Assessment Activity Concentrations of Rice Components (Root, Stem, Leaf, and Grain) and Transfer Factors (TF) from Paddy Soil to Rice Grain of Radionuclides 40K, 226Ra, 232Th, and 137Cs Investigation in Taiwan

Abstract

This study analyzed the activity concentrations of various radionuclides in irrigation water, rice components, and corresponding soil samples from eleven paddy fields, revealing significant findings with potential environmental and health implications. The soil exhibited high levels of activity concentrations ranging from 350 to 829, 12.4 to 41.2, and 18.5 to 60.3 Bq/kg, with mean values of 609, 31.1, and 45.0 Bq/kg for ⁴⁰K, ²²⁶Ra, and ²³²Th respectively. Additionally, 12 soil samples from two paddy fields showed ¹³⁷Cs activity concentrations of 5.6 ± 1.3 Bq/kg. The rice plant roots accumulated the highest percentages of total activity concentrations for ²²⁶Ra, ²³²Th, and ¹³⁷Cs, ranging from 76–86%, while only 1.1–10.0% were found in the un-hulled grain. For ⁴⁰K, activity concentrations were distributed among the root (23%), stem (32%), leaf (35%), and un-hulled grain (10%). The mean activity concentrations were 99 ± 12, 0.49 ± 0.09, 0.43 ± 0.12, and 0.10–0.31 Bq/kg for ⁴⁰K, ²²⁶Ra, ²³²Th, and ¹³⁷Cs for un-hulled rice grain, respectively. Transfer factors (TFs) from soil to un-hulled rice grain were calculated as (1.21–2.86) × 10⁻¹ for ⁴⁰K, (0.07–0.11) × 10⁻¹ for ²³²Th, (0.11–0.29) × 10⁻¹ for ²²⁶Ra, and (0.16–0.61) × 10⁻¹ for ¹³⁷Cs. Notably, significant negative correlations were observed between TFs and soil concentrations for ⁴⁰K (r = 0.92, p < 0.001, n = 11) and ²²⁶Ra (r = 0.98, p = 0.026, n = 4), suggesting that macronutrients in soil solutions may inhibit the linear transfer of natural nuclides from the soil solution to rice plants.

1. Introduction

Natural radionuclides are ubiquitously present in the environment, primarily originating from the weathering of minerals in soil, which leads to significant geographical variations in their activity concentrations [1,2,3,4,5]. Common natural radionuclides such as ⁴⁰K, ²²⁶Ra, and ²³²Th and artificial nuclide ¹³⁷Cs are found in soil and food, but their activity concentrations vary across different regions worldwide [5,6,7,8,9]. Plants absorb these radionuclides along with essential nutrients through their roots and transport them to other parts of the plant [4,8,10,11,12]. The presence of radioactivity in the edible parts of crops can lead to internal exposure in humans [8,12,13].

Assessing the concentration of radionuclides in food chains is crucial, with the soil-to-plant transfer factor (TF) playing a significant role in this process [4,8,11,12,14,15,16]. TF is defined as the ratio of radioactivity in the dry mass of the crop to that in the dry mass of the soil, considering the uptake of radionuclides through roots [4,10,17]. This complex process involves physical, chemical, and biological mechanisms and depends on the type of plant and the isotope-binding characteristics of the soil system [1,4,8,10,12,18,19]. The TF can vary significantly depending on the site and plant components, influenced by the nuclide’s chemical form, the physical and chemical properties of the soil, and environmental conditions [4,17,20]. Therefore, it is essential to consider all these factors when evaluating the potential concentration of radionuclides in food chains [1,4,6,8,10,12,15,19].

Rice is a vital cereal crop, serving as the main source of food and nutrients for approximately half of the global population, particularly in tropical and Asian countries such as Taiwan [4,8,10,12,20,21]. Unlike dryland crops, rice is grown in waterlogged fields, which may affect its nutrient and radionuclide absorption mechanisms [4,11,22]. While previous studies have primarily focused on artificial nuclides like ¹³⁷Cs and ⁹⁰Sr, the presence of natural radionuclides in rice and their transport from soil to rice components has recently become a concern [1,2,4,6,8,10,12,14,21,23]. The activity concentrations in rice grains show significant variations, ranging from 7 to 110 Bq/kg for ⁴⁰K, below detection limits (BDL) to 25 Bq/kg for ²²⁶Ra, and BDL to 65 Bq/kg for ²³²Th [4]. Additionally, the TF values from soil to rice grain vary by one to three orders of magnitude for various natural radionuclides [1,6,8,14,24]. For example, TF values for rice grain under various conditions (e.g., polished rice, brown rice, white rice, hulled rice) range from 8.1 × 10⁻² to 1.72 for ⁴⁰K [1,2,4,10,12,14,25], 2 × 10⁻³ to 8.1 × 10⁻¹ for ²²⁶Ra [1,2,4,6,10,14,25], 1.0 × 10⁻³ to 1.03 for ²³²Th [1,2,4,6,10,14,25], and 1.6 × 10⁻³ to 2.4 × 10⁻¹ for ¹³⁷Cs [2,11,12,15,26,27,28]. These ranges highlight the significant variability in TF values across different radionuclides and conditions, which are influenced by factors such as soil properties, rice plant components, and environmental conditions. Understanding these variations is crucial for assessing the potential radiological risks associated with rice consumption. Continued research on these factors is imperative to ensure the safety and well-being of those who rely on rice as a staple food source.

To accurately determine the transfer factor (TF) for a specific location, site-specific data is recommended [1,4,8,12,21]. Previous studies have focused on soil properties and soil activity concentration as influencing factors for TFs [4,6,8,12], but they lacked information on the properties and activity concentration of irrigation water [10]. Additionally, few studies have investigated how soil activity concentrations of radionuclides are altered after rice plantation [6]. This study selected eleven main rice production areas in Taiwan to measure the properties and activity concentrations of irrigation water and soil before rice planting. After harvesting the paddy rice, the study detected the radionuclide activity concentrations in soil and various rice components, including roots, stems, leaves, and un-hulled grains. The purpose of this study was to analyze the distribution of nuclides in different components of rice and determine the transfer factors (TFs) of ⁴⁰K, ²²⁶Ra, ²³²Th, and ¹³⁷Cs from soil to un-hulled grains. Additionally, the study aimed to investigate the impact of soil and water activity concentrations and soil physical-chemical characteristics on radionuclide soil-to-grain TFs. This study hypothesizes that the uptake and transfer factors (TFs) of natural and artificial radionuclides (⁴⁰K, ²²⁶Ra, ²³²Th, and ¹³⁷Cs) by rice plants are influenced by the properties of soil and irrigation water. Specifically, the study anticipates that higher activity concentrations of radionuclides in soil may not always result in a proportional increase in transfer factors, as macronutrients in soil solutions may inhibit the uptake of trace radionuclides.

2. Materials and Methods

2.1. Study Area

The study was conducted in eleven rice paddy fields located in Taiwan’s main rice production area. These sites were precisely mapped using GPS, with their coordinates provided in Figure 1. The criteria for selecting the paddy fields included their geographical location in Taiwan’s main rice-producing areas, the diversity of irrigation sources, and the willingness of landowners to cooperate with the study.

Taiwan features a subtropical climate, characterized by a monsoon influence: the north experiences a subtropical monsoon climate, while the south has a tropical monsoon climate. The region maintains a warm climate year-round, with an average annual temperature of approximately 22 °C. Monthly temperatures range from a low of 12 °C to a high of 35 °C. The average annual rainfall is 2515 mm [29].

Rice is typically planted twice a year, with the first planting season in January and February, followed by harvesting from May to June [30]. For this study, soil samples were collected from January to February and May to June 2019, while paddy plants were sampled during May and June 2019.

2.2. Sample Collection and Preparation

2.2.1. Soil and Water Samples

Before planting, soil and irrigation water samples were collected from 11 paddy fields. Each field provided three soil samples and a two-liter sample of irrigation water. Water sources included groundwater, surface water from lakes and reservoirs, and downstream river water from hot springs. Water samples were weighed, placed in Marinelli beakers, and sealed for one month to allow equilibrium between ²²⁶Ra and its decay products.

Soil samples were collected from a depth of 0–15 cm using a hand shovel. Unwanted materials such as stones and roots were removed. During harvest, nine soil samples were randomly collected from each field and combined into three pooled samples of about 1 kg each. These samples were air-dried for over a week, then oven-dried at 105 °C to remove moisture, pulverized, and sieved through a 2 mm mesh. Approximately 150 g of dry soil was placed into a polyethylene bottle and sealed for one month to achieve equilibrium between ²²⁶Ra and its decay products.

2.2.2. Paddy Plant Samples

During the harvest season, 50 paddy plants, each containing 7–10 plants, were collected from each site. The soil was excavated to a depth of approximately 30 cm to ensure intact roots. In the laboratory, plants were washed with tap water to remove soil residue and divided into four components: root, stem, leaf, and un-hulled grain. Roots were further washed with deionized water to remove any remaining soil. Each component was cut into pieces of 1–2 cm.

All plant parts were oven-dried at 105 °C until reaching a constant mass and then ashed in a furnace, with a gradual increase in temperature to 450 °C over two days. The resulting ash samples, about 110 g, were weighed, recorded, and placed into a polyethylene bottle (60 mm in diameter, 45 mm in height). These were sealed for one month before measurement to allow equilibrium between ²²⁶Ra and its short-lived decay products.

2.3. Water and Soil Properties Measurement

The pH and electrical conductivity (EC) of water samples were measured at sampling stations (pH: pH315/SET, Xylem, Germany. EC: LF330/SET, Xylem, Germany). The other properties of soil and water samples were analyzed following the standard methods of the Ministry of Environment of Taiwan, such as suspended solid (SS, NIEA W424.52A), total solid (TS, NIEA W210.56A), and chemical oxygen demand (COD, NIEA W515.55A) of water. The soil texture (sand, silt, and clay content) was determined by using the sieve and hydrometer method [31]. The pH and electrical conductivity (EC) of soil samples were measured using the given procedures [32]. Other main distinguishing features, such as organic matter (OM) and cation exchange capacity (CEC), were determined using the methods described by Thomas [33].

2.4. Gamma-Ray Spectrometry and Activity Measurements

For accurate measurements, a high-purity germanium (HPGe) p-type detector with a 59 mm active diameter and 79.8 mm length was used. The detector was enclosed in a cylindrical lead shield with 10 cm thickness, 28 cm inner diameter, and 40 cm height. The low background ORTEC system featured a 1.85 keV FWHM energy resolution at the 1.33 MeV ⁶⁰Co photopeak and a 40% relative efficiency counting system, connected to a multi-channel analyzer.

Energy calibration was performed using standard gamma sources (¹⁰⁹Cd, ⁵⁷Co, ²⁰³Hg, ⁵¹Cr, ¹¹³Sn, ⁸⁵Sr, ¹³⁷Cs, ⁶⁰Co, and ⁸⁸Y) from the International Atomic Energy Agency. A certified multi-nuclide source with similar geometry and density to the samples was used for efficiency calibration over the energy range of 88–2000 keV.

Samples were counted for 30,000 s, with a background count conducted using an empty container under the same conditions. Spectrum analysis was performed using Gamma Vision software (Gamma Vision-32 V6), focusing on the photopeaks at 609.3, 1120.3, and 1764.5 keV for ²²⁶Ra, 583.0 keV for ²³²Th, and 1460.8 keV for ⁴⁰K. Additionally, the 661.66 keV emission line was utilized to determine the ¹³⁷Cs concentration.

The activity concentration A (Bq/kg) of each radionuclide in each sample was calculated using Equation (1) from Azeez et al. [34]:

(1)$\mathrm{A}={\displaystyle \frac{N}{{ϵP}_{\gamma }tm}}$

where N is the net count of the corresponding photopeak, P_γ is the emission probability per disintegration, ϵ is the detector efficiency at this specific gamma line, t is the counting time in seconds, and m is the mass of the sample in kg. For decay series radionuclides like ²²⁶Ra, the activity was quantified by averaging values from relevant photopeaks.

The transfer factor (TF) is defined as the ratio of the radionuclide activity concentration in paddy plant components to that in soil. TF values were calculated using Equation (2) [35]:

(2)$\mathrm{T}\mathrm{F}={\displaystyle \frac{A_i^p\left(\mathrm{B}\mathrm{q}\mathrm{k}{\mathrm{g}}^{-1},\hspace{1em}\mathrm{d}\mathrm{r}\mathrm{y}\mathrm{w}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t}\right)}{A_i^s\left(\mathrm{B}\mathrm{q}\mathrm{k}{\mathrm{g}}^{-1},\hspace{1em}\mathrm{d}\mathrm{r}\mathrm{y}\mathrm{w}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t}\right)}}$

where TF is the transfer factor of the soil-to-paddy component, $A_i^p$ is the activity concentration of radionuclides i in Bq/kg dry paddy plant weight, and $A_i^s$ is the activity concentration of radionuclides i in Bq/kg dry soil weight.

2.5. Statistical Analysis

All statistical analyses were conducted using S-Plus 6.2, a widely recognized commercial statistical software known for its robust and validated algorithms. The primary analyses included linear regression, one-way analysis of variance (ANOVA), and independent sample t-tests, with a significance level set at p < 0.05. Potential confounding variables, such as soil and water properties, were identified based on prior literature and included as covariates in the regression models to adjust for their effects. Sensitivity analyses were performed to validate the robustness of the results.

3. Results and Discussion

3.1. Water and Soil Properties

In this study, we collected irrigation water and soil samples from eleven paddy fields. The basic properties of these samples are listed in Table 1. The water samples exhibited varying pH, electrical conductivity (EC), suspended solids (SS), and total solids (TS) values, which can be attributed to the diverse sources of water (groundwater, river, reservoir, and spring water). Notably, all water properties complied with the irrigation water standards in Taiwan [36].

Figure 2 provides a comparison of soil properties before paddy plantation and at harvest. Statistical analysis showed no significant changes in pH, EC, CEC, and OM values between these two periods (p-values ranging from 0.12 to 0.94), indicating stability in soil conditions. The soil samples had a mean pH of 6.71 ± 0.84, ranging from 5.00 to 8.28, suggesting a slightly acidic nature. The CEC averaged 6.16 ± 3.29 meq/100 g of dry soil, with a range from 1.25 to 13.02 meq/100 g. Meanwhile, the EC had an average of 553 ± 443 μS/cm, ranging from 92 to 1582 μS/cm. Organic matter content ranged from 2.3% to 14.0%, with a mean of 6.45 ± 2.69%. Although slight variations were observed, these values fall within the reported ranges for paddy fields and agricultural farmlands [4,8,12,13,37].

The soil textures were categorized based on their sand, silt, and clay fractions as shown in Figure 3. The results indicated that the soils had an average sand fraction of 36.3 ± 14.1%, a silt fraction of 45.6 ± 9.9%, and a clay fraction of 18.1 ± 8.5%. According to the USDA soil texture classification, the paddy field soils were primarily loam, sandy loam, and silty loam [8].

3.2. Water and Soil Radioactivity Concentrations

The concentration of ⁴⁰K in the water samples was detectable, while the concentrations of ²³²Th and ²²⁶Ra were below the detection limit. The activity concentration of ⁴⁰K ranged from 0.34 to 6.62 Bq/L, with an average of 3.34 ± 1.66 Bq/L, consistent with values reported for natural surface waters [38,39,40,41].

Figure 4 shows the soil activity concentrations of each radionuclide before plantation and at harvest, which were not significantly different (p-values ranging from 0.29 to 0.84), suggesting that short-term farming operations did not affect soil radionuclide activity concentrations [42]. The average ⁴⁰K activity concentration in soil samples was 591 ± 134 Bq/kg-dw, higher than the global average of 420 Bq/kg-dw [43]. The average activity concentrations of ²³²Th and ²²⁶Ra were similar to the global averages of 45 and 32 Bq/kg-dw, respectively [43]. The ⁴⁰K activity was significantly higher than that of ²³²Th and ²²⁶Ra (p < 0.001). The ¹³⁷Cs activity was 5.57 ± 1.29 Bq/kg-dw, lower than the other radionuclides, comparable to soils planted with vegetables and rice in various countries [12,15,16,26,37]. The soil activity concentrations were within the range detected in other global sites [2,3,4,7,8,10,12,18,23,25,35,44,45]. The slight increase in ⁴⁰K activity after rice cultivation might be due to NPK fertilizer use to enhance rice yield [34,37,45,46].

There was a weak correlation between the ⁴⁰K concentration in soil and irrigation water before and after rice cultivation, with correlation coefficients of 0.36 and −0.07 and p-values of 0.24 and 0.84, respectively. This suggests that geological factors may have a more significant influence on soil radionuclide activity levels than irrigation water and short-term farming practices.

3.3. Activity Concentrations of Rice Plant Components

The paddy rice plant is divided into four parts: root, stem, leaf, and un-hulled grain. Figure 4 shows soil radionuclide activity concentrations of ⁴⁰K, ²³²Th, ²²⁶Ra, and ¹³⁷Cs across eleven paddy fields before plantation and at harvest. Table 2 presents the average of activity concentrations for each component. Generally, the activity concentrations in soil (Figure 4) were higher than those in the rice components. Notably, the activity concentrations of ⁴⁰K in two stem samples and three leaf samples exceeded their corresponding soil concentrations, suggesting potential differences in uptake mechanisms.

In the analyzed samples, ⁴⁰K concentrations ranged from 173 to 362 Bq/kg-dw in roots, 149 to 820 Bq/kg-dw in stems, 161 to 749 Bq/kg-dw in leaves, and 86 to 125 Bq/kg-dw in un-hulled grains. The concentrations of ²³²Th were 6.9 to 17.9 Bq/kg-dw in roots, below detection limit (BDL) to 1.0 Bq/kg-dw in stems, BDL to 8.1 Bq/kg-dw in leaves, and BDL to 0.56 Bq/kg-dw in un-hulled grains. For ²²⁶Ra, the concentrations were 6.1 to 14.3 Bq/kg-dw in roots, BDL to 2.2 Bq/kg-dw in stems, BDL to 12.6 Bq/kg-dw in leaves, and BDL to 0.6 Bq/kg-dw in un-hulled grains. Only two samples showed ¹³⁷Cs activity, with mean concentrations of 1.8 Bq/kg-dw in roots, 0.1 Bq/kg-dw in stems, and 0.2 Bq/kg-dw in un-hulled grains, while leaf concentrations were below detection limits.

The root exhibited higher activity concentrations of ²³²Th, ²²⁶Ra, and ¹³⁷Cs compared to the stem, leaf, and un–hulled grain, whereas the un-hulled grain had the lowest concentrations of ²³²Th, ²²⁶Ra, and ⁴⁰K. Leaf concentrations were also higher than those in the stem for ²³²Th and ²²⁶Ra, consistent with findings in other studies [15,47].

Table 3 also compares activity concentrations of rice components from the literature. Previous studies’ concentrations in rice components have results similar to those of the present study. Roots typically had higher concentrations of ²³²Th, ²²⁶Ra, and ¹³⁷Cs than other components (straw, leaf, and grain). However, straw and leaf had relatively higher ⁴⁰K concentrations than roots and grains. The grain had lower concentrations than other rice components. In comparison to literature, the ⁴⁰K and ¹³⁷Cs concentrations of rice grain in this study were within reported ranges [1,4,6,8,12,15,25,27]. However, ²³²Th and ²²⁶Ra concentrations were lower than reported concentrations of rice grain [1,4,6,8,25,27]. High ⁴⁰K concentrations may result from high soil activity, as ⁴⁰K is more mobile than heavier elements like ²³²Th and ²²⁶Ra [31,48,49].

Figure 5 illustrates the distribution percentages of activity concentrations in rice components. The distribution pattern of ⁴⁰K in rice plants differs from that of ²³²Th, ²²⁶Ra, and ¹³⁷Cs. Specifically, the mean percentages of ⁴⁰K were 23.0 ± 6.7% in roots, 31.9 ± 9.2% in stems, 35.2 ± 9.8% in leaves, and 9.9 ± 3.5% in un-hulled grains. The roots, leaves, and stems percentages were significantly higher than those in un-hulled grains (p < 0.001). This pattern reflects the mobility and transport of ⁴⁰K from roots to other rice components, with notable accumulation in leaves and stems [8,12,15].

Roots accumulated an average of 75.8–86.0% of the total ²³²Th, ²²⁶Ra, and ¹³⁷Cs, while leaves contained 11.5% and 17.5% of the total ²²⁶Ra and ²³²Th, respectively. Less than 5.1% of ²²⁶Ra and ²³²Th were found in stems and un-hulled grains. Stems and un-hulled grains had 4.8% and 10.0% accumulation of ¹³⁷Cs, respectively. Consistent with other studies [8,15,48], un-hulled grains had the lowest concentrations of ²²⁶Ra and ²³²Th. The higher concentrations of ²³²Th, ²²⁶Ra, and ¹³⁷Cs in roots may be due to their role as a natural barrier to radionuclide transport to aboveground parts [49]. The transport extent of radionuclides from roots to aboveground parts is influenced by different plant components, as shown in other studies [8,12,37,46,48].

The distribution percentages of radionuclides in our study slightly differ from those reported by Alsaffar et al. [8]. They found that the root percentages were 47%, 57%, and 13% for ²²⁶Ra, ²³²Th, and ⁴⁰K, respectively, with grain and husk percentages at 23%, 19%, and 28% and straw at 30%, 24%, and 59%. Our results indicate that ⁴⁰K had a high percentage of straw (combined stem and leaf) at 67%, similar to the 59% straw percentage in Alsaffar et al. [8]. Our findings also show that roots had the highest percentages for ²³²Th and ²²⁶Ra, while un-hulled grains had the lowest, indicating similar distribution behavior. Variations in distribution behavior across studies may be due to differences in location, soil, and rice physical properties, climate conditions, and fertilizers used for crop production [48].

3.4. Transfer Factor from Soil to Grain

The transfer factors (TFs) were calculated using radionuclide concentrations in soil and rice components (Equation (2)). In two paddy samples where ¹³⁷Cs was detected, the mean TFs for ¹³⁷Cs were 0.31, 0.016, and 0.039 for the root, stem, and grain, respectively. The TF of root was significantly higher than those of stem and grain. The transfer factor of ¹³⁷Cs in rice grains was similar to the transfer factor values reported in Table 4 for the transfer from soil to grains [2,11,12,15,28,50].

Figure 6a–c display box plots of TFs for ²²⁶Ra, ²³²Th, and ⁴⁰K in rice components, with values listed in Table S1. The average TFs for ⁴⁰K were 0.43 ± 0.14, 0.66 ± 0.41, 0.71 ± 0.32, and 0.18 ± 0.06 for the root, stem, leaf, and grain, respectively. The TFs for the stem and leaf were significantly higher than those for the un-hulled grain (p < 0.001). In contrast, the TFs for ²³²Th and ²²⁶Ra showed a different pattern, with significantly higher TFs in the root compared to the stem, leaf, and un-hulled grain (p < 0.001). Additionally, the higher TFs in the leaf for ²³²Th and ²²⁶Ra than in the stem and grain may be attributed to the leaf’s metabolic activity [51,52].

The soil-to-grain TFs are crucial for assessing rice grain concentrations and potential human ingestion [4,11,13,26]. The TFs ranged from (1.21–2.86) × 10⁻¹, (0.07–0.11) × 10⁻¹, and (0.11–0.29) × 10⁻¹ for ⁴⁰K, ²³²Th, and ²²⁶Ra, respectively. The mean TFs were (1.8 ± 0.6) × 10⁻¹, (0.09 ± 0.02) × 10⁻¹, and (0.18 ± 0.08) × 10⁻¹ for ⁴⁰K, ²³²Th, and ²²⁶Ra, respectively. In grains, ⁴⁰K TFs were higher than those for ²²⁶Ra and ²³²Th (p < 0.001), aligning with most reported values in Table 4. The ⁴⁰K TFs for soil-to-grain in this study were compared to other studies in Table 4. The ⁴⁰K TFs were lower than some reported cases [4,12], while the TFs for ²²⁶Ra and ²³²Th were comparable to some reported values [2,6,10] but lower than most of the reported values [1,4,6,14,21,25]. In this study, the TFs were calculated using the ratio of un-hulled grain concentration to soil concentration. The rice husk has higher activity than the grain [12,15], which may increase the TFs for un-hulled grain.

The ²²⁶Ra TF for un-hulled grain was higher than the ²³²Th TF (p = 0.115), whereas the soil concentration of ²³²Th was significantly higher than that of ²²⁶Ra (Table 2, p < 0.001). This inverse relationship suggests that paddy rice uptake of ²²⁶Ra is greater than that of ²³²Th, consistent with findings by Alsaffar et al. [8], due to the higher solubility of radium compared to thorium.

3.5. Influence Factors of TFs for Soil to Rice Grain

The accumulation of radionuclides in rice grains can be influenced by various factors, including soil properties, nuclide chemical properties, and components of paddy plants [4,6,8,10,13,20]. In this study, we analyzed the correlation between soil-to-grain TFs and irrigation water and soil properties, as well as radionuclide concentrations in water and soil. Table 4 presents the correlation coefficients for ⁴⁰K, ²³²Th, and ²²⁶Ra TFs with selected parameters. The results indicate that the TFs for these radionuclides were not significantly correlated with water and soil properties (p > 0.05), except for ²²⁶Ra TFs, which showed a negative correlation with soil pH (p = 0.018, r = −0.98, 95% CI: −1.00 to −0.85). This negative correlation is attributed to the lower solubility of radionuclides at higher pH levels, as noted by Alsaffar et al. [8] and Asaduzzaman et al. [4]. The TFs for ¹³⁷Cs were not included in the correlation analysis due to the limited sample size.

Sampling was conducted across various locations in Taiwan with different geological compositions. The irrigation water originated from different sources, resulting in varying properties. Significant variations were observed in soil EC, OM, and CEC, with differences of up to 12, 5, and 10 times between their maximum and minimum values, respectively. Similarly, irrigation water properties, including EC, SS, TS, and COD, showed significant differences, with factors of 6, 144, 9, and 33, respectively. These diverse soil and water properties and geological environments contributed to the lack of significant correlation between soil-to-grain TFs and soil and water properties. While soil OM, pH, CEC, and EC impacted the TFs of ²²⁶Ra, ²³²Th, and ⁴⁰K in rice grain [4,8,12,13], studies suggest that TF is a site-specific parameter not solely influenced by a single factor [4,12].

Our study found that contrary to previous studies, the absorption of radionuclides in the soil-to-grain system does not always follow a linear relationship [12,53]. Figure 7 demonstrates a strong negative correlation between the TFs of ⁴⁰K and ²²⁶Ra and their soil activity concentrations (p < 0.001 for ⁴⁰K, 95% CI: −0.95 to −0.75; p = 0.024 for ²²⁶Ra, 95% CI: −0.92 to −0.12). This inverse relationship suggests that the transfer of natural nuclides is likely inhibited by macronutrients in soil moisture. Soluble nuclides absorbed by plants, considered trace elements, may also be inhibited by macronutrients such as K and Ca in soil moisture [4,8,13,26,54]. To improve paddy rice growth, excessive amounts of K are often applied as fertilizers, potentially inhibiting root uptake of radionuclides [8,26]. Similar negative correlations have been observed in rice plants [12]. Furthermore, Tsukada et al. [26] and Fujimura et al. [13] found that ¹³⁷Cs and stable Cs transfer factors decreased with increasing soil K concentration.

The observed negative correlations between transfer factors (TFs) and soil radionuclide concentrations (Figure 7) can be explained by several mechanisms. First, the saturation effect in root absorption may occur when the absorption pathways in plant roots reach their capacity at higher soil radionuclide concentrations, limiting additional radionuclide uptake. This phenomenon has been observed in studies where the uptake of radionuclides such as ⁴⁰K and ²²⁶Ra decreased with increasing soil concentrations due to the limited capacity of root ion channels and transport systems [4,8,54].

Second, the aging effect in soil may also play a role. Over time, radionuclides in the soil bind strongly to clay minerals and organic matter, transitioning from exchangeable forms to fixed forms, which reduces their bioavailability. This process has been documented in studies on ¹³⁷Cs and ⁴⁰K transfer in agricultural systems [13,20,54].

Lastly, the dilution of the concentration gradient between soil and root surfaces may also contribute. When soil radionuclide concentrations are high, the relative gradient driving radionuclide uptake decreases, resulting in lower transfer rates to plants. Similar findings have been reported for ⁴⁰K and ¹³⁷Cs in rice and other crops [8,26,54]. These mechanisms collectively suggest that the relationship between soil radionuclide concentrations and TFs is non-linear and influenced by both soil chemistry and plant physiological factors.

Moreover, the reduction in TFs with increasing soil radionuclide concentrations can also be attributed to competitive inhibition by macronutrients. Higher soil concentrations of radionuclides, such as ⁴⁰K and ²²⁶Ra, may compete with essential nutrients like potassium K⁺ and calcium Ca²⁺ for uptake pathways in plant roots. This competition reduces the absorption efficiency of radionuclides, as observed in similar studies [4,8,54]. Additionally, at higher concentrations, radionuclides are more likely to form insoluble compounds or bind strongly to soil particles, reducing their availability in the soil solution. For example, thorium ²³²Th and radium ²²⁶Ra exhibit low mobility in soil due to their strong affinity for clay minerals and organic matter [20]. Finally, the absorption and transport systems in plant roots have a finite capacity, and when soil radionuclide concentrations exceed this capacity, the transfer efficiency decreases [13].

Soil nutrients also play a significant role in radionuclide absorption by plants, primarily through competitive interactions and modifications of the soil-plant system. Potassium (K), for instance, is chemically similar to cesium ¹³⁷Cs and competes for the same uptake pathways in plant roots. High potassium concentrations in soil, often resulting from fertilizer application, inhibit the absorption of cesium isotopes. This competitive inhibition has been observed in studies on rice and other crops [8,26,54]. Similarly, calcium Ca²⁺ and magnesium Mg²⁺ ions can reduce the absorption of radium ²²⁶Ra by competing for uptake sites in plant roots [4,54].

Future studies could include more regions and diverse soil types across Taiwan and neighboring areas to build a more comprehensive dataset. This would provide a broader understanding of regional variations in ¹³⁷Cs activity and its transfer to rice. Establishing long-term monitoring of ¹³⁷Cs in soil and rice would allow us to observe dynamic changes over time, providing insights into its long-term environmental and agricultural impacts. Collaborating with other research institutions could integrate meteorological, geological, and agricultural data, enhancing the precision and depth of the analysis. For instance, understanding rainfall patterns and soil erosion could help explain variations in ¹³⁷Cs distribution. Utilizing high-resolution spectrometers or other advanced technologies could improve the accuracy of ¹³⁷Cs measurements, especially in low-activity samples, reducing uncertainties in TF calculations. Creating a centralized database to collect and share ¹³⁷Cs data from different studies would facilitate global comparisons and meta-analyses, providing stronger evidence to support conclusions. By implementing these strategies, future research can overcome the current limitations, strengthen the reliability of the data, and contribute to a more comprehensive understanding of radionuclide behavior in agricultural systems.

4. Conclusions

The results show that short-term farming activities did not have a significant impact on the soil activity concentrations of ⁴⁰K, ²³²Th, ²²⁶Ra, and ¹³⁷Cs, before plantation and at harvest. The uptake of selected radionuclides depended on plant components and species of nuclides, reflecting their mobility and accumulation in each part. The distribution of ²²⁶Ra and ²³²Th in rice plant components followed a root > leaf, stem, and un-hulled grain pattern, while ⁴⁰K followed a leaf and stem > root and un-hulled grain order. The mean soil-to-grain TFs for ⁴⁰K, ²³²Th, ²²⁶Ra, and ¹³⁷Cs were (1.84 ± 0.56) × 10⁻¹, (0.09 ± 0.02) × 10⁻¹, (0.18 ± 0.08) × 10⁻¹, and 0.39 × 10⁻¹, respectively. The grain TFs for ⁴⁰K, ²³²Th, and ²²⁶Ra were found to have insignificant correlations with water and soil properties due to the variations of properties of water and soil as well as geological conditions. However, the TFs for ⁴⁰K and ²²⁶Ra had a significant negative correlation with corresponding soil activity concentrations, suggesting that macro elements such as K and Ca may inhibit the absorption of nuclides. These results provide valuable information and serve as the basis for establishing a database of TFs in soil-to-grain.

Author Contributions

Conceptualization, W.-H.H., T.-C.C. and Y.-L.Y.; methodology, W.-H.H. and S.-C.L.; formal analysis, W.-H.H., T.-C.C., Z.-M.C. and Y.-L.Y.; investigation, W.-H.H., Z.-M.C. and S.-C.L.; writing—original draft preparation, W.-H.H. and T.-C.C.; writing—review and editing, T.-C.C. and Y.-L.Y.; project administration, Y.-L.Y.; funding acquisition, Y.-L.Y. All authors have read and agreed to the published version of the manuscript.

Data Availability Statement

Data are available through a request to the corresponding author.

Acknowledgments

The authors would like to thank the financial support from the National Science and Technology Council and Nuclear Safety Commission, Executive Yuan, Taiwan. The authors also appreciate the technical assistance from the Radiation Monitoring Center, Nuclear Safety Commission, and sampling help by Hsiang-Chun Tsai and Jhih-Cyuan Chang.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

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Figures and Tables

Figure 1. The sampling stations and corresponding latitude and longitude of the eleven stations.

Figure 2. Soil properties (pH, electrical conductivity [EC, μS/cm], organic matter [OM, %], cation exchange capacity [CEC, meq/100 g]) before plantation and at harvest.

Figure 3. Box plot of soil texture (sand, silt, and clay) content of the eleven paddy fields.

Figure 4. Soil radionuclide activity concentrations of 40K, 232Th, 226Ra, and 137Cs of eleven paddy fields before plantation and at harvest.

Figure 5. The percentages of distribution for nuclides activity concentrations in rice components (root, stem, leaves, and un-hulled grain).

Figure 6. Box plots of TF values of rice root, stem, leaf, and grain for TF values of 40K (a), TF values of 232Th (b), and TF values of 226Ra (c).

Figure 7. Linear relationship between 40K and 226Ra TFs and corresponding soil activity concentration.

Table 1

Basic properties of the irrigation water collected from the eleven paddy fields.

Properties	Value
pH	7.80 ± 0.49 (7.17–8.80)
EC (μS/cm)	586 ± 398 (263–1665)
SS (mg/L)	16 ± 28 (1–108)
TS (mg/L)	463 ± 365 (164–1525)
COD (mg/L)	15.5 ± 15.8 (2.0–65.0)

Table 2

Radionuclide activity concentrations of rice components (root, stem, leaf, and grain) for ⁴⁰K ²³²Th ²²⁶Ra, and ¹³⁷Cs and the reported activity concentrations of rice components (Bq/kg).

Component	40K	226Ra	232Th	137Cs	Reference
Root	238 (11) *	10.7 (11)	12.6 (11)	1.7–1.9 (2)	PS **
Root	147.4	7.8	6.9		Alsaffar et al., 2015 [8]
Root	199			3.0	Karunakara et al., 2013 [12]
Root	48			0.18	Wang et al., 1998 [15]
Stem	368 (11)	0.94 (9)	0.79 (3)	0.07–0.13 (2)	PS
Stem a	641	5.04	2.91		Alsaffar et al., 2015 [8]
Stem a	523			1.4	Karunakara et al., 2013 [12]
Stem	85–290			0.15–0.19	Wang et al., 1998 [15]
Leaf	404 (11)	4.43 (8)	3.83 (6)		PS
Leaf b	37–240			0.16–0.30	Wang et al., 1998 [15]
Grain c	99 (11)	0.49 (4)	0.43 (4)	0.10–0.31 (2)	PS
Grain d	72.2	1.42	1.03		Alsaffar et al., 2015 [8]
Grain d	152			1.3	Karunakara et al., 2013 [12]
Grain e	52–210			0.15–0.56	Wang et al., 1998 [15]
Grain d	60–92	1.5–2.8	3.6–7.5		Asaduzzaman et al., 2015 [4]
Grain d	38–39	7.5–7.9	8.7–9.1		Okeme et al., 2016 [25]
Grain d	188	13.4	8.2		Oladele et al., 2023 [1]
Grain d		8–12 f	3–4		Ugbede et al., 2021 [6]
Grain d	89.2	2.71 f	4.50		Ugbede et al., 2021 [14]
Grain d	24.1	0.28	0.17	0.10	Kessaratikoon et al., 2023 [2]
Grain d	18	1.3	0.24		Nguyen et al., 2021 [10]
Polished rice	120	3.07	4.56		Shanthi et al., 2010 [27]

* within the parenthesis is the detected sample numbers; ** PS: present study; ^a straw; ^b young and old leaves; ^c un-hulled grain; ^d hulled grain; ^e including polish rice, brown rice, rachis, fine hull, and coarse hull; ^{f 238}U.

Table 3

The transfer factors (TFs) of soil-to-grain for selected radionuclides ⁴⁰K, ²³²Th, ²²⁶Ra, and ¹³⁷Cs in the present study and TF values reported in other studies.

Types/Country	40K	226Ra	232Th	137Cs	References
Unhulled/Taiwan	1.8 × 10−1	1.8 × 10−2	9.0 × 10−3	3.9 × 10−2	PS a
Rice/Nigeria	(8.1–9.8) × 10−2	(3.1–8.1) × 10−1	(5.9–8.7) × 10−1		Okeme et al., 2016 [25]
Rice/ Nigeria	1.72	0.81	1.03		Oladele et al., 2023 [1]
Rice/Malaysia	0.96–1.13 (K) b	0.16–0.64 (U) b	6.2–6.6 × 10−2 (Th) b		Saeed et al., 2012 [21]
Rice/Nigeria		0.18–0.24 c	0.21–0.41		Ugbede et al., 2021 [6]
Rice/Nigeria	0.72	0.27 c	0.21		Ugbede et al., 2021 [14]
Rice/Thailand	3.7 × 10−2	2 × 10−3	1 × 10−3	5.5 × 10−2	Kessaratikoon et al., 2023 [2]
Rice/Vietnam	4.2 × 10−2	3.2 × 10−2	4.6 × 10−3		Nguyen et al., 2021 [10]
Polished rice/Japan	8.6 × 10−2			1.6 × 10−3	Tsukada et al., 2002 [26]
Grain/Malaysia	2.35 × 10−1	1.8 × 10−2	9 × 10−3		Ugbede et al., 2021 [6]
Brown rice/Japan	0.2 (K) b	4.9 × 10−5 (U) b	9.4 × 10−5 (Th) b		Uchida et al., 2007 [24]
White rice/Japan	0.064 (K) b	1.8 × 10−4 (U) b	1.3 × 10−4 (Th) b		Uchida et al., 2007 [24]
Grain/Malaysia	1.5			0.21	Karunakaraet al., 2013 [12]
Unhulled rice/Malaysia	1.4			0.24	Karunakaraet al., 2013 [12]
White rice/Malaysia	0.18			0.03	Karunakaraet al., 2013 [12]
Brown rice/Malaysia	0.91	0.26	0.37		Asaduzzaman et al., 2015 [4]
Hulled rice/Korea				(1.3–4.1) × 10−2	Keum et al., 2007 [28]
Rice/Korea				5.7 × 10−2	Choi et al., 2011 [11]
Brown rice/Taiwan				1.4 × 10−1	Wang et al., 1998 [15]
Polished rice/Taiwan				9.7 × 10−2	Wang et al., 1998 [15]
Polished rice/Japan				(0.8–1.3) × 10−2	Endo et al., 2013 [50]
Brown rice/Japan				(1.3–1.7) × 10−2	Endo et al., 2013 [50]

^a Present study, ^b element, ^c (²³⁸U).

Table 4

Correlation coefficients between soil-to-grain TFs and properties of water and soil as well as water activity of ⁴⁰K for ⁴⁰K, ²³²Th, ²²⁶Ra.

Parameters	40K (n = 11)	232Th (n = 4)	226Ra (n = 4)
pH_water	0.37	−0.45	0.13
EC_water	−0.21	0.13	−0.45
SS_water	−0.29	−0.81	−0.61
TS_water	−0.15	−0.18	−0.84
COD_water	−0.09	0.09	0.26
pH_soil	−0.16	−0.08	−0.98 *
EC_soil	−0.29	0.37	−0.81
OM_soil	0.14	−0.43	0.27
CEC_soil	0.28	−0.66	0.19
Sand_soil	0.37	−0.27	0.86
Clay_soil	0.06	−0.49	0.27
Silt_soil	−0.57	0.44	−0.85
40K_water	−0.44	−0.10	−0.20

* p < 0.05.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/agronomy15010023/s1: Table S1: TF values of ²²⁶Ra, ²³²Th, ¹³⁷Cs, and ⁴⁰K for rice components in the present study.

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