CS401; Japan Radioisotope Association, Tokyo, Japan) samples for obtaining background and channel adjustment data, and tested annually by the manufacturer using reference samples to ensure measurement accuracy.
Statistical analyses
A linear mixed model (LMM) was employed to identify the easy-to-measure factor(s) that affected the 137Cs activity concentrations in A. elata buds. Correlations between all pairs of environmental variables (dose rate at the soil surface, mean organic soil layer thickness, and slope steepness) were analyzed using Pearson’s correlation coefficient analysis; highly correlated variables (ρ > 0.7) were excluded from the models to avoid multicollinearity. The 137Cs activity concentrations in A. elata buds and the dose rates at the soil surfaces were loge-transformed to normalize the distributions and standardize the variance before constructing the model. A Gaussian error structure was used for the response variables. The sampling year and identifiers for each A. elata plant were included as random terms in the LMM to consider potential variabilities between years and among plants. The LMM was constructed using the lmer function of the lme4 package [25] in R 3.6.3 [24]. To visualize the relationship between 137Cs concentrations in buds and a single explanatory variable, the other explanatory variables were fixed at their mean values using the ggeffects R package [26]. The effect of the presence/absence of decontamination practices on 137Cs activity concentrations in A. elata buds was tested using analysis of covariance (ANCOVA), with presence/absence of decontamination practices as a factor and 137Cs deposition estimated from the Fifth Airborne Radiation Monitoring [18] as the covariate. The 137Cs activity concentrations in the buds were loge-transformed to normalize the distribution and standardize variance before ANCOVA. The analysis was performed using R 3.6.3 software.
Results
137Cs concentrations in A. elata buds and the environmental variables
The 137Cs activity concentrations in A. elata buds ranged from 1 to 6,280 Bq/kg fresh weight. The values of the easy-to-measure environmental variables were dose rate at the soil surface, 0.10–6.50 μSv/h (Fig 2A and S1 Table); mean organic soil layer thickness, 0–10.5 cm (Fig 2B and S1 Table); and slope steepness, 3–49° (Fig 2C and S1 Table). Because there was no pair of highly correlated explanatory variables with ρ > 0.7, all three environmental variables were used as explanatory variables in the LMM. The LMM indicated that the dose rate at the soil surface had a significant positive effect on the 137Cs activity concentrations in A. elata buds (Table 1; Fig 2). The 137Cs activity concentrations in A. elata buds showed a weak positive relationship with organic soil layer thickness and a negative relationship with slope steepness, but the relationships were not significant. The presence/absence of decontamination practices did not affect the 137Cs activity concentrations in A. elata buds (t = –1.124, P = 0.268), but the 137Cs depositition had a significant positive effect (t = 7.552, P < 0.001), as illustrated in Fig 3. These results indicate that the 137Cs activity concentrations in A. elata buds were lower at sites with less initial 137Cs deposited, regardless of the presence/absence of decontamination practices.
Relationships between 137Cs activity concentrations in A. elata buds and (a) the dose rate at the soil surface, (b) organic soil layer thickness, and (c) slope steepness. The blue horizontal lines indicate the Japanese reference level for food (100 Bq/kg). Regression lines were generated based on the results of the full linear mixed model. Explanatory variables other than those shown on the x axis were fixed at their mean values. Shaded bands indicate 95% confidence intervals.
Relationship between 137Cs activity concentrations in A. elata buds and 137Cs depositions at the decontaminated (light blue) and abandoned (pink) sites. The blue horizontal line indicated the Japanese reference level for food (100 Bq/kg).
Bold characters indicate statistical significance.
Aggregated transfer factors
As previously reported [22], the 137Cs inventory in the soil and the dose rate at the soil surface were positively correlated (Fig 4). The relationship was expressed as Eq 1:
(1)
Shaded bands indicate 95% confidence intervals.
The slope and intercept were significant (P < 0.001) and the adjusted R2 was 0.856. The 137Cs inventory in the soil estimated based on the relationship ranged from 24 to 4,200 kBq/m2 at the base of the A. elata plants. The estimated 137Cs inventory in the soil and 137Cs activity concentrations in A. elata buds were used to calculate the Tag values, and the geometric mean (GM) and geometric standard deviation (GSD) of the Tag were 3.7 × 10−4 m2/kg and 1.3, respectively (with a minimum of 2.3 × 10−5 m2/kg and a maximum of 8.5 × 10−3 m2/kg).
Discussion
The present study confirmed that 137Cs activity concentrations varied widely among A. elata buds, including concentrations above and below the Japanese reference level for food [27]. In particular, plants at sites with a higher dose rate at the soil surface exhibited elevated 137Cs activity concentrations in their buds. These findings emphasize the importance of refraining from collecting and consuming A. elata buds from such habitats as a way to mitigate internal exposure. Interestingly, contrary to our expectations, decontamination practices did not lead to reduced 137Cs activity concentrations in the A. elata buds. This result further emphasizes the value of directly assessing the current dose rate at the soil surface at the base of A. elata plants rather than a decontamination record. This approach offers a practical means to avoid collecting buds with higher 137Cs concentrations.
Given that the dose rate at the soil surface was a useful indicator for estimating the 137Cs inventory in the soil (Eq 1) [22], using a portable dosimeter was a convenient way to instantly estimate the 137Cs inventory in soil and associated transfer factors between the soil and organisms. The GM and GSD of the Tag for A. elata buds were 3.7 × 10−4 m2/kg and 1.3 for 2022–2023, respectively. The GM and GSD values were smaller than those reported previously for A. elata buds (1.1 × 10−3 m2/kg and 3.1 for 2016–2018 [22] and 4.3 × 10−4 m2/kg and 4.0 for 2014–2019 [21]). The smaller GM value suggests a gradual reduction in the transfer of 137Cs from the soil to A. elata buds [28]. This decrease may be attributable to downward 137Cs migration in soils [29], followed by fixation in clay minerals, which subsequently decreases the bioavailability of 137Cs [30]. In addition, the remarkably smaller GSD value suggests that such a migration may induce a steady-like state of 137Cs dynamics in the soil, showing the clear positive relationship between the dose rate at the soil surface and 137Cs activity concentrations in A. elata buds. Although Tag is generally rather variable (and thus often represented with GM and GSD) [8,21,22], the positive relationship may become observable under the current soil conditions more than 10 years after the contamination event.
The LMM demonstrated that the dose rate at the soil surface had a significant effect on 137Cs activity concentrations in A. elata buds. This finding agrees with previous studies that have reported positive relationships between the dose rate (or 137Cs inventories in the soil) and the 137Cs concentrations in various taxa [12–14]. The 137Cs inventory in the soil described herein was presumably affected by the amount of 137Cs deposited and by slope steepness, which is an important driver of soil runoff and affects the amount of 137Cs in soil [17]. However, the effect of steepness on concentrations in A. elata buds was minimal, suggesting that runoff of 137Cs may have been limited in the slopes of the A. elata habitats, where open sunlit environments often give rise to luxuriant vegetation that prevents soil erosion [31].
In addition, the thickness of the organic soil layer did not increase the 137Cs activity concentrations in A. elata buds, while the soil layer was assumed to possess abundant bioavailable 137Cs that can be transferred to plants [30]. For example, Eleutherococcus sciadophylloides (Koshiabura, the Queen of sansai), which develops extensive roots in the interface between the organic and mineral soil layers [32] exhibit one of the highest bud 137Cs concentrations among Japanese wild vegetables [6–8]. In addition, 137Cs activity concentrations in E. sciadophylloides are well correlated with 137Cs inventories in the organic soil layer [8]. Thus, 137Cs in the organic soil layer is still notable to understand 137Cs transfer from the soil to wild vegetables. However, the thickness of the layer may not always be correlated with the 137Cs inventory in it; thus, our result may not show a clear positive relationship between organic soil layer thickness and 137Cs activity concentrations in A. elata buds. Although the inventory in this layer is expected to be a good predictor of the 137Cs concentrations in A. elata buds, the estimate is generally time-consuming and is not a feasible way for the public and thus not fitted to the objective of this study.
The presence/absence of decontamination practices did not affect the 137Cs activity concentrations in A. elata buds. Although the specific processes leading to this result are unclear, it can be speculated from several processes. First, the decontamination practices were designed to decrease external exposure to less than 1 mSv/y (0.23 μSv/h) for local residents, and achieving this purpose in highly contaminated areas is a challenge [15]. Therefore, our sites may possess sufficient 137Cs in soils to have high 137Cs concentrations in A. elata buds even if decontamination practices were implemented. Second, the 137Cs deposition data we used [18] might be too coarse (250 m mesh) to detect the effect of decontamination on 137Cs activity concentrations in A. elata buds. Third, recontamination from surrounding environments might mask the potential effect of decontamination. For example, several studies have reported that soil surface removal as a decontamination practice does not effectively reduce the 137Cs concentrations in tree species [33,34]. Moreover, recontamination from the surrounding environment can increase the levels in soils after decontamination [19]. The assessment of such effects is of utmost importance to mitigate external exposure and revive traditional practices of wild vegetable collection and consumption.
The present study revealed that 137Cs activity concentrations in A. elata buds increased as the dose rate at the soil surface increased. This environmental factor is easily measurable and helpful to avoid collecting A. elata buds with high 137Cs concentrations. Our findings indicate that the presence/absence of a decontamination practice did not affect the concentrations in A. elata buds. Further studies that examine the causality among the relationships between these environmental variables and 137Cs concentrations in A. elata are needed to understand the 137Cs dynamics between the soil and plants. The significant positive relationship between 137Cs activity concentrations in A. elata buds and dose rate at the soil surface observed here can be a useful information to decrease the risk of collecting and consuming highly contaminated A. elata buds. Because cooking potentially decreases 137Cs concentrations in wild vegetables [35], a combination of collecting and cooking measures could further help revive this tradition. Developing measures to decrease the risk of collecting and consuming wild vegetables as reported here is now growing in significance to facilitate the revival of traditional cultures in polluted regions.
Supporting information
S1 Table. The raw data of 137Cs activity concentrations in Aralia elata buds and environmental variables analyzed in Sakai et al. Exploring simple ways to avoid collecting highly 137Cs-contaminaed Aralia elata buds for the revival of local wild vegetable cultures.
https://doi.org/10.1371/journal.pone.0292206.s001
(XLSX)
Acknowledgments
We thank Mr. Kazuo Sasaki and Dr. Yoichi Tao for enabling us to collect samples, anonymous editor and reviewers for the improvement of the manuscript, and the Ministry of the Environment for providing us with the data of presence/absence of decontamination practice at the study sites.
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